Binding of β-d-glucosides and β-d-mannosides by rice and barley β-d-glycosidases with distinct substrate specificities

Biochemistry

Volumn 49, Issue 40, 2010, Pages 8779-8793

  Kuntothom, Teerachai ^a,f   Raab, Michal ^b   Tvaroška, Igor ^b   Fort, Sebastien ^c   Pengthaisong, Salila ^a   Cañada, Javier ^d   Calle, Luis ^d   Jiménez Barbero, Jesús ^d   Ketudat Cairns, James R ^a   Hrmova, Maria ^b,e  

^a SURANAREE UNIVERSITY OF TECHNOLOGY   (Thailand)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

^c CENTRE DE RECHERCHES SUR LES MACROMOLÉCULES VÉGÉTALES CERMAV CNRS   (France)

^d CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^e UNIVERSITY OF ADELAIDE   (Australia)

^f MAHASARAKHAM UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ACTIVE SITE RESIDUES; APPARENT K; CATALYTIC SITES; COMPUTATIONAL DATA; GLUCOSIDASE; GLYCOSIDASES; KINETIC ANALYSIS; MANNOSIDASE; NUCLEAR OVERHAUSER EFFECTS; O-LINKED; SATURATION-TRANSFER DIFFERENCES; SMALL VARIATIONS; SUBSTRATE SPECIFICITY;

CATALYSTS; CONFORMATIONS; DOCKING; ENZYMES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; RESONANCE; SUBSTRATES; SUGARS;

NUCLEAR MAGNETIC RESONANCE;

CARBON; GLUCOSIDE; GLYCOSIDASE; MANNOSIDE; THIOGLYCOSIDE;

ARTICLE; BARLEY; COMPETITIVE INHIBITION; CONFORMATION; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; GEOMETRY; KINETICS; MOLECULAR DOCKING; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PREDICTION; PRIORITY JOURNAL; QUANTUM MECHANICS; RICE; SCORING SYSTEM;

BETA-GLUCOSIDASE; BETA-MANNOSIDASE; GLYCOSIDES; HORDEUM; MANNOSIDES; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; ORYZA SATIVA; PROTEIN BINDING; SUBSTRATE SPECIFICITY;

HORDEUM;

EID: 77957668081     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101112c     Document Type: Article

References (60)

1. Cantarel, B. L., 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-D238
2. Hrmova, M. and Fincher, G. B. (2009) Depolymerizing enzymes. In Chemistry, Biochemistry and Biology of (1,3)-β- d -Glucans and Related Polysaccharides (Bacic, T., Fincher, G. B., and Stone, B. A., Eds.) pp 119 - 170, Academic Press and Elsevier Inc., San Diego.
3. Hrmova, M., Harvey, A. J., Wang, J., Shirley, N. J., Jones, G. P., Stone, B. A., Høj, P. B., and Fincher, G. B. (1996) Barley β- d -glucan exohydrolases with β- d -glucosidase activity. Purification and determination of primary structure from a cDNA clone J. Biol. Chem. 271, 5277-5286
4. Hrmova, M., MacGregor, E. A., Biely, P., Stewart, R. J., and Fincher, G. B. (1998) Substrate binding and catalytic mechanism of a barley β- d -glucosidase/(1,4)-β- d -glucan exohydrolase J. Biol. Chem. 273, 11134-11143
5. Hrmova, M., Burton, R. A., Biely, P., Lahnstein, J., and Fincher, G. B. (2006) Hydrolysis of (1,4)-β- d -mannans in barley (Hordeum vulgare L.) is mediated by a concerted action of a (1,4)-β- d -mannan endohydrolase and a β- d -mannosidase Biochem. J. 399, 77-90
6. Kuntothom, T., Luang, S., Fincher, G. B., Opassiri, R., Hrmova, M., and Ketudat Cairns, J. R. (2008) Closely related barley and rice family GH1 glycosyl hydrolases with β- d -glucosidase and β- d -mannosidase activities Arch. Biochem. Biophys. 491, 85-95
7. Opassiri, R., Hua, Y., Wara-aswapati, O., Akiyama, T., Svasti, J., Esen, A., and Ketudat Cairns, J. R. (2004) β-Glucosidase, exo-β-glucanase and pyridoxine transglucosylase activities of rice BGlu1 Biochem. J. 379, 125-131
8. Marana, S. R. (2006) Molecular basis of substrate specificity in family 1 glycoside hydrolases IUMB Life 58, 6-73
9. Vocadlo, D. J. and Davies, G. J. (2008) Mechanistic insights into glycosidase chemistry Curr. Opin. Chem. Biol. 12, 539-555
10. Burmeister, W. P., Cottaz, S., Driguez, H., Iori, R., Palmieri, S., and Henrissat, B. (1997) The crystal structures of Sinapis alba myrosinase and a covalent glycosyl-enzyme intermediate provide insights into the substrate recognition and active-site machinery of an S-glycosidase Structure 5, 663-675
11. Zechel, D. L. and Withers, S. G. (2001) Dissection of nucleophilic and acid-base catalysis in glycosidases Curr. Opin. Chem. Biol. 5, 643-649
12. Vallmitjana, M., Ferrer-Navarro, M., Planell, R., Abel, M., Querol, E., Planas, A., and Pérez-Pons, J.-A. (2001) Mechanism of the family β-glucosidase from Streptomyces sp.: Catalytic residues and kinetic studies Biochemistry 40, 5975-5982
13. Ly, H. D. and Withers, S. G. (1999) Mutagenesis of glycosidases Annu. Rev. Biochem. 68, 487-522
14. Cicek, M., Blanchard, D., Bevan, D. R., and Esen, A. (2000) The aglycone specificity-determining sites are different in 2,4-dihydroxy-7-methoxy-1,4- benzoxazin-3-one (DIMBOA)-glucosidase (maize β-glucosidase) and dhurrinase (sorghum β-glucosidase) J. Biol. Chem. 275, 20002-20011
15. Czjzek, M., Cicek, M., Zamboni, V., Bevan, D. R., Henrissat, B., and Esen, A. (2000) The mechanism of substrate (aglycone) specificity in β-glucosidases is revealed by crystal structures of mutant maize β-glucosidase-DIMBOA, -DIMBOAGlc, and -dhurrin complexes Proc. Natl. Acad. Sci. U.S.A. 97, 13555-13560
16. Chuenchor, W., Pengthaisong, S., Robinson, R. C., Jirundon, Y., Esen, A., Chen, C.-J., Opassiri, R., Svasti, J., and Ketudat Cairns, J. R. (2008) Structural insights into rice BGlu1 β-glucosidase oligosaccharide hydrolysis and transglycosylation J. Mol. Biol. 377, 1200-1215
17. Street, I. P., Kempton, J. B., and Withers, S. G. (1992) Inactivation of a β-glucosidase through the accumulation of a stable 2-deoxy-2-fluoro- β- d -glucopyranosyl-enzyme intermediate: A detailed investigation Biochemistry 31, 9970-9978
18. 3 from Aspergillus wentii Biochim. Biophys. Acta 626, 459-465
19. Aguilar, C. F., Sanderson, I., Moracci, M., Ciaramella, M., Nucci, R., Rossi, M., and Pearl, L. H. (1997) Crystal structure of the β-glycosidase from the hyperthermophilic archeon Sulfolobus solfataricus: Resilience as a key factor in thermostability J. Mol. Biol. 271, 789-802
20. Verdoucq, L., Moriniere, J., Bevan, D. R., Esen, A., Vasella, A., Henrissat, B., and Czjzek, M. (2004) Structural determinants of substrate specificity in family 1 β-glucosidases: Novel insights from the crystal structure of sorghum dhurrinase-1, a plant β-glucosidase with strict specificity, in complex with its natural substrate J. Biol. Chem. 279, 31796-31803
21. Sulzenbacher, G., Driguez, H., Henrissat, B., Schülein, M., and Davies, G. J. (1996) Structure of the Fusarium oxysporum endoglucanase I with a nonhydrolyzable substrate analogue: Substrate distortion gives rise to the preferred axial orientation for the leaving group Biochemistry 35, 15280-15287
22. Hrmova, M., De Gori, R., Smith, B. J., Fairweather, J. K., Driguez, H., Varghese, J. N., and Fincher, G. B. (2002) Structural basis for a broad specificity in higher plant β- d -glucan glucohydrolases Plant Cell 14, 1033-1052
23. Money, V., Cartmell, A., Guerreiro, C. I. P. D., Ducros, V. M.-A., Fontes, C. M. G. A., Gilbert, H. J., and Davies, G. J. (2008) Probing the β-1,3:1,4 glucanase, Ct Lic26A, with a thio-oligosaccharide and enzyme variants Org. Biomol. Chem. 6, 851-853
24. Opassiri, R., Ketudat Cairns, J. R., Akiyama, T., Wara-aswapati, O., Svasti, J., and Esen, A. (2003) Characterization of a rice β-glucosidase highly expressed in flower and germinating shoot Plant Sci. 165, 627-638
25. Blanc-Muesser, M., Defaye, J., and Driguez, H. (1978) Syntheses stereoselectives de 1-thioglucosides Carbohydr. Res. 67, 305-328
26. Chuenchor, W., Pengthaisong, S., Yuvaniyama, J., Opassiri, R., Svasti, J., and Ketudat Cairns, J. R. (2006) Purification, crystallization and preliminary X-ray analysis of rice BGlu1 β-glucosidase with and without 2-deoxy-2-fluoro-β- d -glucoside inhibitor Acta Crystallogr. F62, 798-801
27. Vogtherr, M. and Peters, T. (2000) Application of NMR based binding assays to identify key hydroxyl groups for intermolecular recognition J. Am. Chem. Soc. 122, 6093-6099
28. Clavel, C., Canales, A., Gupta, G., Cañada, F. J., Penadés, S., Suriola, A., and Jiménez-Barbero, J. (2007) NMR investigation of the bound conformation of natural and synthetic oligomannosides to banana lectin Eur. J. Org. Chem. 10, 1577-1585
29. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997) The CLUSTAL-X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res. 24, 4876-4882
30. Kim, D. E., Chivian, D., and Baker, D. (2004) Protein structure prediction and analysis using the Robetta server Nucleic Acids Res. 32 (Suppl. 2) W256-W231
31. Sali, A. and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234, 779-815
32. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291
33. Vriend, G. (1990) WHAT IF: A molecular modeling and drug design program J. Mol. Graphics 8, 52-56
34. Lüthy, R., Bowie, J. E., and Eisenberg, D. (1992) Assessment of protein models with three-dimensional profiles Nature 356, 83-85
35. Sippl, M. J. (1993) Recognition of errors in 3-dimensional structures of proteins Proteins: Struct., Funct., Bioinf. 17, 355-362
36. Sumathi, K., Ananthalakshmi, P., Md Roshan, M. B. A., and Sekar, K. (2006) 3dSS: 3D structural superposition Nucleic Acids Res. 34, W128-W134
37. DeLano, W. (2009) The PyMOL Molecular Graphics System, DeLano Scientific LLC, San Carlos, CA.
38. Weisel, M., Proschak, E., and Schneider, G. (2007) PocketPicker: Analysis of ligand-binding sites with shape descriptors Chem. Cent. J. 1, 7
39. MacroModel, version 9.6 (2008) Schrödinger, LLC, New York.
40. Zhao, Y., Schultz, N. E., and Truhlar, D. G. (2005) Exchange-correlation functional with broad accuracy for metallic and nonmetallic compounds, kinetics, and noncovalent interactions J. Chem. Phys. 123, 161103
41. Zhao, Y., Schultz, N. E., and Truhlar, D. G. (2006) Design of density functionals by combining the method of constraint satisfaction with parametrization for thermochemistry, thermochemical kinetics, and noncovalent interactions J. Chem. Theory Comput. 2, 364-382
42. Zheng, J., Zhao, Y., and Truhlar, D. G. (2007) Representative benchmark suites for barrier heights of diverse reaction types and assessment of electronic structure methods for thermochemical kinetics J. Chem. Theory Comput. 3, 569-582
43. Jorgensen, W. L., Maxwell, D. S., and Tirado-Rives, J. (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids J. Am. Chem. Soc. 118, 11225-11236
44. Friesner, R. A., Banks, J. L., Murphy, R. B., Halgren, T. A., Klicic, J. J., Mainz, D. T., Repasky, M. P., Knoll, E. H., Shelley, M., Perry, J. K., Shaw, D. E., Francis, P., and Shenkin, P. S. (2004) Glide: A new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy J. Med. Chem. 47, 1739-1749
45. Tvaroška, I. and Carver, J. P. (1996) Ab initio molecular orbital calculation of carbohydrate model compounds. 5. Anomeric, exo-anomeric, and reverse anomeric effects in C-, N-, and S-glycosyl compounds J. Phys. Chem. 100, 11305-11313
46. Rempel, B. P. and Withers, S. G. (2008) Covalent inhibitors of glycosidases and their applications in biochemistry and biology Glycobiology 18, 570-586
47. Blanchard, J. E. and Withers, S. G. (2001) Rapid screening of the aglycone specificity of glycosidases: Applications to enzymatic synthesis of oligosaccharides Chem. Biol. 8, 627-633
48. Davulcu, O., Flynn, P. F., Chapman, M. S., and Skalicky, J. J. (2009) Intrinsic domain and loop dynamics commensurate with catalytic turnover in an induced-fit enzyme Structure 17, 1356-1367
49. Ermert, P., Rupitz, K., Vasella, A., Weber, M., and Withers, S. G. (1993) Transition state analogue inhibitors of glycosidases are configurationally selective: A study with nojiritetrazoles, a new class of glycosidase inhibitors Carbohydr. Res. 250, 113-128
50. Hrmova, M., Streltsov, V. A., Smith, B. J., Vasella, A., Varghese, J. N., and Fincher, G. B. (2005) Structural rationale for low nanomolar binding of transition state mimics to a family GH3 β- d -glucan glucohydrolase from barley Biochemistry 44, 16529-16539
51. Gloster, T. M., Meloncelli, P., Stick, R. V., Zechel, D., Vasella, A., and Davies, G. J. (2007) Glycosidase inhibition: An assessment of the binding of 18 putative transition-state mimics J. Am. Chem. Soc. 129, 2345-2354
52. Bras, N. F., Moura-Tamares, A., Fernandes, P. A., and Ramos, M. J. (2008) Mechanistic studies on the formation of glycosidase-substrate and glycosidase-inhibitor covalent intermediates J. Comput. Chem. 29, 2565-2574
53. Martin-Pastor, M., Vega-Vázquez, M., De Capua, A., Canales, A., Andre, S., Gabius, H. J., and Jiménez-Barbero, J. (2006) Enhanced signal dispersion in saturation transfer difference experiments by conversion to a 1D-STD-homodecoupled spectrum J. Biomol. NMR 36, 103-109
54. Englebienne, P., Fiaux, H., Kuntz, D. A., Corbeil, C. R., Gerber-Lemaire, S., Rose, D. R., and Moitessier, N. (2007) Evaluation of docking programs for predicting binding of Golgi α-mannosidase II inhibitors: A comparison with crystallography Proteins 69, 160-176
55. Money, V. A., Smith, N. L., Scaffidi, A., Stick, R. V., Gilbert, H. J., and Davies, G. J. (2006) Substrate distortion by a lichenase highlights the different conformational itineraries harnessed by related glycoside hydrolases Angew. Chem., Int. Ed. 45, 5136-5140
56. Offen, W. A., Zechel, D. L., Withers, S. G., Gilbert, H. J., and Davies, G. J. (2009) Structure of the Michaelis complex of β-mannosidase, Man2A, provides insight into the conformational itinerary of mannoside hydrolysis Chem. Commun., 2484-2486
57. Nam, K. H., Sung, M. W., and Hwang, K. Y. (2010) Structural insights into the substrate specificity of β-glucosidase Biochem. Biophys. Res. Commun. 391, 1131-1135
58. Tailford, L. E., Ducros, V. M., Flint, J. E., Roberts, S. M., Morland, C., Zechel, D. L., Smith, N., Bjørnvad, M. E., Borchert, T. V., Wilson, K. S., Davies, G. J., and Gilbert, H. J. (2009) Understanding how diverse β-mannanases recognize heterogeneous substrates Biochemistry 48, 7009-7018
59. Fersht, A. (1999) Structure and Mechanism in Protein Science, pp 1 - 631, W. H. Freeman and Co., New York.
60. Hrmova, M. and Fincher, G. B. (2009) Functional genomics and structural biology in the definition of gene function. In Methods in Molecular Biology: Plant Genomics (Somers, D., Langridge, P., and Gustafson, P., Eds.) Vol. 513, pp 175 - 198, Humana Press Inc., Totowa, NJ.