Catalysis and specificity in enzymatic glycoside hydrolysis: A 2,5 B conformation for the glycosyl-enzyme intermediate revealed by the structure of the Bacillus agaradhaerens family 11 xylanase

Chemistry and Biology

Volumn 6, Issue 7, 1999, Pages 483-492

  Sabini, Elisabetta ^a   Sulzenbacher, Gerlind ^a,b   Dauter, Miroslava ^a   Dauter, Zbigniew ^a   Jørgensen, Per Linå ^c   Schülein, Martin ^c   Dupont, Claude ^d   Davies, Gideon J ^a   Wilson, Keith S ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c NOVO NORDISK A S   (Denmark)

^d INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

Boat conformation; Enzyme specificity; Transition state; Xylanase

Indexed keywords

EID: 0033169002     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-5521(99)80066-0     Document Type: Article

References (48)

1. Henrissat, B. & Bairoch, A. (1996). Updating the sequence-based classification of glycosyl hydrolases. Biochem. J. 316, 695-696.
2. Henrissat, B. (1991). A classification of glycosyl hydrolases based on amino-acid sequence similarities. Biochem. J. 280, 309-316.
3. Davies, G., Sinnott, M.L. & Withers, S.G. (1997). Glycosyl transfer. In Comprehensive Biological Catalysis Vol. 1. (Sinnott, M.L. ed.) pp. 119-209. Academic Press, London.
4. Koshland, D.E. (1953). Stereochemistry and the mechanism of enzymatic reactions. Biol. Rev. 28, 416-436.
5. Withers, S.G., Street, I.P., Bird, P. & Dolphin, D.H. (1987). 2-deoxy-2-fluoroglucosides: A novel class of mechanism-based glucosidase inhibitors. J. Am. Chem. Soc. 109, 7530-7531.
6. Burmeister, W.P., Cottaz, S., Driguez, H., Palmieri, S. & Henrissat, B. (1997). The crystal structures of Sinapis alba myrosinase and of a covalent glycosyl-enzyme intermediate provide insights into the substrate recognition and active-site machinary of an S-glycosidase. Structure 5, 663-675.
7. Davies, G.J., et al., & Withers, S.G.(1998). Shots along an enzymatic reaction coordinate: Analysis of a retaining β-glycoside hydrolase. Biochemistry 37, 11707-11713.
8. White, A., Tull, D., Johns, K., Withers, S.G. & Rose, D.R. (1996). Crystallographic observation of a covalent catalytic intermediate in a β-glycosidase. Nat. Struct. Biol. 3, 149-154.
9. Notenboom, V., Birsan, C., Warren, R.A.J., Withers, S.G. & Rose, D.R. (1998). Exploring the cellulose/xylan specificty of the β-1,4-glycanase Cex from Cellulomonas fimi through crystallography and mutation. Biochemistry 37, 4751-4758.
10. Notenboom, V., et al., & Withers, S.G.(1998). Insights into transition state stabilisation of the β-1,4 glycosidase Cex by covalent intermediate accumulation in active site mutants. Nat. Struct. Biol. 5, 812-818.
11. Sulzenbacher, G., et al., & Davies, G. (1999). The crystal structure of the 2-fluorocellotriosyl-complex of the Streptomyces lividans endoglucanase, CelB2, at 1.2 Å resolution. Biochemistry 38, 4826-4833.
12. Visser, J., Beldman, G., Someran, M.A.K.-v. & Voragen, A.G.J. (1992). Xylans and xylanases. In Progress in Biotechnology Vol. 7. Elsevier, Amsterdam.
13. Sulzenbacher, G., Shareck, F., Morosoli, R., Dupont, C. & Davies, G.J. (1997). The Streptomyces lividans family 12 endoglucanase: Construction of the catalytic core, expression and X-ray structure at 1.7 Å resolution. Biochemistry 36, 16032-16039.
14. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. (1997). Refinement of macromolecular structures by the maximum likelihood method. Acta Crystallogr. D 53, 240-255.
15. Matthews, B.W. (1968). Solvent content of protein crystals. J. Mol. Biol, 33, 491-497.
16. Ramachandran, G.N., Ramakrishnan, C. & Sasisekharan, V. (1963). Stereochemistry of polypeptide chain configurations. J. Mol. Biol. 7, 95-99.
17. Laskowski, R.A., McArthur, M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 282-291.
18. Campbell, R.L. et al. (1993). A comparison of the structures of the 20 kDa xylanases from Trichoderma harzianum and Bacillus circulans. In Proceedings of the Second TRICEL Symposium on Trichoderma Reesei Cellulases and Other Hydrolases Vol. 8. (Suominen, P. & Reinikainen, T. eds). pp. 63-72, Foundation for Biotechnical and Industrial Fermentation Research, Espoo.
19. Törrönen, A., Harkki, A. & Rouvinen, J. (1994). Three-dimensional structure of endo-1,4-β-xylanase II from Trichoderma reesei: Two conformational states in the active site. EMBO J. 13, 2493-2501.
20. Gruber, K., et al., & Kratky, C. (1998). Thermophilic xylanase from Thermomyces langinosus: High resolution X-ray structure and modelling studies. Biochemistry 37, 13475-13485.
21. Miao, S., Ziser, L., Aebersold, R. & Withers, S.G. (1994). Identification of glutamic acid 78 as the active site nucleophile in Bacillus subtilis xylanase using electrospray tandem mass spectometry. Biochemistry 33, 7027-7032.
22. 13C-NMR study of Bacillus circulans xylanase. Biochemistry 35, 9958-9966.
23. Davies, G.J., Wilson, K.S. & Henrissat, B. 1997). Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem. J. 321, 557-559.
24. Namchuk, M.N. & Withers, S.G. (1995). Mechanism of Agrobacterium β-glucosidase: Kinetic analysis of the role of noncovalent enzyme/substrate interactions. Biochemistry 34, 16194-16202.
25. Heightman, T.D. & Vasella, A.T. (1999). Recent insights into inhibition, structure and mechanism of configuration-retaining glycosidases. Angew. Chem. Int Ed. 38, 750-770.
26. Varrot, A., Schulein, M., Pipelier, M., Vasella, A. & Davies, G.J. (1999). Lateral protonation of a glycosidase inhibitor: Structure of the Bacillus agaradhaerens Cel5A in complex with a cellobio-derived imidazole at 0.97 Å resolution. J. Am. Chem. Soc. 121, 2621-2622.
27. Sidhu, G. et al., & Breyer, G.D. (1999). Sugar ring distortion in the glycosyl-enzyme intermediate of a family G/11 xylanase. Biochemistry 38, 5346-5354.
28. Sinnott, M.L. (1990). Catalytic mechanisms of enzymic glycosyl transfer. Chem. Rev. 90, 1171-1202.
29. Hosie, L. & Sinnott, M.L. (1985). Effects of deuterium substitution alpha and beta to the reaction centre, 18O substitution in the leaving group, and aglycone acidity on hydrolyses of aryl glucosides and glucosyl pyridinium ions by yeast alpha-glucosidase. A probable failure of the antiperiplanar-lone-pair hypothesis in glycosidase catalysis. Biochem. J. 226, 437-446.
30. Saarilahti, H.T., Henrissat, B. & Pavla, E.T. (1990). CelS: A novel endoglucanase identified from Erwinia carotovora subsp. carotovora Gene 90, 9-14.
31. Törrönen, A., Kubicek, C.P. & Henrissat, B. (1993). Amino acid sequence similarities between low molecular weight endo-1,4,β-xylanases and family H cellulases revealed by clustering analysis. FEBS Lett. 321, 135-139.
32. Atkins, E.D.T. (1992). Three-dimensional structure, interactions and properties of xylans. In Xylanas and Xylanases Vol. 7. (Visser, J., Beldman, G., Someren, M.A.K.v. & Voragen, A.G.J., eds) pp. 39-50. Elsevier, Amsterdam.
33. Sulzenbacher, G., Driguez, H., Henrissat, B., Schülein, M. & Davies, G.J. (1996). Structure of the Fusarium oxysporum endoglucanase I with a nonhydrolysable substrate analogue: Substrate distortion gives rise to a pseudo-axial orientation for the leaving group. Biochemistry 35, 15280-15287.
34. Sulzenbacher, G., Schülein, M. & Davies, G.J. (1997). Structures of the endoglucanase I from Fusarium oxysporum: Native, cellobiose and 3,4-epoxybutyl β-D-cellobioside inhibited forms at 2.3 Å resolution. Biochemistry 36, 5902-5911.
35. Henrissat, B., et al., & Davies, G. (1995). Conserved catalytic machinary and the prediction of a common fold for several families of glycosyl hydrolases. Proc. Natl Acad. Sci. USA 92, 7090-7094.
36. Pitcher, D.G., Saunders, N.A. & Owen, R.J. (1989). Rapid extraction of bacterial genomic DNA with guanidinium thiocyanate. Lett. Appl. Microbiol. 8, 151-156.
37. Jørgensen, S. (1994). An Amolytic Enzyme, in Particular a Pyrococcus Alpha Amylase. World patent WO 94/19454, 1 September 1994.
38. Jørgensen, S., Jørgensen, P.L. & Diderichsen, B.K. (1991). Stable Integration of DNA in Bacterial Genomes. World patent WO 91/09129, 27 June 1991.
39. Otwinowski, Z. & Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. In Methods in Enzymology: Macromolecular Crystallography, Part A Vol. 276. (C W Carter, J. & Sweet, R.M., eds) pp. 307-326. Academic Press, London & New York.
40. Collaborative Computational Project Number 4. (1994). The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D 50, 760-763.
41. Sulzenbacher, G.D. (1999). Structural Studies of Cellulases and Xylanases [PhD Thesis]. University of York, York, UK.
42. Navaza, J. (1994). AMoRe: An automated package for molecular replacement. Acta Crystallogr. A 50, 157-163.
43. Navaza, J. & Saludijan, P. (1997). AMoRe: An automated molecular replacement program package. Methods Enzymol. 276, 581-594.
44. Brünger, A.T. (1992). Free R value: A novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-475.
45. Murshudov, G.N., Vagin, A.A., Lebedev, A., Wilson, K.S. & Dodson, E.J. (1999). Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr. D 55, 247-255.
46. Lamzin, V.S. & Wilson, K.S. (1993). Automated refinement of protein models. Acta Crystallogr. D 49, 129-147.
47. Bernstein, F.C., et al., & Tasumi, M. (1977). Protein data bank: A computer-based archival file for macromolecular structures. J. Mol. Biol. 112, 535-542.
48. Esnouf, R.M. (1997). An extensively modified version of MolScript that includes greatly enhanced colouring capabilities. J. Mol. Graphics 15, 133-138.