Crystallographic evidence for substrate ring distortion and protein conformational changes during catalysis in cellobiohydrolase Cel6A from Trichoderma reesei

Structure

Volumn 7, Issue 9, 1999, Pages 1035-1045

  Zou, Jin Yu ^a   Kleywegt, Gerard J ^a   Ståhlberg, Jerry ^a,e   Driguez, Hugues ^b   Nerinckx, Wim ^c   Claeyssens, Marc ^c   Koivula, Anu ^d   Teeri, Tuula T ^d,f   Jones, T Alwyn ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b CNRS   (France)

^c GHENT UNIVERSITY   (Belgium)

^d VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^e SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^f ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

Cellobiohydrolase; Cellulase; Cellulose; Crystal structure; Ring distortion

Indexed keywords

CELLULOSE 1,4 BETA CELLOBIOSIDASE; MUTANT PROTEIN;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTALLOGRAPHY; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ANALYSIS; TRICHODERMA REESEI;

HYPOCREA JECORINA; TRICHODERMA;

EID: 0033199581     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(99)80171-3     Document Type: Article

References (46)

1. 1. Henrissat, B. & Bairoch, A. (1996). Updating the sequence-based classification of glycosyl transferases. Biochem. J. 316, 695-696.
2. 2. Henrissat, B. & Davies, G. (1997). Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7, 637-644.
3. 3. Nevalainen, H. & Penttilä, M. (1995). Molecular biology of cellulolytic fungi. In The Mycota II. Genetics and Biotechnology. (Kuck, H., ed.), pp. 303-319, Springer-Verlag, Berlin.
4. 4. Teeri, T.T. (1997). Crystalline cellulose degradation: new insight into function of cellobiohydrolases. Trends Biotech. 15, 160-167.
5. 5. Henrissat, B., Teeri, T.T. & Warren, A. (1998). A scheme for designating enzymes that hydrolyse the polysaccharides in the cell walls of plants. FEBS Lett. 425, 352-354.
6. 6. Rouvinen, J., Bergfors, T., Teeri, T., Knowles, J.K.C. & Jones, T.A. (1990). Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei. Science 249, 380-386.
7. 7. Spezio, M., Wilson, D.B & Karplus, P.A. (1993). Crystal structure of the catalytic domain of a thermophilic endoglucanase. Biochemistry 32, 9906-9916.
8. 8. Meinke, A., et al., & Gilkes, N.R. (1995). Enhancement of the endo-β- 1,4-glucanase activity of an exocellulase by deletion of a surface loop. J Biol. Chem. 270, 4383-4386.
9. 9. Divne, C., et al., & Jones, T.A. (1994). The three-dimensional crystal structure of the catalytic core of cellobiohydrolase I from Trichoderma reesei. Science 265, 524-528.
10. 10. Kleywegt, G.J., et al., & Jones, T.A. (1997). The crystal structure of the catalytic core domain of endoglucanase I from Trichoderma reesei at 3.6 Å resolution, and a comparison with related enzymes. J. Mol. Biol. 272, 383-397.
11. 11. Brändén, C.I. (1991). The TIM barrel - the most frequently occurring folding motif in proteins. Curr. Opin. Struct. Biol. 1, 978-983.
12. 12. Hyde, C.C., Ahmed, S.A., Padlan, E.A., Miles, E.W. & Davies, D.R. (1988). Three-dimensional structure of the tryptophan synthase α2, β2 multienzyme complex from Salmonella typhimurum. J. Biol. Chem. 263, 17857-17868.
13. 13. Brünger, A.T., Krukowski, A. & Erickson, J.W. (1990). Slow-cooling protocols for crystallographic refinement by simulated annealing. Acta Crystallogr. A 46, 585-593.
14. 14. Brünger, A.T. (1992). Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-475.
15. 15. Kleywegt, G.J. & Jones, T.A. (1995). Where freedom is given, liberties are taken. Structure 3, 535-540.
16. 16. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119.
17. 17. Kleywegt, G.J. & Jones, T.A. (1997). Model-building and refinement practice. Methods Enzymol. 277, 208-230.
18. 18. Kleywegt, G.J. & Jones, T.A. (1996). Phi/Psi-chology: Ramachandran revisited. Structure 4, 1395-1400.
19. 19. Davies, G., Wilson, K. & Henrissat, B. (1997). Nomenclature for the sugar-binding subsites in glycosyl hydrolases. Biochem. J. 321, 557-559.
20. 20. Reverbel-Leroy, C., et al., & Haser, R. (1998). Crystallisation of the catalytic domain of Clostridium cellulolyticum cellulase CelF in the presence of a new cellulase inhibitor. Acta Crystallogr. D 54, 114-118.
21. 21. Gessler, K., Krauss, N., Steiner, T., Betzel, C., Sandmann, C. & Saenger, W. (1994). Crystal structure of β-D-cellotetraose hemihydrate with implications for the structure of cellulose II. Science 266, 1027-1029
22. 22. Bailey, M.J., Siika-aho, M., Valkeajärvi, A. & Penttilä, M.E. (1993). Hydrolytic properties of two cellulases of Trichoderma reesei expressed in yeast. Biotechnol. Appl. Biochem. 17, 65-76.
23. 23. Kleman-Leyer, K.M., Siika-aho, M., Teeri, T.T. & Kirk, K. (1996). The endoglucanase I and cellobiohydrolase II of Trichoderma reesei act synergistically to solubilize native cotton cellulose but not to decrease its molecular size. Appl. Environ. Microbiol. 62, 2883-2887.
24. 24. Penttilä, M., Andre, L., Lehtovaara, P., Bailey, M., Teeri, T.T. & Knowles, J. (1988). Efficient secretion of two fungal cellobiohydrolases in Saccharomyces cerevisiae. Gene 4563, 103-112.
25. 25. Henriksson, K. et al., & Poutanen, K., (1995). Hydrolysis of barley (1→3), (1→4)-β-D-glucan by a cellobiohydrolase II preparation from Trichoderma reesei. Carbohydr. Polym. 26, 109-119.
26. 26. Armand, S., Drouilard, S., Schulein, M., Henrissat, B. & Driguez, H. (1997). A bifunctionalized fluorogenic tetrasaccharide as a substrate to study cellulases. J. Biol. Chem. 272, 2709-2713.
27. 27. Harjunpää, V., et al., & Drakenberg, T. (1996). Cello-oligosaccharide hydrolysis by cellobiohydrolase II from Trichoderma reesei; association and rate constants derived from an analysis of progress curves. Eur. J. Biochem. 240, 584-591.
28. 28. Koivula, A., et al., & Teeri, T.T. (1998). Tryptophan 272: an essential determinant of crystalline cellulose degradation by Trichoderma reesei cellobiohydrolase Cel6A. FEBS Lett. 429, 341-346.
29. 29. Konstantinidis, A.K., Marsden, I. & Sinnott, M.L. (1993). Hyrolyses of α- and β-cellobiosyl fluorides by cellobiohydrolases of Trichoderma reesei. Biochem. J. 291, 833-838.
30. 30. Koshland, D.E., Jr. (1953). Stereochemistry and the mechanism of enzymatic reactions. Biol. Rev. 28, 416-436.
31. 31. Damude, H.G., Withers, S.G., Kilburn, D.G., Miller, R.C. & Warren, R.A. (1995). Site-directed mutation of the putative catalytic residues of endoglucanase CenA from Cellulomonoas fimi. Biochemistry 34, 2220-2224.
32. 32. Damude, H.G., Ferro, V, Withers, S.G. & Warren, R.A. (1996). Substrate specificity of endoglucanase A from Cellulomonoas fimi: fundamental differences between endoglucanases and exoglucanases from family 6. Biochem. J. 315, 467-472.
33. 33. Varrot, A., Hastrup, S., Schülein, M. & Davies, G.J. (1999). Crystal structure of the catalytic core domain of the family 6 cellobiohydrolase II, Cel6A, from Humicola insolens, at 1.92 Å resolution. Biochem J. 337, 297-304.
34. 34. Zhang, S. & Wilson, D.B. (1997). Surface residue mutations which change the substrate specificity of Thermomonospora fusca endoglucanase E2. J. Biochem. 57, 101-113.
35. 35. Barr, B., Wolfgang, D.E., Piens, K., Claeyssens, M. & Wilson, D.B. (1998). Active-site binding of glycosides by Thermomonospora fusca endocellulase E2. Biochem. 37, 9220-9229.
36. 36. Fersht, A.R, et al., & Winter, G. (1985). Hydrogen bonding and biological specificity analysed by protein engineering. Nature 314, 235-238.
37. 37. Wolfgang, D.E. & Wilson, D.B. (1999). Mechanistic studies of active site mutants of Thermomonospora fusca endocellulase E2. Biochemistry, in press.
38. 38. Koivula, A., et al., & Teeri, T.T. (1996). The active site of Trichoderma reesei cellobiohydrolase II: the role of tyrosine-169. Prot. Eng. 9, 691-699.
39. 39. Deslongchamps, P. (1983) Stereoelectronic effects in organic chemistry. Pergamon Press, London.
40. 40. Divne, C., Ståhlberg, J., Teeri, T.T. & Jones, T.A. (1998). High resolution crystal structures reveal how a cellulose chain is bound in the 50 Å long tunnel of cellobiohydrolase I from Trichoderma reesei. J. Mol. Biol. 275, 309-325.
41. 41. Bergfors, T., et al., & Jones, T.A. (1989). Crystallisation of the core protein of cellobiohydrolase II from Trichoderma reesei. J. Mol. Biol. 209, 167-169.
42. 42. Otwinowski, Z. & Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
43. 43. Collaborative Computational Project, Number 4 (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763.
44. 44. Brünger, A.T. (1990). X-PLOR: A system for crystallography and NMR. Yale University Press, New Haven, CT.
45. 45. Brünger, A.T., et al., & Warren, G.L. (1998). Crystallography & NMR System: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921.
46. 46. Engh, R.A. & Huber, R. (1991). Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallogr. A 47, 392-400.