[1st Edition] 9780128121832, 9780128120804

Table of contents :
Content:
Series PagePage ii
CopyrightPage iv
ContributorsPages ix-x
PrefacePage xiAleš Iglič, Ana J. Garcia-Sáez, Michael Rappolt
Chapter One - Could Titanium Dioxide Nanotubes Represent a Viable Support System for Appropriate Cells in Vascular Implants?Pages 1-39I. Junkar, M. Kulkarni, P. Humpolíček, Z. Capáková, B. Burja, A. Mazare, P. Schmuki, K. Mrak-Poljšak, A. Flašker, P. Žigon, S. Čučnik, M. Mozetič, M. Tomšič, A. Iglič, S. Sodin-Semrl
Chapter Two - Ras Proteolipid Nanoassemblies on the Plasma Membrane Sort Lipids With High SelectivityPages 41-62Y. Zhou, J.F. Hancock
Chapter Three - Membrane-Mimetic Inverse Bicontinuous Cubic Phase Systems for Encapsulation of Peptides and ProteinsPages 63-94T.G. Meikle, C.J. Drummond, F. Separovic, C.E. Conn
Chapter Four - Interactions of Flavonoids With Lipidic MesophasesPages 95-123A. Sadeghpour, D. Sanver, M. Rappolt
Chapter Five - Preparation and Characterization of Supported Lipid Bilayers for Biomolecular Interaction Studies by Dual Polarization InterferometryPages 125-159T.-H. Lee, M.-I. Aguilar
Chapter Six - Gold Nanomaterials: Recent Advances in Cancer TheranosticsPages 161-180S. Sudhakar, P.B. Santhosh
IndexPages 181-186

Citation preview

EDITORIAL BOARD Dr. Mibel Aguilar (Monash University, Australia) Dr. Angelina Angelova (Universit
e de Paris-Sud, France) Dr. Paul A. Beales (University of Leeds, United Kingdom) Dr. Habil. Rumiana Dimova (Max Planck Institute of Colloids and Interfaces, Germany) Dr. Yuru Deng (Changzhou University, China) Prof. Dr. Nir Gov (The Weizmann Institute of Science, Israel) Prof. Dr. Wojciech Góźdź (Institute of Physical Chemistry Polish Academy of Sciences, Poland) Prof. Dr. Thomas Heimburg (Niels Bohr Institute, University of Copenhagen, Denmark) Prof. Dr. Tibor Hianik (Comenius University, Slovakia) Dr. Chandrashekhar V. Kulkarni (Centre for Materials Science, University of Central Lancashire, Preston, United Kingdom) Prof. Dr. Angelica Leitmannova Liu (USA) Dr. Ilya Levental (University of Texas, USA) Prof. Dr. Reinhard Lipowsky (MPI of Colloids and Interfaces, Potsdam, Germany) Prof. Dr. Sylvio May (North Dakota State University, USA) Prof. Dr. Philippe Meleard (Ecole Nationale Superieure de Chimie de Rennes, France) Prof. Dr. Yoshinori Muto (Gifu, Japan) V. A. Raghunathan (Raman Research Institute, India) Dr. Amin Sadeghpour (University of Leeds, United Kingdom) Prof. Kazutami Sakamoto (Chiba Institute of Science, Japan) Prof. Dr. Bernhard Schuster (University of Natural Resources and Life Sciences, Vienna) Prof. Dr. P.B. Sunil Kumar (Indian Institute of Technology Madras, India) Prof. Dr. Mathias Winterhalter (Jacobs University Bremen, Germany)

Academic Press is an imprint of Elsevier 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States 525 B Street, Suite 1800, San Diego, CA 92101-4495, United States The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom 125 London Wall, London, EC2Y 5AS, United Kingdom First edition 2017 Copyright © 2017 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. ISBN: 978-0-12-812080-4 ISSN: 2451-9634 For information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals

Publisher: Zoe Kruze Acquisition Editor: Poppy Garraway Editorial Project Manager: Shellie Bryant Production Project Manager: Magesh Kumar Mahalingam Cover Designer: Greg Harris Typeset by SPi Global, India

CONTRIBUTORS M.-I. Aguilar Monash University, Clayton, VIC, Australia B. Burja University Medical Centre Ljubljana, Ljubljana, Slovenia Z. Capa´kova´ Centre of Polymer Systems, Tomas Bata University in Zlin, Zlin, Czech Republic  ˇ nik S. Cuc University Medical Centre Ljubljana; Faculty of Pharmacy, University of Ljubljana, Ljubljana, Slovenia C.E. Conn School of Science, College of Science, Engineering and Health, RMIT University, Melbourne, VIC, Australia C.J. Drummond School of Science, College of Science, Engineering and Health, RMIT University, Melbourne, VIC, Australia A. Flasˇker Chemical Institute, Ljubljana, Slovenia J.F. Hancock McGovern Medical School, University of Texas Health Science Center, Houston, TX, United States P. Humpolı´cˇek Centre of Polymer Systems, Tomas Bata University in Zlin, Zlin, Czech Republic A. Iglicˇ Laboratory of Biophysics, Faculty of Electrical Engineering, University of Ljubljana, Ljubljana, Slovenia I. Junkar Josef Stefan Institute, Ljubljana, Slovenia M. Kulkarni Laboratory of Biophysics, Faculty of Electrical Engineering, University of Ljubljana, Ljubljana, Slovenia T.-H. Lee Monash University, Clayton, VIC, Australia A. Mazare Chair of Surface Science and Corrosion, University of Erlangen–Nuremberg, Erlangen, Germany

ix

x

Contributors

T.G. Meikle School of Chemistry, Bio21 Institute, University of Melbourne, Melbourne, VIC, Australia M. Mozeticˇ Josef Stefan Institute, Ljubljana, Slovenia K. Mrak-Poljsˇak University Medical Centre Ljubljana, Ljubljana, Slovenia M. Rappolt School of Food Science and Nutrition, University of Leeds, Leeds, United Kingdom A. Sadeghpour School of Food Science and Nutrition, University of Leeds, Leeds, United Kingdom P.B. Santhosh Indian Institute of Technology, Chennai, India D. Sanver School of Food Science and Nutrition, University of Leeds, Leeds, United Kingdom P. Schmuki Chair of Surface Science and Corrosion, University of Erlangen–Nuremberg, Erlangen, Germany F. Separovic School of Chemistry, Bio21 Institute, University of Melbourne, Melbourne, VIC, Australia S. Sodin-Semrl University Medical Centre Ljubljana, Ljubljana; Faculty of Mathematics, Natural Science and Information Technologies, University of Primorska, Koper, Slovenia S. Sudhakar Centre for Biotechnology, Anna University, Chennai, India M. Tomsˇicˇ University Medical Centre Ljubljana; Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia Y. Zhou McGovern Medical School, University of Texas Health Science Center, Houston, TX, United States ˇ igon P. Z University Medical Centre Ljubljana, Ljubljana, Slovenia

PREFACE A combination of chapters covering fundamental aspects of membrane organization and current concepts for membrane- and lipid-based technologies are included in Volume 25 of Advances in Biomembranes and Lipid Self-Assembly (ABiLSA). With a focus on the applied aspects of lipids and biomembranes, Volume 25 not only covers the exploitation of the rich variety in lipid phases for encapsulation of biomolecules but also cutting-edge methods to characterize biomembranes and the effect of peptides and proteins on their organization. From the basic biology side, the molecular mechanism of Ras at the plasma membrane is covered, as an example of membrane lateral compartmentalization in protein–lipid assemblies with a role in signal transduction and cellular function. At the technological end, the major parameters affecting the compatibility of nanotubes at the interface with the plasma membrane of adhering cells for the improvement of vascular implants are discussed. Also at the interface between material sciences and biological systems, gold nanomaterials offer new possibilities for diagnosis and as therapeutic agents, for example, the treatment of cancer or in drug delivery. Along these lines, the encapsulation of peptides and proteins in cubic phase systems as well as flavonoids in self-assembled lipid mesophases as delivery systems for biomedical applications are considered. All this would not be possible without the appropriate tools to characterize the organization of lipids in membranes. Differential polarization interferometry offers a label-free approach to quantify changes in molecular mass and packing order in membranes. We would like to thank all authors that contributed to Volume 25: Snezna Sodin-Semrl, Yong Zhou, Frances Separovic, Amin Sadeghpour, Mibel Aguilar, Poornima Budime Santhosh, and their coauthors. We are also grateful to Shellie Bryant and Poppy Garraway from the Elsevier Office in London, to Magesh Mahalingam from the Elsevier Office in Chennai, and to all members of the Editorial Board that contributed to the preparation of this volume of ABiLSA. ALESˇ IGLICˇ ANA J. GARCIA-SA´EZ MICHAEL RAPPOLT

xi

CHAPTER ONE

Could Titanium Dioxide Nanotubes Represent a Viable Support System for Appropriate Cells in Vascular Implants? I. Junkar*, M. Kulkarni†, P. Humpolíček{, Z. Capáková{, B. Burja§, A. Mazare¶, P. Schmuki¶, K. Mrak-Poljšak§, A. Flašker||, P. Žigon§, §,#
, M. Mozetič*, M. Tomšič§,**, A. Iglič†, S. Sodin-Semrl§,††,1 S. Cučnik

*Josef Stefan Institute, Ljubljana, Slovenia † Laboratory of Biophysics, Faculty of Electrical Engineering, University of Ljubljana, Ljubljana, Slovenia { Centre of Polymer Systems, Tomas Bata University in Zlin, Zlin, Czech Republic § University Medical Centre Ljubljana, Ljubljana, Slovenia ¶ Chair of Surface Science and Corrosion, University of Erlangen–Nuremberg, Erlangen, Germany jj Chemical Institute, Ljubljana, Slovenia # Faculty of Pharmacy, University of Ljubljana, Ljubljana, Slovenia **Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia †† Faculty of Mathematics, Natural Science and Information Technologies, University of Primorska, Koper, Slovenia 1 Corresponding author: e-mail address: [email protected]

Contents 1. Introduction 2. Selected Clinical Conditions Associated With Vessel Implants 2.1 Atherosclerosis 2.2 Coronary Heart Disease 2.3 Carotid Artery Disease 2.4 Peripheral Artery Disease 2.5 Atherosclerotic Renovascular Disease 3. Types of Vascular Implants 3.1 Stents 3.2 Grafts 3.3 Stent–Graft 3.4 Complications Connected With Stenting Procedures 4. Nanotopography, Surface Modifications, and Biocompatibility of Implants 5. TiO2 Nanotubes 5.1 Growth of TiO2 Nanotubes 5.2 Surface Properties of TiO2 Nanotubes 6. Surface Modification of TiO2 Nanotubes 6.1 Gaseous Plasma: Its Prospective Use in Medical Applications 6.2 Gaseous Plasma Treatment of TiO2 Nanotubes

Advances in Biomembranes and Lipid Self-Assembly, Volume 25 ISSN 2451-9634 http://dx.doi.org/10.1016/bs.abl.2016.12.001

#

2017 Elsevier Inc. All rights reserved.

2 3 4 5 5 6 6 6 7 8 9 9 11 14 15 16 19 19 21

1

2

I. Junkar et al.

6.3 Surface Analysis of Plasma-Modified TiO2 Nanotubes 7. Interaction of TiO2 Nanotubes With Cells 7.1 Platelets 7.2 Endothelial Cells 7.3 Mesenchymal Stem Cells 8. Antiinfective Properties of TiO2 Nanotubes 9. Concluding Remarks and Perspectives References

22 22 23 27 30 32 33 34

Abstract Nanoscale topography on various titanium surfaces has already been shown to improve vascular response in vitro. To propose a novel strategy for translation into clinically used vascular implants, it is imperative that the surface should also be properly conditioned to provide a better environment for adhesion and proliferation of cells. Electrochemical anodization process is one of the well-established strategies to produce controlled nanotopographic features on the surface of titanium. By combining electrochemical anodization process and gaseous plasma surface modification, it would be possible to fine-tune surface properties to enable improved biological response for specific application. The key surface properties that may influence biological responses, such as surface topography, surface chemistry, and surface wettability were studied in detail and their influences on in vitro biological responses were evaluated. Performance of platelets, human coronary artery endothelial cells (HCAEC), and stem cells on those surfaces was studied. It was shown that altering nanotube diameter (electrochemical anodization) and changing surface chemistry and wettability (gaseous plasma modification) significantly influenced platelet adhesion and activation as well as proliferation of HCAEC. The results provide evidence that by combining specific nanotopographic features and surface chemical modification by gaseous oxygen plasma, the optimized surface features necessary for improved performance of vascular implants in coronary arteries could be achieved.

1. INTRODUCTION The cardiovascular implant market is expanding rapidly due to population aging in developing countries, with a growing incidence of chronic and cardiovascular diseases (CVDs) on one side and technological advancement with limited biological replacement options available on the other side. The basic function of a vascular implant (either grafts or stents) is to function as an artificial conduit or substitute for an abnormality in veins or arteries [1]. The durability and functionality of long-term implanted medical devices are influenced by many factors, among them the type of affliction or injury, the materials used, the immunological state of the patient, and

TiO2 Nanotubes Represent a Viable Support System

3

the healing process itself. The quality of the materials relies largely on their ability to mimic the structure and properties of the native vessel wall and tissue. To date, the ability to match the attributes of a vascular substitute to those of a native vessel still remains a challenge [1] and further development is needed in the field of biocompatibility to shape future innovations. In the following sections, we will address the role of atherosclerosis (ASc), the major precursor of CVDs, and discuss a selected group of clinical complications that can occur in different vascular regions. Selected emphasis will be placed on coronary heart disease (CHD), carotid artery disease (CAD), peripheral artery disease (PAD), and atherosclerotic renovascular disease (ARVD), with focus on conditions ranging from stenosis, occlusions, aneurysms to ruptures. Next, we will investigate when and why grafts and stents are chosen as preferred types of vascular implants. Biomaterials will be discussed, as well as nanotopography leading to the use of titanium and titanium dioxide (TiO2) for implants. Treatment of TiO2 nanotubes will be explored from the biophysical and biochemical aspects, as well as the potential consequences of treatment on cellular growth of platelets, coronary artery endothelial cells, and mesenchymal stem cells (MSCs). Lastly, we will focus on the antiinfective properties of TiO2 vascular implants and propose future directions.

2. SELECTED CLINICAL CONDITIONS ASSOCIATED WITH VESSEL IMPLANTS The circulatory system is a complex network responsible for supplying the organism with nutrients and oxygen, while at the same time removing metabolic waste products. It is the first organ system to form and function during the development of the vertebral embryo [2], which indicates its important role. There are numerous different internal and external (genetic and environmental) factors than can alter vessel integrity and interfere with appropriate blood supply to tissues throughout the body. Major risk factors for developing CVD encompass smoking, diabetes, physical inactivity, unhealthy diet, cholesterol, obesity, increasing age, autoimmune diseases, hypertension, infections, gender, and a family history of vascular disease, among others [3]. They may also lead to early development of atherosclerotic plaques, complications which can bring about CVD pathogenesis, representing the leading cause of morbidity, and mortality in the Western world [4]. In 2006, CVD cost the health care systems within the EU just under €110 billion. The cost of inpatient hospital care for patients with CVD accounts for about 54% of these costs, while the cost of drugs accounts for about 28% [1].

4

I. Junkar et al.

2.1 Atherosclerosis ASc is the underlying pathology of CVD and events leading up to implant replacement therapy. It is defined as a focal, inflammatory fibro-proliferative response to multiple forms of endothelial injury [2]. It is a degenerative condition [3], characterized by the presence of intimal lesions called atheroma. Atheromatous plaques are raised lesions composed of soft lipid cores (mainly cholesterol along with cholesterol esters and necrotic debris) covered by fibrous caps [4]. ASc represents a chronic disease, with atherosclerotic plaques developing slowly over decades. The clinical outcomes (or consequences) of this process depend on the size of the affected vessel and most importantly, the stability of the plaques. Stable plaques (constituting of dense fibrous cap, minimal lipid accumulation, and little inflammation) [4] are associated with vessel occlusion (blockage) and inadequate blood flow to organs from the affected artery. As a consequence, there is a loss of the ability to respond with increased blood flow through the fixed artery lumen, most dangerously observed in coronary arteries. In patients with chronic occlusive disease, one can detect vessels adapting to this condition by forming new vessels or collateral circulation. Chronic occlusion will not change resting blood flow until lumen is largely blocked. Patients will develop symptoms of blood flow restriction in supplying blood to tissues, which is first noted under conditions of stress [5]. ASc also predisposes a person to aneurysm formation (widening of an artery due to destruction of the arterial wall). These aneurysms may favor the formation of blood clots that can break off and block vessels downstream, or they may burst and hemorrhage, which may be fatal [5]. In addition to occlusion and aneurysm formation, aortic dissection is a condition with the most abrupt onset, and if untreated, may be rapidly fatal [6]. Compared to other clinical manifestations, ASc is not the major factor promoting aortic dissection, but hypertension, connective tissue disorders, and injuries are factors that can promote a tear in the weak intimal layer of the aorta, resulting in a separation of the layers of the aortic wall (aortic dissection). The vast majority of aortic dissections originate with an intimal tear in either the ascending aorta (65% of the cases), the aortic arch (10%), or just distal to the ligamentum arteriosum in the descending thoracic aorta (20%) [7]. ASc individual plaques vary greatly in composition and acute manifestations of ASc can also occur. Vulnerable or unstable fibrolipid plaques (thin cap, large lipid cores, and dense inflammatory infiltrates) [4] can rupture and expose highly thrombogenic, red blood cell-rich necrotic core material

TiO2 Nanotubes Represent a Viable Support System

5

resulting in a cascade of inflammatory events [8]. This may lead to thrombus formation and platelet aggregation that can cause a complete obstruction of the arterial lumen and ultimately, myocardial infarction, or ischemic stroke in the brain. ASc can affect any artery in the body, but most commonly large elastic arteries (aorta, carotid, and iliac artery) and large/medium-sized muscular arteries (carotid, coronary, renal, and popliteal artery) [4] are altered. Consequently, any organ in the body can be involved, but most likely symptomatic disease is confined to the arteries supplying the heart, brain, lower limbs, and kidneys. Depending on which arteries are affected, different diseases, such as CHD, CAD, PAD, or ARVD may develop. Myocardial and cerebral infarction, aortic aneurysm, and PAD are by far the most important, clinically significant consequences of ASc [4,9].

2.2 Coronary Heart Disease In patients with CHD, atherosclerotic plaques build up in the coronary arteries, thus reducing blood flow to the heart. Fixed obstructions that block more than 70% of a vessel lumen may cause stable angina pectoris, with symptoms observed only under conditions of stress. In acute coronary syndrome, vulnerable plaque ruptures and thrombus formation may cause complete vessel obstruction and consequently, tissue necrosis (myocardial infarction). In the past, the predominant surgical treatment of diseased coronary arteries was bypass surgery, where the affected artery is “bypassed,” for example using a vein graft removed from the leg of the patient to divert blood around the blockage [10]. Considering all the possible complications of this surgery, more recently, cardiologists have resorted to using minimally invasive medical devices to “open up” blocked blood vessels. For certain patients with stable, as well as unstable coronary disease, rapid percutaneous coronary intervention with stent placement in the occluded artery, along with appropriate therapy, is the optimal treatment strategy.

2.3 Carotid Artery Disease Plaques may build up in the carotid arteries, generally supplying oxygen-rich blood to the neck and brain. The developing plaques can be either stable (asymptomatic) or symptomatic, when ischemic complications (reduced blood flow to tissues or organs) emerge with acute blockage of the carotid artery. If a clot breaks off an atherosclerotic plaque, emboli can travel

6

I. Junkar et al.

through the circulation to blood vessels in the brain. As the vessels become smaller, the clots can lodge in the vessel wall and restrict blood flow to parts of the brain. Ischemia (reduced blood flow to tissues or organs) can either be temporary, yielding a transient ischemic attack (TIA), or permanent, resulting in a thromboembolic stroke. Treatment of asymptomatic and symptomatic patients still remains debatable. Revascularization with carotid endarterectomy (surgical procedure to open and clean a carotid artery) has proven to be most beneficial for patients with large stenosis or narrowing of the blood vessel. However, for certain subgroups (patients with moderate stenosis and high surgical risk) carotid artery stenting has been proposed, as a less invasive alternative to surgery [11].

2.4 Peripheral Artery Disease Patients with PAD experience a narrowing of the peripheral arteries most frequently in the lower extremities. Symptoms are muscle pain, numbness, cramps, generally in the calf muscle, which occur during walking and can be relieved by a period of rest. Critical limb ischemia is a manifestation of PAD that describes patients with chronic ischaemic rest pain or patients with ischaemic skin lesions, ulcers, and/or nonhealing wounds that can lead to tissue death or gangrene. In certain cases, this requires amputation of the affected limbs. Percutaneous revascularization stenting has generally replaced invasive surgery as the first-line treatment for PAD [12].

2.5 Atherosclerotic Renovascular Disease ARVD may develop following plaque formation in the renal arteries causing stenosis. Plaque accumulation may lead to decreased kidney blood flow and renovascular hypertension. Later, chronic kidney disease can develop, which is typically asymptomatic until late stages. Renal artery stent revascularization can represent a treatment of choice for patients with hemodynamically significant stenosis with progressive renal insufficiency and/or deteriorating arterial hypertension [12,13].

3. TYPES OF VASCULAR IMPLANTS There are different types of vascular implants, such as stents, grafts, or a combination of both.

TiO2 Nanotubes Represent a Viable Support System

7

3.1 Stents A stent (defined as a tubular metal mesh) is a scaffolding device used to hold tissue in place in a specific stretched or taut position. In Fig. 1, a vascular stent and its surface morphology is presented as observed by scanning electron microscopy. Modern intravascular stents are available in balloon-expandable and self-expanding varieties [14]. The procedure that leads to the placing of a stent is called angioplasty and it involves mechanical widening of a narrowed blood vessel with a balloon catheter that forces the expansion of the vessel and the surrounding muscular wall. Thus, the blood vessel acquires improved flow. The stent may or may not be inserted at the time of ballooning to ensure that the blood vessel remains open. In many cases, the delivered stent becomes permanently implanted to provide additional support to the artery. Vascular stents have been indicated to be predominantly metal structures inserted into partially clogged arteries to promote normal blood flow and prevent myocardial infarctions [15]. Usually stents are made of hemocompatible and durable material, such as Titanium (Ti), 316L stainless steel (SS-medical grade), Nitinol (an alloy of Nickel and Titanium), and Cobalt-Chromium (CoCr). In some instances, a stent can elicit allergic reactions most commonly with Nickel, such as Nitinol and stainless steel [16]. In 2013, Acton (Ed.) [17] has described and quoted that coronary angioplasty or coronary percutaneous intervention is a therapeutic procedure to treat stenotic coronary artery, in case of severe angina pectoris or myocardial infarction. Peripheral angioplasty refers to the use of mechanical widening to open blood vessels other than the coronary arteries. This procedure is

Fig. 1 Example of a vascular stent (left) and scanning electron microscopy (SEM) image (right) of its surface.

8

I. Junkar et al.

referred to as percutaneous transluminal angioplasty (PTA), most commonly used to treat narrowing in the leg arteries (common iliac, external iliac, superficial femoral, and popliteal arteries). PTA can also be used to treat narrowing of the veins. In addition, atherosclerotic obstruction of the renal artery and carotid artery can also be treated with angioplasty. Any of these procedures can include placement of a stent to prevent or counteract constriction of localized blood flow. A stent is typically inserted through a main artery in the groin (femoral artery) or arm (brachial artery) on a wire or catheter and extended up to the narrowed section of the vessel. Once in place, the stent can help hold the vessel open, thus improving blood flow [17].

3.2 Grafts Surgical procedures also include using grafts, in which one or more blocked arteries are bypassed by a blood vessel graft in order to restore normal blood flow. The purpose of bypass grafting is to supply blood to distal circulation beyond the significant stenosis, using a graft which is made of biological materials (usually patients’ own venous or arterial conduits) [18] or synthetic materials. Wherever possible, replacement of the diseased blood vessel by an autograft is the best choice. Unfortunately, patients with preexisting vascular diseases usually do not have healthy enough blood vessels that could adequately replace the diseased parts. It needs to also be emphasized that some replacement parts, such as the aorta or large vessels, are not available. Therefore artificial materials, such as Dacron (PET—polyethylene terephthalate) or ePTFE (expanded polytetra fluoroethylene) are used as replacements. In Fig. 2, the two types of Dacron and ePTFE vascular grafts are presented.

Fig. 2 Vascular grafts made from polyethylene terephthalate (left, a) and expanded polytetrafluoroethylene (right, b).

TiO2 Nanotubes Represent a Viable Support System

9

Both materials have a through-pore microporous wall structure and are highly flexible, which enables easy implantation in the body. Such materials have successfully replaced diseased blood vessels of larger diameter, while in the case of smaller diameter vascular grafts ( Na+ > K+ [95]. The critical coverage of liposomes and time required for liposomes to reach the critical coverage also varies with ion type. The effect of ion types on the relative reduction in critical liposome coverage by monovalent ions is the same order as their effect on deposition kinetics, i.e., Li+ > Na+ > K+, where the lowest critical coverage is observed for Li+ and highest critical coverage for K+. In addition to the effect of monovalent ions type and concentration on SLB formation, addition of divalent cations has a much stronger promoting effect on vesicle adsorption and vesicle-bilayer transformation at a lower critical coverage [95–97]. It has been shown that vesicles adsorbed on substrates without the formation of an SLB in commonly used buffers with 100–150 mM NaCl but can be promoted to form an SLB by adding low concentrations of divalent cations such as Ca2+. Low concentration ranges between 1 and 5 mM of either Ca2+ or Mg2+ are commonly used in promoting the SLB formation via vesicle fusion. However, different divalent cations at the same concentration exhibit different quantitative effects on vesicle stability during the vesicle–substrate interaction, which affect vesicle

144

T.-H. Lee and M.-I. Aguilar

deformation and the rate of vesicle-bilayer transformation to different extents. The SLB-promoting effect of divalent cations also varies with their interaction with the lipid head group, the acyl chain structure, and the composition. Thus, inducing vesicle-bilayer transformation at high ionic strength and low concentration of divalent cation can be initially selected for optimization methods.

3.6 pH and Osmotic Pressure Adjusting pH also represents an effective way to modulate the process of vesicle-bilayer transformation and demonstrates the critical role of electrostatic attraction and repulsion between the liposome and substrate promoting the formation of either vesicle layers or complete SLBs [98,99]. In general, the adsorption kinetics of liposomes on the oxide substrate as a function of pH have shown that SLB formation can be promoted by lowering the solution pH, while the formation of vesicle layers without rupture can be maintained at high pH [99]. Furthermore, the phase instability of SLBs, intact vesicles, or a mixture of these two structures have been observed for vesicle–substrate interaction around pH 9 where significant ionization of the substrate lowers the adhesion energy preventing vesicle rupture and spreading [98]. While the pH affects the surface charge density of both liposome and substrate, the role of pH in modulating the kinetic process of vesicle-bilayer formation can also be complicated by the lipid composition, in particular, negatively charged lipids such as phosphatidylserine, phosphatidylglycerol, and phosphatidylinositol. To prepare SLBs with complex negatively charged lipid components, conditions such as medium-high ionic strength and low pH can be used to minimize electrostatic repulsions between liposomes and substrate by either screening or reducing the negative charge. For example, it has been demonstrated that the formation of complete phosphatidylinositol4,5-biphosphate (PI(4,5)P2)/POPC SLBs can be promoted by 2 mM Ca2+, 200 mM NaCl, or acidic pH [94]. Different distributions of PI(4,5)P2 within the POPC SLBs are greatly influenced by solution conditions. PI(4,5)P2 forms clusters in the bilayers in the presence of 2 mM Ca2+ and 200 m NaCl, whereas the PI(4,5)P2 molecules are homogeneously distributed without clustering in the SLBs at pH 4.8. Only the homogeneously distributed PI(4,5)P2 allows high coverage binding of PI(4,5)P2-specific proteins. In contrast, the membrane interaction of PI(4,5)P2-specific proteins is significantly reduced with SLBs containing clusters of PI(4,5)P2.

Preparation and Characterization of Supported Lipid Bilayers for DPI

145

Thus, optimizing the solution pH to enhance the attractive electrostatic interaction is critical for the homogeneous lateral distribution of lipid molecules on the substrate at low pH. After formation of a complete bilayer at an appropriate pH, the bulk buffer can be exchanged to match the physiological pH while still maintaining the membrane structural integrity for the molecular-binding assay. The rupture of adsorbed liposomes is also mediated by increased membrane tension. Parameters increasing the membrane tension include a small liposome diameter with high curvature, high ionic strength, and osmotic stress. Osmotic pressure is caused by a difference in solute concentration between the bulk solution and the intravesicle environment. The vesicle-bilayer transformation can be affected by the osmotic pressure from several prominent effects on vesicle shape deformation, lowering critical surface coverage, and faster rupturing kinetics [73]. As the solute concentration is higher in the bulk solution, compression of vesicles occurs with a reduction of the vesicle volume to equilibrate the solute concentration across the membrane. In contrast, expansion of vesicles with increasing in volume occurs as the solute concentration inside the vesicles is higher. Studies on the process of vesicle adsorption to the substrate have shown that significant deformation of vesicles is a prerequisite change prior to rupturing. This vesicle deformation can also be induced by the osmotic stress and depending on the direction of osmotic gradient across the membrane, the osmotic pressure plays a complex role in vesicle-bilayer transformation. Generally, SLB formation can be promoted by compressed vesicles when the osmotic stress is created by a higher NaCl concentration in the bulk solution while the formation of complete SLBs is hindered by a lower bulk ionic strength [73,100–102]. Thus, the formation of SLB can be promoted by enhancing the vesicle deformation through modulating the osmotic pressure by increasing the ionic strength of bulk solution, or addition of osmotically active substances such as glycerol and sucrose [103].

3.7 Limitations and Challenges of SLB Formation via Vesicle Fusion Although the vesicle fusion method is simple and efficient in preparing the SLBs composed of a few simple lipid components, challenges still exist in optimizing conditions for some lipid compositions that form incomplete SLBs coadsorbed with vesicles. For example, SLB via vesicle fusion is hindered by a high content of cholesterol and hexagonal phase-forming lipids such as PE [104,105]. Transbilayer asymmetry in the composition, lateral

146

T.-H. Lee and M.-I. Aguilar

distribution, and diffusion of lipid molecules are also important properties for membrane function [5]. The lipid molecules in SLBs prepared via vesicle fusion methods are generally the same in both leaflets. Several methods have therefore been used to prepare asymmetric bilayers via vesicle fusion [106,107]. These methods generally involve additional steps of lipid exchange mediated by lipid-specific-binding proteins and liposomes composed of different lipids [108–110]. However, the extent and ratio of transbilayer asymmetry for a particular lipid cannot be accurately controlled and maintained by these methods. Significant discrepancies have also been reported for conditions preparing SLBs composed of lipids derived from native cells such as bacterial inner and outer membranes and yeast [40,42,111–117]. The final SLBs structural properties prepared from the same source of native cell lipids can also vary with the conditions. Unsuccessful SLB formation for adsorbed vesicles comprised of native cell lipids is typically explained in terms of the complex lipid components containing some nonlamellar promoting lipids, which may prevent the planar structure [39,118]. Thus, a better understanding of the parameters that guide the vesicle-bilayer transformation is essential for developing protocols for reconstituting native cell membranes with native asymmetric properties on solid substrates for specific measurement techniques [79]. Consequently, the ultimate goals of understanding dynamic structural features and the physical properties of the native cell membrane on their interaction with biomolecules can be attained.

3.8 Anchored Liposomes on the Modified Chip In addition to the deposition of a complete unilamellar SLB on the DPI chip, liposomes can also be tethered onto a chemically modified chip. This free-standing configuration provides advantages for the incorporation of transmembrane receptors to explore the role of the membrane in regulating the ligand-induced receptor activation/inhibition, and the role of lipid specificity in mediating membrane insertion or rupture induced by peptides/proteins for differentiating the membrane disruption mechanisms [82]. The ability of DPI in measuring the temporal changes of multistructural parameters is advantageous over other surface sensitive techniques for determining the critical amount of bound vesicles at the point of rupture and bilayer formation, assessing the adsorption rate of the liposome when reaching the critical rupturing amount, and evaluating the time between rupture and bilayer formation. These are all crucial in understanding the

Preparation and Characterization of Supported Lipid Bilayers for DPI

147

transition mechanisms and method optimization for preparing defect-free SLBs. Choosing conditions optimized for liposomes adsorbed at a maximum surface coverage and the instantaneous rupture of all vesicles to a single bilayer is ideal for further characterizing the molecular interaction with membrane in DPI.

4. CHANGES IN LIPID MOLECULAR ORGANIZATION IN RELATION TO THE SOLUTE–MEMBRANE INTERACTION 4.1 Advantages of Multistructural Parameters The unique feature of DPI in measuring the multistructural parameters of molecular layers on the substrate can be exploited in two stages. First, this analysis can be useful in screening the key experimental parameters for successful SLB formation. Second, this highly sensitive multiparameter analysis of bilayer properties can be further extended to characterize very subtle dynamic changes in orientation and packing order of lipid molecules associated with the binding of molecules to the membrane, revealing mechanisms of interaction that are difficult if not impossible to see by other means. The mechanism of interaction with a membrane is commonly characterized by the variation in amount (low-high), rate (slow-fast), and strength (weak-strong) of molecules associating with and dissociating from the membranes. However, the extent and rate of membrane changes associated with these binding characteristics are generally not quantitatively determined with conventional biophysical methods and require independent measurement using separate techniques. Although these different measurements provide valuable information on the structural changes in membrane, these studies are not able to obtain both mass binding and membrane structure changes simultaneously and limits validity of conclusions drawn about the interaction mechanism. The simultaneous measurement of temporal changes in mass and birefringence for solute–membrane interaction with DPI therefore offers a distinctive multidimensional understanding on the impact of molecules on the membrane structure together with the role of specific lipid composition in selective binding. This can either be analyzed in terms of the dependence of mass and birefringence on time or more significantly, the correlation of birefringence with molecular mass. In particular, a number of transitions in the birefringence-mass plots have been quantitatively obtained to evaluate peptide behavior and mechanism of action on the membrane. Both the initial

148

T.-H. Lee and M.-I. Aguilar

binding of an analyte (such as a peptide), and any subsequent processes, may affect both the mass and structural ordering of the membrane, and the relationship between the two can be visualized with the birefringence-mass plots. With the study of appropriate membrane models, knowledge of the dynamic relationships between mass and structural organization significantly advance our understanding of the action of molecules on the membrane environment. The specific examples of antimicrobial peptides (AMPs) are described later.

4.2 Case Studies on AMPs The interaction, insertion/penetration, and self-assembly of AMPs within a membrane can result in different degrees of structural and topological changes in the lipid molecules and perturbation of membrane integrity leading to the loss of membrane function. The process of AMP-induced membrane destabilization is determined by complex factors and the ability of AMPs to discriminate between pathogen and host cell membranes. Delineating the mechanisms of AMPs action thus requires the dynamic changes in membrane structure to be characterized quantitatively with respect to the peptide mass associating/dissociating with the membrane. Some bilayer structural changes induced by AMP binding result in an essentially linear decrease in the bilayer birefringence with increasing peptide mass bound to membrane (Fig. 4A–C). This decrease in birefringence due to lipid disordering immediately after peptide binding is a characteristic pattern for peptides incorporated into the membrane without a critical threshold on the membrane surface. These patterns have been observed for HPA3 and HPA3P binding to DMPC and DMPC/DMPG (Fig. 4A) [119]; aurein1.2 binding to E. coli lipid extract and DMPE/DMPG [85]; citropin1.1, maculatin1.1 (Mac1.1), and caerin1.1 binding to DMPC (Fig. 4B and C) [120]; novicidin to DOPC/DOPG [121], KYE28, KYE21; and NLF binding to DOPE/DOPG [110], NaD1 binding to POPC/POPE/POPS/PI and POPC/POPE/POPS/PI(4,5)P2 [122]. However, the changes in peptide sequence and/or variations in membrane fluidity and lipid compositions can significantly alter their interaction process resulting in deviations from a linear relationship between the bilayer disorder and the peptide mass. The binding of Mac1.1 to the gel-DMPC bilayer below Tm displayed a linear increase in mass with bilayer disordering (Fig. 4C) [119,123–125]. However, Mac1.1 induced a biphasic change in the fluid DMPC above Tm exhibiting an initial mass increase without significant changes in lipid order

A

B 0.025 HPA3 DMPC

0.023

Δnf

C

0.025

0.025 Citropin1.1 DMPC

0.023

0.021

0.021

0.021

0.019

0.019

0.019

0.017

0.017

0.017

0.015

0.015

5 μM 10 μM 20 μM

0.013 4

5

6

7

8

0.011 3

9

4

Mass (ng/mm2)

5

6

7

8

Aurein1.2 DMPC

0.021

0.019

0.019

0.017

0.017

0.013 4

5

6

7

Mass (ng/mm2)

8

9

9

0.019 1.25 μM 2.5 μM 5 μM 10 μM 20 μM 40 μM

0.017 0.015 0.013

0.011 3

8

Ala8,13,18-Mag DMPC

0.023

1.25 μM 2.5 μM 5 μM 10 μM 20 μM 40 μM

0.013

0.011

7

0.021

0.015

5 μM 10 μM 20 μM

6

0.025 Mag2 DMPC

0.023

0.021

5

F

0.025

0.015

4

Mass (ng/mm2)

E 0.025 0.023

3

9

Mass (ng/mm2)

D

Δnf

0.013

0.011 3

1 μM 2 μM 5 μM 10 μM 20 μM

0.015

5 μM 10 μM 20 μM

0.013

0.011

Mac1.1 DMPC

0.023

0.011 3

4

5

6

7

Mass (ng/mm2)

8

9

3

4

5

6

7

8

9

Mass (ng/mm2)

Fig. 4 The changes of birefringence (Δnf) as a function of DMPC–bilayer bound peptide mass (mp) for various antimicrobial peptides. A linear dependence of the DMPC disordering on the mp was showed for (A) HPA3, (B) citropin1.1, (C) maculatin1.1 (Mac1.1), (D) aurein 1.2, (E) magainin 2 (Mag2), and (F) Ala8,13,18-Mag2. The mass binding and bilayer disordering can be either fully reversible or partially reversible and a possible model for these changes is shown in Fig. 5. Modified from K. Hall, T.H. Lee, A.I. Mechler, M.J. Swann, M.I. Aguilar, Real-time measurement of membrane conformational states induced by antimicrobial peptides: balance between recovery and lysis, Sci. Rep. 4 (2014) 5479; T.H. Lee, C. Heng, M.J. Swann, J.D. Gehman, F. Separovic, M.I. Aguilar, Real-time quantitative analysis of lipid disordering by aurein 1.2 during membrane adsorption, destabilisation and lysis, Biochim. Biophys. Acta 1798 (2010) 1977–1986; T.H. Lee, K.N. Hall, M.J. Swann, J.F. Popplewell, S. Unabia, Y. Park, K.S. Hahm, M.I. Aguilar, The membrane insertion of helical antimicrobial peptides from the N-terminus of Helicobacter pylori ribosomal protein L1, Biochim. Biophys. Acta 1798 (2010) 544–557; T.H. Lee, C. Heng, F. Separovic, M.I. Aguilar, Comparison of reversible membrane destabilisation induced by antimicrobial peptides derived from Australian frogs, Biochim. Biophys. Acta 1838 (2014) 2205–2215.

150

T.-H. Lee and M.-I. Aguilar

followed by a second phase with an abrupt nonlinear disordering with further increases in mass. Furthermore, the binding of Mac1.1 to DMPC/ DMPG resulted in a significant disordering at low membrane-bound peptide mass (mp) and more peptide binding resulted in the loss of total mass as a consequence of membrane disruption. The substitution, deletion, and insertion of sequence in the Mac1.1 also changed the correlation of mp and bilayer disordering to both neutral POPC and negatively charged POPC/POPG bilayers. The differences in these mp-birefringence changes have allowed the characterization of the functional role of proline residues and the sequences flanking the proline residues in mediating membrane disruption. The action of AMPs has also been characterized by the critical threshold of peptide concentration in membrane destruction for bactericidal activity [15,20]. While many studies focus on defining the critical solution concentration of peptides for membrane destruction, characterizing the sequential steps associated with different degrees of bilayer perturbation at a distinctive ratio of absolute mp to lipid (mp:L) threshold provides a much more detailed understanding of the distinctive action of different AMPs on the membrane. These characteristics of AMPs on a membrane were also analyzed by DPI with specific examples of aurein 1.2 and magainin 2 (Mag2) [84,85]. Aurein 1.2 and Mag2 are found naturally in the dorsal secretion of an Australia tree frog and an African frog, respectively, and differ in sequence and length, with 13 and 23 amino acids, respectively. Both peptides adopt an amphipathic helix in an anionic membrane environment, while no structure was observed for Mag2 in a neutral membrane. Both peptides are thought to lyse membranes via a carpet mechanism due to a similar critical peptide:lipid (P/L) solution ratio as determined by conventional means [126,127]. From these P/L solution ratios measured at the point of membrane disruption, no differentiation in the proposed “carpet mechanism” is possible for each peptide. However, by examining the relationship of mp to bilayer order for these two peptides by DPI, each peptide displays distinctive mp-birefringence profile and difference in mp:L ratio for membrane structure changes immediately prior to, during and after membrane lysis. First, the mp-birefringence profile displays a reversible reduction in birefringence for aurein 1.2 disrupting both neutral DMPC (Fig. 4D) and anionic DMPC/DMPG membranes. In contrast, “partially reversible” birefringence changes with membrane disruption correlated with the Ala8,13,18-Mag2 insertion and bilayer expansion as also evident from AFM studies [84] (Fig. 4F). Second, the critical mp:L ratio for anionic membrane disruption was markedly higher for Mag2 than aurein1.2. In addition, an

151

Preparation and Characterization of Supported Lipid Bilayers for DPI

alanine-substituted analog of Mag2, Ala8,13,18-Mag2, with enhanced bactericidal activity, showed a critical mp:L ratio for anionic membrane disruption similar to Mag2. However, disruption of the neutral DMPC membrane was examined for the Ala8,13,18-Mag2 at nearly double critical mp:L ratio for anionic membrane disruption, while no disruption of neutral DMPC was observed for Mag2 [84] (Fig. 4E and discussed later). Thus, these subtle but clearly measureable differences in membrane disordering with the membrane-bound peptide mass and the effective mp:L ratio have demonstrated the necessity of characterizing the number of sequential mechanistic steps for AMPs action (as shown in Fig. 5) and that definition of AMP action in terms of a global model can be misleading. Overall, the DPI analysis of peptide–membrane interactions clearly demonstrates that the reversible packing disorder–order behavior observed for different bilayers is quite distinctive for various AMPs. This more informative relationship between peptide mass and membrane disorder obtained by DPI analysis can be complemented with the structural data obtained with other spectroscopic techniques. The analysis of membrane disordering has therefore extended our understanding of how the membrane undergoes

A

Ala8,13,18-Mag-DMPC 0.025 mp*

mp*

A B B

mp**

Δnf

0.021 C

0.017

mp**

mp*/L = 1/32 mp**/L = 1/8 4.0

C

5.0

6.0

Mass (ng/mm2)

7.0

Bilayer expansion with mass loss

Fig. 5 The changes in the membrane order as a function of peptide mass are demonstrated by the binding of Ala8,13,18-Mag2 (Ala-substituted magainin 2) to the supported DMPC bilayer. The peptide-induced structural changes in membrane involves multiple conformational states (A, B, and C) of peptide–lipid complexes. Distinctive changes in membrane structures occur at two different peptide/lipid (mp/L) ratio. The initial disordering of lipid molecules occurs when the mp/L reached about 1/32 (State B). As more peptides continuing binding to the membrane and reached to an mp/L about 1/8, membrane disruption and expansion occurs and results in the loss of total mass (State C).

152

T.-H. Lee and M.-I. Aguilar

a reversible structural change upon exposure to AMPs and how the bilayer can either recover or, at a critical peptide concentration, begins to disintegrate (as shown in Fig. 5).

5. SUMMARY AND OUTLOOK Characterizing the changes in structural and physical properties associated with biomolecule–membrane interactions is important in delineating the molecular mechanism of various membrane-mediated biochemical processes. Although various membrane model systems have been developed for studying the membrane properties and molecule–membrane interactions, a new generation of natural membrane systems is still in high demand and which are fabricated with controllable structure and morphology of the membrane and allow the incorporation of proteins in their active/ functional states. The knowledge of various factors affecting the structure, morphology and physical properties of model membranes will aid in optimizing conditions for preparing the natural membranes in a more controllable manner. The unique features of DPI described in this chapter now allow the simultaneous characterization of membrane structural properties and molecule–membrane interactions. Various complex profiles obtained from the DPI open up new routes for defining the extent of membrane structural changes associated with different kinetic events of molecule– membrane interaction. The combination of DPI with other surface sensitive technologies together with new development of natural membrane system will advance our understanding the membrane function in mediating these important molecular interactions.

REFERENCES [1] G.E. Atilla-Gokcumen, E. Muro, J. Relat-Goberna, S. Sasse, A. Bedigian, M.L. Coughlin, S. Garcia-Manyes, U.S. Eggert, Dividing cells regulate their lipid composition and localization, Cell 156 (2014) 428–439. [2] J.C. Holthuis, A.K. Menon, Lipid landscapes and pipelines in membrane homeostasis, Nature 510 (2014) 48–57. [3] M.S. Koberlin, B. Snijder, L.X. Heinz, C.L. Baumann, A. Fauster, G.I. Vladimer, A.C. Gavin, G. Superti-Furga, A conserved circular network of coregulated lipids modulates innate immune responses, Cell 162 (2015) 170–183. [4] A. Shevchenko, K. Simons, Lipidomics: coming to grips with lipid diversity, Nat. Rev. Mol. Cell Biol. 11 (2010) 593–598. [5] G. van Meer, D.R. Voelker, G.W. Feigenson, Membrane lipids: where they are and how they behave, Nat. Rev. Mol. Cell Biol. 9 (2008) 112–124. [6] M.A. Lemmon, Membrane recognition by phospholipid-binding domains, Nat. Rev. Mol. Cell Biol. 9 (2008) 99–111.

Preparation and Characterization of Supported Lipid Bilayers for DPI

153

[7] F.C. Los, T.M. Randis, R.V. Aroian, A.J. Ratner, Role of pore-forming toxins in bacterial infectious diseases, Microbiol. Mol. Biol. Rev. 77 (2013) 173–207. [8] L.T. Nguyen, E.F. Haney, H.J. Vogel, The expanding scope of antimicrobial peptide structures and their modes of action, Trends Biotechnol. 29 (2011) 464–472. [9] R.E. Hancock, H.G. Sahl, Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies, Nat. Biotechnol. 24 (2006) 1551–1557. [10] P. Dutta, S. Das, Mammalian antimicrobial peptides: promising therapeutic targets against infection and chronic inflammation, Curr. Top. Med. Chem. 16 (2016) 99–129. [11] S. Riedl, D. Zweytick, K. Lohner, Membrane-active host defense peptides— challenges and perspectives for the development of novel anticancer drugs, Chem. Phys. Lipids 164 (2011) 766–781. [12] A.I. de Kroon, P.J. Rijken, C.H. De Smet, Checks and balances in membrane phospholipid class and acyl chain homeostasis, the yeast perspective, Prog. Lipid Res. 52 (2013) 374–394. [13] Y.M. Zhang, C.O. Rock, Membrane lipid homeostasis in bacteria, Nat. Rev. Microbiol. 6 (2008) 222–233. [14] T.G. Pomorski, T. Nylander, M. Cardenas, Model cell membranes: discerning lipid and protein contributions in shaping the cell, Adv. Colloid Interf. Sci. 205 (2014) 207–220. [15] V. Teixeira, M.J. Feio, M. Bastos, Role of lipids in the interaction of antimicrobial peptides with membranes, Prog. Lipid Res. 51 (2012) 149–177. [16] S.E. Blondelle, K. Lohner, M. Aguilar, Lipid-induced conformation and lipid-binding properties of cytolytic and antimicrobial peptides: determination and biological specificity, Biochim. Biophys. Acta 1462 (1999) 89–108. [17] S. Galdiero, A. Falanga, M. Cantisani, M. Vitiello, G. Morelli, M. Galdiero, Peptide-lipid interactions: experiments and applications, Int. J. Mol. Sci. 14 (2013) 18758–18789. [18] B. Bechinger, A dynamic view of peptides and proteins in membranes, Cell. Mol. Life Sci. 65 (2008) 3028–3039. [19] M. Deleu, J.M. Crowet, M.N. Nasir, L. Lins, Complementary biophysical tools to investigate lipid specificity in the interaction between bioactive molecules and the plasma membrane: a review, Biochim. Biophys. Acta 1838 (2014) 3171–3190. [20] T.H. Lee, K.N. Hall, M.I. Aguilar, Antimicrobial peptide structure and mechanism of action: a focus on the role of membrane structure, Curr. Top. Med. Chem. 16 (2016) 25–39. [21] S. McLaughlin, The electrostatic properties of membranes, Annu. Rev. Biophys. Biophys. Chem. 18 (1989) 113–136. [22] C. Peetla, S. Vijayaraghavalu, V. Labhasetwar, Biophysics of cell membrane lipids in cancer drug resistance: implications for drug transport and drug delivery with nanoparticles, Adv. Drug Deliv. Rev. 65 (2013) 1686–1698. [23] J. Misiewicz, S. Afonin, A.S. Ulrich, Control and role of pH in peptide-lipid interactions in oriented membrane samples, Biochim. Biophys. Acta 1848 (2015) 833–841. [24] G.L. Nicolson, Cell membrane fluid-mosaic structure and cancer metastasis, Cancer Res. 75 (2015) 1169–1176. [25] C. Ciminelli, C.M. Campanella, F. Dell’Olio, C.E. Campanella, M.N. Armenise, Label-free optical resonant sensors for biochemical applications, Prog. Quant. Electron. 37 (2013) 51–107. [26] T.H. Lee, D.J. Hirst, M.I. Aguilar, New insights into the molecular mechanisms of biomembrane structural changes and interactions by optical biosensor technology, Biochim. Biophys. Acta 1848 (2015) 1868–1885.

154

T.-H. Lee and M.-I. Aguilar

[27] T.H. Lee, H. Mozsolits, M.I. Aguilar, Measurement of the affinity of melittin for zwitterionic and anionic membranes using immobilized lipid biosensors, J. Pept. Res. 58 (2001) 464–476. [28] A. Abbas, M.J. Linman, Q. Cheng, New trends in instrumental design for surface plasmon resonance-based biosensors, Biosens. Bioelectron. 26 (2011) 1815–1824. [29] R. Konradi, M. Textor, E. Reimhult, Using complementary acoustic and optical techniques for quantitative monitoring of biomolecular adsorption at interfaces, Biosensors (Basel) 2 (2012) 341–376. [30] A. Fernandez Gavela, D. Grajales Garcia, J.C. Ramirez, L.M. Lechuga, Last advances in silicon-based optical biosensors, Sensors (Basel) 16 (2016) 285. [31] E.K. Sackmann, A.L. Fulton, D.J. Beebe, The present and future role of microfluidics in biomedical research, Nature 507 (2014) 181–189. [32] A. Ainla, I. Gozen, B. Hakonen, A. Jesorka, Lab on a biomembrane: rapid prototyping and manipulation of 2D fluidic lipid bilayers circuits, Sci. Rep. 3 (2013) 2743. [33] J.T. Groves, S.G. Boxer, Micropattern formation in supported lipid membranes, Acc. Chem. Res. 35 (2002) 149–157. [34] D. Marsh, R. Bartucci, L. Sportelli, Lipid membranes with grafted polymers: physicochemical aspects, Biochim. Biophys. Acta 1615 (2003) 33–59. [35] G.H. Cross, A.A. Reeves, S. Brand, J.F. Popplewell, L.L. Peel, M.J. Swann, N.J. Freeman, A new quantitative optical biosensor for protein characterisation, Biosens. Bioelectron. 19 (2003) 383–390. [36] V.A. Frolov, A.V. Shnyrova, J. Zimmerberg, Lipid polymorphisms and membrane shape, Cold Spring Harb. Perspect. Biol. 3 (2011) a004747. [37] G.L. Nicolson, The fluid-mosaic model of membrane structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years, Biochim. Biophys. Acta 1838 (2014) 1451–1466. [38] C.Y. Hsia, L. Chen, R.R. Singh, M.P. DeLisa, S. Daniel, A molecularly complete planar bacterial outer membrane platform, Sci. Rep. 6 (2016) 32715. [39] L.A. Clifton, S.A. Holt, A.V. Hughes, E.L. Daulton, W. Arunmanee, F. Heinrich, S. Khalid, D. Jefferies, T.R. Charlton, J.R. Webster, C.J. Kinane, J.H. Lakey, An accurate in vitro model of the E. coli envelope, Angew. Chem. Int. Ed. Engl. 54 (2015) 11952–11955. [40] T.K. Lind, H. Wacklin, J. Schiller, M. Moulin, M. Haertlein, T.G. Pomorski, M. Cardenas, Formation and characterization of supported lipid bilayers composed of hydrogenated and deuterated Escherichia coli lipids, PLoS One 10 (2015), e0144671. [41] S. Kaufmann, K. Ilg, A. Mashaghi, M. Textor, B. Priem, M. Aebi, E. Reimhult, Supported lipopolysaccharide bilayers, Langmuir 28 (2012) 12199–12208. [42] C. Merz, W. Knoll, M. Textor, E. Reimhult, Formation of supported bacterial lipid membrane mimics, Biointerphases 3 (2008) FA41. [43] S. Mashaghi, T. Jadidi, G. Koenderink, A. Mashaghi, Lipid nanotechnology, Int. J. Mol. Sci. 14 (2013) 4242–4282. [44] E. Reimhult, M. Baumann, S. Kaufmann, K. Kumar, P. Spycher, Advances in nanopatterned and nanostructured supported lipid membranes and their applications, Biotechnol. Genet. Eng. Rev. 27 (2010) 185–216. [45] V.D. Gordon, T.J. O’Halloran, O. Shindell, Membrane adhesion and the formation of heterogeneities: biology, biophysics, and biotechnology, Phys. Chem. Chem. Phys. 17 (2015) 15522–15533. [46] M.S. Khan, N.S. Dosoky, J.D. Williams, Engineering lipid bilayer membranes for protein studies, Int. J. Mol. Sci. 14 (2013) 21561–21597. [47] E. Sackmann, Supported membranes: scientific and practical applications, Science 271 (1996) 43–48.

Preparation and Characterization of Supported Lipid Bilayers for DPI

155

[48] C.T. Saeui, M.P. Mathew, L. Liu, E. Urias, K.J. Yarema, Cell surface and membrane engineering: emerging technologies and applications, J. Funct. Biomater. 6 (2015) 454–485. [49] S.F. Evans, D. Docheva, A. Bernecker, C. Colnot, R.P. Richter, M.L. Knothe Tate, Solid-supported lipid bilayers to drive stem cell fate and tissue architecture using periosteum derived progenitor cells, Biomaterials 34 (2013) 1878–1887. [50] A.E. Oliver, A.N. Parikh, Templating membrane assembly, structure, and dynamics using engineered interfaces, Biochim. Biophys. Acta 1798 (2010) 839–850. [51] I. Czolkos, A. Jesorka, O. Orwar, Molecular phospholipid films on solid supports, Soft Matter 7 (2011) 4562–4576. [52] E.T. Castellana, P.S. Cremer, Solid supported lipid bilayers: from biophysical studies to sensor design, Surf. Sci. Rep. 61 (2006) 429–444. [53] E. Reimhult, K. Kumar, Membrane biosensor platforms using nano- and microporous supports, Trends Biotechnol. 26 (2008) 82–89. [54] P. Kozma, F. Kehl, E. Ehrentreich-Forster, C. Stamm, F.F. Bier, Integrated planar optical waveguide interferometer biosensors: a comparative review, Biosens. Bioelectron. 58 (2014) 287–307. [55] G.H. Cross, N.J. Freeman, M.J. Swann, Dual polarization interferometry: a real-time optical technique for measuring (bio)molecular orientation, structure and function at the solid/liquid interface, in: D.C.C.R.S. Marks, I. Karube, C.R. Lowe, H.H. Weetall (Eds.), Handbook of Biosensors and Biochips, John Wiley & Sons, Ltd., 2008. [56] G.H. Cross, Fundamental limit to the use of effective medium theories in optics, Opt. Lett. 38 (2013) 3057–3060. [57] P.D. Coffey, M.J. Swann, T.A. Waigh, Q. Mu, J.R. Lu, The structure and mass of heterogeneous thin films measured with dual polarization interferometry and ellipsometry, RSC Adv. 3 (2013) 3316–3324. [58] A. Mashaghi, M. Swann, J. Popplewell, M. Textor, E. Reimhult, Optical anisotropy of supported lipid structures probed by waveguide spectroscopy and its application to study of supported lipid bilayer formation kinetics, Anal. Chem. 80 (2008) 3666–3676. [59] Z. Salamon, G. Tollin, Optical anisotropy in lipid bilayer membranes: coupled plasmon-waveguide resonance measurements of molecular orientation, polarizability, and shape, Biophys. J. 80 (2001) 1557–1567. [60] S.J. Johnson, T.M. Bayerl, D.C. McDermott, G.W. Adam, A.R. Rennie, R.K. Thomas, E. Sackmann, Structure of an adsorbed dimyristoylphosphatidylcholine bilayer measured with specular reflection of neutrons, Biophys. J. 59 (1991) 289–294. [61] J.A. De Feijter, J. Benjamins, F.A. Veer, Ellipsometry as a tool to study the adsorption behavior of synthetic and biopolymers at the air–water interface, Biopolymers 17 (1978) 1759–1772. [62] J. Li, Q. He, X. Yan, Biomimetic membranes, in: Molecular Assembly of Biomimetic Systems, Wiley-VCH Verlag GmbH & Co. KGaA, 2010, pp. 7–39. Chapter 1. [63] H. Brockman, Lipid monolayers: why use half a membrane to characterize protein-membrane interactions? Curr. Opin. Struct. Biol. 9 (1999) 438–443. [64] L.K. Tamm, H.M. McConnell, Supported phospholipid bilayers, Biophys. J. 47 (1985) 105–113. [65] S.Y. Jung, M.A. Holden, P.S. Cremer, C.P. Collier, Two-component membrane lithography via lipid backfilling, ChemPhysChem 6 (2005) 423–426. [66] U. Mennicke, T. Salditt, Preparation of solid-supported lipid bilayers by spin-coating, Langmuir 18 (2002) 8172–8177. [67] S. Lenhert, C.A. Mirkin, H. Fuchs, In situ lipid dip-pen nanolithography under water, Scanning 32 (2010) 15–23.

156

T.-H. Lee and M.-I. Aguilar

[68] S. Lenhert, P. Sun, Y. Wang, H. Fuchs, C.A. Mirkin, Massively parallel dip-pen nanolithography of heterogeneous supported phospholipid multilayer patterns, Small 3 (2007) 71–75. [69] M.D. Mager, N.A. Melosh, Lipid bilayer deposition and patterning via air bubble collapse, Langmuir 23 (2007) 9369–9377. [70] C.J. Brinker, Y.F. Lu, A. Sellinger, H.Y. Fan, Evaporation-induced self-assembly: nanostructures made easy, Adv. Mater. 11 (1999) 579–585. [71] F. Tiberg, I. Harwigsson, M. Malmsten, Formation of model lipid bilayers at the silica-water interface by co-adsorption with non-ionic dodecyl maltoside surfactant, Eur. Biophys. J. 29 (2000) 196–203. [72] H.P. Vacklin, F. Tiberg, R.K. Thomas, Formation of supported phospholipid bilayers via co-adsorption with beta-D-dodecyl maltoside, Biochim. Biophys. Acta 1668 (2005) 17–24. [73] E. Reimhult, F. H€ oo €k, B. Kasemo, Intact vesicle adsorption and supported biomembrane formation from vesicles in solution: influence of surface chemistry, vesicle size, temperature, and osmotic pressure, Langmuir 19 (2003) 1681–1691. [74] R.P. Richter, R. Berat, A.R. Brisson, Formation of solid-supported lipid bilayers: an integrated view, Langmuir 22 (2006) 3497–3505. [75] A.O. Hohner, M.P. David, J.O. Radler, Controlled solvent-exchange deposition of phospholipid membranes onto solid surfaces, Biointerphases 5 (2010) 1–8. [76] S.R. Tabaei, J.H. Choi, G. Haw Zan, V.P. Zhdanov, N.J. Cho, Solvent-assisted lipid bilayer formation on silicon dioxide and gold, Langmuir 30 (2014) 10363–10373. [77] H. Bayley, B. Cronin, A. Heron, M.A. Holden, W.L. Hwang, R. Syeda, J. Thompson, M. Wallace, Droplet interface bilayers, Mol. Biosyst. 4 (2008) 1191–1208. [78] K. Funakoshi, H. Suzuki, S. Takeuchi, Lipid bilayer formation by contacting monolayers in a microfluidic device for membrane protein analysis, Anal. Chem. 78 (2006) 8169–8174. [79] I. Gozen, A. Jesorka, Instrumental methods to characterize molecular phospholipid films on solid supports, Anal. Chem. 84 (2012) 822–838. [80] T. McArdle, T.P. McNamara, F. Fei, K. Singh, C.F. Blanford, Optimizing the mass-specific activity of bilirubin oxidase adlayers through combined electrochemical quartz crystal microbalance and dual polarization interferometry analyses, ACS Appl. Mater. Interfaces 7 (2015) 25270–25280. [81] B.J. Cowsill, X. Zhao, T.A. Waigh, S. Eapen, R. Davies, V. Laux, M. Haertlein, V.T. Forsyth, J.R. Lu, Interfacial structure of immobilized antibodies and perdeuterated HSA in model pregnancy tests measured with neutron reflectivity, Langmuir 30 (2014) 5880–5887. [82] M.M. Ouberai, J. Wang, M.J. Swann, C. Galvagnion, T. Guilliams, C.M. Dobson, M.E. Welland, alpha-Synuclein senses lipid packing defects and induces lateral expansion of lipids leading to membrane remodeling, J. Biol. Chem. 288 (2013) 20883–20895. [83] M.K. Baumann, M.J. Swann, M. Textor, E. Reimhult, Pleckstrin homologyphospholipase C-delta1 interaction with phosphatidylinositol 4,5-bisphosphate containing supported lipid bilayers monitored in situ with dual polarization interferometry, Anal. Chem. 83 (2011) 6267–6274. [84] K. Hall, T.H. Lee, A.I. Mechler, M.J. Swann, M.I. Aguilar, Real-time measurement of membrane conformational states induced by antimicrobial peptides: balance between recovery and lysis, Sci. Rep. 4 (2014) 5479. [85] T.H. Lee, C. Heng, M.J. Swann, J.D. Gehman, F. Separovic, M.I. Aguilar, Real-time quantitative analysis of lipid disordering by aurein 1.2 during membrane adsorption, destabilisation and lysis, Biochim. Biophys. Acta 1798 (2010) 1977–1986.

Preparation and Characterization of Supported Lipid Bilayers for DPI

157

[86] T.H. Anderson, Y. Min, K.L. Weirich, H. Zeng, D. Fygenson, J.N. Israelachvili, Formation of supported bilayers on silica substrates, Langmuir 25 (2009) 6997–7005. [87] N.J. Cho, S.J. Cho, K.H. Cheong, J.S. Glenn, C.W. Frank, Employing an amphipathic viral peptide to create a lipid bilayer on Au and TiO2, J. Am. Chem. Soc. 129 (2007) 10050–10051. [88] N.J. Cho, G. Wang, M. Edvardsson, J.S. Glenn, F. Hook, C.W. Frank, Alpha-helical peptide-induced vesicle rupture revealing new insight into the vesicle fusion process as monitored in situ by quartz crystal microbalance-dissipation and reflectometry, Anal. Chem. 81 (2009) 4752–4761. [89] N.-J. Cho, L.Y. Hwang, J.J.R. Solandt, C.W. Frank, Comparison of extruded and sonicated vesicles for planar bilayer self-assembly, Materials 6 (2013) 3294. [90] E. Reimhult, F. Hook, B. Kasemo, Temperature dependence of formation of a supported phospholipid bilayer from vesicles on SiO2, Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 66 (2002) 051905. [91] L. Redondo-Morata, M.I. Giannotti, F. Sanz, Influence of cholesterol on the phase transition of lipid bilayers: a temperature-controlled force spectroscopy study, Langmuir 28 (2012) 12851–12860. [92] S. Boudard, B. Seantier, C. Breffa, G. Decher, O. Felix, Controlling the pathway of formation of supported lipid bilayers of DMPC by varying the sodium chloride concentration, Thin Solid Films 495 (2006) 246–251. [93] E.M. Pereira, D.F. Petri, A.M. Carmona-Ribeiro, Adsorption of cationic lipid bilayer onto flat silicon wafers: effect of ion nature and concentration, J. Phys. Chem. B 110 (2006) 10070–10074. [94] J.A. Braunger, C. Kramer, D. Morick, C. Steinem, Solid supported membranes doped with PIP2: influence of ionic strength and pH on bilayer formation and membrane organization, Langmuir 29 (2013) 14204–14213. [95] B. Seantier, B. Kasemo, Influence of mono- and divalent ions on the formation of supported phospholipid bilayers via vesicle adsorption, Langmuir 25 (2009) 5767–5772. [96] M. Dacic, J.A. Jackman, S. Yorulmaz, V.P. Zhdanov, B. Kasemo, N.J. Cho, Influence of divalent cations on deformation and rupture of adsorbed lipid vesicles, Langmuir 32 (2016) 6486–6495. [97] R. Richter, A. Mukhopadhyay, A. Brisson, Pathways of lipid vesicle deposition on solid surfaces: a combined QCM-D and AFM study, Biophys. J. 85 (2003) 3035–3047. [98] P.S. Cremer, S.G. Boxer, Formation and spreading of lipid bilayers on planar glass supports, J. Phys. Chem. B 103 (1999) 2554–2559. [99] N.J. Cho, J.A. Jackman, M. Liu, C.W. Frank, pH-driven assembly of various supported lipid platforms: a comparative study on silicon oxide and titanium oxide, Langmuir 27 (2011) 3739–3748. [100] J.A. Jackman, J.H. Choi, V.P. Zhdanov, N.J. Cho, Influence of osmotic pressure on adhesion of lipid vesicles to solid supports, Langmuir 29 (2013) 11375–11384. [101] N. Hain, M. Gallego, I. Reviakine, Unraveling supported lipid bilayer formation kinetics: osmotic effects, Langmuir 29 (2013) 2282–2288. [102] S. Stanglmaier, S. Hertrich, K. Fritz, J.F. Moulin, M. Haese-Seiller, J.O. Radler, B. Nickel, Asymmetric distribution of anionic phospholipids in supported lipid bilayers, Langmuir 28 (2012) 10818–10821. [103] T. Zhu, Z. Jiang, M.R. Nurlybaeva el, J. Sheng, Y. Ma, Effect of osmotic stress on membrane fusion on solid substrate, Langmuir 29 (2013) 6377–6385. [104] C. Hamai, T. Yang, S. Kataoka, P.S. Cremer, S.M. Musser, Effect of average phospholipid curvature on supported bilayer formation on glass by vesicle fusion, Biophys. J. 90 (2006) 1241–1248.

158

T.-H. Lee and M.-I. Aguilar

[105] G.J. Hardy, R. Nayak, S.M. Alam, J.G. Shapter, F. Heinrich, S. Zauscher, Biomimetic supported lipid bilayers with high cholesterol content formed by alpha-helical peptide-induced vesicle fusion, J. Mater. Chem. 22 (2012) 19506–19513. [106] K. Kamiya, R. Kawano, T. Osaki, K. Akiyoshi, S. Takeuchi, Cell-sized asymmetric lipid vesicles facilitate the investigation of asymmetric membranes, Nat. Chem. 8 (2016) 881–889. [107] D. Marquardt, B. Geier, G. Pabst, Asymmetric lipid membranes: towards more realistic model systems, Membranes (Basel) 5 (2015) 180–196. [108] X. Shi, M. Kohram, X. Zhuang, A.W. Smith, Interactions and translational dynamics of phosphatidylinositol bisphosphate (PIP2) lipids in asymmetric lipid bilayers, Langmuir 32 (2016) 1732–1741. [109] I. Visco, S. Chiantia, P. Schwille, Asymmetric supported lipid bilayer formation via methyl-beta-cyclodextrin mediated lipid exchange: influence of asymmetry on lipid dynamics and phase behavior, Langmuir 30 (2014) 7475–7484. [110] S. Singh, P. Papareddy, M. Kalle, A. Schmidtchen, M. Malmsten, Importance of lipopolysaccharide aggregate disruption for the anti-endotoxic effects of heparin cofactor II peptides, Biochim. Biophys. Acta 1828 (2013) 2709–2719. [111] P. Nollert, H. Kiefer, F. Jahnig, Lipid vesicle adsorption versus formation of planar bilayers on solid surfaces, Biophys. J. 69 (1995) 1447–1455. [112] C.E. Dodd, B.R. Johnson, L.J. Jeuken, T.D. Bugg, R.J. Bushby, S.D. Evans, Native E. coli inner membrane incorporation in solid-supported lipid bilayer membranes, Biointerphases 3 (2008) FA59. [113] N. Ruiz, S. Merino, M. Vinas, O. Domenech, M.T. Montero, J. Hernandez-Borrell, Preliminary studies of the 2D crystallization of Omp1 of Serratia marcescens: observation by atomic force microscopy in native membranes environment and reconstituted in proteolipid sheets, Biophys. Chem. 111 (2004) 1–7. ` . Dome`nech, I. Dı´ez, F. Sanz, M. Vin˜as, M.T. Montero, [114] S. Merino, O J. Herna´ndez-Borrell, Effects of ciprofloxacin on Escherichia coli lipid bilayers: an atomic force microscopy study, Langmuir 19 (2003) 6922–6927. [115] S. Garcia-Manyes, G. Oncins, F. Sanz, Effect of ion-binding and chemical phospholipid structure on the nanomechanics of lipid bilayers studied by force spectroscopy, Biophys. J. 89 (2005) 1812–1826. [116] O. Domenech, S. Merino-Montero, M.T. Montero, J. Hernandez-Borrell, Surface planar bilayers of phospholipids used in protein membrane reconstitution: an atomic force microscopy study, Colloids Surf. B: Biointerfaces 47 (2006) 102–106. [117] A. de Ghellinck, G. Fragneto, V. Laux, M. Haertlein, J. Jouhet, M. Sferrazza, H. Wacklin, Lipid polyunsaturation determines the extent of membrane structural changes induced by Amphotericin B in Pichia pastoris yeast, Biochim. Biophys. Acta 1848 (2015) 2317–2325. [118] C. Sohlenkamp, O. Geiger, Bacterial membrane lipids: diversity in structures and pathways, FEMS Microbiol. Rev. 40 (2016) 133–159. [119] T.H. Lee, K.N. Hall, M.J. Swann, J.F. Popplewell, S. Unabia, Y. Park, K.S. Hahm, M.I. Aguilar, The membrane insertion of helical antimicrobial peptides from the N-terminus of Helicobacter pylori ribosomal protein L1, Biochim. Biophys. Acta 1798 (2010) 544–557. [120] T.H. Lee, C. Heng, F. Separovic, M.I. Aguilar, Comparison of reversible membrane destabilisation induced by antimicrobial peptides derived from Australian frogs, Biochim. Biophys. Acta 1838 (2014) 2205–2215. [121] S.B. Nielsen, D.E. Otzen, Impact of the antimicrobial peptide Novicidin on membrane structure and integrity, J. Colloid Interface Sci. 345 (2010) 248–256. [122] J.A. Payne, M.R. Bleackley, T.H. Lee, T.M. Shafee, I.K. Poon, M.D. Hulett, M.I. Aguilar, N.L. van der Weerden, M.A. Anderson, The plant defensin NaD1

Preparation and Characterization of Supported Lipid Bilayers for DPI

[123] [124] [125] [126] [127]

159

introduces membrane disorder through a specific interaction with the lipid, phosphatidylinositol 4,5 bisphosphate, Biochim. Biophys. Acta 1858 (2016) 1099–1109. D.I. Fernandez, A.P. Le Brun, T.H. Lee, P. Bansal, M.I. Aguilar, M. James, F. Separovic, Structural effects of the antimicrobial peptide maculatin 1.1 on supported lipid bilayers, Eur. Biophys. J. 42 (2013) 47–59. D.I. Fernandez, T.H. Lee, M.A. Sani, M.I. Aguilar, F. Separovic, Proline facilitates membrane insertion of the antimicrobial peptide maculatin 1.1 via surface indentation and subsequent lipid disordering, Biophys. J. 104 (2013) 1495–1507. D.J. Hirst, T.H. Lee, M.J. Swann, S. Unabia, Y. Park, K.S. Hahm, M.I. Aguilar, Effect of acyl chain structure and bilayer phase state on binding and penetration of a supported lipid bilayer by HPA3, Eur. Biophys. J. 40 (2011) 503–514. H.W. Huang, Molecular mechanism of antimicrobial peptides: the origin of cooperativity, Biochim. Biophys. Acta 1758 (2006) 1292–1302. N.C. Santos, M. Prieto, M.A. Castanho, Quantifying molecular partition into model systems of biomembranes: an emphasis on optical spectroscopic methods, Biochim. Biophys. Acta 1612 (2003) 123–135.

CHAPTER SIX

Gold Nanomaterials: Recent Advances in Cancer Theranostics S. Sudhakar*, P.B. Santhosh†,1 *Centre for Biotechnology, Anna University, Chennai, India † Indian Institute of Technology, Chennai, India 1 Corresponding author: e-mail address: [email protected]

Contents 1. Introduction to Different Forms of Gold Nanomaterials 1.1 Gold Nanoparticles 1.2 Gold Nanorods 1.3 Gold Nanocages 1.4 Gold Nanoshells 1.5 Gold Nanostars 2. Synthesis of Different Forms of Gold Nanomaterials 2.1 Chemical-Mediated Synthesis of Gold Nanomaterials 2.2 Green Synthesis of Gold Nanomaterials 2.3 Microbial Synthesis of Gold Nanomaterials 3. Diagnostic and Imaging Applications of Gold Nanomaterials 4. Therapeutic and Drug Delivery Applications of Gold Nanomaterials 5. Conclusion and Perspectives References

162 162 163 163 164 164 164 164 167 168 170 171 173 173

Abstract This chapter describes the potential of various shapes of gold nanomaterials such as nanoparticles, nanorods, nanostars, nanocages, and nanoshells in cancer nanotheranostics, i.e., both as diagnostic and therapeutic agent. This study includes the synthesis of different gold nanomaterials using several methods like chemical-, green-, and microbial-mediated synthesis. The ability of gold nanomaterials to absorb light in the near-infrared region and transform it into heat and their unique optical properties make them a promising tool in photothermal cancer therapy. Herein, we present the recent advances and the ability of gold nanomaterials to show its multiple roles in the field of cancer biology.

Advances in Biomembranes and Lipid Self-Assembly, Volume 25 ISSN 2451-9634 http://dx.doi.org/10.1016/bs.abl.2017.01.003

#

2017 Elsevier Inc. All rights reserved.

161

162

S. Sudhakar and P.B. Santhosh

1. INTRODUCTION TO DIFFERENT FORMS OF GOLD NANOMATERIALS Gold nanomaterials have gained huge interest in various biomedical applications and considered to have a promising potential in the field of cancer biology. Based on the synthesis procedure and experimental conditions, various shapes of gold nanomaterials including spherical gold nanoparticles, nanorods, nanoshells, nanocages, nanostars, nanoboxes, nanocubes, nanocrystals, and triangular bipyramids have been investigated [1–7]. In this chapter about gold nanomaterials, first we are going to have a look on synthesis of different shapes of gold nanomaterials and applications as diagnostic and therapeutic agents in cancer.

1.1 Gold Nanoparticles When compared to many other metallic nanoparticles, noble metals like gold nanoparticles (AuNPs) have distinct electronic and optical properties. When the AuNPs are excited by light at specific wavelengths, the incident photons interact strongly with the conduction band of electrons and cause them to oscillate with resonant frequency. This collective oscillation is known as localized surface plasmon resonance (LSPR) which creates strong and localized electromagnetic fields and allows sensitive detection of changes in dielectric environment surrounding the nanoparticle surface. This property makes them to be prominently utilized in imaging, drug delivery, cosmetics, and in cancer theranostic applications [8,9]. The AuNPs display various colors based on their shape, size, and amount of aggregation of particles [10]. The AuNPs are evolving as an innovative platform for both, cancer targeted imaging and drug delivery usually represented as theranostic application. When irradiated with near-infrared (NIR) light, they induce hyperthermia (increased temperature to kill cancer cells) [11,12]. Furthermore, AuNPs could be successfully and selectively delivered to malignant and benign tumors and could act as carriers for chemotherapeutic drugs like curcumin, and paclitaxel in cancer treatment [13]. Apart from therapeutic applications, AuNPs are employed as imaging agents and biosensors due to their capability to emit photons upon irradiation. The gold nanomaterials of different shapes are schematically represented in Fig. 1.

Recent Advances in Cancer Theranostics

163

Fig. 1 Schematic presentation of differently shaped gold nanoparticles: (A) nanosphere, (B) nanorod, (C) nanocube, (D) nanoshell, and (E) nanostar.

1.2 Gold Nanorods When compared to spherical gold particles, the AuNRs have drawn worldwide attention because of their inimitable shape-dependent optical properties. What makes the AuNRs as exclusive materials for biological imaging, sensing, photo thermal therapy, and drug delivery is their ability to possess different plasmon bands [14–17]. Even though, they have attracting features, their usage is restricted because even a small change in the shape, size, and surface nature will alter their properties which in turn affect their biological applications. The major advantages of using AuNRs include their surface plasmon resonance extinction in the NIR region which makes their use appropriately in the medical field for photo thermal therapy, biological sensing, and imaging.

1.3 Gold Nanocages Next, we move on to a novel nanostructure called gold nanocages (AuNCgs) which are usually characterized by the ultrathin porous walls and hollow interiors. Usually they are prepared by keeping the silver nanoparticles as templates which involves galvanic replacement reaction [18–20]. The penetration depth of light can be maximized in soft tissues, by limiting the light source to NIR region from 650 to 900 nm, where the absorption by hemoglobin and water is negligible. To make AuNCgs suitable for this application, the LSPR peaks can be concisely tuned throughout the visible and NIR regions [21–24]. Prevalently, AuNCgs

164

S. Sudhakar and P.B. Santhosh

are also functionalized with biological molecules to target cancer cells for both photothermal therapy and diagnosis at an early stage [25,26].

1.4 Gold Nanoshells Gold nanoshells (AuNShs) are composed of a silica core coated by a thin gold metallic shell. One of the interesting properties about the AuNShs is their unique surface plasmon resonance property which can be finely tuned ranging from visible to NIR region. Multiple templates are employed for the formation of hollow AuNShs which includes silica particles [27], metal particles [28–31], etc. The AuNShs have demonstrated their potential in a variety of biomedical applications ranging from substrates for whole-blood immunoassays to photothermal cancer therapy [32–34]. By using magnetic resonance thermal guidance, in vitro cancer cells were successfully ablated using AuNShs. Similar use of AuNShs for photothermal ablation of tumors in mice showed complete regression of tumors with the mice remaining healthy compared with the controls [35–38].

1.5 Gold Nanostars The gold nanostars (AuNSts) have multiple sharp branch structure which sharply increases the electromagnetic field. The AuNSts also have unique plasmon bands which are tunable from visible to NIR region. The fabrication of AuNSts has been driven by the interest on the LSPR response to the environment, especially on sharp tips and edges, where light can be highly concentrated [39–43]. Because of their exclusive property, they serve as effective tools in the field of nanomedicine. Furthermore, AuNSts also display stronger surface-enhanced resonance spectrum activity than gold spheres or even rods.

2. SYNTHESIS OF DIFFERENT FORMS OF GOLD NANOMATERIALS 2.1 Chemical-Mediated Synthesis of Gold Nanomaterials 2.1.1 Synthesis of Gold Nanoparticles The simplest protocol commonly used for the groundwork of AuNPs is the facile reduction of gold salt in aqueous medium using sodium citrate [44,45], in which Au3+ ions are reduced to neutral gold atoms which slowly precipitates to form nanometer-sized gold particles. The widely used reducing agents for the synthesis of AuNPs include aminoboranes, borohydrides, hydrazine, hydroxylamine, formaldehyde, polyols, sugars, saturated and

Recent Advances in Cancer Theranostics

165

unsaturated alcohols, hydrogen peroxide, citric and oxalic acids, carbon monoxide, sulfites, acetylene, and hydrogen [46–48]. A variety of stabilizers such as phosphorus ligands, trisodium citrate dihydrate, nitrogen-based ligands, sulfur ligands, dendrimers, oxygen-based ligands, polymers, and surfactants are used to impart the colloidal stability to AuNPs [49,50]. Synthesis of AuNPs by citrate-stabilized method, introduced by Turkevich, is the most popular method in which trisodium citrate dihydrate is added to the boiling chloroauric acid under vigorous stirring, leading to the formation of wine-red colloidal suspension after a few minutes [51,52]. To improve this method, Frens altered the ratio of gold and trisodium citrate, resulting in the synthesis of AuNPs of wide size range (from 15 to 150 nm) [46]. The size of the AuNPs obtained using Brust–Schiffrin method ranges from 2 to 5 nm, which is much smaller in size than particles synthesized by Turkevich method. Another popular technique for synthesis of AuNPs is seed growth method where one can easily control the size and shape of the particle. Usually, it involves two steps, preparation of small sized AuNPs followed by addition of seeds to the growth solution. 2.1.2 Synthesis of Gold Nanorods In general, AuNRs are produced using cetyltrimethyl ammonium bromide (CTAB) which acts as both reducing and stabilizing agent to produce homogeneous AuNRs with high yield [53–56,4,57–61]. The LSPR resonances of AuNRs are generally observed both in the visible and NIR region [62–70]. Since CTAB is cytotoxic, various biocompatible agents like proteins and lipids are being used to provide stability, reduce cytotoxicity, and to retain its properties. A number of studies have focused on surface modification of AuNRs to address the above mentioned issues. An intrinsic problem in the synthesis of AuNRs using conventional method is its meager efficiency to convert chloroauric acid into nanorods. Reports have shown that only 15% of gold seeds are usually converted into the rods. The AuNRs yield could be increased by preparing the AuNRs in consecutive supernatant solutions. There is an urgent need for novel synthetic protocols in order to make the synthesis process more scalable and efficient as AuNRs progress greatly toward commercial applications. 2.1.3 Synthesis of Gold Nanocages Recently, AuNCgs with hollow interiors, porous walls, and tunable LSPR in the NIR region have become a new promising platform for therapeutic applications. The unique structures of AuNCgs make them well suited for

166

S. Sudhakar and P.B. Santhosh

drug encapsulation and photothermal controlled drug release with high spatial and temporal resolution. The AuNCgs are generally synthesized through a simple galvanic replacement reaction between solutions containing salts of metal precursors and Ag nanostructures prepared through polyol reduction. The reduced metal deposits on the surface of the AuNCgs, adopting their underlying cubic form. Concurrent with this deposition, the interior Ag is oxidized and removed, together with alloying and dealloying, AuNCgs are produced. [71]. 2.1.4 Synthesis of Gold Nanoshells The commonly used method for the synthesis of gold nanoshells (AuNShs) involves the reduction of chloroauric acid with ascorbic acid at ambient temperature on presynthesized gold nanoseeds and in the presence of surfactants (in most cases CTAB). A general one-pot synthetic strategy for the synthesis of hollow AuNShs includes the reduction of chloroauric acid in 3-aminopropyltriethoxysilane in water suspension [72]. The AuNShs show a high photothermal conversion efficiency (up to 45%) and excellent stability under laser irradiation. 2.1.5 Synthesis of Gold Nanostars The AuNSts are synthesized by anisotropic growth process, by altering the growth rates along the specific crystallographic directions [73]. The shape of AuNSts could be controlled by varying the concentration of silver nitrate. The stirring speed, pH, and the ratios of ascorbic acid, silver nitrate, and chloroauric acid determine the size and shape of the AuNSts. Murphy and coworkers have studied the influence of reducing agent by replacing bromide ions of CTAB with its chloride equivalent to achieve a better control over size [74]. Few groups have used hydroxylamine sulfate in the preparation of polycrystalline-branched AuNSts in a stepwise growth approach with sizes ranging from 48 up to 186 nm [75]. It is also reported that addition of polyvinyl pyrrolidone with 15 nm chloroauric acid solution leads to the formation of highly branched AuNSts [76]. Recently, a simple one-step synthesis of AuNSts using hydroxylamine as a reducing agent was reported [77]. The controlled synthesis of high-yield AuNSts ranging from 45 to 116 nm was reported by Khoury and Vo-Dinh [78]. The AuNSts were synthesized by extending the protocol reported by Liz-Marzan et al. [79], in order to enable size control of the stars from approximately 45 to 116 nm in size. This size range translates to tuning capabilities of the longitudinal plasmon peak in the NIR region from around 725 to 850 nm. They have used 20 nm

Recent Advances in Cancer Theranostics

167

polyvinylpyrrolidone-coated gold seeds in ethanol and investigated the growth of AuNSts as a function of time during the synthesis by monitoring the spectrum of the AuNSts suspension and by imaging morphological changes of stars from time to time via transmission electron microscopy.

2.2 Green Synthesis of Gold Nanomaterials Even though there are several methods like thermal decomposition, sonochemical, microwave irradiation, chemical reduction, electrochemical ablation for the synthesis of gold nanomaterials, many of these routine methods use hazardous chemicals. Hence, synthesis of nanoparticles in an ecofriendly way is essential. The green synthesis method is more advantageous when compared to other conventional methods which requires extended and high cost for downstream processing. The main components in plants responsible for the reduction of gold ions are usually phenols, proteins, and flavonoids which also acts as a stabilizing agent by capping the nanoparticles. Researchers have explored industrially and botanically important plants for the synthesis of nanoparticles. The active ingredients present in the plant extracts will provide special surface characteristics to the nanoparticles. Citrus maxima fruit extracts are widely used for the inexpensive synthesis of AuNPs [80]. Ghodake et al. [81] demonstrated casein hydrolytic peptides (CHPs)-mediated synthesis of crystalline AuNPs. The mechanism behind the nanoparticle formation is attributed to the catalytic properties of hydroxyl groups present in the CHPs. The CHPs are capable of forming a monolayer on the surface of AuNPs via electrostatic interactions, thus playing an important role in long-term stability. Yana et al. [82] reported a facile, one-pot green synthesis of biomaterial-supported AuNPs using cellulose with superior catalytic activity. In general, cellulosemediated AuNPs with a size range of 5–10 nm are prepared by heating the aqueous mixture of chloroauric acid, with cellulose and poly ethylene glycol. Nazirova et al. [83] reported water-soluble luminescent AuNPs with average size 2.3 nm synthesized from N-(4-imidazolyl) methylchitosan. The biological activity of imidazolyl-containing polymers and their capability to bind proteins and drugs have huge applications in the field of bioimaging, biomolecules detection, catalysis, and drug delivery. Suarasana et al. [84] reported the one-pot, green synthesis of AuNPs using gelatin biopolymer having unique reducing, stabilizing, and eminent growth controlling ability. Sadeghi et al. [85] reported that the plant Stevia rebaudiana have higher amount of polyphenols and flavonoids which makes them more

168

S. Sudhakar and P.B. Santhosh

Table 1 Green Synthesis of Gold Nanoparticles Using Different Plant Sources Size of the Plants Particle (nm) Shapes References

Acanthella elongata

15

Spherical

[87]

Sugar beet pulp

20

Triangular

[88]

Cinnamomun zyelanicum

20

Spherical

[89]

Zingiber officinale

5–15

Spherical

[90]

Olive leaf extract

50–100

Spherical, triangular

[91]

Coriander leaf extract

6–58

Spherical, triangular

[92]

Cassia auriculata

38

Spherical, triangular

[93]

Hibiscus rosasinensis

15–25

Spherical, triangular, hexagonal

[94]

Terminalia chebula

50–100

Spherical

[95]

Rosa hybrida

35

Spherical

[96]

Morinda citrifolia

10–40

Triangular

[97]

Tamarind leaf extract

20

Spherical

[98]

Palm oil mill effluent

50

Spherical

[99]

specific to act as reducing agent in the synthesis of AuNPs. Yuan et al. [86] reported a facile and rapid a single-pot synthesis process for AuNPs using capsicum. The synthesis of AuNps of various shapes from different plant sources is shown in Table 1.

2.3 Microbial Synthesis of Gold Nanomaterials Synthesis of nanomaterials using microorganisms is an emerging field of industrial microbiology. Biological approaches using either unicellular or multicellular organisms for the synthesis of gold nanomaterials are simple, viable, and ecofriendly alternate to chemical methods. Different biological entities like bacteria, fungi, algae, yeast, and plants are drastically studied for their ability to synthesize metal nanoparticles for various pharmacological applications (Table 2) [109]. There are two ways by which AuNPs can be synthesized by microbes, either extracellularly or intracellularly. The most popular method is extracellular synthesis, as it eliminates numerous downstream processing steps

169

Recent Advances in Cancer Theranostics

Table 2 Microbial Synthesis of Gold Nanoparticles of Different Sizes Microorganism Size of the Particle (nm)

References

Bacillus subtilis

5–25

[100]

Sulfate-reducing bacteria

15–200

[101]

Shewanella algae

10

[102]

Escherichia coli DH5α

10–20

[103]

Pseudomonas stutzeri

200

[104]

Corynebacterium

10

[105]

Rhodobacter

10–20

[106]

Bacillus sp.

10

[107]

Pseudomonas aeruginosa

17.2

[108]

during the synthesis. The usual procedure followed is to centrifuge the second day well-grown culture to discard the biomass and add the supernatant to chloroauric acid. The enzymes like NADH dehydrogenase, NADPHdependent sulfite reductase in the microbes act as reducing agents [110]. After bioreduction, the AuNPs can be collected by similar methodologies as in plant extract-mediated synthesis. Cell-free viable approach for synthesis of AuNPs using Escherichia coli has also been reported [111]. Despite the stability, biological nanoparticles are usually not monodisperse, and the rate of synthesis is slow. To overcome these problems, several factors such as microbial cultivation methods and the extraction techniques have to be optimized, and the combinatorial approach such as photobiological methods may be used. In the case of intracellular-mediated synthesis process, the particles are released to the external environment either by ultrasound treatment or by adding apt detergents. Geobacter ferrireducens, a Fe (III) reducing bacterium, reduces and precipitates the gold in periplasmic space intracellularly. Similarly, in the presence hydrogen gas microbes like Shewanella algae, mesophilic bacteria reduce Au+3 ions in anaerobic conditions. Plectonema boryanum, a filamentous cyanobacterium, precipitates AuNPs in abiotic and cyanobacterial systems. Escherichia coli DH5α-mediated bioreduction of chloroauric acid to Au0 nanoparticles has been reported recently [112]. The accumulated particles on the cell surface were mostly spherical. These cell-bound nanoparticles have been reported for promising applications in realizing the direct electrochemistry of hemoglobin and other proteins [113]. Similarly, the bioreduction of trivalent aurum was also reported in

170

S. Sudhakar and P.B. Santhosh

photosynthetic bacterium, Rhodobacter capsulatus which showed biosorption capacity of 92.43 mg chloroauric acid/g dry weight in the logarithmic phase of its growth. The carotenoids and NADPH-dependent enzymes embedded in plasma membrane and/or secreted extracellularly were found to be involved in the biosorption and bioreduction of Au+3 to Au0 on the plasma membrane and also extracellularly [100]. Owing to the rich biodiversity of microbes, their potential as biological materials for nanoparticle synthesis is yet to be fully explored.

3. DIAGNOSTIC AND IMAGING APPLICATIONS OF GOLD NANOMATERIALS As discussed earlier, gold nanomaterials have unique properties which attract researchers to focus their studies in the field of tumor molecular imaging and diagnostics. Herein, Zhou and Jia [114] reported a facile approach in which polyethylenimine (PEI) modified with polyethylene glycol (PEG), a cost effective template, is used for the synthesis of folic acid (FA)-targeted multifunctional AuNPs. The PEI was consecutively modified with FA-linked PEG, PEG monomethyl ether and with fluorescein isothiocyanate for the synthesis of AuNPs. The prepared AuNPs were noncytotoxic and colloidally stable. They acted as novel nanoprobe for targeted CT imaging of FAR-expressing cancer cells. Lozano et al. [115] demonstrated the hybrid vesicular systems composed of liposomes and AuNRs aid in deep tissue detection, therapy, and monitoring in living animals using multispectral optoacoustic tomography [116]. Gallina et al. [117] reported that fluorescent, biocompatible, aptamerconjugated AuNRs act as perfect agents for diagnostics and therapeutics. Bioconjugation of AuNRs with anticancer oligonucleotide AS1411 was employed and the aptamer-conjugated AuNRs acted as ideal cancerselective multifunctional probes for imaging. Huang et al. [12] reported the synthesis of multifunctional nanoprobes in which silica functionalized gold was decorated with FA molecule which displayed strong computed tomography imaging and X-ray attenuation. Vo-Dinh and coworkers reported the synthesis of AuNSts for in vivo imaging with adjustable geometry. They exhibited strong two-photon photoluminescence process which is confirmed by the quadratic dependence of the luminescence signal up to excitation power which may originate from electron–holerecombination. They also reported TPL imaging on BT549 cancer cells by wheat germ agglutinin-functionalized AuNSts for imaging.

Recent Advances in Cancer Theranostics

171

The reconstituted images appeared white due to the emission of red, blue, and green channels by AuNSts [118]. Tracking of AuNPs needs some fluorescent label but the imaging and tracking of AuNSts are possible without the need of fluorophores due to their unique strong two-photon action cross sections (TPACS) [119]. Due to the high TPACS of nanostars, tracking the motion of PEGylated AuNSts in blood vessels is also possible. In medicine, novel techniques with high specificity, such as positron emission tomography, require probe labeling and offer low spatial resolution which can be obtained by AuNSts. Photoacoustic microscopy is an emerging imaging modality that combines both rich optical absorption and high ultrasonic resolution in a single-imaging modality [120], and it is based on the use of highly absorbance nanoparticles. It also provides in vivo functional imaging information at clinically relevant penetration depths. Recently, AuNSts have been effectively used as enhancing agents in photoacoustic imaging [121]. Nie and coworkers reported the three-dimensional image reconstruction using AuNSts [122]. The AuNSts conjugated with cyclic RGD (Arg-Gly-Asp) peptides and anticancer drug doxorubicin (DOX) were studied in different tumor cell lines, and in vivo imaging was done using S180 tumor-bearing mouse model cells (MDA-MB-231) [123]. The fluorescence images of Au-RGD-DOX after incubating with MDA-MB-231cells for 8 h were collected in order to understand the intracellular kinetics of the multifunctional nanoparticles. The obtained data clearly indicated that Au-RGD-DOX or released DOX entered the nucleus with only a small fraction remaining in the cytoplasm. The AuNSts with size less than 100 nm can accumulate selectively in tumors via the enhanced permeability and retention effect which is due to the increased leakiness of blood vasculature in tumors [124–126]. Combining this statement and their unique properties, AuNSts are considered to be suitable platforms for multimodal imaging for cancer diagnostics.

4. THERAPEUTIC AND DRUG DELIVERY APPLICATIONS OF GOLD NANOMATERIALS From spheres to rods, different geometrical configurations of gold nanomaterials have been used as drug delivery agents. The tumor targeting ligands associated with AuNPs have shown improved tumor targeting and enhanced cellular uptake efficiency. In addition to delivering

172

S. Sudhakar and P.B. Santhosh

chemotherapeutic agents successfully to the tumor site, PEGylated AuNPs with human transferrin exert photothermal therapy upon irradiation. Taghdisi et al. [124] reported a modified polyvalent aptamers–Daunorubicin-AuNPs complex which exhibited efficient drug loading, tumor targeting, and controllable delivery of anticancer drug to tumor cells. Marques et al. [127] reported the polymeric AuNPs as a potential carrier system for drug delivery. Surface modification of AuNPs by polymers plays a significant role in conjugating the therapeutic entities for drug delivery via ionic, covalent bonding, or by physical adsorption. The anticancer drugs can be loaded in AuNPs by adopting various methods. For instance, the drug can be either attached to the capping agent or loaded inside the AuNPs. The AuNCgs and AuNShs have higher drug loading efficiency due to the presence of hollow spaces. By utilizing these strategies, various therapeutic drugs have been successfully delivered using AuNCus and gold AuNShs. Many drugs including doxorubicin, paclitaxel, docetaxel, tamoxifen, oxaliplatin, and 3-mercaptopropionic acid have been successfully loaded in gold nanomaterials and used for anticancer therapy. Zhang et al. [128] reported the polymer encapsulated, doxorubicin-loaded AuNRs coupled the photothermal properties of AuNRs and the thermo and pH responsive properties of polymers. This nanocomposite provides an ideally versatile platform to simultaneously deliver heat and anticancer drugs in a laser-activation mechanism with facile control of the area, time, and dosage. Iodice et al. [129] reported that poly (lactic acid-co-glycolic acid) (PLGA)-coated AuNPs exhibited direct cytotoxic effect on breast cancer cells (SUM-159) and in glioblastoma multiform cells (U87-MG). Betzer et al. [130] proposed a theranostic approach for the detection and therapy of head and neck cancer. Huang et al. [12] reported that plasmonic photothermal therapy acts as a promising cancer treatment and causes cell death, mainly via apoptosis and necrosis. The AuNRs displayed significant reduction in viability of breast, oral, and liver cancer cell lines. Yang et al. [131] reported that the chitosan-coated AuNRs tagged with siRNA (small interfering RNA) inhibited the oncogene expression in MDA-MB-231 triple-negative breast cancer cells, and moreover their anticancer efficacy was enhanced through NIR-mediated photothermal ablation. Zhong [132] reported FA-conjugated AuNRs were effectively used in photoacoustic therapy for selectively killing cancer cells within few seconds. Vo-Dinh et al. [78] reported photothermal ablation in SKBR3 cells by AuNSts. Zou et al. [75] synthesized dual-aptamer-modified AuNSts for photothermal therapy in prostate cancers. These studies have confirmed that

Recent Advances in Cancer Theranostics

173

different types of gold nanomaterials act as promising materials for photothermal cancer application.

5. CONCLUSION AND PERSPECTIVES On the whole, different types of gold nanomaterials including nanoparticles, nanorods, nanocages, nanostars, and nanoshells have shown multifunctional potential in tumor imaging, tumor targeting, and drug delivery and therapy. The synthesis of gold nanomaterials with tunable sizes and surface properties aims to reduce their toxicity, decrease their nonspecific cellular uptake, and to increase their targeting efficiency. They are also used to improve the contrast in MRI and to enhance their load to target tumor cells in drug delivery. Their unique optical properties and their multifunctional potential to simultaneously diagnose and treat tumors enhance their reliability and versatility in the field of theranostics. The identification and synthesis of biocompatible cross-linking polymers will increase the stability and scope of gold nanomaterials in cancer treatment. The use of NIR rays and gold nanomaterials will be beneficial to target tumors that are located deep inside the body. To increase their half-life, stealth nanoparticles with improved characteristics have to be designed which will have prolonged circulation rates to facilitate the uptake of gold nanomaterials into cancer cells. The direction of future research regarding gold nanomaterials should focus on the need to overcome these hurdles and to develop novel therapies to provide solutions for the current problems. Promising clinical trials have given considerable hope that gold nanomaterials with improved characters help to develop safe and efficient tumor treatment/eradication methods in the near future.

REFERENCES [1] J. Ye, P. Van Dorpe, W. Van Roy, G. Borghs, G. Maes, Fabrication, characterization, and optical properties of gold nanobowl submonolayer structures, Langmuir 25 (2009) 1822–1827. [2] C.J. Murphy, L.B. Thompson, D.J. Chernak, J.A. Yang, S.T. Sivapalan, S.P. Boulos, J.Y. Huang, A.M. Alkilany, P.N. Sisco, Gold nanorod crystal growth: from seedmediated synthesis to nanoscale sculpting, Curr. Opin. Colloid Interface Sci. 16 (2011) 128–134. [3] C.C. Li, K.L. Shuford, M.H. Chen, E.J. Lee, S.O. Cho, A facile polyol route to uniform gold octahedra with tailorable size and their optical properties, ACS Nano 2 (2008) 1760–1769. [4] M.Z. Liu, P. Guyot-Sionnest, Mechanism of silver(I)-assisted growth of gold nanorods and bipyramids, J. Phys. Chem. B 109 (2005) 22192–22200.

174

S. Sudhakar and P.B. Santhosh

[5] N.G. Khlebtsov, L.A. Dykman, Optical properties and biomedical applications of plasmonic nanoparticles, J. Quant. Spectrosc. Radiat. Transf. 111 (2010) 1–35. [6] C.L. Nehl, H.W. Liao, J.H. Hafner, Optical properties of star-shaped gold nanoparticles, Nano Lett. 6 (2006) 683–688. [7] C. Kim, E.C. Cho, J.Y. Chen, K.H. Song, L. Au, C. Favazza, Q.A. Zhang, C.M. Cobley, F. Gao, Y.N. Xia, L.H.V. Wang, In vivo molecular photoacoustic tomography of melanomas targeted by bioconjugated gold nanocages, ACS Nano 4 (2010) 4559–4564. [8] S.S. Shankar, A. Rai, A. Ahmad, M. Sastry, Rapid synthesis of Au, Ag, and bimetallic Au core-Ag shell nanoparticles using neem (Azadirachta indica) leaf broth, J. Colloid Interface Sci. 275 (2004) 496–502. [9] P. Mukherjee, A. Ahmad, D. Mandal, S. Senapati, S.R. Sainkar, M.I. Khan, R. Ramani, R. Parischa, P.A.V. Kumar, M. Alam, M. Sastry, R. Kumar, Bioreduction of AuCl(4)( ) ions by the fungus, Verticillium sp. and surface trapping of the gold nanoparticles formed D.M. and S.S. thank the Council of Scientific and Industrial Research (CSIR), Government of India, for financial assistance, Angew. Chem. Int. Ed. Engl. 40 (2001) 3585–3588. [10] M.C. Daniel, D. Astruc, Gold nanoparticles: assembly, supramolecular chemistry, quantum-size-related properties, and applications toward biology, catalysis, and nanotechnology, Chem. Rev. 104 (2004) 293. [11] S.S. Dash, B.G. Bag, Synthesis of gold nanoparticles using renewable Punica granatum juice and study of its catalytic activity, Appl. Nanosci. 4 (2012) 455–459. [12] P. Huang, L. Bao, C.L. Zhang, J. Lin, T. Luo, D.P. Yang, M. He, Z.M. Li, G. Gao, B. Gao, S. Fu, D.X. Cui, Folic acid-conjugated silica-modified gold nanorods for X-ray/Ct imaging-guided dual-mode radiation and photo-thermal therapy, Biomaterials 32 (2011) 9796–9809. [13] V.S. Marangoni, I.M. Paino, V. Zucolotto, Synthesis and characterization of jacalingold nanoparticles conjugates as specific markers for cancer cells, Colloids Surf. B 112 (2013) 380–386. [14] J.F. Hainfeld, F.A. Dilmanian, D.N. Slatkin, H.M. Smilowitz, Radiotherapy enhancement with gold nanoparticles, J. Pharm. Pharmacol. 60 (2008) 977–985. [15] M. Kodiha, E. Hutter, S. Boridy, M. Juhas, D. Maysinger, U. Stochaj, Gold nanoparticles induce nuclear damage in breast cancer cells: which is further amplified by hyperthermia, Cell. Mol. Life Sci. 71 (2014) 4259–4273. [16] J.W. Nichols, Y.H. Bae, EPR: evidence and fallacy, J. Control. Release 190 (2014) 451–464. [17] C.H.J. Choi, C.A. Alabi, P. Webster, M.E. Davis, Mechanism of active targeting in solid tumors with transferrin-containing gold nanoparticles, Proc. Natl. Acad. Sci. U.S.A. 107 (2010) 1235–1240. [18] S.E. Skrabalak, L. Au, X. Li, Y. Xia, Facile synthesis of Ag nanocubes and Au nanocages, Nat. Protoc. 2 (2007) 2182–2190. [19] X. Lu, J. Chen, S.E. Skrabalak, Y. Xia, Galvanic replacement reaction: a route to highly ordered bimetallic nanotubes, J. Nanoeng. Nanosyst. 221 (2008) 1–16. [20] S.E. Skrabalak, J. Chen, Y. Sun, X. Lu, L. Au, M. Cobley, Y. Xia, Gold nanocages: synthesis, properties, and applications, Acc. Chem. Res. 4 (2008) 1587–1595. [21] M.J. Kwon, J. Lee, A.W. Wark, H.J. Lee, Nanoparticle-enhanced surface plasmon resonance detection of proteins at attomolar concentrations: comparing different nanoparticle shapes and sizes, Anal. Chem. 84 (2012) 1702–1707. [22] M.A. Mahmoud, B. Snyder, M.A. El-Sayed, Surface Plasmon fields and coupling in the hollow gold nanoparticles and surface-enhanced Raman spectroscopy. Theory and experiment, J. Phys. Chem. C 113 (2010) 19475–19481.

Recent Advances in Cancer Theranostics

175

[23] L. Au, Y. Chen, F. Zhou, P.H.C. Camargo, B. Lim, Z.D.S. Ginger, Y. Xia, Synthesis and optical properties of cubic gold nanoframes, Nano Res. 4 (2008) 441–449. [24] M.A. Mahmoud, M.A. El-Sayed, Gold nanoframes: very high surface Plasmon fields and excellent near-infrared sensors J, Am. Chem. Soc. 132 (2010) 12704–12710. [25] E.C. Dreaden, A.M. Alkilany, X. Huang, C.J. Murphy, M.A. El-Sayed, The golden age: gold nanoparticles for biomedicine, Chem. Soc. Rev. 41 (2012) 2740–2779. [26] Y. Chen, Y. Zhang, W. Liang, X. Li, Gold nanocages as contrast agents for twophoton luminescence endomicroscopy imaging, Nanomedicine 8 (2012) 1267–1270. [27] R.D. Averitt, D. Sarkar, N.J. Halas, Plasmon resonance shifts of Au-coated Au2 S nanoshells: insight into multicomponent nanoparticle growth, Phys. Rev. Lett. 78 (1997) 4217–4220. [28] S.J. Oldenburg, R.D. Averitt, S.L. Westcott, N.J. Halas, Nano engineering of optical resonances, Chem. Phys. Lett. 288 (1998) 243–247. [29] R.D. Averitt, S.L. Westcott, N.J. Halas, Linear optical properties of gold nanoshells, J. Opt. Soc. Am. B 16 (1999) 1824–1832. [30] S.J. Oldenburg, J.B. Jackson, S.L. Westcott, N.J. Halas, Infrared extinction properties of gold nanoshells, Appl. Phys. Lett. 75 (1999) 2897–2899. [31] P. Tuersun, X. Han, Optical absorption analysis and optimization of gold nanoshells, Appl. Opt. 52 (2013) 1325–1329. [32] C. Loo, L. Hirsch, M. Lee, E. Chang, J. West, N. Halas, R. Drezek, Gold nanoshell bio-conjugates for molecular imaging in living cells, Opt. Lett. 30 (2005) 1012–1014. [33] J. Park, A. Estrada, K. Sharp, K. Sang, J.A. Schwartz, D.K. Smith, C. Coleman, J.D. Payne, B.A. Korgel, A.K. Dunn, J.W. Tunnell, Two-photon-induced photoluminescence imaging of tumors using near-infrared excited gold nanoshells, Opt. Express 16 (2008) 1590–1599. [34] L.R. Bickford, G. Agollah, R. Drezek, T. Yu, Silica–gold nanoshells as potential intra operative molecular probes for HER2-overexpression in ex vivo breast tissue using near-infrared reflectance confocal microscopy, Breast Cancer Res. Treat. 120 (2010) 547–555. [35] A.M. Gobin, M.H. Lee, N.J. Halas, W.D. James, R.A. Drezek, J.L. West, Nearinfraredresonant nanoshells for combined optical imaging and photothermal cancer therapy, Nano Lett. 7 (2007) 1929–1934. [36] L.R. Hirsch, R.J. Stafford, J.A. Bankson, S.R. Sershen, B. Rivera, R.E. Price, J.D. Hazle, N.J. Halas, J.L. West, Nanoshell-mediated near-infrared thermal therapy of tumors under magnetic resonance guidance, Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 13549–13554. [37] A.R. Lowery, A.M. Gobin, E.S. Day, N.J. Halas, J.L. West, Immuno nanoshells for targeted photothermal ablation of tumor cells, Int. J. Nanomed. 1 (2006) 149–154. [38] A.M. Gobin, J.J. Moon, J.L. West, Ephrinal-targeted nanoshells for photo thermal ablation of prostate cancer cells, Int. J. Nanomed. 3 (2008) 351–358. [39] H. Feng, C.L. Nehl, J.H. Hafner, P. Nordlander, Plasmon resonances of gold nanostars, Nano Lett. 7 (2007) 729–732. [40] L. Rodriguez-Lorenzo, R.A. Alvarez-Puebla, I. Pastoriza-Santos, S. Mazzucco, O. Stephan, M. Kociak, L.M. Liz-Marzan, F.J. Garcia de Abajo, Zeptomol detection through controlled ultrasensitive surface-enhanced Raman scattering, J. Am. Chem. Soc. 131 (2009) 4616–4618. [41] C. Hrelescu, T.K. Sau, A.L. Rogach, F. Jackela, F. Feldmann, Single gold nanostars enhance Raman scattering, Appl. Phys. Lett. 94 (2009) 153–183. [42] S.K. Dondapati, T.K. Sau, C. Hrelescu, T.A. Klar, F.D. Stefani, J. Feldmann, Labelfree biosensing based on single gold nanostars as plasmonic transducers, ACS Nano 4 (2010) 6318–6322.

176

S. Sudhakar and P.B. Santhosh

[43] P. Mulvaney, Surface plasmon spectroscopy of nanosized metal particles, Langmuir 12 (1996) 788–800. [44] F. Schulz, T. Homolka, N.G. Bastus, V. Puntes, H. Weller, T. Vossmeyer, Little adjustments significantly improve the turkevich synthesis of gold nanoparticles, Langmuir 30 (2014) 10779–10784. [45] M. Brust, J. Fink, D. Bethell, D.J. Schiffrin, C. Kiely, Synthesis and reactions of functionalized gold nanoparticles, Chem. Commun. 16 (1995) 1655–1656. [46] J.W. Park, J.S. Shumaker-Parry, Structural study of citrate layers on gold nanoparticles: role of intermolecular interactions in stabilizing nanoparticles, J. Am. Chem. Soc. 136 (2014) 1907–1921. [47] F. Westerlund, T. Bjornholm, Directed assembly of gold nanoparticles, Curr. Opin. Colloid Interface Sci. 14 (2009) 126–134. [48] R. Sardar, A.M. Funston, P. Mulvaney, R.W. Murray, Gold nanoparticles: past, present, and future, Langmuir 25 (2009) 13840–13851. [49] E. Boisselier, D. Astruc, Gold nanoparticles in nanomedicine: preparations, imaging, diagnostics, therapies and toxicity, Chem. Soc. Rev. 38 (2009) 1759–1764. [50] R.A. Sperling, P. Rivera Gil, F. Zhang, M. Zanella, W.J. Parak, Biological applications of gold nanoparticles, Chem. Soc. Rev. 37 (2008) 1896–1922. [51] J. Turkevich, P.C. Stevenson, J. Hillier, The formation of colloidal gold, J. Phys. Chem. 57 (1953) 670–673. [52] J. Turkevich, P.C. Stevenson, J. Hillier, A study of the nucleation and growth processes in the synthesis of colloidal gold, Discuss. Faraday Soc. 11 (1951) 55–75. [53] Y.Y. Yu, S.S. Chang, C.L. Lee, C.R.C. Wang, Gold nanorods: electrochemical synthesis and optical properties, J. Phys. Chem. B 101 (1997) 6661–6664. [54] N.R. Jana, L. Gearheart, C.J. Murphy, Wet chemical synthesis of high aspect ratio gold nanorods, J. Phys. Chem. B 105 (2001) 4065–4067. [55] K.R. Brown, D.G. Walter, M.J. Natan, Seeding of colloidal Au nanoparticle solutions. 2. Improved control of particle size and shape, Chem. Mater. 12 (2000) 306–313. [56] P.L. Gai, M.A. Harmer, Surface atomic defect structures and growth of gold nanorods, Nano Lett. 2 (2002) 771–774. [57] C.J. Johnson, E. Dujardin, S.A. Davis, C.J. Murphy, S. Mann, Growth and form of gold prepared by seed-mediated-directed synthesis, J. Mater. Chem. 12 (2002) 1765–1770. [58] J.X. Gao, C.M. Bender, C.J. Murphy, Dependence of the gold nanorod aspect ratio on the nature of the directing surfactant in aqueous solution, Langmuir 19 (2003) 9065–9070. [59] B. Nikoobakht, M.A. El-Sayed, Preparation and growth mechanism of gold nanorods (NRs) using seed-mediated growth method, Chem. Mater. 15 (2003) 1957–1962. [60] B.M.I. van der Zande, M.R. Bohmer, L.G.J. Fokkink, C. Schonenberger, Colloidal dispersions of gold rods: synthesis and optical properties, Langmuir 16 (2000) 451–458. [61] L.Y. Cao, T. Zhu, Z.F. Liu, Formation mechanism of nonspherical gold nanoparticles during seeding growth: Roles of anion adsorption and reduction rate, J. Colloid Interface Sci. 293 (2006) 69–76. [62] A. Gole, C.J. Murphy, Seed-mediated synthesis of gold nanorods: role of the size and nature of the seed, Chem. Mater. 16 (2004) 3633–3640. [63] N.R. Jana, L. Gearheart, C.J. Murphy, Seed-mediated growth approach for shapecontrolled synthesis of spheroidal and Rod-like gold nanoparticles using a surfactant template, Adv. Mater. 13 (2001) 1389–1393. [64] L.F. Gou, C.J. Murphy, Fine-tuning the shape of gold nanorods, Chem. Mater. 17 (2005) 3668–3672.

Recent Advances in Cancer Theranostics

177

[65] N.D. Burrows, S. Harvey, F.A. Idesis, C.J. Murphy, Understanding the seed-mediated growth of gold nanorods through a fractional factorial design of experiments, Langmuir 33 (2017) 1891–1907. [66] C.J. Murphy, N.R. Jana, Controlling the aspect ratio of inorganic nanorods and nanowires, Adv. Mater. 14 (2002) 80–82. [67] S. Ross, C.E. Kwartler, J.H. Bailey, Colloidal association and biological activity of some related quaternary ammonium salts, J. Colloid Sci. 8 (1953) 385–401. [68] M.S. Bakshi, I. Kaur, Unlike surfactant–polymer interactions of sodium dodecyl sulfate and sodium dodecylbenzene sulfonate with water-soluble polymers, Colloid Polym. Sci. 281 (2003) 10–18. [69] S.B. Velegol, B.D. Fleming, S. Biggs, E.J. Wanless, R.D. Tilton, Counterion effects on hexa decyl trimethyl ammonium surfactant adsorption and self-assembly on silica, Langmuir 16 (2000) 2548–2556. [70] B. Nikoobakht, M.A. El-Sayed, Evidence for bilayer assembly of cationic surfactants on the surface of gold nanorods, Langmuir 17 (2001) 6368–6374. [71] Z. Wang, Z. Chen, Z. Liu, P. Shi, K. Dong, A multi-stimuli responsive gold nanocage hyaluronic platform for targeted photothermal and chemotherapy, Biomaterials 35 (2014) 9678–9688. [72] Y. Guan, X. Zheng, L. Jinglun, H. Zhenzhen, W. Yang, One-pot synthesis of sizetunable hollow gold nanoshells via APTES-in-water suspension, Colloids Surf. A 502 (2016) 6–12. [73] C.H. Kuo, M.H. Huang, Synthesis of branched of gold nanocrystals by a seeding growth approach, Langmuir 21 (2005) 2012–2016. [74] C.J. Murphy, N.R. Jana, Controlling the aspect ratio of inorganic nanorods and nanowires, Adv. Mater. 14 (2002) 80–82. [75] H. Zou, E. Ying, S. Dong, Seed-mediated synthesis of branched gold nanoparticles with the assistance of citrate and their surface-enhanced Raman scattering properties, Nanotechnology 17 (2006) 4758–4764. [76] H. Yuan, C.G. Khoury, Gold nanostars: surfactant-free synthesis, 3D modelling and two-photon photoluminescence imaging, Nanotechnology 23 (2012) 75–102. [77] L. Minati, One-step synthesis of star-shaped gold nanoparticles, Colloids Surf. A. 441 (2014) 623–628. [78] C.G. Khoury, T. Vo-Dinh, Gold nanostars for surface-enhanced Raman scattering: synthesis, characterization and optimization, J. Phys. Chem. C 112 (2008) 18849–18859. [79] S. Barbosa, A. Agarwal, L.R. Lorenzo, L.M. Liz-Marzan, Size tuning and sensing capabilities of gold nanostars, Langmuir 26 (2010) 14943–14950. [80] J. Yu, D. Xub, G. Hua, W. Chao, H. Li, Facile one-step green synthesis of gold nanoparticles using Citrus maxima aqueous extracts and its catalytic activity, Mater. Lett. 166 (2016) 110–112. [81] G. Ghodake, S.R. Lim, D.S. Lee, Casein hydrolytic peptides mediated green synthesis of antibacterial silver nanoparticles. Colloids Surf. B Biointerfaces 108 (2013) 147–151. [82] W. Yana, C. Chena, L. Wanga, D. Zhang, Facile and green synthesis of cellulose nanocrystal-supported gold nanoparticles with superior catalytic activity, Carbohydr. Polym. 140 (2016) 66–73. [83] A. Nazirova, A. Pestova, Y. Privara, A. Ustinova, E. Modina, S. Bratskayaa, One-pot green synthesis of luminescent gold nanoparticles using imidazole derivative of chitosan, Carbohydr. Polym. 151 (2016) 649–655. [84] S. Suarasana, M. Focsana, O. Soritaub, D. Maniua, S. Astileana, One-pot, green synthesis of gold nanoparticles by gelatin and investigation of their biological effects on Osteoblast cells, Colloids Surf. B Biointerfaces 132 (2015) 122–131.

178

S. Sudhakar and P.B. Santhosh

[85] B. Sadeghi, M. Mohammadzadeh, B. Babakhani, Green synthesis of gold nanoparticles using Stevia rebaudiana leaf extracts: characterization and their stability, J. Photochem. Photobiol. B 148 (2015) 101–106. [86] C.G. Yuan, H. Can, Y. Shuixin, Biosynthesis of gold nanoparticles using Capsicum annuum var. grossum pulp extract and its catalytic activity, Physica E 85 (2017) 19–26. [87] D. Inbakandan, R. Venkatesan, S.A. Khan, Biosynthesis of gold nanoparticles utilizing marine sponge Acanthella elongata, Colloids Surf. B Biointerfaces 81 (2010) 634–639. [88] L. Castro, M.L. Blazquez, F. Gonza´lez, J.A. Munoz, A. Ballester, Extracellular biosynthesis of gold nanoparticles using sugarbeet pulp, Chem. Eng. J. 164 (2010) 92–97. [89] A.D. Dwivedi, K. Gopal, Biosynthesis of silver and gold nanoparticles using Chenopodium album leaf extract, Colloids Surf. A 369 (2010) 27–33. [90] K.P. Kumar, W. Paul, C.P. Sharma, Green synthesis of gold nanoparticles with Zingiber officinale extract: characterization and blood compatibility, Process Biochem. 46 (2011) 2007–2013. [91] M.M.H. Khalil, E.H. Ismail, F. El-Magdoub, Biosynthesis of Au nanoparticles using Olive leaf extract: 1st nano updates, Arabian J. Chem. 5 (2012) 431–437. [92] S. Kaviya, J. Santhanalakshmi, B. Viswanathan, Biosynthesis of silver nano-flakes by Crossandra infundibuliformis leaf extract, Mater. Lett. 67 (2012) 64–66. [93] V.G. Kumar, S.D. Gokavarapu, A. Rajeswari, T.S. Dhas, V. Karthick, Z. Kapadia, Facile green synthesis of gold nanoparticles using leaf extract of antidiabetic potent Cassia auriculata, Colloids Surf. B Biointerfaces 87 (2011) 159–163. [94] F. Cai, J. Li, J. Sun, Y. Ji, Biosynthesis of gold nanoparticles by biosorption using Magnetospirillum gryphiswaldense MSR-1, Chem. Eng. J. 175 (2011) 70–75. [95] K.M. Kumar, B.K. Mandal, M. Sinha, V. Krishnakumar, Terminalia chebula mediated green and rapid synthesis of gold nanoparticles, Spectrochim. Acta A Mol. Biomol. Spectrosc. 86 (2012) 490–494. [96] M. Noruzi, D. Zare, K. Khoshnevisan, D. Davoodi, Rapid green synthesis of gold nanoparticles using Rosa hybrida petal extract at room temperature, Spectrochim. Acta A Mol. Biomol. Spectrosc. 79 (2011) 1461–1465. [97] T.Y. Suman, S.R.R. Rajasree, R. Ramkumar, C. Rajthilak, P. Perumal, The green synthesis of gold nanoparticles using an aqueous root extract of Morinda citrifolia L., Spectrochim. Acta A Mol. Biomol. Spectrosc. 118 (2014) 11–16. [98] B. Ankamwar, M. Chaudhary, M. Sastry, Gold nanotriangles biologically synthesized using tamarind leaf extract and potential application in vapor sensing, Nano-Met. Chem. 35 (2005) 19–26. [99] P.P. Gan, S.H. Ng, Y. Huang, S. Fong, Y. Li, Green synthesis of gold nanoparticles using palm oil mill effluent (POME): a low-cost and eco-friendly viable approach, Bioresour. Technol. 113 (2012) 132–135. [100] T. Klaus, R. Joerger, E. Olsson, C.G. Granqvist, Silver-based crystalline nanoparticles, microbially fabricated, Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 13611. [101] T.J. Beveridge, R.G.E. Murray, Sites of metal deposition in the cell wall of Bacillus subtilis, J. Bacteriol. 141 (1980) 876. [102] Y. Konishi, T. Tsukiyama, Room-temperature synthesis of gold nanoparticles and nanoplates using Shewanella algae cell extract, Electrochim. Acta 53 (2007) 186. [103] N. Pugazhenthiran, S. Anandan, G. Kathiravan, N.K.U. Prakash, Microbial synthesis of silver nanoparticles by Bacillus sp., J. Nanopart. Res. 11 (2009) 1811. [104] V. Yadav, N. Sharm, Generation of selenium containing nano-structures by soil bacterium, Pseudomonas aeruginosa, Biotechnology 7 (2008) 299. [105] L. Wen, Z. Lin, P. Gu, Extracellular biosynthesis of monodispersed gold nanoparticles by a SAM capping route, J. Nanopart. Res. 11 (2009) 279.

Recent Advances in Cancer Theranostics

179

[106] B. Zhoua, Y. Jia, PEGylated polyethylenimine-entrapped gold nanoparticles modified with folic acid for targeted tumor CT imaging, Colloids Surf. B Biointerfaces 140 (2016) 489–496. [107] C. Gui, D. xiang, Functionalized gold nanorods for tumor imaging and targeted therapy, Cancer Biol. Med. 9 (2012) 221–233. [108] H. Yuan, Gold nanostars: surfactant-free synthesis, 3D modelling, and two-photon photoluminescence imaging, Nanotechnology 23 (2012) 75102. [109] M. Lengke, M.E. Fleet, G. Southam, Morphology of gold nanoparticles synthesized by filamentous cyanobacteria from gold (I) thiosulfate and gold (III) chloride complexes, Langmuir 22 (2006) 2780. [110] M. Lengke, B. Ravel, M.E. Fleet, G. Wanger, Mechanisms of gold bioaccumulation by filamentous cyanobacteria from gold (III)-chloride complex, Environ. Sci. Technol. 40 (2006) 6304. [111] L. Du, H. Jiang, H. Xiaohua, E. Wang, Biosynthesis of gold nanoparticles assisted by Escherichia coli DH5α and its application on direct electrochemistry of hemoglobin, Electrochem. Commun. 9 (2007) 1165. [112] Y. Feng, Y. Yu, Y. Wang, Biosorption and bioreduction of trivalent aurum by photosynthetic bacteria Rhodobacter capsulatus, Curr. Microbiol. 55 (2007) 402. [113] R. Joerger, T. Klaus, C.G. Granqvist, The biochemistry of apoptosis, Adv. Mater. 12 (2000) 407. [114] B. Zhou, Y. Jia, PEGylated polyethylenimine-entrapped gold nanoparticles modified with folic acid for targeted tumor CT imaging, Colloids Surf. B Biointerfaces 140 (2016) 489–496. [115] N. Lozano, T. Wafa, A. Jamal, Liposome-gold nanorod hybrids for high-resolution visualization deep in tissues, J. Am. Chem. Soc. 134 (2012) 13256–13258. [116] X. Huang, A reexamination of active and passive tumor targeting by using rod shaped gold nanocrystals and covalently conjugated peptide ligands, ACS Nano 4 (2010) 5887–5896. [117] M.E. Gallina, Y. Zhou, J. Christopher, Aptamer-conjugated, fluorescent gold nanorods as potential cancer theradiagnostic agents, Mater. Sci. Eng. C 59 (2016) 324–332. [118] H. Wang, In vitro and in vivo two-photon luminescence imaging of single gold nanorods, Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 15752–15756. [119] W. Li, In vivo quantitative photoacoustic microscopy of gold nanostars kinetics in mouse organs, Biomed. Opt. Express 5 (2014) 2679–2685. [120] C.H. Lee, Near-infrared mesoporous silica nanoparticles for optical imaging: characterization and in vivo distribution, Adv. Funct. Mater. 19 (2009) 7688–7693. [121] S. Ye, Label-free imaging of zebrafish larvae in vivo by photoacoustic microscopy, Biomed. Opt. Express 3 (2012) 360–365. [122] L. Nie, Plasmonic nanostars: in vivo volumetric photoacoustic molecular angiography and therapeutic monitoring with targeted plasmonic nanostars, Small 10 (2014) 1585–1593. [123] S.M. Taghdisi, N.M. Danesh, Double targeting, controlled release and reversible delivery of daunorubicin to cancer cells by polyvalent aptamers-modified gold nanoparticles, Mater. Sci. Eng. C 61 (2016) 753–761. [124] Z. Yang, T. Liu, X. Yan, Chitosan layered gold nanorods as synergistic therapeutics for photothermal ablation and gene silencing in triple-negative breast cancer, Acta Biomater. 25 (2015) 194–204. [125] D.H. Dam, Direct observation of nanoparticles-cancer cell nucleus interaction, ACS Nano 6 (2012) 3318–3326. [126] D.H. Dam, Shining light on nuclear-targeted therapy using gold nanostars constructs, Ther. Deliv. 3 (2012) 1263–1267.

180

S. Sudhakar and P.B. Santhosh

[127] T. Marques, M. Schwarcke, Gel dosimetry analysis of gold nanoparticle application in kilovoltage radiation therapy, J. Geophys. Res. 250 (2010) 12084. [128] Z. Zhang, J. Wang, X. Nie, Near infrared laser-induced targeted cancer therapy using thermoresponsive polymer encapsulated gold nanorods, J. Am. Chem. Soc. 136 (2014) 7317–7326. [129] C. Iodice, Enhancing photothermal cancer therapy by clustering gold nanoparticles into spherical polymeric nanoconstructs, Opt. Lasers Eng. 76 (2016) 74–81. [130] O. Betzer, R. Ankri, M. Motiei, R. Popovtzer, Theranostic approach for cancer treatment: multifunctional gold nanorods for optical imaging and photothermal therapy, J. Nanomater. 5 (2015) 646713. [131] L. Yang, Quintuple-modality (SERS-MRI-CT-TPL-PTT) plasmonic nanoprobe for theranostics, Nanoscale 5 (2013) 12126. [132] J. Zhong, Imaging-guided high-efficient photoacoustic tumor therapy with targeting gold nanorods, Nanomedicine 11 (2015) 1499–1509.

INDEX Note: Page numbers followed by “f ” indicate figures, and “t” indicate tables.

A Acid sphingomyelinase (ASM), 58 Acyl chain structures, 54 Amino acid encapsulation, 74–75 Amino acids arginine, 75f Amphiphile-aqueous solution system inverse bicontinuous cubic phases, 64–66, 64f Amphiphilic amino acids, 74–75 Amphiphilic enzyme, 87 Aneurysms, 4 Anisotropy, 133–134 Antimicrobial peptides (AMPs), 77–78, 112–113 aurein 1.2, 150–151, 151f birefringence changes, 148–150, 149f cubosomes, 112–113 DMPC, 149f, 150–151 magainin 2 (Mag2), 150–151, 151f membrane destruction, 150–151 AP114 peptide, 78–79 Aspirin, 56–57 Atheromatous plaques, 4 Atherosclerosis (ASc), 4–5 Atherosclerotic renovascular disease (ARVD), 6 Atomic force microscopy (AFM), 99–100 AuNCgs. See Gold nanocages (AuNCgs) AuNPs. See Gold nanoparticles (AuNPs) AuNRs. See Gold nanorods (AuNRs) AuNShs. See Gold nanoshells (AuNShs) AuNSts. See Gold nanostars (AuNSts)

B Bacteriorhodopsin (bR), 84–85, 84f Bare-metal stents (BMS), 9–10 β2 adrenergic receptor, 84f Bicontinuous cubic phases, 108–111 Bilayer thicknesses, 98–99 Bile acids, 57 Biocompatibility, 12–13 Biofilms, 33

Biomembranes, 126, 128 Biomolecule system vs. lipidic cubic phase, 66, 66f Birefringence, 133–135 Bivariate K-function analysis, 50–52, 51f bR. See Bacteriorhodopsin (bR)

C Caille theory, 98–99 Cardiovascular diseases (CVDs) atherosclerosis (ASc), 4–5 risk factors, 3 vascular implant, 2–3 Carotid artery disease, 5–6 Casein hydrolytic peptides (CHPs), 167–168 Caveolae, 55 Cetyltrimethyl ammonium bromide (CTAB), 165 Cholesterol, 99–100, 142 CHPs. See Casein hydrolytic peptides (CHPs) Coronary heart disease (CHD), 5 Critical micelle concentrations (CMCs), 57, 109–111 Critical packing parameter (CPP) lipidic mesophases, 109–111 values of lipids, 67–68, 67f Cryogenic transmission electron microscopy (cryo-TEM), 74 CTAB. See Cetyltrimethyl ammonium bromide (CTAB) Cubic phase nanoparticles, 71–73 Cubosomes, 71–73, 72f, 111–113 Curcumin, 112–113 Curvature-dependent selectivity, 115–116 Curved membranes curvature-dependent selectivity, 115–116 lipidic mesophases bicontinuous cubic phases, 108–111 critical packing parameter (CPP), 109–111 mean curvature, 109–111 181

182 Curved membranes (Continued ) molecular shapes, 109–111 monoglycerides, 108–109 mesosomes applications, 112–113 cubosomes, 111–113 curcumin, 112–113 hexosomes, 111 pluronic F127, 111 quercetin, 113–115, 114f small-angle X-ray scattering (SAXS), 113–114, 114f structural analysis of, 112f

D DAPI staining, 29 De Feijter formula, 135 DES. See Drug-eluting stents (DES) Dioleoylphosphatidylcholine (DOPC), 102 Dipalmitoylphosphatidylcholine (DPPC), 102 Divalent cations, 143–144 D2L dopamine receptor, 84–85 DMPC, 143 DPK-060 peptide, 78–79 Drug-eluting stents (DES), 9–11, 23 Dual polarization interferometry (DPI) anisotropy, 132–135 birefringence, 132–135 instrumentation, 129–131 lipid molecular organization, changes in antimicrobial peptides (AMPs), 148–152 birefringence changes, 148–150, 149f multistructural parameters, 147–148 operating principle, 129–131 optogeometrical parameters, 135 polarization modes, 131–132, 132f supported lipid bilayers (SLBs) biomembrane layer preparation, 136–138 challenges, 145–146 divalent cations, 143–144 ionic strength, 143 limitations, 145–146 liposomes, 138–141 modified chip, anchored liposomes on, 146–147

Index

osmotic pressure, 145 pH, 144–145 salt, 143–144 substrate, 138 temperature, 142 Dynamic light scattering (DLS) spectroscopy, 74

E Electrochemical anodization, 12–13 TiO2 fabrication, 19 Elyzol Dental Gel, 70–71 Encapsulated proteins, 66 Encapsulation. See specific types of encapsulation Endothelial cells (EC) culturing, 28 human coronary artery endothelial cells (HCAEC), 27–28, 28f, 30f immunofluorescent microscopy, 28–29 staining, 29 vascular stent, 27 Endovascular stent-grafting, 9 Epidermal growth factor (EGF), 46–47 Escherichia coli, 168–170 ClC transporter protein, 87

F Fabricated nanotubes (NTs), 16 Fendiline, 57–58 Flavonoid-lipid interactions with curved membranes curvature-dependent selectivity, 115–116 lipidic mesophases, in bulk, 108–111 mesosomes, 111–115, 112f, 114f with planar membranes functions, 98–100 influence, 100–108, 103–107t structures, 98–100 Fluorescein phalloidin, 28–29 Fluorescence recovery after photobleaching (FRAP), 73–74, 86 Fluorescence resonance energy transfer (FRET), 43–45 Food and Drug Administration (FDA), 22–23 FRAP. See Fluorescence recovery after photobleaching (FRAP)

183

Index

G

I

Gaseous plasma in medical applications, 19–21 TiO2 nanotubes, 21 treatment, 16–17 G-domain conformational orientation, 49–50 GDP-bound H-Ras, 49 Geobacter ferrireducens, 168–170 GFP-LactC2 probe, 57–58 Giant plasma membrane vesicles (GPMVs), 57 Gold nanocages (AuNCgs), 163–164 synthesis of, 165–166 Gold nanomaterials, 162–164 diagnostic and imaging applications of, 170–171 synthesis of chemical-mediated, 164–167 green, 167–168, 168t microbial, 168–170, 169t therapeutic and drug delivery applications of, 171–173 Gold nanoparticles (AuNPs), 162 PEGylated, 171–172 shape types, 163f surface modification of, 171–172 synthesis of, 164–165 tracking of, 171 Gold nanorods (AuNRs), 163 bioconjugation of, 170–171 synthesis of, 165 Gold nanoshells (AuNShs), 164 synthesis of, 166 Gold nanostars (AuNSts), 164 synthesis of, 166–167 TPACS of, 171 Gramicidin A, 76–77, 76f Green synthesis, of gold nanomaterials, 167–168, 168t

Indomethacin, 56–57 Infrared reflection absorption spectroscopy (IRRA), 50 In meso crystallization, 69–70, 86 Integral membrane protein encapsulation, 83–87 Interfacial curvature, 67–68 ISAsomes. See Mesosomes Ischemia, 5–6

H Heptapeptides, 81 Hexosomes, 111 Hydrophilic moieties, 65–66

L Lateral pressure, 67–68 Lipid(s), 68f anchors atomic force microscopy (AFM), 48–49 H-Ras, 48 K-Ras, 48–49 methyl-β-cyclodextrin (MβCD), 48 N-Ras, 48–49 CPP values of, 67–68, 67f inverse bicontinuous cubic phases in pure, 64f wedge-shaped, 67–68 Lipid A phosphoethanolamine transferase (LptA), 87 Lipidic cubic phase vs. biomolecule system, 66, 66f Lipid mesophase, 74, 76 physicochemical parameters of, 67 structural parameters of, 70–71 Lipid packing, 67–68 Liposomes birefringence, 140–141 mechanical extrusion, 138–140 on modified chip, 146–147 osmotic pressure, 145 POPC SLBs formation, 140–141, 141f unilamellar, 138–139 vesicle-to-SLB transformation, 139 LL-37 peptide, 78–79 Localized surface plasmon resonance (LSPR), 162–166 of AuNRs, 165 Lyotropic liquid crystalline systems, 96–97

184

M MAPK signal transduction, 46–47, 47f Maxwell’s equations, 131–132 MβCD. See Methyl-β-cyclodextrin (MβCD) Membrane fluidity, 102–108, 103–107t Membrane proteins, 65–66, 69–70, 80, 82, 84–87 Mesenchymal stem cells (MSCs), 30–32, 31f Mesophase, 74, 77, 79–80, 87 in excess water condition, 96–97 phase behavior of, 85 structural evolution of, 86 Mesosomes applications, 112–113 cubosomes, 111–113 curcumin, 112–113 hexosomes, 111 pluronic F127, 111 quercetin, 113–115, 114f small-angle X-ray scattering (SAXS), 113–114, 114f structural analysis of, 112f Methyl-β-cyclodextrin (MβCD), 48–49 Monoacylglycerols, 65 Monoglycerides, 108–109 Monoolein, 79–80, 84–85 Monopalmitolein system, 86 Multilamellar vesicles (MLVs), 97–98 Multistructural parameters, 147–148

N Nanotopography, 11–12 Near-infrared (NIR) light, 162 Nonbilayer-forming lipids, 115–116 Nonsteroidal antiinflammatory drugs (NSAIDs), 56–57 Nonthermal plasmas, 19–21

O Oleoylethanolamide-based cubic phase system, 75 Optical biosensor, 127–128, 131 Orthogonal polarization, 131, 133–134 transverse electric (TE) mode, 131–132, 132f

Index

transverse magnetic (TM) mode, 131–132, 132f Osmotic pressure, 145 Osteoblasts, 13

P 1-Palmitoyl-sn-glycero-3-phosphocholine (PLPC) cubic phase, 78 Peptide encapsulation, 66, 76–83 applications of bicontinuous cubic phases for drug delivery, 70–71 in meso crystallization, 69–70 Peptides melittin, 76f Percutaneous transluminal angioplasty (PTA), 7–8 Peripheral artery disease (PAD), 6 Phase transition temperature, 142 Phenylalanine, 74–75 Phosphatidylethanolamine (PE), 52–53 Phosphatidylserine (PS) acyl chain structures, 54–55 of K-Ras nanoclusters, 52–54, 52f Phosphoethanolamide, 87 Phosphoinositol 3-kinase (PI3K), 45–46 Phospholipids, 97–100 Phytantriol, 65 Planar lipid bilayers, 97–98 atomic force microscopy (AFM), 99–100 bilayer thicknesses, 98–99 cholesterol, 99–100 dioleoylphosphatidylcholine (DOPC), 102 dipalmitoylphosphatidylcholine (DPPC), 102 flavonoids, 101–102 in fluid phase (Lα), 98–99 fluorescence anisotropic measurements, 101 in gel phase (Lβ), 99 liquid-ordered phases, 99–100 membrane fluidity, 102–108, 103–107t Plasma membrane (PM) depolarization, 53–54 Plasma modification, 19–21 Plasma reactor, 21, 22f Plasma sterilization, 19–21 Platelets, 23–27, 24f

185

Index

incubation, with whole blood, 24–25 SEM analysis, 25–27, 26f Plectonema boryanum, 168–170 Pluronic F127, 111 Polyethylenimine (PEI), 170 Protein bicontinuous cubic phase, characterization of, 73–87 membrane, 84–87 transmembrane domain of, 85 Protein encapsulation, 66 applications of bicontinuous cubic phases for, 69 drug delivery, 70–71 in meso crystallization, 69–70 integral membrane, 83–87 Protein ompF porin, 87 PS synthases (PSS), 52–53

Q Quercetin, 113–115, 114f

R Ras nanoclusters acidic lipid selectivity, 50–55 alters Ras effector binding and signaling, 56–58 on cell plasma membrane, 42–45 definition, 42–43 electron microscopy (EM), 43–45, 44f fluorescence resonance energy transfer (FRET), 43–45, 45f H-Ras, 42–43 isoforms, 42–43 K-Ras, 42–43 MAPK signal transduction, 45–47, 47f N-Ras, 42–43 ordered vs. disordered domains, in cell PM G-domain conformational orientation, 49–50 lipid anchors, 48–49 signal mechanisms, 43–45 spatial distribution, 43–45 Rhodobacter capsulatus, 168–170

S SAXS. See Small angle X-ray scattering (SAXS) spectroscopy Scanning electron microscopy (SEM), 16, 16f Silicon oxynitride chip, 129, 138 Small angle X-ray scattering (SAXS) spectroscopy, 73–74, 113–114, 114f Smooth muscle cells (SMCs), 9–11 Sphingolipids, 142 Stable plaques, 4 Stent–grafts, 9 Stevia rebaudiana, 167–168 Structural coloration, 96–97 Supported lipid bilayers (SLBs) biomembrane layer preparation, 136–138 challenges, 145–146 divalent cations, 143–144 ionic strength, 143 limitations, 145–146 liposomes, 138–141 modified chip, anchored liposomes on, 146–147 osmotic pressure, 145 pH, 144–145 salt, 143–144 substrate, 138 temperature, 142 Surface modification, 12–13 Surface wettability, 18, 18f Synthetic peptide WLFLLKKK, 81

T Thermal plasmas, 19–21 Thrombosis, 23 Ti foil, 17–18 Titanium dioxide (TiO2) nanotubes antiinfective properties, 32–33 electrochemical anodization, 12–13 growth of, 15, 15t interaction endothelial cells (EC), 27–29, 28f, 30f mesenchymal stem cells (MSCs), 30–32, 31f platelets, 23–27, 24f surface modification gaseous plasma, 19–21, 22f

186 Titanium dioxide (TiO2) nanotubes (Continued ) plasma-modified NTs, 22 surface properties chemistry, 16–18, 17f morphology, 16, 16f wettability, 18, 18f Tryptophan, 74–75, 75f Two-photon action cross sections (TPACS) of nanostars, 171

U UV-ozone cleaning, 138

V Vascular grafts bypass grafting, 8–9 polyethylene terephthalate, 8–9, 8f polytetrafluoroethylene, 8–9, 8f Vascular implants atherosclerosis (ASc), 4–5 atherosclerotic renovascular disease (ARVD), 6 biocompatibility, 12–13 carotid artery disease, 5–6 coronary heart disease (CHD), 5 nanotopography, 11–12

Index

peripheral artery disease (PAD), 6 surface modification, 12–13 titanium dioxide (TiO2) nanotubes antiinfective properties, 32–33 growth of, 15, 15t interaction, 22–32, 24f, 26f, 28f, 31f surface modification, 19–22, 22f surface properties, 16–18, 16f, 18f types grafts, 8–9, 8f stent-graft, 9 stents, 7–11, 7f Vascular stents angioplasty, 7–8 complications, 9–11 definition, 7 metal structures, 7

W WALP peptides, 80 WALPS53 peptides, 80–81 WALPS73 peptides, 80–81 Wedge-shaped lipids, 67–68

X X-ray photoelectron spectroscopy (XPS), 16–18, 17f