Calcium and domain interactions contribute to the thermostability of domains of the multimodular cellobiohydrolase, CbhA, a subunit of the Clostridium thermocellum cellulosome

Biochemical Journal

Volumn 372, Issue 1, 2003, Pages 151-161

  Kataeva, Irina A ^a   Uversky, Vladimir N ^b,c   Ljungdahl, Lars G ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

Author keywords

Domain structured polypeptide; Glycoside hydrolase; Multimodular protein; Stabilization of protein fold; Temperature induced denaturation; Thermodynamics

Indexed keywords

CALCIUM; POLYPEPTIDES; PROTEINS; THERMODYNAMIC STABILITY; ULTRAVIOLET SPECTROSCOPY;

DOMAIN INTERACTIONS;

BIOCHEMISTRY;

CALCIUM; CELLULOSE 1,4 BETA CELLOBIOSIDASE;

ARTICLE; CIRCULAR DICHROISM; CLOSTRIDIUM THERMOCELLUM; CONFORMATIONAL TRANSITION; ENZYME SUBUNIT; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; THERMODYNAMICS; THERMOSTABILITY;

CALCIUM; CELLULASE; CELLULOSE 1,4-BETA-CELLOBIOSIDASE; CIRCULAR DICHROISM; CLOSTRIDIUM; ENZYME STABILITY; HEAT; MULTIENZYME COMPLEXES; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY;

CLOSTRIDIUM THERMOCELLUM;

EID: 0038291937     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021621     Document Type: Article

References (41)

1. Janin, J. and Wodak, S. J. (1983) Structural domains in protein and their role in the dynamics of protein function. Prog. Biophys. Mol. Biol. 42, 21-78
2. Jaenicke, R. (1999) Stability and folding of domain proteins. Prog. Biophys. Mol. Biol. 71, 155-241
3. Bayer, E. A., Shoham, Y. and Lamed, R. (2000) Cellulose-decomposing bacteria and their enzyme systems. In The Prokaryotes, an Evolving Electronic Resource for the Microbiological Community (Dvorkin, M., Falkow, S, Rosenberg, E., Schleifer, K.-H. and Stackebrandt, E., eds), 3rd edn, pp. 1-41, Springer Verlag, New York
4. Coutinho, P. M. and Henrissat, B. (1999) Carbohydrate-Active Enzymes server at http://afmb.cnrs-mrs.fr/~cazy/CAZY/index.html
5. Tomme, P., Warren, R. A. J., Miller, Jr, R. C., Kilburn, D. G. and Gilkes, N. R. (1995) Cellulose-binding domains: classification and properties. In Enzymatic Degradation of Insoluble Carbohydrates (Saddler, J. N. and Penner, M. P., eds), pp. 142-163, American Chemical Society, Washington DC
6. Little, E., Bork, P. and Doolittle, R. F. (1994) Tracing and spread of fibronectin type III domain in bacterial glycohydrolases. J. Mol. Evolution 89, 631-643
7. Wenk, M. and Jaenicke, R. (1998) Kinetic stabilization of a modular protein by domains interactions. FEBS Letters 488, 127-130
8. 2+-binding βγ-crystallin homolog protein S from Myxococcus xanthus: intrinsic stability and mutual stabilization of domains. J. Mol. Biol. 298, 117-124
9. Wassenberg, D., Schurig, H., Liebl, W. and Jaenicke, R. (1997) Xylanase XynA from the hyperthermophilic bacterium Thermotoga maritima: structure and stability of the recombinant enzyme and its isolated cellulose-binding domain. Protein Sci. 6, 1718-1726
10. Bolam, D. N., Ciruela, A., McQueen-Mason, S., Simpson, P., Williamson, M. P., Rixon, J. B., Boraston, A., Hazlewood, J. P. and Harry, J. (1998) Pseudomonas cellulose-binding domains mediate their effects by increasing enzyme substrate proximity. Biochem. J. 881, 775-781
11. Kataeva, I. A., Li, X.-L., Chen, H. and Ljungdahl, L. G. (1999) CelK - a new cellobiohydrolase from Clostridium thermocellum cellulosome: role of N-terminal cellulose-binding domain. In Genetics, Biochemistry and Ecology of Cellulose Degradation (Ohmiya, K., Sakka, K., Karita, S., Hayashi, K., Kobayashi, Y. and T. Kimura eds), pp. 454-460, UniPublishers Co., Tokyo, Japan
12. Shin, E.-S., Yang, M.-J., Jung, K.-H., Kwon, E.-J., Jung, J. S., Park, S. K., Kim, J., Yun, H. D. and Kim, H. (2002). Influence of the transposition of the thermostabilizing domain of Clostridium thermocellum xylanase (XynX) on xylan binding and thermostabilization. Appl. Environ. Microbiol. 68, 3496-3501
13. 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
14. Xie, H., Gilbert, H. J., Charnock, S. J., Davies, G. J., Williamson, M. P., Simpson, P. J., Raghothama, S., Fontes, C. M. G. A., Dias, F. M. V., Ferreira, L. M. A. and Bolam, D. N. (2001) Clostridium thermocellum Xyn10B carbohydrate-binding module 22-2: the role of conserved amino acids in ligand binding. Biochemistry 40, 9167-9176
15. Kataeva, I. A., Blum, D. L., Li, X.-L. and Ljungdahl, L. G. (2001) Do domain interactions of glycosyl hydrolases from Clostridium thermocellum cellulosome contribute to protein thermostability? Protein Eng. 14, 167-172
16. Notenboom, V., Boraston, A. B., Kilburn, D. G. and Rose, D. R. (2001) Crystal structures of the family 9 carbohydrate-binding module from Thermotoga maritima xylanase 10A in native and ligand-bound form. Biochemistry 40, 6248-6256
17. Zverlov, V. V., Velikodvorskaya, G. V., Schwarz, W. H., Bronnenmeier, K., Kellermann, J. and Staudenbauer, W. L. (1998) Multidomain structure and cellulosomal localization of the Clostridium thermocellum cellobiohydrolase CbhA. J. Bacteriol. 180, 3091-3099
18. 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
19. Johnson, P. E., Creagh, A. L., Brun, E, Joe, K., Tomme, P., Haynes, C. A. and McIntosh, L. P. (1998) Calcium binding by the N-terminal cellulose-binding domain. Biochemistry 37, 12772-12781
20. Kataeva, I. A., 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 thermocellum: evidence of gene duplication and recombination. J. Bacteriol. 181, 5288-5295
21. Pace, C. N. and Scholtz, J. M. (1997) Measuring the conformational stability of a protein. In Protein Structure: A Practical Approach (Creighton, T. E., ed.), pp. 291-321, Oxford University Press, Oxford
22. Becktel, W. J. and Schellman, J. A. (1987) Protein stability curves. Biopolymers 26, 1859-1877
23. Burstein, E. A. (1976) Intrinsic Protein Fluorescence: Origin and Applications. In series: Biophysics 7, VINITI, Moscow
24. Permyakov, E. A., Yarmolenko, V. V., Emelyanenko, V. I., Burstein, E. A., Closset, J. and Gerday, C. (1980) Fluorescence studies of the calcium binding to whiting (Gadus merlangus) parvalbumin. Eur. J. Biochem. 109, 307-315
25. Kuznetsova, I. M., Stepanenko, O. V., Turoverov, K. K., Zhu, L., Zhou, J. M., Fink, A. L. and Uversky, V. N. (2002) Unraveling multistate unfolding of rabbit muscle creatine kinase. Biochim. Biophys. Acta 1596, 138-155
26. Bushmarina, N. A., Kuznetsova, I. M., Biktashev, A. G., Turoverov, K. K. and Uversky, V. N. (2001) Partially folded conformations in the folding pathway of bovine carbonic anhydrase II: a fluorescence spectroscopic analysis. Chembiochem 2, 813-821
27. Bolotina, I. A. and Lugauskas, V. Yu. (1985) Determination of the secondary structure of proteins from circular dichroism spectra. IV. Contribution of aromatic amino acid residues into circular dichroism spectra of proteins in the peptide region. Mol. Biol. (Moscow) 19, 1409-1421
28. Manning, M. C. and Woody, R. W. (1989) Theoretical study of the contribution of aromatic side chains to the circular dichroism of basic bovine pancreatic trypsin inhibitor. Biochemistry 28, 8609-8613
29. Chakrabartty, A., Kortemme, T., Padmanabhan, S. and Baldwin, R. L. (1993) Aromatic side-chain contribution to far-ultraviolet circular dichroism of helical peptides and its effect on measurement of helix propensities. Biochemistry 32, 5560-5565
30. Uversky, V. N. and Ptitsyn, O. B. (1996) Further evidence on the equilibrium 'pre-molten globule state': four-state guanidinium chroride-induced unfolding of carbonic anhydrase B at low temperature. J. Mol. Biol. 255, 215-228
31. Abramov, V. M., Vasiliev, A. M., Vasilenko, R. N., Kulikova, N. L., Kosarev, I. V., Khlebnikov, V. S., lshchenko, A. T., MacIntyre, S., Khurana, R., Gillespie, J. R. et al. (2001) Structural and functional similarity between Yersinia pestis capsular protein Caf1 and human interreukin-1β. Biochemistry 40, 6076-6084
32. Ptitsyn O. B. (1995) Mollen grobule and protein folding. Adv. Protein Chem. 47, 83-229
33. Permyakov, E. A. (1993) Calcium-Binding Proteins. pp.1-190, Nauka, Moscow
34. Mayr, E. M., Jaenicke, R. and Glockshuber, R. (1997) The domains in γβ-crystallin: identical fold - different stabilities. J. Mol. Blol. 269, 260-269
35. Lytle, B. L., Volkman, B. F., Westler, W. H. and Wu, J. H. D. (2000) Secondary structure and calcium-induced folding of the Clostridium thermocellum dockerin domain determined by NMR spectroscopy. Arch. Biochem. Bicphys. 379, 237-244
36. Kataeva, I. A., Seidel, III, R. D., Li, X.-I. and Ljungdahl, L. G. (2001) Properties and mutation analysis of the CelK cellulose-binding domain from the Clostridium thermocellum celluloscme. J. Bacteriol. 183, 5288-5295
37. Juy, M., Amit, A. G., Alzari, P. M., Poljak, R. J., Claeyssens, M., Béguin, P., and Aubert, J.-P. (1992) Crystal structure of a thermostable bacterial cellulose-degraduing enzyme. Nature (London) 357, 89-91
38. Chauvaux, S., Souchon, S., Alzari, P. M., Chariot, P. and Beguin, P. (1995) Structural and functional analysis of the metal-binding sites of Clostridium thermocellum endoglucanase CelD. J. Biol. Chem. 270, 9757-9762
39. Rudolph, R., Siebendritt, R, Nesslauer, G., Sharma, A. K. and Jaenicke, R. (1990) Folding of an all-β protein: independent domain folding in γ II-crystallin from calf eye lens. Proc. Natl. Acad. Sci. U.S.A. 87, 4625-4629
40. Burley, S. K. and Petsko, G. A. Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science (Washington, D.C.) 229, 23-28
41. Kannan, N. and Vishveshwara, S. (2000) Aromatic clusters: a determinant of thermal stability of thermophilic proteins. Protein Eng. 13, 753-761