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The crystal structure of the family 6 carbohydrate binding module from Cellvibrio mixtus endoglucanase 5a in complex with oligosaccharides reveals two distinct binding sites with different ligand specificities.

Pires VM, Henshaw JL, Prates JA, Bolam DN, Ferreira LM, Fontes CM, Henrissat B, Planas A, Gilbert HJ, Czjzek M
J Biol Chem 279 21560-8 (2004)
Related entries: 1uxx, 1uxz, 1uy0, 1uyx, 1uyy, 1uyz

Cited: 44 times
EuropePMC logo PMID: 15010454

Abstract

Glycoside hydrolases that release fixed carbon from the plant cell wall are of considerable biological and industrial importance. These hydrolases contain non-catalytic carbohydrate binding modules (CBMs) that, by bringing the appended catalytic domain into intimate association with its insoluble substrate, greatly potentiate catalysis. Family 6 CBMs (CBM6) are highly unusual because they contain two distinct clefts (cleft A and cleft B) that potentially can function as binding sites. Henshaw et al. (Henshaw, J., Bolam, D. N., Pires, V. M. R., Czjzek, M., Henrissat, B., Ferreira, L. M. A., Fontes, C. M. G. A., and Gilbert, H. J. (2003) J. Biol. Chem. 279, 21552-21559) show that CmCBM6 contains two binding sites that display both similarities and differences in their ligand specificity. Here we report the crystal structure of CmCBM6 in complex with a variety of ligands that reveals the structural basis for the ligand specificity displayed by this protein. In cleft A the two faces of the terminal sugars of beta-linked oligosaccharides stack against Trp-92 and Tyr-33, whereas the rest of the binding cleft is blocked by Glu-20 and Thr-23, residues that are not present in CBM6 proteins that bind to the internal regions of polysaccharides in cleft A. Cleft B is solvent-exposed and, therefore, able to bind ligands because the loop, which occludes this region in other CBM6 proteins, is much shorter and flexible (lacks a conserved proline) in CmCBM6. Subsites 2 and 3 of cleft B accommodate cellobiose (Glc-beta-1,4-Glc), subsite 4 will bind only to a beta-1,3-linked glucose, whereas subsite 1 can interact with either a beta-1,3- or beta-1,4-linked glucose. These different specificities of the subsites explain how cleft B can accommodate beta-1,4-beta-1,3- or beta-1,3-beta-1,4-linked gluco-configured ligands.

Reviews - 1uz0 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 - 1uz0 mentioned but not cited (2)

  1. Structure and function of an arabinoxylan-specific xylanase. Correia MA, Mazumder K, Brás JL, Firbank SJ, Zhu Y, Lewis RJ, York WS, Fontes CM, Gilbert HJ. J Biol Chem 286 22510-22520 (2011)
  2. The β-glucanase ZgLamA from Zobellia galactanivorans evolved a bent active site adapted for efficient degradation of algal laminarin. Labourel A, Jam M, Jeudy A, Hehemann JH, Czjzek M, Michel G. J Biol Chem 289 2027-2042 (2014)


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  4. Structural insights into Bacillus thuringiensis Cry, Cyt and parasporin toxins. Xu C, Wang BC, Yu Z, Sun M. Toxins (Basel) 6 2732-2770 (2014)
  5. Using structure to inform carbohydrate binding module function. Abbott DW, van Bueren AL. Curr Opin Struct Biol 28 32-40 (2014)

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  17. Binding sub-site dissection of a carbohydrate-binding module reveals the contribution of entropy to oligosaccharide recognition at "non-primary" binding subsites. Lammerts van Bueren A, Boraston AB. J Mol Biol 340 869-879 (2004)
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  27. Development and Evaluation of GlycanDock: A Protein-Glycoligand Docking Refinement Algorithm in Rosetta. Nance ML, Labonte JW, Adolf-Bryfogle J, Gray JJ. J Phys Chem B (2021)
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  30. The family 6 Carbohydrate Binding Module (CtCBM6) of glucuronoxylanase (CtXynGH30) of Clostridium thermocellum binds decorated and undecorated xylans through cleft A. Verma AK, Bule P, Ribeiro T, Brás JL, Mukherjee J, Gupta MN, Fontes CM, Goyal A. Arch Biochem Biophys 575 8-21 (2015)
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  34. Over 100-Year Preservation and Temporal Fluctuations of Cell Wall Polysaccharides in Marine Sediments. Salmeán AA, Willats WGT, Ribeiro S, Andersen TJ, Ellegaard M. Front Plant Sci 13 785902 (2022)
  35. GH-16 Type β-1,3-Glucanase from Lysobacter sp. MK9-1 Enhances Antifungal Activity of GH-19 Type Chitinase, and Its Glucan-binding Domain Binds to Fungal Cell-wall. Otsuka Y, Sato K, Yano S, Kanno H, Suyotha W, Konno H, Makabe K, Taira T. J Appl Glycosci (1999) 69 49-56 (2022)
  36. Novel thermostable GH5_34 arabinoxylanase with an atypical CBM6 displays activity on oat fiber xylan for prebiotic production. Norlander S, Jasilionis A, Ara ZGK, Grey C, Adlercreutz P, Karlsson EN. Glycobiology 33 490-502 (2023)


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