Differential Oligosaccharide Recognition by Evolutionarily-related β-1,4 and β-1,3 Glucan-binding Modules

Abstract Enzymes active on complex carbohydrate polymers frequently have modular structures in which a catalytic domain is appended to one or more carbohydrate-binding modules (CBMs). Although CBMs have been classified into a number of families based upon sequence, many closely related CBMs are specific for different polysaccharides. In order to provide a structural rationale for the recognition of different polysaccharides by CBMs displaying a conserved fold, we have studied the thermodynamics of binding and three-dimensional structures of the related family 4 CBMs from Cellulomonas fimi Cel9B and Thermotoga maritima Lam16A in complex with their ligands, β-1,4 and β-1,3 linked gluco-oligosaccharides, respectively. These two CBMs use a structurally conserved constellation of aromatic and polar amino acid side-chains that interact with sugars in two of the five binding subsites. Differences in the length and conformation of loops in non-conserved regions create binding-site topographies that complement the known solution conformations of their respective ligands. Thermodynamics interpreted in the light of structural information highlights the differential role of water in the interaction of these CBMs with their respective oligosaccharide ligands.

[1]  Birte Svensson,et al.  Recent Advances in Carbohydrate Bioengineering , 1999 .

[2]  S. Withers,et al.  The cellulose-binding domains from Cellulomonas fimi beta-1, 4-glucanase CenC bind nitroxide spin-labeled cellooligosaccharides in multiple orientations. , 1999, Journal of molecular biology.

[3]  R J Read,et al.  Crystallography & NMR system: A new software suite for macromolecular structure determination. , 1998, Acta crystallographica. Section D, Biological crystallography.

[4]  M. D. Joshi,et al.  Structure of the N-terminal cellulose-binding domain of Cellulomonas fimi CenC determined by nuclear magnetic resonance spectroscopy. , 1996, Biochemistry.

[5]  D. Bundle,et al.  Thermodynamics of oligosaccharide binding to a monoclonal antibody specific for a Salmonella O-antigen point to hydrophobic interactions in the binding site. , 1992, The Journal of biological chemistry.

[6]  L. McIntosh,et al.  Structure and binding specificity of the second N-terminal cellulose-binding domain from Cellulomonas fimi endoglucanase C. , 2000, Biochemistry.

[7]  P. Simpson,et al.  A family IIb xylan-binding domain has a similar secondary structure to a homologous family IIa cellulose-binding domain but different ligand specificity. , 1999, Structure.

[8]  R. Woods,et al.  Involvement of water in carbohydrate-protein binding. , 2001, Journal of the American Chemical Society.

[9]  B. Henrissat,et al.  The Location of the Ligand-binding Site of Carbohydrate-binding Modules That Have Evolved from a Common Sequence Is Not Conserved* , 2001, The Journal of Biological Chemistry.

[10]  K. P. Murphy,et al.  Structural energetics of protein folding and binding. , 2000, Current opinion in biotechnology.

[11]  H. Saitǒ,et al.  Relationship between conformation and biological response for (1----3)-beta-D-glucans in the activation of coagulation factor G from limulus amebocyte lysate and host-mediated antitumor activity. Demonstration of single-helix conformation as a stimulant. , 1991, Carbohydrate research.

[12]  Z. Otwinowski,et al.  [20] Processing of X-ray diffraction data collected in oscillation mode. , 1997, Methods in enzymology.

[13]  D. Kilburn,et al.  C1-Cx revisited: intramolecular synergism in a cellulase. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[14]  C. Haynes,et al.  Binding specificity and thermodynamics of a family 9 carbohydrate-binding module from Thermotoga maritima xylanase 10A. , 2001, Biochemistry.

[15]  K. P. Murphy,et al.  Group additivity thermodynamics for dissolution of solid cyclic dipeptides into water , 1990 .

[16]  Pedro M. Coutinho,et al.  Carbohydrate-active enzymes : an integrated database approach , 1999 .

[17]  B. Matthews.  Solvent content of protein crystals. , 1968, Journal of molecular biology.

[18]  C. Haynes,et al.  Binding of the cellulose-binding domain of exoglucanase Cex from Cellulomonas fimi to insoluble microcrystalline cellulose is entropically driven. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[19]  C. Khosla,et al.  Modular enzymes : Biocatalysis: Synthesis methods that exploit enzymatic activities , 2001 .

[20]  D. Kilburn,et al.  beta-1,3-Glucan binding by a thermostable carbohydrate-binding module from Thermotoga maritima. , 2001, Biochemistry.

[21]  D. Kilburn,et al.  Precise excision of the cellulose binding domains from two Cellulomonas fimi cellulases by a homologous protease and the effect on catalysis. , 1988, The Journal of biological chemistry.

[22]  R. Read.  Improved Fourier Coefficients for Maps Using Phases from Partial Structures with Errors , 1986 .

[23]  D. Kilburn,et al.  Recognition of cello-oligosaccharides by a family 17 carbohydrate-binding module: an X-ray crystallographic, thermodynamic and mutagenic study. , 2001, Journal of molecular biology.

[24]  R. S. Spolar,et al.  Coupling of local folding to site-specific binding of proteins to DNA. , 1994, Science.

[25]  Randy J. Read,et al.  Pushing the boundaries of molecular replacement with maximum likelihood. , 2001, Acta crystallographica. Section D, Biological crystallography.

[26]  Anastassis Perrakis,et al.  Automated protein model building combined with iterative structure refinement , 1999, Nature Structural Biology.

[27]  J M Sturtevant,et al.  Heat capacity and entropy changes in processes involving proteins. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[28]  A. Surolia,et al.  Thermodynamics of Monosaccharide and Disaccharide Binding to Erythrina corallodendron Lectin* , 1996, The Journal of Biological Chemistry.

[29]  T J Oldfield,et al.  SQUID: a program for the analysis and display of data from crystallography and molecular dynamics. , 1992, Journal of molecular graphics.

[30]  V. Zverlov,et al.  The binding pattern of two carbohydrate-binding modules of laminarinase Lam16A from Thermotoga neapolitana: differences in beta-glucan binding within family CBM4. , 2001, Microbiology.

[31]  Spencer J. Williams,et al.  High-resolution crystal structures of the lectin-like xylan binding domain from Streptomyces lividans xylanase 10A with bound substrates reveal a novel mode of xylan binding. , 2002, Biochemistry.

[32]  Walter H.J. Ward,et al.  The entropic penalty of ordered water accounts for weaker binding of the antibiotic novobiocin to a resistant mutant of DNA gyrase: a thermodynamic and crystallographic study. , 1997, Biochemistry.

[33]  D. Kilburn,et al.  Crystal structures of the family 9 carbohydrate-binding module from Thermotoga maritima xylanase 10A in native and ligand-bound forms. , 2001, Biochemistry.

[34]  P. Simpson,et al.  The Structural Basis for the Ligand Specificity of Family 2 Carbohydrate-binding Modules* , 2000, The Journal of Biological Chemistry.

[35]  R. Huber,et al.  Accurate Bond and Angle Parameters for X-ray Protein Structure Refinement , 1991 .

[36]  G J Davies,et al.  The X6 "thermostabilizing" domains of xylanases are carbohydrate-binding modules: structure and biochemistry of the Clostridium thermocellum X6b domain. , 2000, Biochemistry.

[37]  J. Vandekerckhove,et al.  Studies of the cellulolytic system of Trichoderma reesei QM 9414. Analysis of domain function in two cellobiohydrolases by limited proteolysis. , 1988, European journal of biochemistry.

[38]  A. Koivula,et al.  Cellulose-binding domains promote hydrolysis of different sites on crystalline cellulose. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[39]  C. Haynes,et al.  Characterization and affinity applications of cellulose-binding domains. , 1998, Journal of chromatography. B, Biomedical sciences and applications.

[40]  E. Toone,et al.  Calorimetric analysis of the binding of lectins with overlapping carbohydrate-binding ligand specificities. , 1995, Biochemistry.

[41]  W. Weis,et al.  Structural basis of lectin-carbohydrate recognition. , 1996, Annual review of biochemistry.

[42]  A. Brunger.  Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. , 1992 .

[43]  U. Baxa,et al.  Enthalpic barriers to the hydrophobic binding of oligosaccharides to phage P22 tailspike protein. , 2001, Biochemistry.

[44]  C. Betzel,et al.  Crystal structure of beta-D-cellotetraose hemihydrate with implications for the structure of cellulose II. , 1994, Science.

[45]  H. Sugiyama,et al.  A study of the conformation of β-1,4-linked glucose oligomers, cellobiose to cellohexaose, in solution , 2000 .

[46]  J. Zou,et al.  Improved methods for building protein models in electron density maps and the location of errors in these models. , 1991, Acta crystallographica. Section A, Foundations of crystallography.

[47]  J Navaza,et al.  Implementation of molecular replacement in AMoRe. , 2001, Acta crystallographica. Section D, Biological crystallography.

[48]  E. García-Hernández,et al.  Structural bases of lectin‐carbohydrate affinities: Comparison with protein‐folding energetics , 1999, Protein science : a publication of the Protein Society.

[49]  S. Young,et al.  Observation of a Partially Opened Triple-helix Conformation in 1→3-β-Glucan by Fluorescence Resonance Energy Transfer Spectroscopy* , 2000, The Journal of Biological Chemistry.

[50]  D. Kilburn,et al.  Cellulose-binding domains : classification and properties , 1995 .

[51]  Specificity and affinity of substrate binding by a family 17 carbohydrate-binding module from Clostridium cellulovorans cellulase 5A. , 2000, Biochemistry.

[52]  J. Richardson,et al.  The anatomy and taxonomy of protein structure. , 1981, Advances in protein chemistry.

[53]  G J Kleywegt,et al.  Phi/psi-chology: Ramachandran revisited. , 1996, Structure.

[54]  B Honig,et al.  Computer simulations of the diffusion of a substrate to an active site of an enzyme. , 1987, Science.

[55]  L. McIntosh,et al.  Binding site analysis of cellulose binding domain CBD(N1) from endoglucanse C of Cellulomonas fimi by site-directed mutagenesis. , 2000, Biochemistry.

[56]  Molecular dynamics study on the conformational stability of laminaran oligomers in various solvents. , 2000, Biomacromolecules.

[57]  C. Haynes,et al.  Interaction of polysaccharides with the N-terminal cellulose-binding domain of Cellulomonas fimi CenC. 1. Binding specificity and calorimetric analysis. , 1996, Biochemistry.

[58]  D. Bolam,et al.  Structure of a Family 15 Carbohydrate-binding Module in Complex with Xylopentaose , 2001, The Journal of Biological Chemistry.

[59]  B. Henrissat,et al.  The crystal structure of methyl beta-cellotrioside monohydrate 0.25 ethanolate and its relationship to cellulose II. , 1995, Carbohydrate research.

[60]  K. P. Murphy,et al.  Dissecting the energetics of a protein-protein interaction: the binding of ovomucoid third domain to elastase. , 1997, Journal of molecular biology.

[61]  B. Henrissat,et al.  Glycoside hydrolases and glycosyltransferases. Families, modules, and implications for genomics. , 2000, Plant physiology.

[62]  P. Simpson,et al.  Pseudomonas cellulose-binding domains mediate their effects by increasing enzyme substrate proximity. , 1998, The Biochemical journal.

[63]  G. Murshudov,et al.  Refinement of macromolecular structures by the maximum-likelihood method. , 1997, Acta crystallographica. Section D, Biological crystallography.