1heh › Citations

Evidence for synergy between family 2b carbohydrate binding modules in Cellulomonas fimi xylanase 11A.

Bolam DN, Xie H, White P, Simpson PJ, Hancock SM, Williamson MP, Gilbert HJ
Biochemistry 40 2468-77 (2001)
Cited: 42 times
EuropePMC logo PMID: 11327868

Abstract

Glycoside hydrolases often contain multiple copies of noncatalytic carbohydrate binding modules (CBMs) from the same or different families. Currently, the functional importance of this complex molecular architecture is unclear. To investigate the role of multiple CBMs in plant cell wall hydrolases, we have determined the polysaccharide binding properties of wild type and various derivatives of Cellulomonas fimi xylanase 11A (Cf Xyn11A). This protein, which binds to both cellulose and xylan, contains two family 2b CBMs that exhibit 70% sequence identity, one internal (CBM2b-1), which has previously been shown to bind specifically to xylan and the other at the C-terminus (CBM2b-2). Biochemical characterization of CBM2b-2 showed that the module bound to insoluble and soluble oat spelt xylan and xylohexaose with K(a) values of 5.6 x 10(4), 1.2 x 10(4), and 4.8 x 10(3) M(-1), respectively, but exhibited extremely weak affinity for cellohexaose (<10(2) M(-1)), and its interaction with insoluble cellulose was too weak to quantify. The CBM did not interact with soluble forms of other plant cell wall polysaccharides. The three-dimensional structure of CBM2b-2 was determined by NMR spectroscopy. The module has a twisted "beta-sandwich" architecture, and the two surface exposed tryptophans, Trp 570 and Trp 602, which are in a perpendicular orientation with each other, were shown to be essential for ligand binding. In addition, changing Arg 573 to glycine altered the polysaccharide binding specificity of the module from xylan to cellulose. These data demonstrate that the biochemical properties and tertiary structure of CBM2b-2 and CBM2b-1 are extremely similar. When CBM2b-1 and CBM2b-2 were incorporated into a single polypeptide chain, either in the full-length enzyme or an artificial construct comprising both CBM2bs covalently joined via a flexible linker, there was an approximate 18-20-fold increase in the affinity of the protein for soluble and insoluble xylan, as compared to the individual modules, and a measurable interaction with insoluble acid-swollen cellulose, although the K(a) (approximately 6.0 x 10(4) M(-1)) was still much lower than for insoluble xylan (K(a) = approximately 1.0 x 10(6) M(-1)). These data demonstrate that the two family 2b CBMs of Cf Xyn11A act in synergy to bind acid swollen cellulose and xylan. We propose that the increased affinity of glycoside hydrolases for polysaccharides, through the synergistic interactions of CBMs, provides an explanation for the duplication of CBMs from the same family in some prokaryotic cellulases and xylanases.

Reviews - 1heh mentioned but not cited (1)

  1. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ. Biochem J 382 769-781 (2004)

Articles - 1heh mentioned but not cited (1)

  1. Prediction of the structural motifs of sandwich proteins. Fokas AS, Gelfand IM, Kister AE. Proc Natl Acad Sci U S A 101 16780-16783 (2004)


Reviews citing this publication (6)

  1. Biotechnology of microbial xylanases: enzymology, molecular biology, and application. Subramaniyan S, Prema P. Crit Rev Biotechnol 22 33-64 (2002)
  2. The biochemistry and structural biology of plant cell wall deconstruction. Gilbert HJ. Plant Physiol 153 444-455 (2010)
  3. Advances in molecular engineering of carbohydrate-binding modules. Armenta S, Moreno-Mendieta S, Sánchez-Cuapio Z, Sánchez S, Rodríguez-Sanoja R. Proteins 85 1602-1617 (2017)
  4. Immunological Approaches to Biomass Characterization and Utilization. Pattathil S, Avci U, Zhang T, Cardenas CL, Hahn MG. Front Bioeng Biotechnol 3 173 (2015)
  5. Enzymatic polishing of cereal grains for improved nutrient retainment. Singh A, Karmakar S, Jacob BS, Bhattacharya P, Kumar SP, Banerjee R. J Food Sci Technol 52 3147-3157 (2015)
  6. Multifunctional cellulases are potent, versatile tools for a renewable bioeconomy. Glasgow E, Vander Meulen K, Kuch N, Fox BG. Curr Opin Biotechnol 67 141-148 (2021)

Articles citing this publication (34)

  1. Carbohydrate-binding modules promote the enzymatic deconstruction of intact plant cell walls by targeting and proximity effects. Hervé C, Rogowski A, Blake AW, Marcus SE, Gilbert HJ, Knox JP. Proc Natl Acad Sci U S A 107 15293-15298 (2010)
  2. 4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein. Urbanowicz BR, Peña MJ, Ratnaparkhe S, Avci U, Backe J, Steet HF, Foston M, Li H, O'Neill MA, Ragauskas AJ, Darvill AG, Wyman C, Gilbert HJ, York WS. Proc Natl Acad Sci U S A 109 14253-14258 (2012)
  3. Differential recognition of plant cell walls by microbial xylan-specific carbohydrate-binding modules. McCartney L, Blake AW, Flint J, Bolam DN, Boraston AB, Gilbert HJ, Knox JP. Proc Natl Acad Sci U S A 103 4765-4770 (2006)
  4. Glycoside hydrolase carbohydrate-binding modules as molecular probes for the analysis of plant cell wall polymers. McCartney L, Gilbert HJ, Bolam DN, Boraston AB, Knox JP. Anal Biochem 326 49-54 (2004)
  5. The modular architecture of Cellvibrio japonicus mannanases in glycoside hydrolase families 5 and 26 points to differences in their role in mannan degradation. Hogg D, Pell G, Dupree P, Goubet F, Martín-Orúe SM, Armand S, Gilbert HJ. Biochem J 371 1027-1043 (2003)
  6. New microbial mannan catabolic pathway that involves a novel mannosylglucose phosphorylase. Senoura T, Ito S, Taguchi H, Higa M, Hamada S, Matsui H, Ozawa T, Jin S, Watanabe J, Wasaki J, Ito S. Biochem Biophys Res Commun 408 701-706 (2011)
  7. Enzymatic treatments reveal differential capacities for xylan recognition and degradation in primary and secondary plant cell walls. Hervé C, Rogowski A, Gilbert HJ, Paul Knox J. Plant J 58 413-422 (2009)
  8. Co-operative binding of triplicate carbohydrate-binding modules from a thermophilic xylanase. Boraston AB, McLean BW, Chen G, Li A, Warren RA, Kilburn DG. Mol Microbiol 43 187-194 (2002)
  9. Processivity and enzymatic mode of a glycoside hydrolase family 5 endoglucanase from Volvariella volvacea. Zheng F, Ding S. Appl Environ Microbiol 79 989-996 (2013)
  10. Tertiary structure and carbohydrate recognition by the chitin-binding domain of a hyperthermophilic chitinase from Pyrococcus furiosus. Nakamura T, Mine S, Hagihara Y, Ishikawa K, Ikegami T, Uegaki K. J Mol Biol 381 670-680 (2008)
  11. Characterization of a double dockerin from the cellulosome of the anaerobic fungus Piromyces equi. Nagy T, Tunnicliffe RB, Higgins LD, Walters C, Gilbert HJ, Williamson MP. J Mol Biol 373 612-622 (2007)
  12. Reduction of starch granule size by expression of an engineered tandem starch-binding domain in potato plants. Ji Q, Oomen RJ, Vincken JP, Bolam DN, Gilbert HJ, Suurs LC, Visser RG. Plant Biotechnol J 2 251-260 (2004)
  13. Crystal structure of a family 45 endoglucanase from Melanocarpus albomyces: mechanistic implications based on the free and cellobiose-bound forms. Hirvonen M, Papageorgiou AC. J Mol Biol 329 403-410 (2003)
  14. Identification and glucan-binding properties of a new carbohydrate-binding module family. Boraston AB, Ghaffari M, Warren RA, Kilburn DG. Biochem J 361 35-40 (2002)
  15. A novel, noncatalytic carbohydrate-binding module displays specificity for galactose-containing polysaccharides through calcium-mediated oligomerization. Montanier CY, Correia MA, Flint JE, Zhu Y, Baslé A, McKee LS, Prates JA, Polizzi SJ, Coutinho PM, Lewis RJ, Henrissat B, Fontes CM, Gilbert HJ. J Biol Chem 286 22499-22509 (2011)
  16. Alpha-amylase starch binding domains: cooperative effects of binding to starch granules of multiple tandemly arranged domains. Guillén D, Santiago M, Linares L, Pérez R, Morlon J, Ruiz B, Sánchez S, Rodríguez-Sanoja R. Appl Environ Microbiol 73 3833-3837 (2007)
  17. Overexpression of the carbohydrate binding module of strawberry expansin2 in Arabidopsis thaliana modifies plant growth and cell wall metabolism. Nardi CF, Villarreal NM, Rossi FR, Martínez S, Martínez GA, Civello PM. Plant Mol Biol 88 101-117 (2015)
  18. The mannobiose-forming exo-mannanase involved in a new mannan catabolic pathway in Bacteroides fragilis. Kawaguchi K, Senoura T, Ito S, Taira T, Ito H, Wasaki J, Ito S. Arch Microbiol 196 17-23 (2014)
  19. Understanding how noncatalytic carbohydrate binding modules can display specificity for xyloglucan. Luís AS, Venditto I, Temple MJ, Rogowski A, Baslé A, Xue J, Knox JP, Prates JA, Ferreira LM, Fontes CM, Najmudin S, Gilbert HJ. J Biol Chem 288 4799-4809 (2013)
  20. Functional and structural characterization of a potent GH74 endo-xyloglucanase from the soil saprophyte Cellvibrio japonicus unravels the first step of xyloglucan degradation. Attia M, Stepper J, Davies GJ, Brumer H. FEBS J 283 1701-1719 (2016)
  21. Identification of novel biomass-degrading enzymes from genomic dark matter: Populating genomic sequence space with functional annotation. Piao H, Froula J, Du C, Kim TW, Hawley ER, Bauer S, Wang Z, Ivanova N, Clark DS, Klenk HP, Hess M. Biotechnol Bioeng 111 1550-1565 (2014)
  22. Structure of a polyisoprenoid binding domain from Saccharophagus degradans implicated in plant cell wall breakdown. Vincent F, Molin DD, Weiner RM, Bourne Y, Henrissat B. FEBS Lett 584 1577-1584 (2010)
  23. Promiscuous, non-catalytic, tandem carbohydrate-binding modules modulate the cell-wall structure and development of transgenic tobacco (Nicotiana tabacum) plants. Obembe OO, Jacobsen E, Timmers J, Gilbert H, Blake AW, Knox JP, Visser RG, Vincken JP. J Plant Res 120 605-617 (2007)
  24. High-resolution crystal structures of Caldicellulosiruptor strain Rt8B.4 carbohydrate-binding module CBM27-1 and its complex with mannohexaose. Roske Y, Sunna A, Pfeil W, Heinemann U. J Mol Biol 340 543-554 (2004)
  25. The carbohydrate-binding module of xylanase from Nonomuraea flexuosa decreases its non-productive adsorption on lignin. Zhang J, Moilanen U, Tang M, Viikari L. Biotechnol Biofuels 6 18 (2013)
  26. Modular organisation and functional analysis of dissected modular beta-mannanase CsMan26 from Caldicellulosiruptor Rt8B.4. Sunna A. Appl Microbiol Biotechnol 86 189-200 (2010)
  27. The family II carbohydrate-binding module of xylanase CflXyn11A from Cellulomonas flavigena increases the synergy with cellulase TrCel7B from Trichoderma reesei during the hydrolysis of sugar cane bagasse. Pavón-Orozco P, Santiago-Hernández A, Rosengren A, Hidalgo-Lara ME, Stålbrand H. Bioresour Technol 104 622-630 (2012)
  28. Enhanced catalytic efficiency of endo-β-agarase I by fusion of carbohydrate-binding modules for agar prehydrolysis. Alkotaini B, Han NS, Kim BS. Enzyme Microb Technol 93-94 142-149 (2016)
  29. Characterization of the substitution pattern of cellulose derivatives using carbohydrate-binding modules. von Schantz L, Schagerlöf H, Nordberg Karlsson E, Ohlin M. BMC Biotechnol 14 113 (2014)
  30. Site-directed mutagenesis of aromatic residues in the carbohydrate-binding module of Bacillus endoglucanase EGA decreases enzyme thermostability. Yin Q, Teng Y, Ding M, Zhao F. Biotechnol Lett 33 2209-2216 (2011)
  31. Characterization and application of carbohydrate-binding modules of beta-1,3-xylanase XYL4. Kiyohara M, Sakaguchi K, Yamaguchi K, Araki T, Ito M. J Biochem 146 633-641 (2009)
  32. Growth modulation effects of CBM2a under the control of AtEXP4 and CaMV35S promoters in Arabidopsis thaliana, Nicotiana tabacum and Eucalyptus camaldulensis. Keadtidumrongkul P, Suttangkakul A, Pinmanee P, Pattana K, Kittiwongwattana C, Apisitwanich S, Vuttipongchaikij S. Transgenic Res 26 447-463 (2017)
  33. Expression and characterization of full-length Ampullaria crossean endoglucanase EG65s and their two functional modules. Yin Q, Teng Y, Li Y, Ding M, Zhao F. Biosci Biotechnol Biochem 75 240-246 (2011)
  34. Native structure of mosquito salivary protein uncovers domains relevant to pathogen transmission. Liu S, Xia X, Calvo E, Zhou ZH. Nat Commun 14 899 (2023)


Quick links