Enzymes as Sensors [1st Edition] 9780128092910, 9780128054062

Volume 589, the latest volume in the Methods in Enzymology series, focuses on enzymes as sensors.

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Enzymes as Sensors [1st Edition]
 9780128092910, 9780128054062

Table of contents :
Content:
Series PagePage ii
CopyrightPage iv
DedicationPage v
ContributorsPages xiii-xv
PrefacePages xvii-xviiiRichard B. Thompson, Carol A. Fierke
Chapter One - Recent Advances in Development of Genetically Encoded Fluorescent SensorsPages 1-49Lynn Sanford, Amy Palmer
Chapter Two - Engineering Rugged Field Assays to Detect Hazardous Chemicals Using Spore-Based Bacterial BiosensorsPages 51-85Daniel Wynn, Sapna Deo, Sylvia Daunert
Chapter Three - Engineering BRET-Sensor ProteinsPages 87-114Remco Arts, Stijn J.A. Aper, Maarten Merkx
Chapter Four - Enzymes as SensorsPages 115-131Maria Staiano, Angela Pennacchio, Antonio Varriale, Alessandro Capo, Adelia Majoli, Clotilde Capacchione, Sabato D’Auria
Chapter Five - Integrated Strategies to Gain a Systems-Level View of Dynamic Signaling NetworksPages 133-170Robert H. Newman, Jin Zhang
Chapter Six - Probing Cdc42 Polarization Dynamics in Budding Yeast Using a BiosensorPages 171-190Satoshi Okada, Mid Eum Lee, Erfei Bi, Hay-Oak Park
Chapter Seven - Novel Fluorescence-Based Biosensors Incorporating Unnatural Amino AcidsPages 191-219Wei Niu, Jiantao Guo
Chapter Eight - Folding- and Dynamics-Based Electrochemical DNA SensorsPages 221-252Rebecca Y. Lai
Chapter Nine - Construction of Protein-Based Biosensors Using Ligand-Directed Chemistry for Detecting Analyte BindingPages 253-280Kei Yamaura, Shigeki Kiyonaka, Itaru Hamachi
Chapter Ten - Measuring and Imaging Metal Ions With Fluorescence-Based Biosensors: Speciation, Selectivity, Kinetics, and Other IssuesPages 281-299Richard B. Thompson, Carol A. Fierke
Chapter Eleven - Bioapplications of Electrochemical Sensors and BiosensorsPages 301-350Eduard Dumitrescu, Silvana Andreescu
Chapter Twelve - A Highly Sensitive Biosensor for ATP Using a Chimeric Firefly LuciferasePages 351-364Bruce R. Branchini, Tara L. Southworth
Chapter Thirteen - Highly Modular Bioluminescent Sensors for Small Molecules and ProteinsPages 365-382Qiuliyang Yu, Rudolf Griss, Alberto Schena, Kai Johnsson
Chapter Fourteen - Sensitive Protein Detection and Quantification in Paper-Based Microfluidics for the Point of CarePages 383-411Caitlin E. Anderson, Kamal G. Shah, Paul Yager
Chapter Fifteen - Microneedle Enzyme Sensor Arrays for Continuous In Vivo MonitoringPages 413-427Anthony E.G. Cass, Sanjiv Sharma
Chapter Sixteen - Visualization of the Genomic Loci That Are Bound by Specific Multiprotein Complexes by Bimolecular Fluorescence Complementation Analysis on Drosophila Polytene ChromosomesPages 429-455Huai Deng, Tom K. Kerppola
Author IndexPages 457-499
Subject IndexPages 501-511

Citation preview

METHODS IN ENZYMOLOGY Editors-in-Chief

ANNA MARIE PYLE Departments of Molecular, Cellular and Developmental Biology and Department of Chemistry Investigator, Howard Hughes Medical Institute Yale University

DAVID W. CHRISTIANSON Roy and Diana Vagelos Laboratories Department of Chemistry University of Pennsylvania Philadelphia, PA

Founding Editors

SIDNEY P. COLOWICK and NATHAN O. KAPLAN

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: 978-0-12-805406-2 ISSN: 0076-6879 For information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals

Publisher: Zoe Kruze Acquisition Editor: Zoe Kruze Editorial Project Manager: Helene Kabes Production Project Manager: Magesh Kumar Mahalingam Cover Designer: Matthew Limbert Typeset by SPi Global, India

DEDICATION Dedicated to Dr. Harold J. Bright, Biochemist, Savant, and Peerless Supporter of Young Scientists

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CONTRIBUTORS Caitlin E. Anderson University of Washington, Seattle, WA, United States Silvana Andreescu Clarkson University, Clarkson, NY, United States Stijn J.A. Aper Laboratory of Chemical Biology and Institute for Complex Molecular Systems, Eindhoven University of Technology, Eindhoven, The Netherlands Remco Arts Laboratory of Chemical Biology and Institute for Complex Molecular Systems, Eindhoven University of Technology, Eindhoven, The Netherlands Erfei Bi University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, United States Bruce R. Branchini Connecticut College, New London, CT, United States Clotilde Capacchione Institute of Food Science, CNR, Avellino, Italy Alessandro Capo Institute of Food Science, CNR, Avellino, Italy Anthony E.G. Cass Department of Chemistry, Imperial College London, London, United Kingdom Sylvia Daunert Miller School of Medicine, University of Miami, Miami, FL, United States Sabato D’Auria Institute of Food Science, CNR, Avellino, Italy Huai Deng University of Michigan, Ann Arbor, MI, United States Sapna Deo Miller School of Medicine, University of Miami, Miami, FL, United States Eduard Dumitrescu Clarkson University, Clarkson, NY, United States Carol A. Fierke University of Michigan, Ann Arbor, MI, United States

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Contributors

Rudolf Griss  cole Polytechnique Federale de Lausanne (EPFL), Institute of Chemical Sciences and E  cole Polytechnique Federale de Lausanne (EPFL), Institute of Engineering (ISIC); E Bioengineering; National Centre of Competence in Research (NCCR) Chemical Biology, Lausanne, Switzerland Jiantao Guo University of Nebraska–Lincoln, Lincoln, NE, United States Itaru Hamachi Graduate School of Engineering, Kyoto University, Katsura, Kyoto; Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency, Kawaguchi, Saitama, Japan Kai Johnsson  cole Polytechnique Federale de Lausanne (EPFL), Institute of Chemical Sciences and E  cole Polytechnique Federale de Lausanne (EPFL), Institute of Engineering (ISIC); E Bioengineering; National Centre of Competence in Research (NCCR) Chemical Biology, Lausanne, Switzerland Tom K. Kerppola University of Michigan, Ann Arbor, MI, United States Shigeki Kiyonaka Graduate School of Engineering, Kyoto University, Katsura, Kyoto, Japan Rebecca Y. Lai University of Nebraska-Lincoln, Lincoln, NE, United States Mid Eum Lee The Ohio State University, Columbus, OH, United States Adelia Majoli Institute of Food Science, CNR, Avellino, Italy Maarten Merkx Laboratory of Chemical Biology and Institute for Complex Molecular Systems, Eindhoven University of Technology, Eindhoven, The Netherlands Robert H. Newman North Carolina Agricultural and Technical State University, Greensboro, NC, United States Wei Niu University of Nebraska–Lincoln, Lincoln, NE, United States Satoshi Okada University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, United States; Kyushu University Graduate School of Medical Sciences, Fukuoka, Japan Amy Palmer University of Colorado Boulder, Boulder, CO, United States Hay-Oak Park The Ohio State University, Columbus, OH, United States

Contributors

xv

Angela Pennacchio Institute of Food Science, CNR, Avellino, Italy Lynn Sanford University of Colorado Boulder, Boulder, CO, United States Alberto Schena Lucentix SA, Lausanne, Switzerland Kamal G. Shah University of Washington, Seattle, WA, United States Sanjiv Sharma Department of Chemistry, Imperial College London, London, United Kingdom Tara L. Southworth Connecticut College, New London, CT, United States Maria Staiano Institute of Food Science, CNR, Avellino, Italy Richard B. Thompson University of Maryland School of Medicine, Baltimore, MD, United States Antonio Varriale Institute of Food Science, CNR, Avellino, Italy Daniel Wynn Miller School of Medicine, University of Miami, Miami, FL, United States Paul Yager University of Washington, Seattle, WA, United States Kei Yamaura Graduate School of Engineering, Kyoto University, Katsura, Kyoto, Japan Qiuliyang Yu  cole Polytechnique Federale de Lausanne (EPFL), Institute of Chemical Sciences and E  cole Polytechnique Federale de Lausanne (EPFL), Institute of Engineering (ISIC); E Bioengineering; National Centre of Competence in Research (NCCR) Chemical Biology, Lausanne, Switzerland Jin Zhang University of California, San Diego, San Diego, CA, United States

PREFACE The Editors are proud to present this volume of Methods in Enzymology, focused largely on Enzymes as Sensors. We are fortunate to have gathered a constellation of star investigators to describe their current work in this field. The editors (and many of the authors) have felt for some years that for sensing and many other tasks, biomolecules, such as enzymes, have outstanding attributes. Indeed, biomolecules now represent the method of choice for recognition of many analytes and transducing their presence or level as a signal one can interpret. In this case, necessity has been the mother of invention because answering the essentially analytical questions in biology of how much of an analyte is present, how fast is that amount changing, and how is it distributed in the matrix (often of a living cell), and collecting this information in real time on a submicron scale is a challenge beyond most traditional analytical methods. The proportion of the chapters herein describing methods focused on answering precisely such difficult questions is an index of the inherent power of enzymes and other biological molecules to address such questions. The volume begins with a chapter by Drs. Sanford and Palmer reviewing one of the central developments of recent years, the use of expressible fluorescent proteins in sensors of many kinds. The second chapter, by Dr. Wynn and colleagues, details a novel development for increasing the ruggedness of biologically derived sensors, namely, encoding them in a very robust form, the bacterial spore. The chapter by Dr. Arts et al. covers a rapidly growing sensing approach with exciting new applications called bioluminescence resonance energy transfer, or BRET. Dr. Staiano and colleagues follow with a chapter on using enzymes as sensors, which focuses on apoenzymes as nonconsuming sensors. Drs. Newman and Zhang take a much broader view in the fifth chapter, using diverse approaches to understand signaling networks well above the cellular scale. Conversely, Dr. Okada et al. in their chapter zoom in on a GTPase component of the signaling cascade that controls the polarity of yeast budding. Drs. Niu and Guo describe a powerful approach, incorporating a variety of different, unnatural amino acids into protein sensors for diverse sensing applications. The eighth chapter by Dr. Lai is an outstanding review of electrochemically based nucleic acid sensors and their unique advantages. In the next chapter, Dr. Yamaura et al. describe a very subtle approach for adapting the recognition capabilities of cell surface xvii

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Preface

receptors such as the GABAA receptor to turn on sensors. The Editors next discuss numerous issues in the sensing of metal ions, with zinc as an archetype. Dr. Dumitrescu and colleagues describe another group of electrochemically transduced sensors, emphasizing determination of key analytes such as neurotransmitters and reactive oxygen species. Drs. Branchini and Southworth in the twelfth chapter also focus on bioluminescent sensing in describing their engineered luciferases for ATP detection. Dr. Johnsson and his colleagues describe a flexible, modular approach to bioluminescent sensing that is well suited for point-of-care applications. In the 14th chapter, Dr. Anderson and her colleagues describe a fascinating approach to sensing in austere environments using paper-based sensing. Dr. Cass and colleagues take us farther afield in describing sensors that incorporate microneedles specifically to gently pierce the skin to provide access to interstitial fluid and its analytes. In the final chapter, Dr. Kerppola and colleagues describe an exciting approach for sensing called bimolecular fluorescence complementation, and its application to studying multiprotein complexes with fly polytene chromosomes. After more than 60 years, Methods in Enzymology as a series, and developing new methods in experimental science in general, is still relevant and worthwhile. Technology development remains a fruitful part of the scientific enterprise, at least as judged by citations: In January, 2017, 13 of the 15 most cited papers in the Proceedings of the National Academy of Sciences (http://www.pnas.org/reports/most-cited) were overtly methodological in nature albeit from many fields, and all of the top 10 most cited papers overall are methodological (Van Noorden et al., Nature 514, 550 (2014)). Moreover, the highly cited nature and consequent impact of methodological papers has been maintained in the biological and chemical sciences for at least 40 years. In the current “business model” of government/nonprofit funding of academic research, a case could be made that (for instance) Sanger et al.’s invention of dideoxy sequencing (cited 68,000 times and counting) represents a good return on investment. We hope you enjoy this collection. RICHARD B. THOMPSON and CAROL A. FIERKE

CHAPTER ONE

Recent Advances in Development of Genetically Encoded Fluorescent Sensors Lynn Sanford, Amy Palmer1 University of Colorado Boulder, Boulder, CO, United States 1 Corresponding author: e-mail address: [email protected]

Contents 1. Introduction 2. Fluorescent Proteins 2.1 Intrinsic Chromophore FPs 2.2 Extrinsic Chromophore FPs 3. Sensor Platforms 3.1 FRET Sensors 3.2 Fluorescence-Modulated Single FP Sensors 3.3 Translocation Sensors 3.4 Complementation Sensors 3.5 Dimerization Sensors 4. Types of Sensors 4.1 Ions/Metals 4.2 pH 4.3 Metabolites 4.4 Signaling 4.5 Redox 4.6 Force and Crowding 4.7 Voltage 5. Conclusion References

2 2 3 4 11 14 20 24 25 26 26 27 28 29 30 32 32 33 34 34

Abstract Genetically encoded fluorescent sensors are essential tools in modern biological research, and recent advances in fluorescent proteins (FPs) have expanded the scope of sensor design and implementation. In this review we compare different sensor €rster resonance energy transfer (FRET) sensors, fluorescenceplatforms, including Fo modulated single FP-based sensors, translocation sensors, complementation sensors, and dimerization-based sensors. We discuss elements of sensor design and engineering for each platform, including the incorporation of new types of FPs and sensor screening

Methods in Enzymology, Volume 589 ISSN 0076-6879 http://dx.doi.org/10.1016/bs.mie.2017.01.019

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2017 Elsevier Inc. All rights reserved.

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Lynn Sanford and Amy Palmer

techniques. Finally, we summarize the wide range of sensors in the literature, exploring creative new sensor architectures suitable for different applications.

1. INTRODUCTION Biological sensors are fundamental to current research, from quantifying metabolites under different perturbations to identifying cell states. Many types of sensors exist with a variety of readouts, with one of the most widely used platforms being fluorescent sensors. Of these, genetically encoded sensors are advantageous for their versatility, modularity, and tunability. In this review we outline different genetically encoded fluorescent sensor platforms and their protein and peptide components. We particularly focus on how engineering approaches vary among different sensor platforms and how new technologies such as novel fluorescent proteins (FPs) have been used to generate and optimize sensors. We also provide interesting examples of the range of sensors developed over the last 20 years. For the purposes of this review, we define “genetically encoded” to mean that sensors require the addition of no exogenous components, such as unnatural amino acids.

2. FLUORESCENT PROTEINS The most important components of genetically encoded fluorescent sensors are FPs. A large number of FPs have been discovered and developed over the past two decades, beginning with the cloning, expression, and optimization of green fluorescent protein (GFP) from Aequorea victoria in the 1990s (Tsien, 1998). These proteins fit under two broad categories: those that generate an intrinsic chromophore during folding and maturation, and those that bind an exogenous chemical chromophore from the cellular environment. The first category includes by far the most widely used FPs in sensors, although in the past decade innovations in extrinsic chromophore FPs have led to their increased utility, especially in circumstances where oxygen requirements or chromophore maturation kinetics do not favor intrinsic chromophore FPs. FPs are available in colors spanning the visible range of the spectrum, and each has a number of properties that are relevant to their use in sensors and in cells. Factors such as quantum yield (φ), extinction coefficient (ε),

Genetically Encoded Fluorescent Sensors

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brightness, and photostability affect how effectively FPs can be visualized for single or repeated measurements. Additionally, the pKa of an FP chromophore and redox sensitivity of the FP affect its photophysics in different in vitro and in vivo environments. Finally, whether FPs are monomeric or tend to oligomerize can substantially change how they operate in sensors, as well as whether they perturb the physiology of cells. All of these properties have been heavily engineered and optimized to generate satisfactory FPs for different types of applications.

2.1 Intrinsic Chromophore FPs The precursors for most intrinsic chromophore FPs were isolated from marine organisms such as jellyfish, coral, and sea anemone (Chudakov, Matz, Lukyanov, & Lukyanov, 2010). The first engineered FPs were derived from GFP, with mutations to improve photostability, brightness, folding, and monomericity, as well as chromophore mutations that altered FP color (Chudakov et al., 2010; Cormack, Valdivia, & Falkow, 1996; Heim, Cubitt, & Tsien, 1995; Zacharias, Violin, Newton, & Tsien, 2002). Since then, several lineages of intrinsic chromophore FPs have emerged and been actively pursued, leading to a wide variety of proteins with different properties (Fig. 1; Table 1). Intrinsic chromophore FPs constitute the bulk of FPs in sensors, due to their extensive characterization, spectral tunability, biophysical stability, and robustness across model systems. There are many excellent reviews of intrinsic chromophore FPs, and we refer the reader to them for more information (Chudakov et al., 2010; Merola et al., 2014; Stepanenko et al., 2011; Subach & Verkhusha, 2012). Recent years have seen three major efforts in FP development. The first is the engineering of better FPs for use in F€ orster resonance energy transfer (FRET) sensors (see Section 3.1.5). The second effort is the generation of brighter and more photostable red and near-infrared (IR) FPs, which have particular use for imaging in vivo (Ng & Lin, 2016). Light of longer wavelengths experiences less scattering and less absorption by endogenous molecules in biological systems, and thus red FPs have a greater signal-to-noise ratio in thick samples such as tissue. The third effort is the development of FP variants that are better suited for different intracellular environments, such as through removal of redox-sensitive surface residues (Costantini et al., 2015; Costantini & Snapp, 2013). FPs developed through these three initiatives have already found use in sensors due to their optimized properties, and further FP development will no doubt lead to further advancement of sensors.

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Fig. 1 Timeline of development of major sensor fluorescent proteins. FPs are sorted into general colors but are not ordered by wavelength. Large text indicates a naturally isolated parent FP, and * specifies that the parent FP was engineered into the indicated FP in the same publication.

Table 1 lists common intrinsic chromophore FPs, many of which of been incorporated into sensors.

2.2 Extrinsic Chromophore FPs As with intrinsic chromophore FPs, proteins in this category have been identified as naturally derived FPs and have been engineered to be practically useful for scientific applications (Table 2) (Shcherbakova, Shemetov, Kaberniuk, & Verkhusha, 2015). Extrinsic chromophore FPs can have significant advantages over intrinsic chromophore FPs, including smaller size, fluorescence under anaerobic conditions, or more red-shifted wavelengths. They are, however, less fully characterized and optimized than intrinsic chromophore FPs. Proteins binding the cofactor flavin mononucleotide (FMN) occur naturally in bacteria, plants, and fungi, and have been heavily developed as optogenetic actuators. A subset of these proteins have specific regions

Table 1 Properties of Common Sensor Intrinsic Chromophore Fluorescent Proteins Brightnessa  1 1  M cm ε Photostabilityb λex/λem 1000 (nm) φ (M1  cm1 ) (s) pKa FP

OSER Maturation Scorec Time (h) (%)

EBFP2

383/448 0.56 32,000

17.9

15.31

4.5

0.42

57.0

Ai, Shaner, Cheng, Tsien, and Campbell (2007)

mTagBFP2

399/454 0.64 50,600

32.4

6.21

2.7

0.20

49.8

Subach, Cranfill, Davidson, and Verkhusha (2011)

mTagBFP

399/456 0.63 52,000

32.8

ND

2.7

0.22

ND

Subach et al. (2008)

mTurquoise

434/474 0.84 30,000

25.2

391.51

4.5

ND

93.3

Goedhart et al. (2010)

mTurquoise2 434/474 0.93 30,000

27.9

71.71

3.1

ND

93.8

Goedhart et al. (2012)

Cerulean

433/475 0.62 43,000

26.7

74.63 (mCerulean)

4.7

ND

78.3 (92.6)

Rizzo, Springer, Granada, and Piston (2004)

mCerulean3

433/475 0.87 40,000

34.8

76.83

3.2

ND

91.0

Markwardt et al. (2011)

ECFP

434/477 0.40 32,500

13.0

ND

4.7

ND

ND

Shaner, Steinbach, and Tsien (2005)

CyPet

435/477 0.51 35,000

17.9

ND

5.0

ND

94.0

Nguyen and Daugherty (2005)

mTFP1

462/492 0.85 64,000

54.4

72.34

4.3

ND

92.0

Ai, Henderson, Remington, and Campbell (2006)

References

Continued

Table 1 Properties of Common Sensor Intrinsic Chromophore Fluorescent Proteins—cont’d Brightness OSER  1 1  M cm ε Photostability Maturation Score λex/λem 1000 (%) (s) pKa Time (h) (nm) φ (M1  cm1 ) FP

References

EGFP

489/509 0.60 55,000

33.0

179.21

5.9

0.42

76.5 (98.1)

Heim et al. (1995)

Clover

505/515 0.76 111,000

84.4

61.83

6.2

0.50

72.9 (90.5)

Lam et al. (2012)

mClover3

506/518 0.78 109,000

85.0

ND

6.5

ND

ND

Bajar, Wang, Lam, et al. (2016)

mNeonGreen 506/517 0.80 116,000

92.8

197.22

5.7