Structural Basis for the Exocellulase Activity of the Cellobiohydrolase CbhA from Clostridium thermocellum

Biochemistry

Volumn 43, Issue 5, 2004, Pages 1163-1170

  Schubot, Florian D ^a,b   Kataeva, Irina A ^a   Chang, Jessie ^a   Shah, Ashit K ^a   Ljungdahl, Lars G ^a   Rose, John P ^a   Wang, Bi Cheng ^a  

^a University of Georgia ^*  (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOLOGY; BIODEGRADATION; CATALYST ACTIVITY; CELLULOSE; CRYSTAL STRUCTURE; ENZYMES; FUNGI; IMMUNOLOGY;

EXOCELLULOLYTIC ACTIVITY;

BIOCHEMISTRY;

BACTERIAL ENZYME; CARBOHYDRATE; CELLULASE; CELLULOSE 1,4 BETA CELLOBIOSIDASE; EXOCELLULASE; GLYCOSIDASE; IMMUNOGLOBULIN; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CLOSTRIDIUM THERMOCELLUM; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BINDING SITES; CATALYTIC DOMAIN; CELLULASES; CELLULOSE; CELLULOSE 1,4-BETA-CELLOBIOSIDASE; CLOSTRIDIUM; CRYSTALLOGRAPHY, X-RAY; IMMUNOGLOBULINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; TETROSES;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM THERMOCELLUM; FUNGI; POSIBACTERIA;

EID: 0842327141     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi030202i     Document Type: Article

References (42)

1. Himmel, M. E., Ruth, M. F., and Wyman, C. E. (1999) Cellulase for commodity products from cellulosic biomass. Curr. Opin. Biotechnol. 10, 358-364.
2. Kataeva, I. A., and Ljungdahl, L. G. (2003) The Clostridium thermocellum cellulosome: a multi-protein complex of module-composed components in Protein Structures: Kaleidoscope of Structural Properties and Functions. (Uversky, V. N., Ed.) pp 1-16, Research Singpost, Kerala, India, in press.
3. Tomme, P., Boraston, A., McLean, B., Kormos, J., Creagh, A. L., Sturch, K., Gilkes, N. R., Haynes, C. A., Warren, R. A., and Kilburn, D. G. (1998) Characterization and affinity applications of cellulose-binding domains. J. Chromatogr. B., Biomed. Sci. Appl. 715, 283-296.
4. Kataeva, I., Li, X.-L., Chen, H., Ljungdahl, L. G. (1998) CelK - a new cellobiohydrolase from Clostridium thermocellum cellulo-some: role of N-terminal cellulose-binding domain in Genetics, Biochemistry and Ecology of Cellulose Degradation (Ohmiya, K., Sakka, K., Kobayashi, Y., and Karita, S., Ed.) pp 456-460, UniPublishers Co., Tokyo, Japan.
5. Matuschek, M., Sahm, K., Zibat, A., and Bahl, H. (1996) Characterization of genes from Thermoanaerobacterium thermosulfurigenes EM1 that encode two glycosyl hydrolases with S-layerlike domains. Mol. Gen. Genet. 252, 493-496.
6. Kataeva, I. A., Seidel, R. D., III, Shah, A., West, L. T., Li, X. L., and Ljungdahl, L. G. (2002) The fibronectin type 3-like repeat from the Clostridium thermocellum cellobiohydrolase CbhA promotes hydrolysis of cellulose by modifying its surface. Appl. Environ. Microbiol. 68, 4292-4300.
7. Tokatlidis, K., Dhurjati, P., and Béguin, P. (1993) Properties conferred on Clostridium thermocellum endoglucanase CelC by grafting the duplicated segment of endoglucanase CelD. Protein Eng. 6, 947-952.
8. Bayer, E. A., Shoham, Y., and Lamed, R. (2000) Cellulose-decomposing prokaryotes and their enzyme systems in The Prokaryotes: An Involving Electronic Resource for the Microbial Community, 3rd ed. (latest update release 3.7, September 2001) (Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H., and Stackebrandt, E., Eds.) Springer-Verlag, New York.
9. Irwin, D., Shin, D. H., Zhang, S., Barr, B. K., Sakon, J., Karplus, P. A., and Wilson, D. B. (1998) Roles of the catalytic domain and two cellulose binding domains of Thermomonospora fusca E4 in cellulose hydrolysis. J. Bacteriol. 180, 1709-1714.
10. Tomme, P., Kwan, E., Gilkes, N. R., Kilburn, D. G., and Warren, R. A. (1996) Characterization of CenC, an enzyme from Cellulomonas fimi with both endo- and exoglucanase activities. J. Bacteriol. 178, 4216-4223.
11. Kataeva, I., Li, X. L., Chen, H., Choi, S. K., and Ljungdahl, L. G. (1999) Cloning and sequence analysis of a new cellulase gene encoding CelK, a major cellulosome component of Clostridium thennocellum: Evidence for gene duplication and recombination. J. Bacteriol. 181, 5288-5295.
12. Kleywegt, G. J., Zou, J. Y., Divne, C., Davies, G. J., Sinning, I., Stahlberg, J., Reinikainen, T., Srisodsuk, M., Teeri, T. T., and Jones, T. A. (1997) The crystal structure of the catalytic core domain of endoglucanase I from Trichoderma reesei at 3.6Å resolution, and a comparison with related enzymes. J. Mol. Biol. 272, 383-397.
13. Divne, C., Ståhlberg, J., Reinikainen, T., Ruohonen, L., Pettersson, G., Knowles, J. K., Teeri, T. T., and Jones, T. A. (1994) The three-dimensional crystal structure of the catalytic core of cellobiohydrolase I from Trichoderma reesei. Science 265, 524-528.
14. Divne, C., Ståhlberg, J., Teeri, T. T., and Jones, T. (1998) High-resolution crystal strutures reveal how a cellulose chain is bound in a 50 Å long tunnel of cellobiohydrolase I from Trichoderma reesei. J. Mol. Biol. 275, 309-325.
15. Sakon, J., Irwin, D., Wilson, D. B., and Karplus, P. A. (1997) Structure and mechanisms of endo/exocellulase E4 from Thermomonospora fusca. Nat. Struct. Biol. 4, 810-818.
16. Mandelman, D., Belaich, A., Belaich, J. P., Aghajari, N., Driguez, H., and Haser, R. (2003) X-ray crystal structure of the multidomain endoglucanase Cel9G from Clostridium cellulolyticum complexed with natural and synthetic cello-oligosaccharides. J. Bacteriol. 185, 4127-4135.
17. Juy, M., Amit, A. G., Alzari, P. M., Poljak, R. J., Claeyssens, M., Béguin, P., and Aubert, J.-P. (1992) Three-dimensional structure of a thermostable bacterial cellulase. Nature 357, 89-91.
18. Parsiegla, G., Belaich, A., Belaich, J. P., and Haser, R. (2002) Crystal structure of the cellulase Cel9M enlightens structure/function relationships of the catalytic modules in glycoside hydrolases. Biochemistry 41, 11134-11142.
19. Zverlov, V. V., Velikodvorskaya, G. V., Schwarz, W. H., Bronnenmeier, K., Kellermann, J., and Staudenbauer, W. (1998) Multidomain structure and localization of the Clostridium thermocellum cellobiohydrolase CbhA. J. Bacteriol. 180, 3091-3099.
20. Chayen, N. E. (1997) The role of oil in macromolecular crystallization. Structure 5, 1269-1274.
21. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
22. Terwilliger, T. C., and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr. D 55 (Pt 4), 849-861.
23. Terwilliger, T. C. (2000) Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56 (Pt 8), 965-972.
24. Jones, T. A., Zou, J.-Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A47, 110-119.
25. Laboratory, S. D. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D50, 760-763.
26. McRee, D. E. (1999) Xtalview/Xfit- -A versatile program for manipulation atomic coordinate, and electron density. J. Struct. Biol. 125, 156-165.
27. Brunger, A. T., Karplus, M., and Petsko, G. A. (1989) Crystallographic refinement by simulated annealing: application to crambin. Acta Crystallogr. A45, 50-61.
28. Perrakis, A., Morris, R., and Lamzin, V. S. (1999) Automated protein model building combined with interactive structure refinement. Nat. Struct. Biol. 6, 458-463.
29. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291.
30. Abola, E. E., Bernstein, F. C., Bryant, S. H., Koetzel, T. F., and Weng, J. (1987) in Crystallographic Databases - Information Content, Software Systems, Scientific Applications (Allen, F. H., Bergerhoff, G., and Sievers, R., Eds.) pp 107-132, Data Commission of the International Union of Crystallography, Bonn.
31. Tuka, K., Zverlov, V. V., Bumazkin, B. K., Velikodvorskaya, G. V., Strongin, A. Ya. (1990) Cloning and expression of Clostridium thermocellum genes coding for thermostable exoglucanases (cellobiohydrolases) in Escherichia coli cells. Biochem. Biophys. Res. Commun. 169, 1055-1060.
32. Béguin, P., and Alzari, P. (1998) The cellulosome of Clostridium thermocellum. Biochem. Soc. Trans. 26, 178-185.
33. Chauvaux, S., Souchon, H., Alzari, P. M., Chariot, P., and Béguin, P. (1995) Structural and functional analysis of the metal-binding sites of Clostridium thermocellum endoglucanase CelD. J. Biol. Chem. 270, 9757-9762.
34. Guerin, D. M., Lascombe, M. B., Costabel, M., Souchon, H., Lamzin, V., Béguin, P., and Alzari, P. M. (2002) Atomic (0.94 A) resolution structure of an inverting glycosidase in complex with substrate. J. Mol. Biol. 316, 1061-1069.
35. Rouvinen, J., Bergfors, T., Teeri, T., Knowles, J. K. C., and Jones, T. A. (1990) Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei. Science 249, 380-386.
36. Li, X.-L., Chen, H., and Ljungdahl, L. G. (1997) Two cellulases, CelA and CelC, from the polycentric anaerobic fungus Orpinomyces strain PC-2 contain N-terminal docking domains for a cellulase-hemicellulase complex. Appl. Environ. Microbiol. 63, 4721-4728.
37. Cutfield, S. M., Davies, G. J., Murshudov, G., Anderson, B. F., Moody, P. C. E., Sullivan, P. A., and Cutfield, J. F. (1999) The structure of the exo-β-(1,3)-glucanase from Candida albicans in native and bound forms: Relationship between a pocket and groove in family 5 glycosyl hydrolases. J. Mol. Biol. 294, 771-783.
38. Dominguez, R., Souchon, H., Spinelly, S., Dauter, Z., Wilson, K. S., Chauvaux,S., Béguin, P., and Alzari, P. M. (1995) A common fold and similar active site in two distinct families of β-glycanases. Nat. Struct. Biol. 2, 569-576.
39. Esnouf, R. M. (1997) An extensively modified version of MolScript that includes greatly enhanced coloring capabilities. J. Mol. Graph. Model. 15, 132-134, 112-113.
40. DeLano, W. L. (2001) DeLano Scientific LLC, San Carlos, CA. http://www.pymol.org.
41. Wallace, A. C., Laskowski, R. A., and Thornton, J. M. (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8, 127-34.
42. Gouet, P., Courcelle, E., Stuart, D. I., and Metoz, F. (1999) ESPript: analysis of multible sequence alignments in PostScript. Bioinformatics 15, 305-308.