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Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved. Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers, Incorporated,

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved. Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

BIOTECHNOLOGY IN AGRICULTURE, INDUSTRY AND MEDICINE SERIES

CARBOHYDRATE BINDING MODULES: FUNCTIONS AND

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

APPLICATIONS

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Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

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BIOTECHNOLOGY IN AGRICULTURE, INDUSTRY AND MEDICINE SERIES

CARBOHYDRATE BINDING MODULES: FUNCTIONS AND

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

APPLICATIONS

SUSANA MOREIRA AND

MIGUEL GAMA EDITORS

Nova Science Publishers, Inc. New York

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

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CONTENTS

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Preface

xi

Chapter 1

Introduction

1

Chapter 2

The CBM Story

3

Chapter 3

CBM Classification

5

Chapter 4

CBMs at Work

11

Chapter 5

CBMs and Physiologic Function

17

Chapter 6

CBMs Applications

25

Chapter 7

Future Perspectives

37

References

39

Index

57

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

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PREFACE Carbohydrate-active enzymes (CAZymes) are associated to the synthesis and breakdown of complex carbohydrates and glycoconjugates. CAZymes, beside the catalytic domain (CD), usually present a substrate-binding module named carbohydrate-binding module (CBM), which has independent fold and function. Nearly 7% of the CAZymes contain at least one CBM module. Presently, 59 CBMs families are described in the CAZy database (http://www.cazy.org/), presenting considerable heterogeneity in binding specificity, towards crystalline, amorphous and soluble polysaccharides, both between and within the families. CBMs are known to potentiate the activity of many enzymes, by targeting and promoting a prolonged interaction with the substrate. Since CBMs are functional and structurally independent of the other protein modules, several applications have been described using CBMs obtained by enzyme proteolysis or by DNA recombinant technology. The present revision focus on recent developments on CBMs applications in the biomedical, biological and biotechnological fields.

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Chapter 1

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INTRODUCTION Carbohydrates play an important role in many biological and biochemical processes, including fertilization 1-3 , cell differentiation and maturation [4, 5], protein folding and degradation [6]. Carbohydrates are also involved in a variety of recognition events, such as cell-cell and cell-matrix interactions [7, 8]. Many of these are immunologically relevant processes, namely inflammation [9], host-pathogen interactions [10], immune response [11] and health disorders, such as arthritis, Alzheimer‘s disease [8], among others. Carbohydrate-active enzymes (CAZymes) play key roles in glycobiology. They are involved in the synthesis and degradation of complex carbohydrates and glyco-conjugates. CAZymes are classified in families according to the amino-acid sequence, correlating enzymes mechanism and folding rather than substrate specificity (http://www.cazy.org/). CAZymes may exhibit a modular structure, a module being defined as a structural and functional unit. These enzymes present, besides a catalytic domain (CD), a substrate-binding module named carbohydrate-binding module (CBM), the two modules being connected by a linker region [12, 13]. CBMs fold autonomously and, although not having enzymatic activity per se, are known to potentiate the activity of many enzymes, by targeting to and promoting a prolonged interaction with the substrate. The present revision does not include a description of CBM structures. Boraston et al published, recently, an excellent and comprehensive review on this subject [12]. Instead, we focus on recent developments on CBMs applications in the biomedical, biological and biotechnological fields.

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Chapter 2

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THE CBM STORY The first CBM was described in 1986 by Tilbeurgh and coworkers [1417]. These authors obtained two peptides by treating a cellulase from Trichoderma reesei with a protease; the higher molecular weight peptide retained the cellulolytic activity, while the smaller one exhibited cellulose affinity, therefore being designated a cellulose-binding domain. Later on, other CBM with different specificities were described. ―Cellulose-binding domain‖ are thus a kind of a more general class of proteins, the ―carbohydrate binding modules‖ [18, 19]. CBMs are present in a large variety of enzymes, with different functions and substrate affinities, crossing a wide range of species, from archea, bacteria and virus to eukaryotic organisms, including fungi, plant and mammalian. The CBM specificities include crystalline cellulose, noncrystalline cellulose, chitin, β-1,3-glucans and β-1,3-1,4-mixed linkage glucans, xylan, mannan, galactan and starch [12]. Furthermore, some CBMs display ‗lectin-like‘ specificity, binding to a variety of cell-surface glycans [20]. The number of CBM families is still growing and since the last review on the subject [12] more than 10 new families were described. Recent findings establish a connection between CBMs and host-pathogen interactions [21], Ngycosylation in eukaryotic organisms [22], cell energy balance [23], among other functions. The knowledge of the CBM structures, elucidating their function and role in nature, may give rise to new biotechnological applications.

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Chapter 3

CBM CLASSIFICATION

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3.1. CBM FAMILIES More than 300 proteins are currently classified in the CAZy database, including glycoside hydrolases (GHs), glicosyl transferases (GTs), polysaccharide lyases (PLs) and carbohydrate esterases (CEs). Usually, CAZymes present a modular structure, nearly 7% of the enzymes having at least one carbohydrate-binding module [13]. CBMs are also classified in families based on sequence similarities. Presently, 59 CBMs families are described in the CAZy database (http://www.cazy.org/). There is considerable heterogeneity in binding specificity, towards crystalline, amorphous and soluble polysaccharides, both between and within the families [12, 18, 24, 25]. A CBM is defined as a contiguous amino acid sequence within a carbohydrateactive enzyme, with a discreet fold having carbohydrate-binding activity [19]. CBMs contain from 30 to about 200 amino acids and exist as a single, double, or triple domain in proteins. The location within the parental protein can be either C- or N-terminal; occasionally, the CBM is centrally positioned within the polypeptide chain [26, 27]. A few exceptions include 1) CBMs that integrate the cellulosomal scaffoldin proteins and 2) those not associated with catalytic domains (rare instances of independent putative CBMs have been described) [12, 28, 29]. Besides having modular architecture with independent structure and function, in the more general case integrating a protein with catalytic activity, CBMs are distinguishable from other non-catalytic sugar binding proteins (such as lectins and sugar transport proteins) by the scarcity of hydrogen bonds between CBMs and their target ligands; instead, binding is dominated by hydrophobic interactions [12].

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The three-dimensional (3D) structures indicate that CBMs from different families share structural similarity. The carbohydrate binding capacity can be attributed, at least in part, to several aromatic amino acids that constitute the hydrophobic surface [19, 30, 31]. Other features are also important for CBMs or CAZymes activity, namely the electrostatic environment (pH, ion strength) and the presence of a linker [32, 33]. For instance, the enzymatic activity of many different cellulolytic enzymes is affected by the deletion, shortening or lengthening of the linker region bridging the CBM and catalytic modules [3337]. Such findings suggest that the two domains act in concert on the cellulose surface during catalysis, and that a flexible linker is needed for full cellulolytic activity.

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3.1.1. Cellulosomes Cellulosomes are extracellular multiprotein complexes first identified in early 1980s, on the thermophilic anaerobic bacteria Clostridium thermocellum. Since then, several other cellulolytic bacteria and fungi have been reported to produce cellulosomes [38]. In 1999, a cellulosome holding a glycosyl hydrolase in the scaffoldin subunity was described, and later on Xu and colleagues (2004) reported another scaffoldin protein from a Bacteroides cellulosolvens cellulosome that includes a cellulase [38-43]. In general, two major types of subunit compose cellulosomes: the noncatalytic scaffoldin(s) and the catalytically active components. Each of these structures may be quite complex. The assembly of the cellulosome is facilitated by the high-affinity recognition between the scaffoldin cohesin and the enzymes dockerin modules. The scaffoldin often contains multiple cohesin modules, thereby enabling numerous different enzymes to be assembled into the cellulosome complex. In addition, in some species, such as Acetivibrio cellulolyticus, the cellulosomes present multiple scaffoldins with different cohesins [41]. The interaction cohesin-dockerins is type and specie-specific. Another important cellulosomal component is the cellulose-specific binding module, the major determinant of substrate recognition. Only a few enzymes in cellulosomes contain a CBM; this is normally present in the scaffoldin protein [30, 38, 40, 44]. As shown for the first time by Goldstein and colleagues, the cellulose-binding protein A (CbpA) from C. cellulovorans, is a functionally independent domain of the scaffoldin protein [45]. Later on, Fierobe and coworkers, using a recombinant engineered cellulosome, showed that the proximity of the cellulosomal enzymes and the presence of the CBM3

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CBM Classification

7

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in the scaffoldin is responsible for the synergy among the components, resulting in the efficient degradation of the native substrate [46].

Figure 1. Schematic representation of a cellulosome attached to the cell membrane. CD- catalytic domain; D-dockerin; C- cohesin, A- anchoring protein.

3.2. CBM TYPES The CBMs may also be classified according to the topology of the binding sites, reflecting the macromolecular structure of the target ligand [12, 18]. Despite the large variability of carbohydrate structures, three types of binding topologies have been identified. This classification is based on both structural and functional similarities. Although the three-dimensional (3D) structure of a number of CBMs has been solved, most CBMs have not been functionally characterized as yet. Furthermore, the binding pattern of CBMs determined so far vary widely, even within each family. However, it was shown that the modules are composed almost exclusively of β-strands arranged in a ―jelly roll‖ motif, whose topography reflects the macroscopic nature of the target substrate. CBMs with this fold recognize several polysaccharides: crystalline

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Susana Moreira and Miguel Gama

and non-crystalline cellulose, chitin, -1-3-glucans and -(1-3)-(1-4)-mixed glucans, xylan, mannan, galactan, and starch. Some CBMs display ‗lectin-like‘ specificity, binding to a variety of cell-surface glycans [12, 18, 47]. Other families of -sandwich CBMs are beginning to emerge with more complex glycan-binding specificities [48-51]. Based on the macroscopic nature of the target ligand, a classification of CBMs in three types, A, B or C, has been proposed. Table 1 presents the CBM families and corresponding type, A B or C. It should be noted that CBMs with type A and B-topology are found in the same family, while others still remains to be classified. Table 1. CBM types and families CBMs Types

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Families

A

B

1, 2, 3, 5, 10 49

4, 6, 11, 15, 17, 22, 27, 28, 29, 30, 35, 36, 44 (?) 2, 20, 25, 26, 34

C

9, 13, 14, 18, 32, 40, 42

Unknown 8, 12, 16, 19, 21, 23, 24, 31, 33, 37, 38, 39, 41, 43

3.2.1. Type A CBMs Type A CBMs, with affinity for crystalline cellulose and chitin, display aromatic amino acid residues forming a planar hydrophobic surface that interacts with the glucosyl-pyranose ring of the substrate. These CBMs recognize multiple cellulose chains and strongly prefer insoluble microfibrils, such as cellulose or chitin, to soluble polysaccharides [12, 18, 19, 52].

3.2.2. Type B CBMs Type B, the commonest class of CBMs, bind less-ordered plant structural polysaccharides such as amorphous cellulose, mannan, or xylan [12]. Conversely to type A, type B CBMs have a cleft that accommodates a single chain of the poly/oligosaccharide ligand [53], comprising several sub-sites able to interact with the individual sugar units of the polymeric ligand.

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CBM Classification

9

Although ligands are recognized by aromatic side chains, similarly to type A CBMs, the side chains of tryptophan and tyrosine – and less commonly phenylalanine - form planar, twisted or sandwich platforms for ligand binding [50]. For instance, CBM4 from xylanase of Rhodothermis marinus, a type B CBM, has a binding groove that recognizes a single polysaccharide strand [18, 54, 55]. Several applications of the CBM fused to other peptides by recombinant DNA technology were described (see below under the topic CBM applications).

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3.2.3. Type C CBMs Type C CBMs have a solvent-exposed binding pocket or blind canyon, small binding sites which interact with mono or disaccharides. Thus, these CBMs are lectin-like, lacking the extended binding site grooves present in type B CBMs [12]. Indeed, type C proteins (i.e. CBM13, 14 and 18 families) were initially identified as lectins. Indeed, both kinds of protein are thought to share similar evolutionary origins. They are involved in toxin delivery, oligosaccharide synthesis, and in host-microbe interaction processes [12, 56]. For example, the β-trefoil fold of CBM13 is classified into the ‗Ricin-Blike family‘ along with a bona fide lectin (ricin toxin B-chain) [57]. CBM42 also has structural similarity to ricin toxin B-chain, binding to small sugar units and displaying multivalency [58]. CBMs from families 6, 32 and 36 are structurally very similar to fucosespecific lectin of Anguilla anguilla, especially regarding the location of their metal ion and carbohydrate-binding sites [59]. Recently, two members of family CBM32 functionally related to lectins were described: they are galacturonic acid-binding proteins, present in the bacterial periplasmic space, that increase the substrate accessibility for pectin-degrading enzymes; however, remarkably, their action is independent of any CAZyme [48, 51].

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Chapter 4

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CBMS AT WORK In general, CBMs are linked to glycoside hydrolases that degrade insoluble polysaccharides. Although many of these modules target components of the plant cell wall or insoluble storage polysaccharides (cellulose, starch, glycogen), CBMs also bind soluble oligosaccharides such as malto-oligosaccharide [12]. Indeed, the non-catalytic CBMs are recognized as an essential component of several CAZymes and are thought to have three primary functions: proximity effects, substrate targeting and microcrystallite disruption [18, 52, 60, 61]. More recently, multivalency was also described for tandem CBMs [62, 63]. These functions are important in several biological mechanisms, such as substrate binding, mediation of protein-protein interactions or cell surface anchoring. Recently, putative cellulose-binding modules that do not bind cellulose were described. Three homologous CBM3b modules from A. cellulolyticus and C. thermocellum were over-expressed, and surprisingly none bound to cellulosic substrates [64]. These results raise fundamental questions concerning the possible role(s) of the newly described CBMs. Phylogenetic analysis and preliminary site-directed mutagenesis studies suggest that the status of the family-3 CBMs and of the family-9 glycoside hydrolases is much more intricate and diverse than hitherto considered [64].

4.1. THE PROXIMITY EFFECT CBMs promote the association of the enzyme with the substrate, insuring a prolonged contact, and thereby increasing their effective concentration (proximity effect – Figure 2) [52, 65]. In fact, several studies show that

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Susana Moreira and Miguel Gama

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enzymes fail to effectively perform when the CBM is removed by proteolysis or by recombinant DNA technology [12, 19, 66-69]. This effect is observed mostly in enzymes that act on insoluble substrates and in cellulosomes. This is the case of CBM3 from C. thermocellum, responsible for the cellulosome binding to the insoluble cellulose substrate [12, 70, 71].

Figure 2. Schematic representation of the CBM mediated proximity effect. CAZymes with CBMs are able to bind to the insoluble substrates (such as crystalline cellulose) increasing the effective concentration of enzyme on substrate.

4.2. THE TARGETING EFFECT CBMs have been shown to have selective substrate affinity, distinguishing different crystalline, amorphous, soluble and non-soluble polysaccharides (targeting function – Figure 3) [26, 68, 72-74]. In 2004, Boraston et al reviewed the mechanisms of polysaccharide recognition [18]. Since then, other CBMs with novel specificities were described. For instance, Henshaw et al showed that family 6 CBMs, present in two different -agarases, bind

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CBM at Work

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specifically to the non-reducing end of agarose chains, recognizing only the first repeat of the disaccharide [61]. Recently, the high-resolution crystal structures of two CBM51 members, from two enzymes of C. perfringens, showed that they have highly similar -sandwich folds. However, in spite of the structural similarity, one of the CBMs bind galactose residues, whereas the other revealed specificity for the blood group A/B antigens through nonconserved interactions [48]. The data suggest that CBMs have fine specificity for polysaccharide substructures. Thus, CBMs may be highly specific, subtle structural differences leading to diverse ligand specificity. This makes them an attractive system for biotechnological applications, namely as tools for the elucidation of protein-carbohydrate interaction mechanisms and as probes to identify different polysaccharides in plant cell-walls [75].

Figure 3. Schematic representation of the targeting effect of CBMs, showing the specificity of the CBM type A for insoluble subtract (such as crystalline cellulose) and CBM type B for soluble derivates of cellulose (such as cellooligosaccharides).

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4.3. THE DISRUPTIVE EFFECT The concept of the CBM disrupting function (Figure 4), rendering the substrate more susceptible to enzymatic hydrolysis, emerged several years ago [18, 70]. It was first demonstrated in 1991, by Din et al. The non-catalytic cellulose-binding domain, isolated by these authors from endoglucanase A (Cellulomonas fimi), was able to disrupt the cellulose fibers, releasing small particles. Further, it was showed that the isolated catalytic domain did not disrupt the fibril structure, rather polishing the fibers surface [76]. Other cellulase-associated CBMs with similar effect on cellulose fibers have been described [77]. Recently, it was showed that the CBM from CBHI (cellobiohydrolase I from T. pseudokoningii S-38) not only addresses the enzyme to the cellulose fibrils, but it also is involved in the structural disruption of the cellulose fiber surface [78]. The disruption effect was also reported for starch-binding modules [79] and for expansins, which have significant sequence identity with microbial cellulases [71, 80]. Recently, Vaaje-Kolstad and colleagues demonstrated that also chitinbinding modules have similar disruption ability. They showed that crystalline chitin is disrupted by a non-catalytic protein, leading to an increase in substrate access for a range of chitinases [63]. The modification of cellulose fibers with CBMs may lead to improved properties of textile and paper pulps [81].

Figure 4. Schematic representation of the disruptive effect of the CBMs on polysaccharide fibers.

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CBM at Work

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4.4. THE AVIDITY EFFECT CBMs can be present in single, tandem or multiples copies within the enzymes architecture [19, 82]. It has been shown that they can bind their specific glycan targets when isolated from the parent molecule, behaving in a cooperative manner when organized in tandem [62, 83]. Boraston and coworkers identified a family 6 CBM present as a triplet in C. stercorarium. The multiple modules act cooperatively in the binding process. It has been suggested that the duplication or triplication of CBMs may, evolutionary, balance the loss of binding affinity of thermophilic glycosyl hydrolases at higher temperatures [62]. The analysis of CAZymes showed that the same enzyme maybe linked to several CBMs (CBM multimodularity), with similar or dissimilar binding specificity. The authors speculate that the homogenous multimodularity increases the avidity of the CAZyme for the substrate, while heterogeneous multimodularity allows the enzyme to bind heterogeneous substrates [48, 51]. Recently, a recombinant protein containing tandem repeats of the CBM40 from a V. cholerae sialidase was constructed. Identical copies of CBM40 can be fused and manipulated in order to enhance its affinity through avidity [84]. This approach may be used for the creation of high affinity, multivalent CBMs, that may have broad application in glycobiology.

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Chapter 5

CBMS AND PHYSIOLOGIC FUNCTION Protein-carbohydrate recognition plays a pivotal role in key biological processes. These macromolecular interactions are central in host-pathogen recognition events, cell–cell communication, cellular defense mechanisms, protein trafficking, and on carbon recycling through the degradation of the plant cell wall.

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5.1. CBMS IN PROTEIN TURNOVER The protein turnover is an important mechanism for the regulation of numerous cellular processes. A major proteolytic route in eukaryotes involves ubiquitin (a highly conserved protein ubiquitously expressed in eukaryotes) and the 26S proteosome [6]. In most cases, selective recognition of the target proteins relies on protein–protein interactions mediated by the C-terminal domain of the F-box proteins. In mammals, the occurrence of F-box proteins with a C-terminal SBD (sugar-binding domain) that specifically interacts with high-mannose N-glycans on target glycoproteins has been documented [5]. The identification and characterization of sugar-binding F-box proteins demonstrated that also protein–carbohydrate interactions trigger the ubiquitin/proteasome pathway [6]. Recently, a close structural similarity of the protein malectin to CBMs of bacterial glycoside hydrolases was proposed. Malectin is a highly conserved protein anchored on the ER membrane (endoplasmic reticulum), with remarkable selectivity for Glc2-N-glycan, playing a role in the pathway of Nglycosylation. It has been speculated that malectin may function as a chaperon,

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or recruiting chaperons to protect the nascent polypeptide against aggregation, during the sensitive early synthesis period [22].

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5. 2. CBMS IN ENERGY BALANCE AND DISEASES CBMs are also probably involved in the degradation of complex glycans, in human hosts, by glycoside hydrolases from pathogenic bacteria [85-87]. Recently, new CBM families have been discovered in secreted or cell surfaceassociated glycoside hydrolases from bacteria. These enzymes are often key virulence factors in pathogenesis [48, 88]. CBMs also play a role in several cellular mechanisms related with energy balance and disease. Recently, McBride and coworkers showed that the AMPK (AMP-activated protein kinase involved in energy balance at single cell and whole-body levels) is inhibited by glycogen and other oligosaccharides with -1-6 branches, via its glycogen-binding domain (GBD) present in -subunity [23]. The glycogen-binding domain has been reclassified as a member of the CBM48 [89]. It binds preferably oligosaccharides with more than five glucose units, but also tri, di, and monosaccharides. The comprehensive characterization of the CBM48 ligand recognition and binding may reveal important clues for the regulation of AMPK and its role in the cell. Another CBM with glycogen affinity belongs to laforin phosphatase, which is implied in a human disorder [26]. Several mutations in the N-terminal CBM were described [90]. The laforin‘s CBM plays a role in protein dimerization [91], subtract binding [26], and interaction with malin (a single subunit E3 ubiquitin ligase necessary and sufficient to mediate ubiquitination) [92, 93]. It was demonstrated that the formation of the laforin-malin complex is a regulated process, where AMPK also plays a critical role [94]. Since laforin is involved in the glycogen metabolism, it might confer cancer resistance to energy deprivation-induced apoptosis [95]. Moreover, Gentry et al showed that the Plantae kingdom, which lacks laforin, possesses a protein with laforin-like properties called starch excess 4 (SEX4). Laforin and SEX4 (from Arabidopsis thaliana) are functional equivalents, suggesting that phosphatase laforin crosses evolutionary boundaries [96]. The 3D structure of CBMs may elucidate the binding mechanism and specificity of several enzymes. New potential applications may emerge from this information. For example, solving the 3D structure of CBM43 from CtDOle e 9 (an olive pollen allergen belonging to group 2 of pathogenesis-related

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proteins) may be a relevant contribution for the understanding of the underlying biochemical function and help determining possible structure– allergenicity relationships, enabling the design of hypoallergenic peptides. Also, they may help elucidating the molecular basis of allergenicity and explaining why highly homologous proteins are allergenic while others are not [97, 98].

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5.3. CBMS ROLES IN PLANT: GROWTH, DEFENSE AND DEGRADATION Cellulose is the major structural component of terrestrial and marine plant cell walls, although it is also produced by some marine animals and bacteria. The dimensions of cellulose fibers and the proportion of the crystalline and amorphous regions vary depending on its origin; moreover, the cellulose fibers in the higher plant cell walls are "encapsulated" by hemicellulose and lignin [29, 40, 99]. Therefore, there are a large number of enzymes acting on cellulose, due to the large variety of cellulosic materials and its different properties [29]. There are three different types of cellulases: endoglucanases (EG), cellobiohydrolases (CBH) and β-glucosidases. Together, they hydrolyze insoluble cellulose, both amorphous and crystalline, in a synergistic way, which is particularly relevant in the case of crystalline cellulose [100]. Considering that cellulose is one of the most abundant polymers in nature, it is not surprising to find organisms that modify and degrade cellulose across kingdoms and environments.

5.3.1 CBMs Acting on Polysaccharides: Cellulose, Starch, Chitin As referred previously, two main types of cellulolytic systems are currently recognized. Those based on ‗free‘, soluble enzymes, produced mostly by aerobic microbes that secrete individual cellulases, which act synergistically on native cellulose; and those based on complexes of cellulolytic enzymes, or ‗cellulosomes‘, produced by some anaerobic bacteria and fungi, which are usually attached to the outer surface of the microorganism [40, 101]. CBMs play a role in the phase transfer of a soluble free enzyme onto the insoluble substrate 68, 69 . CBMs are present in several polysaccharide-degrading enzymes, namely in hemicellulases [56, 58, 102],

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endomannanases [12], xylanases [56, 103], acetyl-xylanesterases [104] and glucosidases [71]. For many years, plant cellulases were thought, contrarily to bacteria and fungi cellulases, not to have CBMs. Nevertheless, putative CBM sequences were found in a tomato cellulose, in 1998 [105]. Since then, putative CBMs were described in peach [106], pear [107], strawberry [108] and mango [109]. However, only recently the first CBM from plant was described (present in a tomato cellulase), and a new CBM family was born (CBM49) [110]. The tomato cellulase is highly sensitive to proteolysis in the linker region, when expressed in a heterologous system. Therefore, the respective sequence was fused with a catalytic domain of another well studied cellulase, from T. fusca. It was shown that the fusion enzyme was able to bind and hydrolyze crystalline cellulose. CBMs are thus essential for the effective degradation of crystalline cellulose, but they are also involved in plant cell wall relaxation, expansion and biosynthesis. During the growth processes, plants respond to many different internal (metabolites, hormones) and external (light, water) signals. In many cases, the loosening of the cell wall arises as an answer to these signals, in order to enable turgor-driven cell expansion [71]. To enable cell wall loosening, the polysaccharide matrix has to be metabolized. Several enzymes play a role in this controlled process [111]. In fact, some of the plant cellulolytic enzymes are structure and functionally similar to those find in microorganisms. Besides its role on the cell wall degradation, several studies showed also the effects of CBMs on plant growth, development, and defense. Valdez et al presented the first report characterizing the role and function of CBMs in the enzymatic machinery of anabolic processes. They showed the importance of the N-terminal SBDs (CBM53) in the binding of starch and in the regulation and catalysis of starch synthase III from Arabidopsis thaliana [112, 113]. CBMs are also found in starch degrading enzymes, namely -amylases, amylases and glucoamylases, which are widely distributed throughout many species of animals, plants and microorganisms [114]. Binding of the starchdegrading enzymes to its substrate is a critical step in starch hydrolysis, since it involves the phase transfer of a soluble enzyme to the insoluble substrate. Today, it is accepted that, similarly to other binding modules, SBMs play a pivotal role in the phase transfer [79]. The expression of artificial tandem repeats of a family 20 SBM, in an amylose-free potato mutant, resulted in the differential accumulation of SBM in the transgenic starch granules and in the production of granules with a different size [115]. Genetically fused SBMs can

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also be used as tools to anchor proteins (that do not have affinity for starch granules) inside starch granules, during their biosynthesis [116]. Modification of starch biosynthesis holds an enormous potential for the production of granules or polymers with new functions [117]. The understanding of the CBM-ligand interaction mechanisms may lead to the development of useful tolls for applications aiming at modulating the architecture of individual cells and even of entire organisms.

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5.3.2. CBMs in Biomass Conversion A significant attention is focused on the quest to replace petroleum with plant biomass for chemical and fuel production. Polysaccharide-degrading enzymes are key tools for this purpose. However, it has long been recognized that crystalline cellulose is recalcitrant to enzymatic hydrolysis, a major limitation in the production of fermentable sugars from plant biomass; therefore, CBMs that target enzymes to crystalline cellulose, promoting the hydrolytic activity, are particularly relevant for biomass conversion [18]. It has been shown that enzymes assembled in a scaffoldin protein act synergistically on the substrate hydrolysis. In addition, the CBM present in many scaffoldin proteins bind the enzymatic complex to the cellulose [40]; therefore, enzymatic complexes may be engineered as to optimize the enzymatic activities and the biomass conversion. In vitro evolution strategies utilize genes encoding thermostable proteins as suitable scaffolds. When developing thermostable enzyme, the starting material is an already stable backbone, thus improving the odds for evolution to optimize function at selected conditions for activity. An example of the application of this strategy is the diversification of the binding specificity of xylanase‘s CBM4-2, from the thermophilic bacterium Rhodothermus marinus. Using this CBM, which has both high thermostability and good productivity in E. coli expression systems, a single heat stable protein could be developed with specificity towards different carbohydrate polymers [118], as well as towards a glycoprotein [119], demonstrating the potential of molecular biology for the development of different selective specificities, starting from a single protein scaffold [120]. The CBMs found in plant proteins, for instance tomato [110], opens new prospects for the use of CBMs in biofuel production. Plants with high expression levels of these proteins maybe engineered, allowing a more efficient ethanol production. For instance, the over-expression of CBM or

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cellulase-containing CBM in vivo may modulate the cellulose structure as to become more accessible to other hydrolytic enzymes. Furthermore, biofuel research may also help uncovering exciting new uses for these enzymes.

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5. 4. PLANT DEVELOPMENT The interaction between cellulose microfibrils and the hemicellulosexyloglucan network is believed to represent the major load-bearing structure in the primary cell wall. In physical terms, cell shape and size are governed by the mechanics of the cell wall. Cell expansion occurs via strictly regulated reorientation of the wall components and several enzymes play a rule in this mechanism [121]. In a in vitro study, it was showed that the cellulose-binding domain from C. cellulovorans modulates the elongation of different plant cells [122]. Further, using a model system of Acetobacter xylinum, it was shown that CBM enhances cellulose synthesis, which is a limiting factor in plant cell elongation [122]. In addition, there are several studies in vivo, using transgenic plants, showing that CBM-expressing plants have their growth behavior altered [123, 124]. For instance, the transgenic potato plant (Solanum tuberosum cv. Desiree) expressing the bacterial CBM3 from the C. cellulovorans CBPA, present significantly more rapid elongation of the main stem, mass accumulation and faster growth rate at earlier stage [123]. These findings suggest that the CBM may significantly alter plant growth, both in tissue culture and in vivo, under field conditions. Besides, CBMs from cellulases and expansins also play a role in cell-wall development. Expansins are plant proteins, expressed in several tissues, which catalyze the disruption of hydrogen bonds between cellulose microfibrils and matrix polysaccharides, promoting the cell expansion. They are involved in the regulation of growth and development [71, 125]. It has been shown that the over-expression of the potato expansin CBM, in transgenic tobacco plants, alter the cell wall structure, namely, stems exhibit enlarged xylem cells and thinner cells walls. However, the plant growth was not affected by the CBM expression [124]. Mixed results have been obtained when expansin genes were overexpressed in transgenic plants. Growth of tomato plants over-expressing endogenous expansin was significantly reduced [126]. However, the height of the tomato plants was not affected by the over-expression of expansin, although leaf size was slightly reduced [127]. Over-expression of OsEXP4

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(expansin gene) resulted in pleiotropic phenotypes in adult transgenic rice plants [128]. A subpopulation of these transgenic plants was characterized by enhanced internodal elongation, while growth rate was inhibited in most of the rice transformants. The authors suggested that differences in expression levels may provide a possible explanation for these phenomena. According to this explanation, lower expression levels promote stem elongation, while higher levels promote leaf development with shorter internodes.

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5. 5. PLANT DEFENSE Among eukaryotic plant pathogens, the genus Phytophthora contains more than 60 species that are pathogenic on a wide array of plants, originating diseases economically important worldwide. The cellulose binding elicitor lectin (CBEL), from Phytophthora parasitica nicotianae, contains two cellulose binding modules belonging to family 1, found almost exclusively in fungi (not detected in higher plants). CBEL is able to bind crystalline cellulose and tobacco cell walls in vitro, in a dose-dependent manner, but in contrast with cellulases, it does not possess any detectable enzyme activity on various polysaccharides [129]. Site-directed mutagenesis of aromatic amino acid residues located within the CBMs, as well as leaf infiltration assays using mutated and truncated recombinant proteins, showed that CBMs are sufficient and necessary for the expression of genes associated to plant defense. Moreover, it has been shown that the CBM1 from swollenin (a protein first identified in the saprophytic fungus Trichoderma reesei), is essential for the protein‘s activity and capable of stimulating local defense responses in cucumber roots and leaves, affording for local protection toward Botrytis cinerea and Pseudomonas syringae pv lachrymans infection. This indicates that the CBM may be recognized by the plant as a microbe-associated molecular pattern in the Trichoderma-plant interaction [130]. However, further studies will be necessary to elucidate how CBMs act on cells-wall defense mechanisms. The understanding of responses to cell wall damages may contribute to the development of strategies for the improvement of the resistance of plants to biotic stresses [131].

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Chapter 6

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CBMS APPLICATIONS The production and process development using CBMs obtained by enzymatic hydrolysis of the enzyme-containing CBMs was described by several authors [132-134]. The recombinant DNA technology allows for several structural and functional studies, and also for different applications using recombinant proteins fused with CBMs. Different applications of CBMs have been described: improvement of fibers in textile and paper industry; tags for recombinant proteins purification and immobilization; probes for proteincarbohydrate interaction and microarrays. CBMs may also find applications in the modification of physical and chemical properties of composite materials, allowing the creation of new materials with improved properties. The CBMs expression in vivo may be also a valuable tool to modify plant characteristics, as discussed above [71]. Several studies have shown that CBMs may be used to modify the characteristics of enzymes. The basic approach in CBM engineering consist in the addition or substitution of a CBM in order to improve the enzyme stability or hydrolytic activity [135].

6.1. CBMS IN THE PAPER INDUSTRY The Kraft pulping is the predominant process used in papermaking. This process involves the high temperature cooking of wood fibers in alkali, followed by the extraction of the colored lignin, using oxidative chemicals [136]. The treatment of wood pulp with hemicellulases has been shown to be a feasible way to enhance the extraction of lignin, in the quest for environmentally benign methods of paper manufacture [55, 136]. This enzymatic pre-treatment leads either to higher final paper brightness or to a

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reduction in the consumption of bleaching chemicals. Enzymes used in pulping can be used to increase the yield of fibers, reduce the refining energy requirements and finally to provide specific modifications to the fiber. Although the effect of enzyme treatment depends on the fiber type [137], several works showed the enhancement of the kraft pulping of sycamore chips and other pulp sources using cellulase, hemicellulase, and pectinase in pulp fibers pretreatments [55, 136, 138, 139]. However, the utilization of hydrolytic enzymes in paper production often results in the loss of tensile strength along with the desired performance [140]. Since CBMs, although not having catalytic activity, can modify the cellulose and starch materials, they have been also tested in the papermaking process. Several strategies were developed using CBMs or CBMs-conjugates [139, 141, 142]. It is well known that the incorporation of secondary fiber in paper production affects the final product quality and the papermaking process. Basically, the recycled pulps have lower fiber quality (smaller fibres with lower flexibility) and higher drainage resistance. These modifications lead to reduce inter-fiber bonding and consequently lower paper strength. Secondly, the sheet formation becomes more difficult, decreasing the paper machine runnability and increasing the energy consumption in the dryers [143]. Mooney et al. reported evidence that selective digestion of the smaller fiber pulp fragments results in increased drainage [137]. However, this effect could also be attributed to removal of cellulose microfibrils from the paper fiber surfaces. In either case, care must be exercised to keep treatments at a low dose, because endoglucanases that attack amorphous cellulose also cause rapid loss of fiber strength [139]. In an attempt to avoid the strength loss, Pala et al. [143] examined the use of cellulose-binding modules isolated from cellulases, following proteolytic digestion. At low doses, CBMs increased both drainage rates and paper strength properties, but at higher dosage rates, the beneficial effect on the strength parameters was less pronounced. The authors hypothesized that the beneficial effect on strength was attributable to an increase in the microfibrilation of the fiber surface. Increased drainage, however, may also be ascribed to the residual hydrolytic activity present in the used CBM formulations. Recently, Machado et al [144] demonstrated that a recombinant CBM from C. thermocellum conjugated with PEG effectively improves the pulps drainability, without significant effects on the strength parameters. Furthermore, the authors showed that the CBM alone does not modify the pulp properties, suggesting that the improved pulp drainability, reported by several researchers, is indeed a strictly interfacial effect, surface

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hydration playing a key role. Taken together, the results suggest that CBM technology may have valuable applications in paper recycling. CBMs can also be used combined with other molecules, as CBMconjugates. Recently, Kitaoka and Tanaka described a CBM-based additive that enhances the paper strength [141]. Functional design of paper materials is in general achieved by addition of papermaking chemicals to an aqueous fiber suspension, at the wet end of a paper machine. The effect of additives is often affected by electrostatic interactions with contaminants present in this wet-end step [142]. This limitation may be circumvented through the development of CBM-based papermaking additives, for improved retention and performance. CBMs obtained by hydrolysis of cellulase with papain and chemically bound to anionic polyacrylamide, retained the ability to interact with pulp fibres, leading to a good retention and high tensile strength under wet-end conditions [142, 145]. Recombinant CBMs were also used to improve paper properties. The dry strength of a three-dimensional cellulose fiber network depends on the strength of the individual fibers, of the inter fiber bonds, and on the number and distribution of interfiber bonds. Inter-fiber bonding, which improves the stress transfer between the fibers under tensile deformation, is one of the most important factors affecting the overall stress development in the fiber web [146]. Levy et al. constructed a bifunctional protein, containing two-fused cellulose-binding modules (CBM3 from C. cellulovorans), able to mimic the chemistry of cellulose cross-linking [66], thus increasing the dry strength of paper. Interestingly, applying a single CBM to the paper also improved its mechanical properties, although to a lower extent. In addition, paper sheets treated with the fusion protein became more hydrophobic and demonstrated water-repellent properties [66]. Later on, the same authors constructed another bifunctional protein containing a cellulose and a starch-binding module. The treatment of paper fibers with the recombinant protein, together with cornstarch, improved the paper dry strength [146]. The significant improvement in the mechanical and surface properties of paper by CBMs-containing molecules demonstrates great potential for the bioengineering of novel papermodification reagents [66].

6.2. CBMS IN THE TEXTILE INDUSTRY The textile industry requires large amounts of water, energy, and auxiliary chemicals [147]. The search for environmental-friendly methods has lead to

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the utilization of enzymes. Several enzymes have been used in textile processes in order to achieve improved and fashionable fabric properties. Among other enzymes for textile processing, amylases (used for desizing), cellulases (denim finishing), laccase (decolourization of textile effluents and textile bleaching) are commercially available [148, 149].

Figure 5. Images of cotton fabrics before and after depilling treatment. Non-treated fabric (a, b), enzyme treated fabric (c, d) and CBD treated fabric (e, f) observed by electronic microscopy at 30x magnification [adapted from 154].

Textile fabric may also be treated with isolated CBMs or CBMs fused with other molecules or enzymes. Banka et al. demonstrated that a fibrilforming protein from T. reesei causes non-hydrolytic disruption of cotton fibers [150]. Lee et al. obtained images, by atomic force microscopy, of holes left in cotton fibers treated with inactivated CBH I. The holes are attributed to the penetration of fibers by the binding domain [151]. It has been shown that the surface of ramie cotton is roughened by treatments with CBM2 from C. fimi. Gilkes et al proposed that the treatment of cellulosic fibers with CBMs

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could be used in order to alter the dyeing characteristics of cellulose fibers [152]. Indeed, it was showed that CBM treatment increased the dye affinity of cotton fibers, especially in the case of acid dyes [153]. Lemos et al. (2002) developed a simple method to purify CBMs from fungal cellulases, by ultrafiltration following digestion with a protease. Using this process, it is possible to obtain gram amounts of CBMs, although with some contaminating enzymatic activity. Those CBMs were used in textile deppiling assays. The CBMs preparation - with residual hydrolytic activity achieved a superior finishing deppiling (Figure 5). Further, using CBM-FITC (Fluorescein isothiocyanate) conjugates, Ramos et al demonstrated that the surface concentration of CBMs adsorbed to cotton fibers is very high [154]. Considering these results, it seems obvious that interfacial properties should be also considered in the design of depilling treatments. Fukuda et al used a new approach for the enzymatic desizing of starched cotton cloth. Sizing is required to prevent abrasion, fluffiness, and cutting of the warp during the weaving process. Among the several desizing methods, the use of enzymes (e.g. amylase) is well known as an environmental-friendly technology [155]. Instead of using an enzyme for desizing, Fukuda et al constructed a yeast strain that codisplayed glucoamylase and CBMs on the cell surface. The yeast cell acquired specific binding ability to cotton cloth with glucoamylase activity. Furthermore, the codisplaying strain showed greater activity than a strain displaying only glucoamylase activity [156]. The development of biotechnological tools for the modification of cellulose fibers may be achieved by combining CBMs, specially cellulose binding modules, with catalytic domains of enzymes that do not normally act on insoluble substrates (e.g. laccase, pectinase or lipase), or with other functional proteins/polypeptides (e.g. hydrophobic or chemically reactive) suitable for the modification ofthe textile surfaces. Since several CBMs belong to enzymes that act in extreme conditions, the CBM fusion proteins may also improve enzyme stability [103, 135, 157, 158]. Further, CBMs can be fused with bioactive molecules in order to functionalize the fabric tissue.

6.3. CBMS IN THE FOOD INDUSTRY Enzymes have been used for more than 20 years in poultry feed, mainly to improve the digestibility of cereals with high soluble non-starchpolysaccharide (NSP) levels, such as wheat, barley, oats and rye [159, 160]. It is well established that the inclusion of cell wall hydrolases in wheat, barley

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and rye-based diets of single-stomach animals, improves the efficiency of feed utilization, enhances growth and contributes to a better use of low-cost feed ingredients [161, 162]. Several studies on the potential application of CBMs for animals feeding are available [163, 164]. CBMs anchor cellulases and hemicellulases to their target substrates, therefore eliciting efficient hydrolysis of recalcitrant polysaccharides. Recombinant derivatives of a xylanase from C. thermocellum, containing a CBM6, were used to supplement poultry cereal-based diets. The data obtained showed that birds fed on a wheat-based diet supplemented with CBM-xylanase display an increased final body weight, when compared with birds receiving the xylanase catalytic module only [163]. Recently, Ribeiro et al studied the effect of supplementing a barley-based diet with a family11 -glucan-binding domain, fused to a recombinant cellulase from C. thermocellum. The results showed that birds fed on diets supplemented with the recombinant proteins, containing the CBM11 or the commercial enzyme mixture, have improved performance when compared to birds fed with diets without the enzyme supplement [162]. Tarahomjoo et al presented a new strategy to enhance the viability of probiotics (living microbial cells as food supplement) in simulated gastric conditions. This strategy consists on the use of starch-binding modules displayed on the cell surface. It is known that starch granules partially hydrolyzed (with hollow cores) may be used to encapsulate living microbes, so protecting them from environmental stress [165, 166]. For this purpose, a protein containing the C-terminal region of a peptidoglycan hydrolase (an efficient anchoring domain to display heterologous proteins on cells) fused to the linker region and the SBM of the α-amylase (from Streptococcus bovis 148) was constructed. The fusion protein was able to bridge the cell surface of Lactobacillus casei NRRL B-441 (a well known probiotic bacteria) and corn starch. The potential usefulness of the SBM cell-surface display technique for the encapsulation of microorganisms and its delivery to the intestinal tract was demonstrated. This strategy does not involve any genetic modification of the probiotic strains [166]. Recombinant enzymes containing CBM may also find applicability on the food industry, for instance for the production of soy sauce using soybeans and optionally other vegetable ingredients, such as wheat and rice. During the production process, starch and other carbohydrates are degraded into sugars, used for aroma development by fermentation. It has been found that amylolytic enzymes comprising a CBM leads to an increased rate of starch

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hydrolysis, as compared to amylolytic enzymes without CBM, under conditions relevant for soy sauce production [167].

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6.4. CBMS AS A MICROARRAY AND PROBING TOOL Microarrays of proteins and peptides make the screening of thousands of binding events possible, in a parallel and high throughput fashion; therefore, they are emerging as a powerful tool for proteomics and clinical assays. Microarrays consist of immobilized biomolecules spatially organized on substrates such as planar surfaces (typically coated microscope glass slides), microwells or arrays of beads. Immobilized biomolecules (probes) usually include oligonucleotides, PCR products, proteins, peptides, carbohydrates and other small molecules [168]. Several strategies are described to immobilize the probe on the support, including adsorption, physical entrapment or covalent binding. The CBM based microarray technology described by some authors offer fundamental advantages over current non-DNA microarray technology, such as retention of protein functionality after immobilization, ease of fabrication, extended stability of the printed microarray, integrated test for quality control (QC) and the capacity to print test proteins without a purification step [55, 169, 170]. These features, together with the intrinsic specificity of CBMs for individual carbohydrates and the facile modification with peptides and fluorescent molecules, allow for efficient production of protein and peptide microarrays. These can be used in a variety of potential applications technically impractical via conventional microarray technologies [55]. Ofir and colleagues developed a microarray system using an affinity-based probe immobilization strategy. They fused the exceptionally stable family-3a CBM, from the cellulosome of C. thermocellum, with antibodies or peptides. The recombinant proteins were immobilized on cellulose surfaces by specific adsorption and used for serodiagnosis of human immunodeficiency virus patients [168, 170]. Recently, Haimovitz and colleagues described a microarray system to analyse the cohesin-dockerin specificity. These authors immobilized recombinant CBM-fused cohesins on cellulose-coated glass slides, to which xylanase-fused dockerin proteins were applied. The fusion of dockerins with a thermostable xylanase was performed, allowing enhanced expression and proper folding. Using this elegant approach, cross-species interactions among type-II cohesins and dockerins was shown for the first time [171].

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The plant cell wall biology studies require more sensitive and specific probes to target individual wall components. Traditionally, antibodies have been the primary workhorses for the spatial localization of cell wall polysaccharides. Currently, nearly 30 monoclonal antibodies directed toward specific arabinan, galactan, xylan, galacturonan, fucosylated xyloglucan, and cell wall glycoprotein epitopes are available, from academic and commercial sources [172]. Nevertheless, CBMs may be used for this purpose, since they present intrinsic specificity for individual carbohydrates. A quantitative fluorimetric method for the analysis of crystalline cellulose on fiber surfaces was developed. This method quantitatively shows differences in crystalline cellulose binding sites of differently processed pulp fibers. The results indicated that CBMs provide useful, novel tools for monitoring changes in carbohydrate content of non uniform substrate surfaces, for example, during wood or pulping processes and possibly also during fiber biosynthesis [169]. The CBM4-2 from xylanase of Rhodothermus marinus was synthesized and utilized in vivoas a xylan-specific protein, for the analysis of hemicelluloses in wood and fibrous materials. It is well known that the CBMs specificity may be altered by genetic engineering; in particular, the CBM4-2 was modified through direct mutagenesis. Variants with specificity for two other polysaccharides were identified using phage display technology [118].

6.5. CBMS AS A PROTEIN SOLUBILIZATION, PURIFICATION AND IMMOBILIZATION TOOL Several works describe the use of CBMs as a tag for recombinant protein purification [24, 173-178] and enzyme immobilization [179-181]. Depending on the binding reversibility, different applications may be envisioned; CBMs with ‗irreversible‘ binding has limited usefulness as an affinity tag for protein purification, because desorption may require strongly denaturing conditions. In turn, such a CBM may be a very useful tag for enzyme immobilization [182]. An obvious extension of the CBM-fusion technology is to enable a singlestep purification and immobilization of fusion proteins by generating active CBM–Protein. Moreover, the utilization of the carbohydrate affinity system, such as cellulose, is attractive because it does not require a derivatized matrix, and cellulose is available in a variety of inexpensive forms, such as preformed microporous beads, highly adsorbent sponges or cloth and microcrystalline powders [181].

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In fact, several CBMs were already commercialized as protein expression systems [179]. A cellulose-binding module from C. cellulovorans scaffoldin CbpA protein has been well characterized and commercialized as a fusion domain for protein purification, using a cellulose matrix (Novagen). In such applications, the use of CBMs offers many industrially attractive advantages. Since CBMs adsorb spontaneously to cellulose, very little or no pretreatment of the samples is required prior to immobilization [67, 183]. In addition, some CBMs seem to enhance the solubility of recombinant protein [184, 185]. Craig and colleagues described the design and application of a recombinant fusion protein containing a cellulose-binding domain (from C. cellulovorans) and an antibody-binding domain (protein LG), for direct immobilization of antibodies and cells onto regenerated cellulose hollow fiber membranes. Hollow fiber affinity cell separation is a monoclonal antibody based cell separation process. Cells are bound directly or indirectly via surface epitopes by monoclonal antibody or secondary ligand immobilized on the lumen side of hollow fibers. Deposited cells are fractionated, on the basis of adhesion strength, using the uniform shear field generated by the culture medium flowing through the hollow fiber modules with well-defined header geometry [186]. With this strategy, several problems associated to covalent binding are avoided: low coupling yield, random orientation of antibody, possible alteration of the structural properties of the hollow fiber membrane resulting from chemical cross-linking or protein degradation.

6.6. CBMS AS BIOREMEDIATION TOOL Another field for CBM application is bioremediation. Richins et al. produced a bifunctional fusion protein, consisting of an organophosphate hydrolase (OPH) linked to a Clostridium-derived cellulose-binding module. The recombinant hydrolase is highly effective in degrading organophosphate compounds. Furthermore, the CBM enable the purification and immobilization onto different cellulosic materials, in a single step [181]. In this manner, OPHactivated cellulose materials are generated for a variety of relatively low cost applications, such as reactors with immobilized enzyme for the detoxification of hazardous organophosphates [181]. In another study, Xu et al presented a strategy to remove heavy metals from contaminated waters. They reported the cloning and expression of a bifunctional fusion protein, consisting of a synthetic phytochelatin linked to a Clostridium-derived cellulose-binding domain. Once again, the CBM enabled

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Susana Moreira and Miguel Gama

purification and immobilization of the fusions onto different cellulose materials, in a single step. The immobilized sorbents were shown to be highly effective in removing cadmium present in parts per million levels [187].

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6.7. CBMS AS BIOMEDICAL TOOL Cellulose is a chemically inert matrix that has stable physical properties, as well as low affinity for non-specific protein binding. It is pharmaceutically safe and relatively inexpensive. The binding of biomolecules to cellulose through a cellulose-binding domain further enhances its potential as a scaffold or carrier material. Maurice et al fused an antigen protein (from Aeromonas salmonicida) with a CBM (from C. cellulovorans), in order to develop a vaccine suitable for fish immunization. Vaccines vary in their efficacy depending on the antigen composition and accompanying adjuvant. Studies have shown that soluble immunogens rarely induce high titers of antibodies, unless strong adjuvants are used [188]. Surprisingly, binding Orbicell cellulose beads to a recombinant protein, Maurice and colleagues obtained a significant adjuvant effect. In addition, Orbicell cellulose beads were well tolerated by the fish and no deleterious response reactions were detected [188]. Guerreiro et al recently described the expression of AMPs (antimicrobial peptides) fused with a CBM3 from C. thermocellum in a bacterial host. AMPs are cationic molecules with a wide range of antimicrobial activities. The authors suggested CBM3 as a good candidate to overcome difficulties related to the expression of these molecules, namely associated to the small size and potential toxicity for host [189]. Furthermore the authors suggested the possible use of the fusion CBM-AMP to confer antimicrobial properties to cellulosic materials. CBMs were also described as a tool to adsorb bioactive peptides to carbohydrate-based materials [190-192]. Bacterial cellulose is being studied as a biocompatible scaffold for the engineering of cartilage and blood vessels, wound dressing, guided tissue regeneration, among other applications [193]. Andrade et al cloned and expressed a recombinant protein containing a cellulose-binding module (CBM3 from C. thermocellum cellulosome) fused with a tripeptide of Arg-Gly-Asp (RGD sequence is a ligand for integrinmediated cell adhesion), showing that the bifunctional protein improved the fibroblast adhesion and spreading on bacterial cellulose [190]. Using a CBM with starch affinity (SBM20 from Bacillus sp. amylase) fused with RGD, it

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CBM Applications

35

was possible to observe similar results for fibroblast adhesion and spread on starch-based hydrogel (Figure 6) [192].

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Figure 6. Results from fibroblast adhesion on starch-based hydrogel. Top – microscopic images showing cell morphology and spread on hydrogel treated with recombinant proteins (SBM or RGD-SBM) and control hydrogel without recombinant protein and polystyrene plate. Bottom – results from viability assay of cell attached to the hydrogels or polystyrene plate [adapted from 192].

The utilization of a recombinant CBM (a domain from the Celk gene from C. thermocellum) to stabilize single-walled carbon nanotubes (SWNTs) in water was recently described [194]. After production of SWNTs, the strong non-covalent interactions give rise to aggregated material. Functional molecules including surfactants, polymers, carbohydrates, nucleic acids and peptides or proteins have been reported to debundle and suspend SWNTs via a non-covalent adsorption. A family 4 CBM, cloned and over-expressed in E. coli, was successfully used to stabilize SWNTs. However, the mechanism of SWNTs - protein interaction has not been explained. Moreover, another recombinant CBM belonging to family 3 (type A) was also tested, but it did not show binding affinity for SWNTs. The authors suggested that, beside aromatic residues, higher-order protein structure could also play a key role [194].

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Chapter 7

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FUTURE PERSPECTIVES Although the functions of CBMs were firstly related to the activity of cellulase and other enzymes, the current CBM research heads in different directions. CBMs are involved in anabolic processes (such as oligosaccharide synthesis), host-microbe interaction, toxin delivery, recognition of complex glycan present on eukaryotic cell surface and extracellular matrix. CBMs may thus be used as tools to elucidate several carbohydrate-protein interactions and targets for the modulation of those processes. The determination of the 3D structures and mechanism of action of protein modules, such as CBM from family 6 or 2a [195] is still ongoing. The finding of new 3D structures may help elucidating the evolution of CBMs. The combined effect of CBMs from glycoside hydrolases in the recognition of host glycans by bacteria for pathogenesis, colonization, as a nutritional source, and evading the host immune system, defines a new avenue of CBM research, apart from plant cell wall recognition. In recent years, besides the utilization in textile or paper industry, the CBMs are seen as tools for biomedical application. Future studies may also reveal new avenues for biotechnology applications, such as design of antibacterial or anti-carcinogenic drugs, functionaliztion of biomaterials or cloth.

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REFERENCES

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[1]

Focarelli R, Sala GB, Balasini M, Rosatia F. Carbohydrate-Mediated Sperm-Egg Interaction and Species Specificity: A Clue from the Unio elongatulus Model. Cells Tissues Organs. 2001;168:76-81. [2] Diekman AB. Glycoconjugates in sperm function and gamete interactions: how much sugar does it take to sweet-talk the egg? Cell Mol. Life Sci. 2003;60(2):298-308. [3] Flori F, Secciani F, Capone A, Paccagnini E, Caruso S, Ricci MG, et al. Menstrual cycle-related sialidase activity of the female cervical mucus is associated with exosome-like vesicles. Fertility and Sterility. 2007;88(2):1212-9. [4] Yoshida Y, Chiba T, Tokunaga F, Kawasaki H, Iwai K, Suzuki T, et al. E3 ubiquitin ligase that recognizes sugar chains. Nature. 2002;418(6896):438-42. [5] Glenn KA, Nelson RF, Wen HM, Mallinger AJ, Paulson HL. Diversity in Tissue Expression, Substrate Binding, and SCF Complex Formation for a Lectin Family of Ubiquitin Ligases. J. Biol. Chem. 2008;283(19):12717-29. [6] Lannoo N, Peumans WJ, Van Damme EJM. Do F-box proteins with a Cterminal domain homologous with the tobacco lectin play a role in protein degradation in plants? Biochem. Soc. Trans. 2008;36:843–7. [7] Lis H, Sharon N. Lectins: Carbohydrate-Specific Proteins That Mediate Cellular Recognition. Chem. Rev. 1998;98(2):637-74. [8] Lutteke T. Analysis and validation of carbohydrate three-dimensional structures. Acta Cryst. 2009;65:156–68. [9] Linden ECMV, Haan PF, Havenaar EC, van Dijk W. Inflammationinduced expression of sialyl Lewisx is not restricted to Glycoconjugate Journal. 1998;15:177-82 [10] Yagi H, Nakagawa M, Takahashi N, Kondo S, Matsubara M, Kato K. Neural complex-specific expression of xylosyl N-glycan in Ciona intestinalis. Glycobiology. 2008;18(2):145–51.

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Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

40

Susana Moreira and Miguel Gama

[11] van Kooyk Y, Rabinovich GA. Protein-glycan interactions in the control of innate and adaptive immune responses. Nat. Immunol. 2008;9(6):593601. [12] Boraston AB, van Bueren AL, Ficko-Blean E, Abbott DW. Carbohydrate–Protein Interactions: Carbohydrate-Binding Modules. In: Kamerling JP, editor. Comprehensive Glycoscience From Chemistry to Systems Biology Victoria: Elsevier Ltd.; 2007. p. 66-696. [13] Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Research. 2009;37. [14] Gilkes NR, Jervis E, Henrissat B, Tekant B, Miller RC, Warren RAJ, et al. The adsorption of a bacterial cellulase and its two isolated domains to crystalline cellulose. Journal of Biological Chemistry. 1992;267(10):6743-9 [15] Gilkes NR, Warren RA, Miller RC, Kilburn DG. Precise excision of the cellulose binding domains from two Cellulomonas fimi cellulases by a homologous protease and the effect on catalysis. The Journal of Biological Chemistry. 1988;263(21):10401-7. [16] Srisodsuk M, Lehtiõ J, M. L, Msrgolles-Clark E, Reinikainen T, Teeri TT. Trichoderma reesei cellobiohydrolase I with an endoglucanase cellulose-binding domain: action on bacterial microcrystalline cellulose. Journal of Bacteriology. 1997;57:49-57. [17] van Tilbeurgh H, Tomme P, Claeyssens M, Bhikhabhai R, Pettersson G. Limited proteolysis of the cellobiohydrolase I from Trichoderma reesei Separation of functional domains FEBS. 1986 2004(2):223-7. [18] Boraston AB, Bolam DN, Gilbert HJ, Davies GJ. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 2004;382:769–81. [19] Shoseyov O, Shani Z, Levy I. Carbohydrate Binding Modules: Biochemical Properties and Novel Applications. Microbiology and Molecular Biology Reviews 2006;70(2): 283–95. [20] Boraston AB, Tomme P, Amandoron EA, Kilburn DG. A novel mechanism of xylan binding by a lectin-like module from Streptomyces lividans xylanase 10A. Biochem. J. 2000;350:933-41. [21] Ficko-Blean E, Boraston AB. The interaction of a carbohydrate-binding module from a Clostridium perfringens N-acetyl-beta-hexosaminidase with its carbohydrate receptor. J. Biol. Chem. 2006(281):37748-57. [22] Schallus T, Jaeckh C, Fehér K, Palma AS, Liu Y, Simpson JC, et al. Malectin: A Novel Carbohydrate-binding Protein of the Endoplasmic Reticulum and a Candidate Player in the Early Steps of Protein NGlycosylation. Molecular Biology of the Cell. 2008;19:3404–14.

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Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

References

41

[23] McBride A, Ghilagaber S, Nikolaev A, Hardie DG. The GlycogenBinding Domain on the AMPK b Subunit Allows the Kinase to Act as a Glycogen Sensor. Cell Metabolism. 2009;9:23-43. [24] Boraston AB, McLean BW, Guarna MM, Amandaron-Akow E, Kilburn DG. A family 2a carbohydrate-binding module suitable as an affinity tag for proteins produced in Pichia pastoris. Protein Expr. Purif. 2001;21(3):417-23. [25] Hachem MA, Karlsson EN, Bartonek-Roxâ E, Raghothama S, Simpson PJ, Gilbert HJ, et al. Carbohydrate-binding modules from a thermostable Rhodothermus marinus xylanase: cloning, expression and binding studies. Biochem. J. 2000;345(Pt 1):53–60. [26] Wang J, Stuckey JA, Wishart MJ, Dixon JE. A unique carbohydrate binding domain targets the lafora disease phosphatase to glycogen. J. Biol. Chem. 2002;277(4):2377-80. [27] Zverlov VV, Volkov IY, Velikodvorskaya GA, Schwarz WH. The binding pattern of two carbohydrate-binding modules of laminarinase Lam16A from Thermotoga neapolitana: differences in ß-glucan binding within family CBM4 Microbiology. 2001;147:621-9. [28] Gilbert HJ. How Carbohydrate Binding Modules Overcome Ligand Complexity. Structure. 2003;11:609-10. [29] Gilbert HJ, Stalbrand H, Brumer H. How the walls come crumbling down: recent structural biochemistry of plant polysaccharide degradation. Current Opinion in Plant Biology. 2008;11:338–48. [30] Bayer EA, Chanzy H, Lamed R, Shoham Y. Cellulose, cellulases and cellulosomes. Current Opinion in Structural Biology. 1998;8:548-57. [31] Vandermarliere E, Bourgois TM, Winn MD, Van Campenhout S, Volckaert G, Delcour JA, et al. Structural analysis of a glycoside hydrolase family 43 arabinoxylan arabinofuranohydrolase in complex with xylotetraose reveals a different binding mechanism compared with other members of the same family. Biochem. J. 2009;418:39–47. [32] Nielsen JE, Borchert TV, Vriend G. The determinants of alpha-amylase pH activity profiles. Protein engineering. 2001;14:505-12. [33] Receveur V, Czjzek M, Schülein M, Panine P, Henrissat B. Dimension, shape and conformational flexibility of a two-domain fungal cellulase in solution probed by small angle X-ray scattering. J. Biol. Chem. 2002;277(43):40887-92. [34] Rixon JE, Clarke JH, Hazlewood GP, Hoyland RW, McCarthy AJ, Gilbert HJ. Do the non-catalytic polysaccharide-binding domains and linker regions enhance the biobleaching properties of modular xylanases? Appl. Microbiol. Biotechnol. 1996;46(5-6):514-20. [35] Shen H, Schmuck M, Pilz I, Gilkes NR, Kilburn DG, Miller RCJ, et al. Deletion of the linker connecting the catalytic and cellulose-binding domains of endoglucanase A (CenA) of Cellulomonas fimi alters its

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

42

[36]

[37]

[38]

[39]

[40]

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

[41]

[42]

[43]

[44]

[45]

[46]

[47]

Susana Moreira and Miguel Gama conformation and catalytic activity. J. Biol. Chem. 1991;266(17):1133540. Howard MB, Ekborg NA, Taylor LE, Hutcheson SW, Weiner RM. Identification and analysis of polyserine linker domains in prokaryotic proteins with emphasis on the marine bacterium Microbulbifer degradans. Protein Sci. 2004;13(5):1422–5. von Ossowski I, Eaton JT, Czjzek M, Perkins SJ, Frandsen TP, Schülein M, et al. Protein disorder: Conformational distribution of the flexible linker in a chimeric double cellulase. Biophysical Journal. 2005;88(4):2823-32. Ding S, Xu Q, Crowley M, Zeng Y, Nimlos M, Lamed R, et al. A biophysical perspective on the cellulosome: new opportunities for biomass conversion. Current Opinion in Biotechnology. 2008;19:218– 27. Ding S, Bayer EA, Steiner D, Shoham Y, Lamed R. A Novel Cellulosomal Scaffoldin from Acetivibrio cellulolyticus That Contains a Family 9 Glycosyl Hydrolase Journal of Bacteriology. 1999;181(21):6720-9. Doi RH, Kosugi A. Cellulosomes: plant-cell-wall-degrading enzyme complexes. Nature Reviews Microbiology. 2004;2:541-51. Xu Q, Barak Y, Kenig R, Shoham Y, Bayer EA, Lamed R. A novel Acetivibrio cellulolyticus anchoring scaffoldin that bears divergent cohesins. J. Bacteriol. 2004;186:5782-9. Rincon MT, Cepeljnik T, Martin JC, Lamed R, Barak Y, Bayer EA, et al. Unconventional mode of attachment of the Ruminococcus flavefaciens cellulosome to the cell surface. J. Bacteriol. 2005;187(22):7569-78. Xu Q, Bayer EA, Goldman M, Kenig R, Shoham Y, Lamed R. Architecture of the Bacteroides cellulosolvens cellulosome: description of a cell surface-anchoring scaffoldin and a family 48 cellulase. J. Bacteriol. 2004;166(4):968-77. Mingardon F, Chanal A, Tardif C, Bayer EA, Fierobe H. Exploration of New Geometries in Cellulosome-Like Chimeras[down-pointing small open triangle. Appl. Environ. Microbiol. 2007;73(22):7138–49. Goldstein MA, Takagi M, Hashida S, Shoseyov O, Doi RH, Segel IH. Characterization of the cellulose-binding domain of the Clostridium cellulovorans cellulose-binding protein A. . J. Bacteriol. 1993;175(18):5762-8. Fierobe H, Bayer EA, Tardif C, Czjzek M, Mechaly A, Bélaïch A, et al. Degradation of Cellulose Substrates by Cellulosome Chimeras J. Biol. Chem. 2002;277(51):49621-30. Ding S, Xu Q, Bayer EA, Quian X, Rumbles G, Himmel ME. Bacterial complexes with potential applications in nanotechnology. In: Rehm B,

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

References

[48]

[49]

[50] [51]

[52]

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

[53]

[54]

[55]

[56]

[57]

[58]

[59]

43

editor. Microbial Bionanotechnology: Biological Self-assembly Systems and Biopolymer-based Nanostructures: Horizon Scientific Press; 2006. p. 269-305. Gregg KJ, Finn R, Abbott DW, Boraston AB. Divergent modes of glycan recognition by a new family of carbohydrat-binding modules. J. Biol. Chem. 2008;283(18):12604-13. McDonougha MA, Kadirvelraja R, Harrisa P, Poulsena JN, Larsen S. Rhamnogalacturonan lyase reveals a unique three-domain modular structure for polysaccharide lyase family 4. FEBS Let. 2004;565(13):188-94. Hashimoto H. Recent structural studies of carbohydrate-binding modules. Cell Mol Life Sci. 2006;63:2954-67. Abbott DW, Eirín-López JM, Boraston AB. Insight into ligand diversity and novel biological roles for family 32 carbohydrate-binding modules. Mol. Biol. Evol. 2008;25:155-67. Bolam DN, Ciruela A, McQueen-Mason S, Simpson P, Williamson MP, Rixon JE, et al. Pseudomonas cellulose-binding domains mediate their effects by increasing enzyme substrate proximity. Biochem. J. 1998;331( 3):775-81. Notenboom V, Boraston AB, Kilburn DG, Rose DR. Crystal structures of the family 9 carbohydrate-binding module from Thermotoga maritima xylanase 10A in native and ligand-bound forms. . Biochemistry. 2001;40:6248–56. Tomme P, Boraston A, McLean B, Kormos J, Alapuranen M, Creagh AL, et al. Characterization and affinity applications of cellulose-binding domains. Journal of Chromatography B. 1998;715:283–96. Filonova L, Gunnarsson LC, Daniel G, Ohlin M. Synthetic xylanbinding modules for mapping of pulp fibres and wood sections. BMC Plant Biology. 2007;7(54). Gunnarsson LC, Montanier C, Tunnicliffe RB, Williamson MP, Gilbert HJ, Karlsson EN, et al. Novel xylan-binding properties of an engineered family 4 carbohydrate-binding module. Biochem. J. 2007;406(Pt 2):20914. Murzin AG, Brenner SE, Hubbard T, Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 1995;247:536-40. Miyanaga A, Koseki T, Miwa Y, Mese Y, Nakamura S, Kuno A, et al. The family 42 carbohydrate-binding module of family 54 alpha-Larabinofuranosidase specifically binds the arabinofuranose side chain of hemicellulose. Biochem. J. 2006;399(3):503-11. Boraston AB, Notenboom V, Warren RA, Kilburn DG, Rose DR, Davies G. Structure and ligand binding of carbohydrate-binding module

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

44

[60]

[61]

[62]

[63]

[64]

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

[65]

[66]

[67]

[68]

[69]

[70]

Susana Moreira and Miguel Gama CsCBM6-3 reveals similarities with fucose-specific lectins and ‗galactose-binding‘ domains. J. Mol. Biol. 2003;327:659-69. Eriksson J, Malmsten M, Tiberg F, Callisen TH, Damhus T, Johansen KS. Model cellulose films exposed to H. insolens glucoside hydrolase family 45 endo-cellulase—the effect of the carbohydrate-binding module. Journal of Colloid and Interface Science. 2005;285:94-9 Henshaw J, Horne-Bitschy A, van Bueren AL, Money VA, Bolam DN, Czjzek M, et al. Family 6 Carbohydrate Binding Modules in betaAgarases Display Exquisite Selectivity for the Non-reducing Termini of Agarose Chains. J. Biol. Chem. 2006;281(25):17099-107. Boraston AB, McLean BW, Chen G, Li A, Warren RAJ, Kilburn DG. Co-operative binding of triplicate carbohydrate-binding modules from a thermophilic xylanase. Molecular Microbiology. 2002;43(1):187–94. Vaaje-Kolstad G, Horn SJ, van Aalten DMF, Synstad B, Eijsink VGH. The Non-catalytic Chitin-binding Protein CBP21 from Serratia marcescens Is Essential for Chitin Degradation. The Journal of Biological Chemistry. 2005;280(31):28492–7. Jindou S, Xu Q, Kenig R, Shulman M, Shoham Y, Bayer EA, et al. Novelarchitectureoffamily-9glycoside hydrolases identified in cellulosomal enzymesof Acetivibrio cellulolyticus and Clostridium thermocellum. FEMS Microbiol Lett. 2006;254:308-16. Reinikainen T, Ruohonen L, Nevanen T, Laaksonen L, Kraulis P, Jones TA, et al. Investigation of the function of mutated cellulose-binding domains of Trichoderma reesei cellobiohydrolase I. Proteins. 1992;14(4):475-82. Levy I, Nussinovitch A, Shpigel E, Shoseyov O. Recombinant cellulose crosslinking protein: a novel paper-modification biomaterial. Cellulose. 2002;9:91–8. Linder M, Nevanen T, Soderholm L, Outi Bengs O, Teeri TT. Improved Immobilization of Fusion Proteins via Cellulose-Binding Domains. Biotechnology and Bioengineering. 1998;60(5):642-7. Tomme P, Driver DP, Amandoron EA, Miller Jr RC, Antony R, Warren J, et al. Comparison of a fungal (family I) and bacterial (family II) cellulose- binding domain. J. Bacteriol. 1995;177(15):4356-63. Gilkes NR, Henrissat B, Kilburn DG, Miller Jr RC, Warren RA. Domains in microbial beta-1, 4-glycanases: sequence conservation, function, and enzyme families. Microbiol. Mol. Biol. Rev. 1991; 55(2):303-15. Din N, Forsythe IJ, Burtnick LD, Gilkes NR, Miller RC, Warren RA, et al. The cellulose-binding domain of endoglucanase A (CenA) from Cellulomonas fimi: evidence for the involvement of tryptophan residues in binding. Mol. Microbiol. 1994;4:747-55.

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

References

45

[71] Levy I, Shani Z, Shoseyov O. Modification of polysaccharides and plant cell wall by endo-1,4-beta-glucanase and cellulose-binding domains. Biomol. Eng. 2002;19(1):17-30. [72] Lamed R, Tormo J, Chirino AJ, Morag E, Bayer EA. Crystallization and preliminary X-ray analysis of the major cellulose-binding domain of the cellulosome from Clostridium thermocellum. J. Mol. Biol. 1994;244(2):236-7. [73] Linder M, Teeri TT. The roles and function of cellulose-binding domains Journal of Biotechnology. 1997;57(1-3):15-28 [74] Ganesh S, Tsurutani N, Suzuki T, Hoshii Y, Ishihara T, DelgadoEscueta AV, et al. The carbohydrate-binding domain of Lafora disease protein targets Lafora polyglucosan bodies. Biochem. Biophys. Res. Commun. 2004;313(4):1101-9. [75] McCartney L, Gilbert HJ, Bolam DN, Boraston AB, Knox JP. Glycoside hydrolase carbohydrate-binding modules as molecular probes for the analysis of plant cell wall polymers. Analytical Biochemistry. 2004;326: 49–54. [76] Din N, Gilkes NR, Tekant B, Miller Jr RC, Warren RAJ, Kilburn DG. Non−Hydrolytic Disruption of Cellulose Fibres by the Binding Domain of a Bacterial Cellulase. Bio/Technology. 1991;9:1096 - 9 [77] Gao PJ, Chen GJ, Wang TH, Zhang YS, Liu J. Non-hydrolytic disruption of crystalline structure of cellulose by cellulose binding domain and linker sequence of cellobiohydrolase I from Penicillium janthinellum. Acta Biochim. Biophys. Sin. 2001;33:13-8. [78] LuShan W, YuZhong Z, PeiJi G. A novel function for the cellulose binding module of cellobiohydrolase I. Sci China Ser C-Life Sci. 2008;51(7):620-9. [79] Giardina T, Gunning AP, Juge N, Faulds CB, Furniss CS, Svensson B, et al. Both binding sites of the starch-binding domain of Aspergillus niger glucoamylase are essential for inducing a conformational change in amylose. J. Mol. Biol. 2001;313:1149-59. [80] Cosgrove DJ. Loosening of plant cell walls by expansins. Nature. 2000;407:321-6. [81] Pinto R, Moreira S, Mota M, Gama M. Studies on the Cellulose-Binding Domains Adsorption to Cellulose. Langmuir. 2004;20(4):1409–13. [82] Flament D, Barbeyron T, Jam M, Potin P, Czjzek M, Kloareg B, et al. Alpha-Agarases Define a New Family of Glycoside Hydrolases, Distinct from Beta-Agarase Families. Applied and Environmental Microbiology. 2007;73(14):4691-4. [83] Crennell S, Garman E, Laver G, Vimr E, Taylor G. Crystal structure of Vibrio cholerae neuraminidase reveals dual lectin-like domains in addition to the catalytic domain Structure. 1994;2(6):535-44.

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46

Susana Moreira and Miguel Gama

[84] Connaris H, Crocker PR, Taylor GL. Enhancing the receptor affinity of the sialic acid-binding dmain of Vibrio cholerase sialidase through multivalncy. JBC. 2009. [85] Burnaugh AM, Frantz LJ, King SJ. Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J. Bacteriol. 2008;190:221-30. [86] Langley DB, Harty DW, Jacques NA, Hunter N, Guss JM, Collyer CA. Structure of N-acetyl-beta-D-glucosaminidase (GcnA) from the endocarditis pathogen Streptococcus gordonii and its complex with the mechanism-based inhibitor NAG-thiazoline. J. Mol. Biol. 2008;377:10416. [87] Sheldon WL, Macauley MS, Taylor EJ, Robinson CE, Charnock SJ, Davies GJ, et al. Functional analysis of a group A streptococcal glycoside hydrolase Spy1600 from family 84 reveals it is a beta-Nacetylglucosaminidase and not a hyaluronidase. Biochem. J. 2006;399:241-7. [88] Boraston AB, Wang D, Burke RD. Blood group antigen recognition by a Streptococcus pneumoniae virulence factor. J. Biol. Chem. 2006;281:35263-71. [89] Koay A, Rimmer KA, Mertens HDT, Gooley PR, Stapleton D. Oligosaccharide recognition and binding to the carbohydrate binding module of AMP-activated protein kinase. FEBS Letters. 2007; 581:5055–9. [90] Minassian BA, Ianzano L, Meloche M, Andermann E, Rouleau GA, Delgado-Escueta AV, et al. Mutation spectrum and predicted function of laforin in Lafora‘s progressive myoclonus epilepsy Neurology. 2000;55:341-6. [91] Liu Y, Wang Y, Wu C, Liu Y, Zheng P. Dimerization of Laforin Is Required for Its Optimal Phosphatase Activity, Regulation of GSK3beta Phosphorylation, and Wnt Signaling. J. Biol. Chem. 2006;281(46):34768-74. [92] Garyali P, Siwach P, Singh PK, Puri R, Mittal S, Sengupta S, et al. The malin–laforin complex suppresses the cellular toxicity of misfolded proteins by promoting their degradation through the ubiquitin– proteasome system. Human Molecular Genetics. 2009;18(4):688-700. [93] Gentry MS, Worby CA, Dixon JE. Insights into Lafora disease: Malin is an E3 ubiquitin ligase that ubiquitinates and promotes the degradation of laforin. PNAS. 2005;102(24):8501-6. [94] Solaz-Fuster MC, Gimeno-Alcañiz JV, Ros S, Fernandez-Sanchez ME, Garcia-Fojeda B, Criado Garcia O, et al. Regulation of glycogen synthesis by the laforin-malin complex is modulated by the AMPactivated protein kinase pathway. Hum. Mol. Genet. 2008;17(5):667-78.

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References

47

[95] Wang Y, Liu Y, Wu C, McNally B, Liu Y, Zheng P. Laforin Confers Cancer Resistance to Energy Deprivation–Induced Apoptosisv. Cancer Research, 2008;68:4039-44 [96] Gentry MS, Dowen RH, Worby CA, Mattoo S, Ecker JR, Dixon JD. The phosphatase laforin crosses evolutionary boundaries and links carbohydrate metabolism to neuronal disease. The Journal of Cell Biology. 2007;178(3):477-88. [97] Treviño MA, Palomares O, Castrillo I, Villalba M, Rodríguez R, Manuel Rico, et al. Solution structure of the C-terminal domain of Ole e 9, a major allergen of olive pollen. Protein Sci. 2008;17(2):371-6. [98] Hurtado-Guerrero R, Schüttelkopf AW, Mouyna I, Ibrahim AFM, Shepherd S, Fontaine T, et al. Molecular Mechanisms of Yeast Cell Wall Glucan Remodeling. J. Biol. Chem. 2009;284(13):8461–9. [99] Atalla RH, Hackney JM, Uhlin I, Thompson NS. Hemicelluloses as structure regulators in the aggregation of native cellulose. Int. J. Biol. Macromol. 1993;15(2):109-12. [100] Singh A, Hayashi K. Microbial Cellulases: Protein Architecture, Molecular Properties, and Biosynthesis Advances in Applied Microbiology. 1995;40:1-44. [101] Wilson DB. Three Microbial Strategies for Plant Cell Wall Degradation. Ann. NY Acad. Sci. 2008;1125:289–97. [102] Fujimoto Z, Kaneko S, Kuno A, Kobayashi H, Kusakabe I, Mizuno H. Crystal structures of decorated xylooligosaccharides bound to a family 10 xylanase from Streptomyces olivaceoviridis E-86. J. Biol. Chem. 2004;279:9606-14. [103] Charnock SJ, Bolam DN, Turkenburg JP, Gilbert HJ, Ferreira LMA, Davies GJ, et al. The X6 ―Thermostabilizing‖ Domains of Xylanases Are Carbohydrate-Binding Modules: Structure and Biochemistry of the Clostridium thermocellum X6b Domain. Biochemistry. 2000;39(17) :5013-21. [104] Gordillo F, Caputo V, Peirano A, Chavez R, Van Beeumen J, Vandenberghe I, et al. Penicillium purpurogenum produces a family 1 acetyl xylan esterase containing a carbohydrate-binding module: characterization of the protein and its gene. Mycological Research. 2006;110(10):1129-39. [105] Catala C, Bennett AB. Cloning and sequence analysis of tomcel8; a new plant endo-beta-1,4-glucanase gene, encoding a protein with a putative carbohydrate binding domain. Plant Physiol. 1998;118:1535. [106] Trainotti L, Pavanello A, Zanin D. PpEG4 is a peach endo-ß-1,4glucanase gene whose expression in climacteric peaches does not follow a climacteric pattern. Journal of Experimental Botany. 2006;57(3):58998.

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

48

Susana Moreira and Miguel Gama

[107] Hiwasa K, Kinugasa Y, Amano S, Hashimoto A, Nakano R, Inaba A, et al. Ethylene is required for both the initiation and progression of softening in pear (Pyrus communis L.) fruit Journal of Experimental Botany. 2003;54(383):771-9. [108] Trainotti L, Spolaore S, Pavanello A, Baldan B, Casadoro G. A novel Etype endo-β-1,4-glucanase with a putative cellulose-binding domain is highly expressed in ripening strawberry fruits. Plant Molecular Biology. 1999;40(2). [109] Chourasia A, Sane VA, Singh RK, Nath P. Isolation and characterization of the MiCel1 gene from mango: ripening related expression and enhanced endoglucanase activity during softening. Plant Growth Regul. 2008;56:117–27. [110] Urbanowicz BR, Catala C, Irwin D, Wilson DB, Ripoll DR, Rose JKC. A Tomato Endo-b-1,4-glucanase, SlCel9C1, Represents a Distinct Subclass with a New Family of Carbohydrate Binding Modules (CBM49). The Journal of Biological Chemistry. 2007 April 20; 282(16):12066–74. [111] Obembe OO, Jacobsen E, Visser RGF, Vincken J. Cellulosehemicellulose networks as target for in planta modification of the properties of natural fibres. Biotechnology and Molecular Biology Review. 2006;1(3):76-86. [112] Valdez HA, Busi MV, Wayllace NZ, Parisi G, Ugalde RA, GomezCasati DF. Role of the N-terminal starch-binding domains in the kinetic properties of starch synthase III from Arabidopsis thaliana. Biochemistry. 2008;47(9):3026-32. [113] Zhang X, Szydlowski N, Delvallé D, D'Hulst C, James MG, Myers AM. Overlapping functions of the starch synthases SSII and SSIII in amylopectin biosynthesis in Arabidopsis. BMC Plant Biol. 2008;8(96). [114] Paldi T, Levy I, Shoseyov O. Glucoamylase starch-binding domain of Aspergillus niger B1: molecular cloning and functional characterization. Biochem. J. 2003;372:905-10. [115] Ji Q, Oomen RJFJ, Vincken J, Bolam DN, Gilbert HJ, Suurs LCJM, et al. Reduction of starch granule size by expression of an engineered tandem starch-binding domain in potato plants. Plant Biotechnology Journal. 2004;2(3):251 - 60. [116] Ji Q, Vincken JP, Suurs LC, Visser RG. Microbial starch-binding domains as a tool for targeting proteins to granules during starch biosynthesis. Plant Mol Biol. 2003;51(5):789-801. [117] Rodriguez-Sanoja R, Oviedo N, Sanchez S. Microbial starch-binding domain. Curr. Opin. Microbiol. 2005 Jun;8(3):260-7. [118] Gunnarsson LC, Karlsson EN, Albrekt A-S, Andersson M, Holst O, Ohlin M. A carbohydrate binding module as a diversity-carrying scaffold Protein Engineering Design and Selection. 2004;17(3):213-21.

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

References

49

[119] Gunnarsson L, Dexlin L, Karlsson EN, Holst O, Ohlin M. Evolution of a carbohydrate binding module into a protein-specific binder. Biomol. Eng. 2006;23( 2-3):111-7. [120] Turner P, Mamo G, Karlsson EN. Potential and utilization of thermophiles and thermostable enzymes in biorefining. Microbial Cell Factories. 2007;6(9). [121] Shani Z, Dekel M, Tsabary G, Goren R, Shoseyov O. Growth enhancement of transgenic poplar plants by overexpression of Arabidopsis thaliana endo-1,4--glucanase (cel1). Molecular Breeding. 2004;14:321–30. [122] Shpigel E, Roiz L, Goren R, Shoseyov O. Bacterial Cellulose-Binding Domain Modulates in Vitro Elongation of Different Plant Cells. Plant Physiol. 1998;117:1185-94. [123] Safra-Dassa L, Shani Z, Danin A, Roiz L, Shoseyov O, Wolf S. Growth modulation of transgenic potato plants by heterologous expression of bacterial carbohydrate-binding module. Molecular Breeding. 2006;17(4):355-64. [124] Obembe OO, Jacobsen E, Visser R, Vincken J. Expression of an expansin carbohydrate-binding module affects xylem and phloem formation. African Journal of Biotechnology. 2007;6(14):1608-16. [125] Qin L, Kudla U, Roze EHA, Goverse A, Popeijus H, Nieuwland J, et al. Plant degradation: A nematode expansin acting on plants. Nature. 2004;427(30). [126] Rochange SF, Wenzel CL, McQueen-Mason SJ. Impaired growth in transgenic plants over-expressing an expansin isoform. . Plant Mol. Biol. 2001;46 581–9. [127] Brummell DA, Harpster MH, Civello PM, Palys JM, Bennett AB, Dunsmuir P. Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell. 1999;11:2203–16. [128] Choi D, Lee Y, Cho H, Kende H. Regulation of Expansin Gene Expression Affects Growth and Development in Transgenic Rice Plants The Plant Cell. 2003;15:1386-98. [129] Villalba-Mateos F, Rickauer M, Esquerré -Tugayé MT. Cloning and characterization of a cDNA encoding an elicitor of Phytophthora parasitica var. nicotianae that shows cellulose-binding and lectin-like activities. Mol. Plant Microbe Interact. 1997;10:1045-53. [130] Brotman Y, Briff E, Viterbo A, Chet I. Role of Swollenin, an ExpansinLike Protein from Trichoderma, in Plant Root Colonization. Plant Physiology. 2008;147:779-89. [131] Dumas B, Bottina A, Gaulina E, Esquerré-Tugayé MT. Cellulosebinding domains: cellulose associated-defensive sensing partners? . Trends in Plant Science. 2008;13(4):160-4

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

50

Susana Moreira and Miguel Gama

[132] Lemos MA, Teixeira JA, Mota M, Gama FM. A simple method to separate cellulose-binding domains of fungal cellulases after digestion by a protease. Biotechnology Letters. 2000;22:703–7. [133] Pinto R, Carvalho J, Mota M, Gama M. Large-scale production of cellulose-binding domains. Adsorption studies using CBD-FITC conjugates. Cellulose. 2006;13:557 –69. [134] Tilbeurgh HV, Tomme P, Claeyssens M, Bhikhabhai R, Pettersson G. Limited proteolysis of the cellobiohydrolas I from Trichoderma reesei. Separation of functional domains. FEBS Letters. 1986;204:223 -7. [135] Ding M, Teng Y, Yin Q, Zhao J, Zhao F. The N-terminal cellulosebinding domain of EGXA increases thermal stability of xylanase and changes its specific activities on different substrates. Acta Biochimica et Biophysica Sinica. 2008;40(11):949 - 54. [136] Esteghlalian AR, Kazaoka MM, Lowery BA, Varvak A, Hancock B, Woodward T, et al. Prebleaching of softwood and hardwood pulps by a high performance xylanase belonging to a novel clade of glycosyl hydrolase family 11. Enzyme and Microbial Technology. 2008;42(5):395-403. [137] Mooney CA, Mansfield SD, Beatson RP, Saddler JN. The effect of fiber characteristics on hydrolysis and cellulase accessibility to softwood substrates. Enzyme and Microbial Technology. 1999;25(8-9):644-50. [138] Gibbs MD. Hemicellulases from extremely thermophilic microorganisms as wood pulp bleaching aids [Doctor of Philosophy]: The University of Auckland; 1995. [139] Kenealy WR, Jeffries TW. Enzyme Processes for Pulp and Paper: A Review of Recent Developments. In: Society AC, editor. Wood deterioration and preservation : advances in our changing world. Washington, DC: Distributed by Oxford University Press; 2003. p. 21039. [140] Lenting HBM, Warmoeskerken MMCG. Guidelines to come to minimized tensile strength loss upon cellulase application. Journal of Biotechnology. 2001;89(2-3):227-32. [141] Kitaoka T, Tanaka H. Novel paper strength additive containing cellulose-binding domain of cellulase Journal of Wood Science. 2001;47(4). [142] Yokota S, Matsuo K, Kitaoka T, Wariishi H. Retention and paperstrength characteristics of anionic polyacrylamides conjugated with carbohydrate-binding modules. BioResources. 2009;4(1):234-44. [143] Pala H, Lemos MA, Mota M, Gama FM. Enzymatic upgrade of old paperboard containers. Enzyme and microbial technology. 2001;29(45):274-9. [144] Machado J, Araújo A, Pinto R, Gama FM. Studies on the interaction of the Carbohydrate Binding Module 3 from the Clostridium thermocellum

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

References

51

CipA scaffolding protein with cellulose and paper fibres. Cellulose. 2009, accepted. [145] Yokota S, Matsuo K, Kitaoka T, Wariishi H. Specific interaction acting at a cellulose-binding domain/cellulose interface for papermaking application. BioResources. 2008;3(4):1030-41. [146] Levy I, Paldi T, Shoseyov O. Engineering a bifunctional starch–cellulose cross-bridge protein. Biomaterials. 2004;25(10):1841-9. [147] Feitkenhauer H, Meyer U. Integration of biotechnological wastewater treatment units in textile finishing factories: from end of the pipe solutions to combined production and wastewater treatment units. J. Biotechnol. 2001;89:185–92. [148] Araújo R, Casal M, Cavaco-Paulo A. Application of enzymes for textile fibres processing Biocatalysis and Biotransformation 2008 332 349;26(5). [149] Saravanan D, Vasanthi NS, Ramachandran T. A review on influential behaviour of biopolishing on dyeability and certain physico-mechanical properties of cotton fabrics. Carbohydrate Polymers 76 (2009) 1–7. 2009;76:1–7. [150] Banka RR, Mishra S, Ghose TK. Fibril formation from cellulose by a novel protein from Trichoderma reesei: A nonhydrolytic cellulolytic component? World J. Microbiol. Biotechnol. 1998;14:551-8. [151] Lee I, Evans BR, Woodward J. The mechanism of cellulase action on cotton fibres: evidence from atomic force microscopy. Ultramicroscopy. 2000;82:213-21. [152] Gilkes NR, Douglas Q, Miller Jr. RC, Warren A, inventors; University of British Columbia (Vancouver, CA), assignee. Methods and compositions for modification of polysaccharide characteristics. United States1998. [153] Cavaco-Paulo A, Morgado J, Andreaus J, Kilburn DG. Interactions of cotton with CBD peptides. Enzyme Microb. Technol. 1999;25:639–43. [154] Ramos R, Pinto R, Mota M, Sampaio L, Gama FM. Textile depilling: Superior finishing using cellulose-binding domains with residual enzymatic activity. Biocatalysis and Biotransformation. 2007;25(1):3542. [155] Murai T, Ueda M, Yamamura M, Atomi H, Shibasaki Y, Kamasawa N, et al. Construction of a starch-utilizing yeast by cell surface engineering. Appl. Environ. Microbiol. 1997(63):1362–6. [156] Fukuda T, Kato-Murai M, Kuroda K, Ueda M, Suye S. Improvement in enzymatic desizing of starched cotton cloth using yeast codisplaying glucoamylase and cellulose-binding domain. Appl. Microbiol. Biotechnol. 2008;77:1225–32. [157] Kim H, Goto M, Jeong HJ, Jung KH, Kwon I, Furukawa K. Functional analysis of a hybrid endoglucanase of bacterial origin having a cellulose

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

52

Susana Moreira and Miguel Gama

binding domain from a fungal exoglucanase. Appl. Biochem. Biotechnol. 1998;75:193-204. [158] Zhao G, Ali E, Araki R, Sakka M, Kimura T, Sakka K. Function of the Family-9 and Family-22 Carbohydrate-Binding Modules in a Modular β-1,3-1,4-Glucanase/Xylanase Derived from Clostridium stercorarium Xyn10B. Bioscience, Biotechnology, and Biochemistry. 2005;69(8):1562-7. [159] Wanga Y, Yuana H, Wang J, Yu Z. Truncation of the cellulose binding domain improved thermal stability of endo-β-1,4-glucanase from Bacillus subtilis JA18 Bioresource Technology. 2009;100(1):345-9. [160] Yua B, Wu ST, Liu CC, Gauthier R, Chiou PWS. Effects of enzyme inclusion in a maize–soybean diet on broiler performance Animal Feed Science and Technology. 2007;134(3-4):283-94. [161] Chesson A. Feed enzymes. Anim. Feed Sci. Tech. 1993;45:65-9. [162] Ribeiro T, Ponte PIP, Guerreiro CIPD, Santos HM, Falcatildeo L, Freire JPB, et al. A family 11 carbohydrate-binding module (CBM) improves the efficacy of a recombinant cellulase used to supplement barley-based diets for broilers at lower dosage rates. British Poultry Science. 2008;49(5):600—8. [163] Fontes CM, Ponte PI, Reis TC, Soares MC, Gama LT, Dias FM, et al. A family 6 carbohydrate-binding module potentiates the efficiency of a recombinant xylanase used to supplement cereal-based diets for poultry. Br. Poult. Sci. 2004;45(5):648-56. [164] Guerreiro CI, Ribeiro T, Ponte PI, Lordelo MM, Falcao L, Freire JP, et al. Role of a family 11 carbohydrate-binding module in the function of a recombinant cellulase used to supplement a barley-based diet for broiler chickens. Br. Poult. Sci. 2008 Jul;49(4):. 2008;49(4):446-54. [165] Crittenden R, Laitila A, Forssell P, Mättö J, Saarela M, MattilaSandholm T, et al. Adhesion of Bifidobacteria to Granular Starch and Its Implications in Probiotic Technologies. Applied and Environmental Microbiology. 2001;67(8):3469-75. [166] Tarahomjoo S, Katakura Y, Shioya S. New strategy for enhancement of microbial viability in simulated gastric conditions based on display of starch-binding domain on cell surface. J. Biosci. Bioeng. 2008 May;105(5):503-7. [167] Nielsen PM, Viksoe-Nielsen A, inventors; Method for producing soy sauce2007. [168] Cretich M, Damina F, Pirria G, Chiari M. Protein and peptide arrays: Recent trends and new directions. Biomolecular Engineering. 2006;23(2-3):77-88. [169] Filonova L, Kallas AM, Greffe L, Johansson G, Teeri TT, Daniel G. Analysis of the surfaces of wood tissues and pulp fibers using

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

References

53

carbohydrate-binding modules specific for crystalline cellulose and mannan. Biomacromolecules. 2007;8(1):91-7. [170] Ofir K, Berdichevsky Y, Benhar I, Azriel-Rosenfeld R, Lamed R, Barak Y, et al. Versatile protein microarray based on carbohydrate-binding modules. Proteomics. 2005;5(5):1806–14. [171] Haimovitz R, Barak Y, Morag E, Voronov-Goldman M, Shoham Y, Lamed R, et al. Cohesin-dockerin microarray: Diverse specificities between two complementary families of interacting protein modules. Proteomics. 2008;8(5):968 - 79. [172] Gunnarsson LC, Zhou Q, Montanier C, Karlsson EN, Brumer H, Ohlin M. Engineered xyloglucan specificity in a carbohydrate-binding module Glycobiology. 2006;16(12):1171-80. [173] Kavoosi M, Meijer J, Kwan E, Creagh AL, Kilburn DG, Haynes CA. Inexpensive one-step purification of polypeptides expressed in Escherichia coli as fusions with the family 9 carbohydrate-binding module of xylanase 10A from T. maritima. J. Chromatogr B Analyt Technol Biomed Life Sci. 2004;807(1):87-94. [174] Kavoosi M, Sanaie N, Dismer F, Hubbuch J, Kilburn DG, Haynes CA. A novel two-zone protein uptake model for affinity chromatography and its application to the description of elution band profiles of proteins fused to a family 9 cellulose binding module affinity tag. Journal of Chromatography A. 2007;1160(1-2):137-49. [175] Rodriguez B, Kavoosi M, Koska J, Creagh AL, Kilburn DG, Haynes CA. Inexpensive and generic affinity purification of recombinant proteins using a family 2a CBM fusion tag. Biotechnol. Prog. 2004;20(5):1479-89. [176] Shpigel E, Goldlust A, Eshel A, Ber IK, Efroni G, Singer Y, et al. Expression, purification and applications of staphylococcal protein A fused to cellulose-binding domain. Biotechnol. Appl. Biochem. 2000;31(3):97-203. [177] Ito S, Kuno A, Suzuki R, Kaneko S, Kawabata Y, Kusakabe I, et al. Rational affinity purification of native Streptomyces family 10 xylanase Journal of Biotechnology. 2004;110(2):137-42. [178] Kavoosi M, Creagh AL, Kilburn DG, Haynes CA. Strategy for selecting and characterizing linker peptides for CBM9-tagged fusion proteins expressed in Escherichia coli. Biotechnology and Bioengineering. 2007;98(3):599–610. [179] Xu Y, Foong FC. Characterization of a cellulose binding domain from Clostridium cellulovorans endoglucanase-xylanase D and its use as a fusion partner for soluble protein expression in Escherichia coli. J. Biotechnol. 2008;135(4):319-25.

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54

Susana Moreira and Miguel Gama

[180] Ong E, Gilkes NR, Warren RAJ, Miller RC, Kilburn DG. Enzyme Immobilization Using the Cellulose-Binding Domain of a Cellulomonas Fimi Exoglucanase. Nature Biotechnology. 1989;7:604 - 7. [181] Richins RD, Mulchandani A, Chen W. Expression, immobilization, and enzymatic characterization of cellulose-binding domain organophosphorus hydrolase fusion enzymes. Biotechnology and Bioengineering. 2000;69(6):591 - 6. [182] Kwan EM, Boraston AB, McLean BW, Kilburn DG, A.J. WR. NGlycosidase–carbohydrate-binding module fusion proteins as immobilized enzymes for protein deglycosylation. PEDS. 2005;18(10):497-501. [183] Morassutti C, De Amicis F, Skerlavaj B, Zanetti M, Marchetti T. Production of a recombinant antimicrobial peptide in transgenic plants using a modified VMA intein expression system. FEBS Letters. 2002;519(1-3):141-6 [184] Murashima K, Kosugi A, Doi RH. Solubilization of cellulosomal cellulases by fusion with cellulose-binding domain of noncellulosomal cellulase engd from Clostridium cellulovorans. Proteins: Structure, Function, and Bioinformatics. 2003;50(4): 620 - 8. [185] Yeh M, Craig SJ, Lum M, Foong FC. Effects of the PT region of EngD and HLD of CbpA on solubility, catalytic activity and purification characteristics of EngD-CBDCbpA fusions from Clostridium cellulovorans. Journal of Biotechnology 2005;116 233-44. [186] Craig SJ, Shu A, Xu Y, Foong FC, Nordon R. Chimeric protein for selective cell attachment onto cellulosic substrates. PEDS. 2007;20(5):235-41. [187] Xu Z, Bae W, Mulchandani A, Mehra RK, Chen W. Heavy metal removal by novel CBD-EC20 sorbents immobilized on cellulose. Biomacromolecules. 2002;3(3):462-5. [188] Maurice S, Dekel M, Shoseyov O, Gertler A. Cellulose beads bound to cellulose binding domain-fused recombinant proteins; an adjuvant system for parenteral vaccination of fish. Vaccine. 2003;21(23):3200-7. [189] Guerreiro CIPD, Fontes CMGA, Gama FM, Domingues L. Escherichia coli expression and purification of four antimicrobial peptides fused to a family 3 carbohydrate-binding module (CBM) from Clostridium thermocellum. Protein Expression and Purification. 2008;59:161-8. [190] Andrade FK, Moreira SMG, Domingues L, Gama FMP. Improving the affinity of fibroblasts for bacterial cellulose using carbohydrate-binding modules fused to RGD. J. Biomed. Mater. Res. A. 2008. [191] Carvalho V, Domingues L, Gama M. The inhibitory effect of an RGDhuman chitin-binding domain fusion protein on the adhesion of fibroblasts to reacetylated chitosan films. Mol. Biotechnol. 2008;40(3):269-79.

Carbohydrate Binding Modules: Functions and Applications : Functions and Applications, Nova Science Publishers,

References

55

Copyright © 2010. Nova Science Publishers, Incorporated. All rights reserved.

[192] Moreira SM, Andrade FK, Domingues L, Gama M. Development of a strategy to functionalize a dextrin-based hydrogel for animal cell cultures using a starch-binding module fused to RGD sequence. BMC Biotechnology. 2008;8(78). [193] Svensson A, Nicklasson E, Harrah T, Panilaitis B, Kaplan DL, Brittberg M, et al. Bacterial cellulose as a potential scaffold for tissue engineering of cartilage. Biomaterials. 2005;26(4):419-31. [194] Xu Q, Song Q, Ai X, McDonald TJ, Long H, Ding S, et al. Engineered carbohydrate-binding module (CBM) protein-suspended single-walled carbon nanotubes in water. Chem. Commun. 2009:337–9. [195] Michel G, Barbeyron T, Kloareg B, Czjzek M. The family 6 carbohydrate binding modules have co-evolved with their appended catalytic modules towards similar substrate specificity. Glycobiology. 2009.

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INDEX

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A accessibility, 9, 50 acid, 1, 5, 8, 9, 23, 29, 46 additives, 27 adhesion, 33, 34, 35, 54 adhesion strength, 33 adsorption, 31, 35, 40 adult, 22 aerobic, 19 AFM, 47 aggregation, 18, 47 alkali, 25 alpha, 41, 43 alters, 41, 49 amino, 1, 5, 6, 8, 23 amino acid, 5, 6, 8, 23 amino acids, 5, 6 amorphous, xi, 5, 8, 12, 19, 26 amylase, 29, 30, 34, 41 amylopectin, 48 anabolic, 20, 37 anaerobic, 6, 19 anaerobic bacteria, 6, 19 animals, 19, 20, 30 antibacterial, 37 antibody, 33 antigen, 34, 46 apoptosis, 18

Arabidopsis thaliana, 18, 20, 48, 49 arthritis, 1 Aspergillus niger, 45, 48 atomic force, 28, 51 atomic force microscopy, 28, 51 attachment, 42, 54

B Bacillus subtilis, 52 bacteria, 3, 6, 18, 19, 20, 30, 37 bacterial, 9, 17, 22, 34, 40, 44, 46, 49, 51, 54 bacterium, 21, 42 barley, 29, 30, 52 behavior, 22 beneficial effect, 26 benign, 25 binding, xi, 1, 3, 5, 6, 7, 9, 11, 12, 14, 15, 17, 18, 20, 21, 22, 23, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55 biocompatible, 34 bioengineering, 27 biofuel, 21 biological processes, 17 biomass, 21, 42

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Index

biomaterials, 37, 44 Biometals, iii biomolecules, 31, 34 bioremediation, 33 biosynthesis, 20, 32, 48 biotechnological, xi, 1, 3, 13, 29, 51 biotechnology, 37 biotic, 23 Biotransformation, 51 birds, 30 bleaching, 26, 28, 50 blood, 13, 34 blood group, 13 blood vessels, 34 body weight, 30 bonding, 26, 27 bonds, 27 breakdown, xi British Columbia, 51 broilers, 52

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C C. thermocellum, 11, 12, 26, 30, 31, 34, 35 cadmium, 34 cancer, 18 carbohydrate, xi, 1, 3, 5, 6, 7, 9, 13, 17, 21, 25, 32, 34, 37, 39, 40, 41, 43, 44, 45, 46, 47, 48, 49, 50, 52, 53, 54, 55 carbohydrate metabolism, 47 carbohydrates, xi, 1, 30, 31, 32, 35 carbon, 17, 35, 55 carbon nanotubes, 35, 55 carcinogenic, 37 carrier, 34 cartilage, 34, 55 catalysis, 6, 20, 40 catalytic activity, 5, 26, 42, 54 catalytic C, 11, 44 cDNA, 49

cell, 1, 3, 7, 8, 11, 13, 17, 18, 19, 20, 22, 23, 29, 30, 32, 33, 34, 35, 37, 42, 45, 49, 51, 52, 54, 55 cell adhesion, 34 cell culture, 55 cell differentiation, 1 cell surface, 11, 18, 29, 30, 37, 42, 51, 52 cellulose, 3, 6, 8, 11, 12, 13, 14, 19, 20, 21, 22, 23, 26, 27, 29, 31, 32, 33, 34, 40, 41, 42, 43, 44, 45, 47, 48, 49, 50, 51, 52, 53, 54, 55 Cellulose, iv, 3, 19, 34, 41, 42, 44, 45, 48, 49, 50, 51, 54 cellulosic, 11, 19, 28, 33, 34, 54 cellulosomes, 6, 12, 19, 41 cereals, 29 chemical properties, 25 chemicals, 25, 27 chickens, 52 China, 45 chitin, 3, 8, 14, 54 Chitin, 19, 44 chitosan, 54 chromatography, 53 Ciona, 39 classification, 7, 8, 43 cloning, 33, 41, 48 cohesins, 6, 31, 42 colonization, 37 combined effect, 37 communication, 17 complex carbohydrates, xi, 1 components, 6, 7, 11, 22, 32 composition, 34 compounds, 33 concentration, 11, 12, 29 conservation, 44 consumption, 26 contaminants, 27 control, 35, 40 conversion, 21, 42 cooking, 25 corn, 27, 30

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Index cotton, 28, 29, 51 coupling, 33 covalent, 31, 33, 35 crosslinking, 44 cross-linking, 27, 33 crystal structure, 13 crystal structures, 13 crystalline, xi, 3, 5, 7, 8, 12, 13, 14, 19, 20, 21, 23, 32, 40, 45, 53 C-terminal, 17, 30, 39, 47 culture, 22, 33

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D database, 5, 40, 43 defense, 17, 20, 23 defense mechanisms, 17, 23 deformation, 27 degradation, 1, 7, 17, 18, 20, 33, 39, 41, 46, 49 degrading, 9, 19, 20, 21, 33, 42 delivery, 9, 30, 37 deprivation, 18 derivatives, 30 desorption, 32 detoxification, 33 diets, 30, 52 differentiation, 1 digestibility, 29 digestion, 26, 29, 50 dimerization, 18 diseases, 23 disorder, 18, 42 distribution, 27, 42 diversification, 21 diversity, 43, 48 DMF, 44 DNA, xi, 31 dockerins, 6, 31 dosage, 26, 52 drainage, 26 drugs, 37

59

duplication, 15 dyeing, 29 dyes, 29

E E. coli, 21, 35 effluents, 28 egg, 39 electrostatic interactions, 27 elongation, 22, 23 encapsulated, 19 encapsulation, 30 encoding, 21, 47, 49 endocarditis, 46 endoplasmic reticulum, 17 energy, 3, 18, 26, 27 energy consumption, 26 entrapment, 31 environment, 6 enzymatic, 1, 6, 14, 20, 21, 25, 29, 51, 54 enzymatic activity, 1, 6, 29, 51 enzyme immobilization, 32 enzymes, xi, 1, 3, 5, 6, 9, 12, 13, 15, 18, 19, 20, 21, 22, 25, 26, 28, 29, 30, 37, 49, 51, 52, 54 epilepsy, 46 epitopes, 32, 33 Escherichia coli, 53, 54 esterase, 47 esterases, 5 ethanol, 21 eukaryotes, 17 eukaryotic cell, 37 evolution, 21, 37 excision, 40 extracellular matrix, 37 extraction, 25

F fabric, 28, 29

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60

Index

fabrication, 31 family, 7, 8, 9, 11, 12, 15, 20, 23, 31, 35, 37, 41, 42, 43, 44, 46, 47, 50, 52, 53, 54, 55 F-box, 17, 39 feeding, 30 fermentation, 30 fertilization, 1 fiber, 14, 26, 27, 32, 33, 50 fiber membranes, 33 fibers, 14, 19, 25, 27, 28, 29, 32, 33, 52 fibrils, 14 fibroblast, 34, 35 fibroblasts, 54 films, 44, 54 fish, 34, 54 FITC, 29, 50 flexibility, 26, 41 folding, 1, 31 food, 30 food industry, 30 fruits, 48 fuel, 21 fungal, 29, 41, 44, 50, 52 fungi, 3, 6, 19, 20, 23 fungus, 23 fusion, 20, 27, 29, 30, 31, 32, 33, 34, 53, 54 fusion proteins, 29, 32, 53, 54

G gamete, 39 gastric, 30, 52 gene, 22, 35, 47, 48 genes, 21, 22, 23 Gibbs, 50 glass, 31 Glucan, 47 glucoamylase, 29, 45, 51 glucose, 18 glucosidases, 19 glucoside, 44 glycans, 3, 8, 17, 18, 37

glycoconjugates, xi, 46 glycogen, 11, 18, 41, 46 glycoprotein, 21, 32 glycoproteins, 17 glycoside, 5, 11, 17, 18, 37, 41, 46 glycosyl, 6, 15, 50 glycosylation, 17 granules, 20, 48 growth, 20, 22, 23, 30, 49

H health, 1 heat, 21 heavy metal, 33 heavy metals, 33 height, 22 hemicellulose, 19, 22, 43, 48 heterogeneity, xi, 5 heterogeneous, 15 high temperature, 25 homogenous, 15 homologous proteins, 19 hormones, 20 host, 1, 3, 9, 17, 34, 37 human, 18, 31, 46, 54 human immunodeficiency virus, 31 hybrid, 51 hydration, 27 hydrogels, 35 hydrogen, 5, 22 hydrogen bonds, 5, 22 hydrolases, 5, 11, 15, 17, 18, 29, 37, 44, 45 hydrolysis, 14, 20, 21, 25, 27, 30, 31, 50 hydrolyzed, 30 hydrophobic, 5, 6, 8, 27, 29 hydrophobic interactions, 5

I identification, 17 identity, 14

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Index images, 28, 35 immobilization, 25, 31, 32, 33, 34, 54 immobilized enzymes, 54 immune response, 1, 40 immune system, 37 immunization, 34 in vitro, 22, 23 in vivo, 21, 22, 25, 32 inclusion, 29, 52 industry, 25, 27, 30, 37 inert, 34 infection, 23 inflammation, 1 inhibitor, 46 inhibitory, 54 inhibitory effect, 54 initiation, 48 integrin, 34 interaction, xi, 1, 6, 9, 13, 18, 21, 22, 23, 25, 35, 37, 40, 50, 51 interaction process, 9 interactions, 1, 3, 5, 11, 13, 17, 27, 31, 35, 37, 39, 40 interface, 51 interfacial properties, 29 intestinal tract, 30 intrinsic, 31, 32 inventors, 51, 52

J Jun, 48 Jung, 51

K kinase, 18, 41, 46

L laccase, 28, 29 Lactobacillus, 30

61

Langmuir, 45 lectin, 3, 8, 9, 23, 39, 40, 45, 49 ligand, 7, 8, 13, 18, 21, 33, 34, 43 ligands, 5, 9 lignin, 19, 25 limitation, 21, 27 linkage, 3 links, 47 lipase, 29 localization, 32 location, 5, 9 lumen, 33

M machinery, 20 maize, 52 mammals, 17 mango, 20, 48 mapping, 43 matrix, 1, 20, 22, 32, 33, 34, 37 maturation, 1 mechanical properties, 27, 51 mediation, 11 menstrual cycle, 39 metabolism, 18, 47, 49 metabolites, 20 microarray, 31, 53 microbes, 19, 30 microbial, 14, 30, 43, 44, 47, 49, 50, 52 microcrystalline cellulose, 40 microorganisms, 19, 20, 30, 50 microscope, 31 microscopy, 28, 51 misfolded, 46 model system, 22 modulation, 37, 49 modules, xi, 1, 3, 6, 7, 11, 14, 15, 20, 23, 26, 27, 29, 30, 33, 37, 40, 41, 43, 44, 45, 50, 53, 54, 55 molecular biology, 21 molecular weight, 3

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62

Index

molecules, 27, 28, 29, 31, 34, 35 monoclonal, 32, 33 monoclonal antibodies, 32 monoclonal antibody, 33 monosaccharides, 18 morphology, 35 mucus, 39 multiples, 15 mutagenesis, 11, 23, 32 mutant, 20 mutations, 18 myoclonus, 46

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N N-acety, 40, 46 Nanostructures, 43 nanotechnology, 42 nanotubes, 35, 55 natural, 48 nematode, 49 network, 22, 27 neuraminidase, 45 Nielsen, 41, 52 non-crystalline, 3, 8 N-terminal, 5, 18, 20, 48, 50 nucleic acid, 35

O oligonucleotides, 31 oligosaccharide, 8, 9, 11, 18, 37 olive, 18, 47 organophosphates, 33 orientation, 33 oxidative, 25

P papermaking, 25, 26, 27, 51 parenteral, 54 particles, 14

pathogenesis, 18, 37 pathogenic, 18, 23 pathogens, 23 patients, 31 PCR, 31 pectin, 9 peptide, 3, 31, 52, 54 peptides, 3, 9, 19, 31, 34, 35, 51, 53, 54 petroleum, 21 pH, 6, 41 phage, 32 phenotypes, 22 phenylalanine, 9 phloem, 49 phosphorylation, 46 physical properties, 34 Pichia pastoris, 41 planar, 8, 9, 31 plants, 20, 22, 23, 39, 48, 49, 54 platforms, 9 pollen, 18, 47 polyacrylamide, 27 polymer, 49 polymers, 19, 21, 35, 45 polypeptide, 5, 18 polypeptides, 29, 53 polysaccharides, xi, 5, 7, 8, 11, 12, 19, 22, 23, 30, 32, 41, 43, 45, 51 polystyrene, 35 potato, 20, 22, 48, 49 poultry, 29, 30, 52 powders, 32 probe, 31 probiotic, 30 probiotics, 30 production, 20, 21, 25, 26, 30, 31, 35, 50, 51 prokaryotic, 42 protection, 23 protein, xi, 1, 5, 6, 7, 9, 11, 13, 14, 15, 17, 18, 21, 23, 25, 27, 28, 30, 31, 32, 33, 34, 35, 37, 39, 42, 44, 45, 46, 47, 49, 51, 53, 54, 55

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Index protein binding, 34 protein folding, 1 protein function, 31 protein structure, 35 protein-protein interactions, 11 proteolysis, xi, 12, 20, 40, 50 proteomics, 31 Pseudomonas, 23, 43 pulps, 14, 26, 50 purification, 25, 31, 32, 33, 34, 53, 54

Q quality control, 31

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R random, 33 range, 3, 14, 34 reagents, 27 recognition, 1, 6, 12, 17, 18, 37, 40, 43, 46 recombinant DNA, 9, 12, 25 recruiting, 18 recycling, 17, 27 refining, 26 regenerated cellulose, 33 regeneration, 34 regulation, 17, 18, 20, 22 regulators, 47 relationships, 19 relaxation, 20 residues, 8, 13, 23, 35, 44 resistance, 18, 23, 26 resolution, 13 retention, 27, 31 reticulum, 17 rice, 22, 30 Rouleau, 46 rye, 29

63

S scaffold, 21, 34, 48, 55 scaffolding, 51 scaffolds, 21 scarcity, 5 scattering, 41 search, 27 secrete, 19 selecting, 53 selectivity, 17 sensing, 49 separation, 33 shape, 22, 41 shear, 33 sialic acid, 46 signals, 20 sites, 7, 8, 9, 32, 45 solubility, 33, 54 solvent, 9 sorbents, 34, 54 soybeans, 30, 52 species, 3, 6, 20, 23, 31 specific adsorption, 31 specificity, xi, 1, 3, 5, 8, 13, 15, 18, 21, 31, 32, 53, 55 spectrum, 46 sperm, 39 sperm function, 39 sponges, 32 stability, 25, 29, 31, 50, 52 stabilize, 35 staphylococcal, 53 starch, 3, 8, 11, 14, 18, 20, 26, 27, 29, 30, 34, 35, 45, 48, 51, 52, 55 starch biosynthesis, 21, 48 starch granules, 20, 30 stomach, 30 storage, 11 strain, 29 strains, 30 strategies, 21, 23, 26, 31

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64

Index

strength, 6, 26, 27, 33, 50 Streptomyces, 40, 47, 53 stress, 27, 30 structural biochemistry, 41 substitution, 25 substrates, 11, 12, 15, 29, 30, 31, 50, 54 sugar, 5, 8, 9, 17, 21, 30, 39 surface properties, 27 surfactants, 35 SWNTs, 35 synergistic, 19 synthesis, xi, 1, 9, 18, 22, 37, 46 systems, 19, 21, 33

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T tandem repeats, 15, 20 targets, 15, 37, 41, 45 technology, 9, 12, 25, 27, 29, 31, 32, 50 temperature, 25 tensile, 26, 27, 50 tensile strength, 26, 27, 50 textile, 14, 25, 27, 29, 37, 51 textile industry, 27 thermal stability, 50, 52 thermophiles, 49 thermostability, 21 three-dimensional, 6, 7, 27, 39 time, 6, 31 tissue, 22, 29, 34, 55 tobacco, 22, 23, 39 tomato, 20, 21, 22, 49 topology, 7, 8 toxicity, 34, 46 toxin, 9, 37 transfer, 19, 20, 27 transgenic, 20, 22, 49, 54 transport, 5 tripeptide, 34 tryptophan, 9, 44 turgor, 20

turnover, 17 tyrosine, 9

U ubiquitin, 17, 18, 39, 46 Ubiquitin, 39 uniform, 32, 33 United States, 51

V vaccination, 54 vaccine, 34 Valdez, 20, 48 validation, 39 variability, 7 vesicles, 39 Vibrio cholerae, 45 virulence, 18, 46 virus, 3, 31

W wastewater treatment, 51 water, 20, 27, 35, 55 wheat, 29, 30 wood, 25, 32, 43, 50, 52

X X-ray analysis, 45 xylem, 22, 49

Y yeast, 29, 51 yield, 26, 33

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