Understanding how noncatalytic carbohydrate binding modules can display specificity for xyloglucan

Journal of Biological Chemistry

Volumn 288, Issue 7, 2013, Pages 4799-4809

  Luís, Ana S ^a   Venditto, Immacolata ^a   Temple, Max J ^b   Rogowski, Artur ^b   Baslé, Arnaud ^b   Xue, Jie ^c   Knox, J Paul ^c   Prates, José A M ^a   Ferreira, Luís M A ^a   Fontes, Carlos M G A ^a   Najmudin, Shabir ^a   Gilbert, Harry J ^b  

^a UNIVERSITY OF LISBON   (Portugal)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE BINDING MODULES; ENZYMATIC DEGRADATION; GLUCANS; NON-CATALYTIC; POLYSACCHARIDE STRUCTURE; SIDE CHAIN STRUCTURE; SIDE-CHAINS; XYLOGLUCANS;

ORGANIC COMPOUNDS;

POLYSACCHARIDES;

BETA GLUCAN; CARBOHYDRATE BINDING MODULE 65A; CARBOHYDRATE BINDING MODULE 65B; CARBOHYDRATE BINDING PROTEIN; GLUCAN SYNTHASE; POLYSACCHARIDE; UNCLASSIFIED DRUG; XYLOGLUCAN;

ARTICLE; BETA SHEET; CARBOHYDRATE SYNTHESIS; CONTROLLED STUDY; ENZYME BINDING; ENZYME DEGRADATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; EUBACTERIUM; EUBACTERIUM CELLULOSOLVENS; HYDROPHOBICITY; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PURIFICATION; SITE DIRECTED MUTAGENESIS; XYLOSE TEST;

BETA-GLUCANS; BINDING SITES; CALORIMETRY; CARBOHYDRATES; CATALYSIS; CELL WALL; CELLULOSE; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GLUCANS; KINETICS; LIGANDS; MUTAGENESIS, SITE-DIRECTED; OLIGOSACCHARIDES; POLYSACCHARIDES; PROTEIN BINDING; PROTEIN CONFORMATION; THERMODYNAMICS; XYLANS;

EID: 84873599781     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.432781     Document Type: Article

References (44)

1. Flint, H. J., and Duncan., S. H., Scott, K. P., and Louis, P. (2007) Interactions and competition within the microbial community of the human colon. Links between diet and health. Environ. Microbiol. 9, 1101-1111
2. Mackie, R. I., and White, B. A. (1990) Recent advances in rumen microbial ecology and metabolism. Potential impact on nutrient output. J. Dairy Sci. 73, 2971-2995
3. Himmel, M. E., and Bayer, E. A. (2009) Lignocellulose conversion to biofuels. Current challenges, global perspectives. Curr. Opin. Biotechnol. 20, 316-317
4. Himmel, M. E., and Ding., S. Y., Johnson, D. K., Adney, W. S., and Nimlos., M. R., Brady, J. W., and Foust, T. D. (2007) Biomass recalcitrance. Engineering plants and enzymes for biofuels production. Science 315, 804-807
5. Gilbert, H. J. (2010) The biochemistry and structural biology of plant cell wall deconstruction. Plant Physiol. 153, 444-455
6. Boraston, A. B., and Bolam., D. N., Gilbert, H. J., and Davies, G. J. (2004) Carbohydrate-binding modules. Fine-tuning polysaccharide recognition. Biochem. J. 382, 769-781
7. Cantarel, B. L., and Coutinho., P. M., Rancurel, C, Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy). An expert resource for Glycogenomics. Nucleic Acids Res. 37, D233-238
8. Boraston, A. B., Kwan, E., Chiu, P., Warren, R.A., and Kilburn, D.G. (2003) Recognition and hydrolysis of noncrystalline cellulose. J. Biol. Chem. 278, 6120-6127
9. Hervé, C, Rogowski, A., Blake, A. W., Marcus, S. E., Gilbert, H. J., and Knox, J. P. (2010) Carbohydrate-binding modules promote the enzymatic deconstruction of intact plant cell walls by targeting and proximity effects. Proc. Natl. Acad. Sci. U.S.A. 107, 15293-15298
10. Tomme, P., Van Tilbeurgh, H., Pettersson, G., Van Damme, J., Vandekerckhove, J., Knowles, J., Teeri, T., and Claeyssens, M. (1988) Studies of the cellulolytic system of Trichoderma reesei QM 9414. Analysis of domain function in two cellobiohydrolases by limited proteolysis. Eur. J. Biochem. 170, 575-581
11. Boraston, A. B., Nurizzo, D., Notenboom, V., Ducros, V., and Rose., D. R., Kilburn, D. G., and Davies, G. J. (2002) Differential oligosaccharide recognition by evolutionarily-related f31, 4-and β1, 3-glucan-binding modules. J. Mol. Biol. 319, 1143-1156
12. Najmudin, S., Guerreiro, C I., Carvalho, A. L., Prates, J. A., Correia, M. A., Alves, V D., Ferreira, L. M., Romão, M. J., Gilbert, H. J., Bolam, D. N., and Fontes, C. M. (2006) Xyloglucan is recognized by carbohydrate-binding modules that interact with β-glucan chains. J. Biol. Chem. 281, 8815-8828
13. Simpson, P. J., and Bolam., D. N., Cooper, A., Ciruela, A., Hazlewood, G. P., and Gilbert., H. J., and Williamson, M. P. (1999) A family IIb xylan-binding domain has a similar secondary structure to a homologous family IIa cellulose-binding domain but different ligand specificity. Structure 7, 853-864
14. Czjzek, M., Bolam, D. N, Mosbah, A., Allouch, J., Fontes, C. M., Ferreira, L. M., Bornet, O., Zamboni, V., Darbon, H., Smith, N. L., Black, G. W., Henrissat, B., and Gilbert, H. J. (2001) The location of the ligand-binding site of carbohydrate-binding modules that have evolved from a common sequence is not conserved. J. Biol. Chem. 276, 48580-48587
15. Montanier, C. Y., and Correia., M. A., Flint, J. E., Zhu, Y., Baslé, A., McKee, L. S., and Prates., J. A., Polizzi, S. J., Coutinho, P. M., and Lewis., R. J., Henrissat, B., Fontes, C. M., and Gilbert, H. J. (2011) A novel, noncatalytic carbohydrate-binding module displays specificity for galactose-containing polysaccharides through calcium-mediated oligomerization. J. Biol. Chem. 286, 22499-22509
16. Creagh, A. L., Ong, E., Jervis, E., Kilburn, D. G., and Haynes, C. A. (1996) Binding of the cellulose-binding domain of exoglucanase Cex from Cellulomonasfimi to insoluble microcrystalline cellulose is entropically driven. Proc. Natl. Acad. Sci. U.S.A. 93, 12229-12234
17. Henshaw, J. L., Bolam, D. N, Pires, V. M., Czjzek, M., Henrissat, B., Ferreira, L. M., Fontes, C. M., and Gilbert, H. J. (2004) The family 6 carbohydrate binding module CmCBM6-2 contains two ligand-binding sites with distinct specificities. J. Biol. Chem. 279, 21552-21559
18. Yoda, K., Toyoda, A., Mukoyama, Y., Nakamura, Y., and Minato, H. (2005) Cloning, sequencing, and expression of a Eubacterium cellulosolvens 5 gene encoding an endoglucanase (Cel5A) with novel carbohydrate-binding modules, and properties of Cel5A. Appl. Environ. Microbiol. 71, 5787-5793
19. Najmudin, S., Guerreiro, C I., Ferreira, L. M., Romão, M. J., Fontes, C. M., and Prates, J. A. (2005) Overexpression, purification and crystallization of the two C-terminal domains of the bifunctional cellulase ctCel9D-Cel44A from Clostridium thermocellum. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61, 1043-1045
20. Carvalho, A. L., Goyal, A., Prates, J. A., and Bolam., D. N., Gilbert, H. J., Pires, V. M., and Ferreira., L. M., Planas, A., Romão, M. J., and Fontes, C. M. (2004) The family 11 carbohydrate-binding module of Clostridium thermocellum Lic26A-Cel5E accommodates β1, 4-and β1, 3-1, 4-mixed linked glucans at a single binding site. J. Biol. Chem. 279, 34785-34793
21. McCartney, L., and Blake., A. W., Flint, J., Bolam, D.N., Boraston, A.B., and Gilbert., H. J., and Knox, J. P. (2006) Differential recognition of plant cell walls by microbial xylan-specific carbohydrate-binding modules. Proc. Natl. Acad. Sci. U.S.A. 103, 4765-4770
22. McCartney, L., and Gilbert., H. J., Bolam, D. N., Boraston, A. B., and Knox, J. P. (2004) Glycoside hydrolase carbohydrate-binding modules as molecular probes for the analysis of plant cell wall polymers. Anal. Biochem. 326, 49-54
23. Marcus, S. E., Verhertbruggen, Y., Hervé, C, Ordaz-Ortiz, J. J., Farkas, V., Pedersen, H. L., Willats, W. G., and Knox, J. P. (2008) Pectic homogalac-turonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol. 8, 60
24. Leslie, A. G. W. (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4/ESF-EAMCB Newsl. Protein Crystallogr. 26, 27-33
25. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
26. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr. D 62, 72-82
27. Winn, M. D., Ballard, C. C, Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N, Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
28. Luis, A. S., and Alves., V. D., Romao, M. J., Prates, J. A., and Fontes., C. M., and Najmudin, S. (2011) Overproduction, purification, crystallization and preliminary x-ray characterization of a novel carbohydrate-binding module of endoglucanase Cel5A from Eubacterium cellulosolvens. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67, 491-493
29. McCoy, A.J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C, and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
30. Murshudov, G. N, Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
31. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
32. Vagin, A., and Teplyakov, A. (1997) MOLREP. An automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025
33. Bolam, D. N, Xie, H, Pell, G., Hogg, D., Galbraith, G., Henrissat, B., and Gilbert, H. J. (2004) X4 modules represent a new family of carbohydrate-binding modules that display novel properties. J. Biol. Chem. 279, 22953-22963
34. Henshaw, J., Horne-Bitschy, A., van Bueren, A. L., Money, V. A., Bolam, D. N., Czjzek, M., Ekborg, N. A., Weiner, R. M., Hutcheson, S. W., Davies, G. J., Boraston, A. B., and Gilbert, H. J. (2006) Family 6 carbohydrate binding modules in β-agarases display exquisite selectivity for the non-reducing termini of agarose chains. J. Biol. Chem. 281, 17099-17107
35. Simpson, P. J., and Jamieson., S. J., Abou-Hachem, M., Karlsson, E. N, Gilbert, H. J., Holst, O., and Williamson, M. P. (2002) The solution structure of the CBM4-2 carbohydrate binding module from a thermostable Rhodothermus marinus xylanase. Biochemistry 41, 5712-5719
36. Money, V. A., Cartmell, A., Guerreiro, C. I., and Ducros., V. M., Fontes, C M., Gilbert, H. J., and Davies, G. J. (2008) Probing the β-1, 3:1, 4-glucanase, CtLic26A, with a thio-oligosaccharide and enzyme variants. Org. Biomol. Chem. 6, 851-853
37. Nieduszy, I., and Marchess, R. H. (1972) Structure of β-D-(1-4')-xylan hydrate. Biopolymers 11, 1335-1344
38. Simpson, P. J., Xie, H, and Bolam., D. N., Gilbert, H. J., and Williamson, M. P. (2000) The structural basis for the ligand specificity of family 2 carbohydrate-binding modules. J. Biol. Chem. 275, 41137-41142
39. Boraston, A. B., Healey, M., Klassen, J., Ficko-Blean, E., Lammerts van Bueren, A., and Law, V. (2006) A structural and functional analysis of α-glucan recognition by family 25 and 26 carbohydrate-binding modules reveals a conserved mode of starch recognition. J. Biol. Chem. 281, 587-598
40. Charnock, S. J., Bolam, D. N, Nurizzo, D., Szabó, L., McKie, V. A., Gilbert, H. J., and Davies, G. J. (2002) Promiscuity in ligand-binding. The three-dimensional structure of a Piromyces carbohydrate-binding module, CBM29-2, in complex with cello-and mannohexaose. Proc. Natl. Acad. Sci. U.S.A. 99, 14077-14082
41. Bolam, D. N, Xie, H, White, P., Simpson, P. J., Hancock, S. M., Williamson, M. P., and Gilbert, H.J. (2001) Evidence for synergy between family 2b carbohydrate binding modules in Cellulomonas fimi xylanase 11A. Biochemistry 40, 2468-2477
42. Flint, J., Nurizzo, D., Harding, S. E., Longman, E., and Davies., G. J., Gilbert, H. J., and Bolam, D. N. (2004) Ligand-mediated dimerization of a carbohydrate-binding molecule reveals a novel mechanism for protein-carbohydrate recognition. J. Mol. Biol. 337, 417-426
43. Szabo, L., Jamal, S., Xie, H., Charnock, S. J., and Bolam., D. N., Gilbert, H. J., and Davies, G.J. (2001) Structure of a family 15 carbohydrate-binding module in complex with xylopentaose. Evidence that xylan binds in an approximate 3-fold helical conformation. J. Biol. Chem. 276, 49061-49065
44. McLean, B. W., and Bray., M. R., Boraston, A. B., Gilkes, N. R., and Haynes., C. A., and Kilburn, D. G. (2000) Analysis of binding of the family 2a carbohydrate-binding module from Cellulomonas fimi xylanase 10A to cellulose. Specificity and identification of functionally important amino acid residues. Protein Eng 13, 801-809