Structural characterization of type II dockerin module from the cellulosome of Clostridium thermocellum: Calcium-induced effects on conformation and target recognition

Biochemistry

Volumn 44, Issue 6, 2005, Pages 2173-2182

  Adams, Jarrett J ^a   Webb, Bradley A ^a   Spencer, Holly L ^a   Smith, Steven P ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CELLULOSE; CENTRIFUGATION; DIMERIZATION; HYDROPHOBICITY; MOLECULAR STRUCTURE; MUTAGENESIS; SCAFFOLDS;

CELLULOSE-DEGRADING COMPLEX; CELLULOSOMAL SCAFFOLDING; COHESINS; DOCKERIN-X-MODULAR MODULE (DOCX);

COMPLEXATION;

BACTERIAL PROTEIN; CALCIUM; CELLULOSE; CELLULOSOME; COHESIN; DIMER; DOCKERIN; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; CLOSTRIDIUM THERMOCELLUM; CONFORMATIONAL TRANSITION; DIMERIZATION; DISSOCIATION; DISSOCIATION CONSTANT; HYDROPHOBICITY; MOLECULAR CLONING; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; MOLECULAR STABILITY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; STRUCTURE ANALYSIS; ULTRACENTRIFUGATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL ADHESION; BACTERIAL PROTEINS; CALCIUM; CELL CYCLE PROTEINS; CELLULOSOMES; CHROMATOGRAPHY, GEL; CHROMOSOMAL PROTEINS, NON-HISTONE; CIRCULAR DICHROISM; CLONING, MOLECULAR; CLOSTRIDIUM THERMOCELLUM; FUNGAL PROTEINS; GENETIC VECTORS; LIGHT; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEAR PROTEINS; PROTEIN CONFORMATION; PROTEIN SUBUNITS; SCATTERING, RADIATION; SOLUTIONS; SPECTROMETRY, FLUORESCENCE; TRYPTOPHAN;

CLOSTRIDIUM THERMOCELLUM;

EID: 13544258645     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048039u     Document Type: Article

References (60)

1. Lamed, R., Kenig, R., Setter, E., and Bayer, E. A. (1983b) The cellulosome: a discrete cell surface organelle of Clostridium thermocellum which exhibits separate antigenic, cellulolose-binding and various cellulolytic activities, Biotechnol. Bioeng. Symp. 13, 163-181.
2. Lamed, R., Setter, E., and Bayer, E. A. (1983a) Characterization of a cellulose-binding, cellulase-containing complex in Clostridium thermocellum, J. Bacteriol. 156, 828-36.
3. Pages, S., Belaich, A., Tardif, C., Reverbel-Leroy, C., Gaudin, C., and Belaich, J. P. (1996) Interaction between the endoglucanase CelA and the scaffolding protein CipC of the Clostridium cellulolyticum cellulosome, J. Bacteriol. 178, 2279-86.
4. Gal, L., Pages, S., Gaudin, C., Belaich, A., Reverbel-Leroy, C., Tardif, C., and Belaich, J. P. (1997) Characterization of the cellulolytic complex (cellulosome) produced by Clostridium cellulolyticum, Appl. Environ. Microbiol. 63, 903-9.
5. Doi, R. H., Goldstein, M., Hashida, S., Park, J. S., and Takagi, M. (1994) The Clostridium cellulovorans cellulosome, Crit. Rev. Microbiol. 20, 87-93.
6. Kakiuchi, M., Isui, A., Suzuki, K., Fujino, T., Fujino, E., Kimura, T., Karita, S., Sakka, K., and Ohmiya, K. (1998) Cloning and DNA sequencing of the genes encoding Clostridium josui scaffolding protein CipA and cellulase CelD and identification of their gene products as major components of the cellulosome, J. Bacteriol. 180, 4303-8.
7. Ding, S. Y., Bayer, E. A., Steiner, D., Shoham, Y., and Lamed, R. (1999) A novel cellulosomal scaffoldin from Acetivibrio cellulolyticus that contains a family 9 glycosyl hydrolase, J. Bacteriol. 181, 6720-9.
8. Xu, Q., Gao, W., Ding, S. Y., Kenig, R., Shoham, Y., Bayer, E. A., and Lamed, R. (2003) The cellulosome system of Acetivibrio cellulolyticus includes a novel type of adaptor protein and a cell surface anchoring protein, J. Bacteriol. 185, 4548-57.
9. Ding, S. Y., Bayer, E. A., Steiner, D., Shoham, Y., and Lamed, R. (2000) A scaffoldin of the Bacteroides cellulosolvens cellulosome that contains 11 type II cohesins, J. Bacteriol. 182, 4915-25.
10. Xu, Q., Bayer, E. A., Goldman, M., Kenig, R., Shoham, Y., and Lamed, R. (2004) Architecture of the Bacteroides cellulosolvens cellulosome: description of a cell surface-anchoring scaffoldin and a family 48 cellulase, J. Bacteriol. 186, 968-77.
11. Ding, S. Y., Rincon, M. T., Lamed, R., Martin, J. C., McCrae, S. I., Aurilia, V., Shoham, Y., Bayer, E. A., and Flint, H. J. (2001) Cellulosomal scaffoldin-like proteins from Ruminococcus flavefaciens, J. Bacteriol. 183, 1945-53.
12. Steenbakkers, P. J., Li, X. L., Ximenes, E. A., Arts, J. G., Chen, H., Ljungdahl, L. G., and Op Den Camp, H. J. (2001) Noncatalytic docking domains of cellulosomes of anaerobic fungi, J. Bacteriol. 183, 5325-33.
13. Bhat, K. M., and Wood, T. M. (1992) The cellulase of anaerobic bacterium Clostridium thermocellum-isolation, dissociation, and resassociation of the cellulosome, Carbohydr. Res. 227, 293-300.
14. Bhat, S., Goodenough, P. W., Bhat, M. K., and Owen, E. (1994) Isolation of four major subunits from Clostridium thermocellum cellulosome and their synergism in the hydrolysis of crystalline cellulose, Int. J. Biol. Macromol. 16, 335-42.
15. Bayer, E. A., Morag, E., and Lamed, R. (1994) The cellulosome-a treasure-trove for biotechnology, Trends Biotechnol. 12, 379-86.
16. Tokatlidis, K., Salamitou, S., Beguin, P., Dhurjati, P., and Aubert, J. P. (1991) Interaction of the duplicated segment carried by Clostridium thermocellum cellulases with cellulosome components, FEBS Lett. 291, 185-8.
17. Tokatlidis, K., Dhurjati, P., and Beguin, P. (1993) Properties conferred on Clostridium thermocellum endoglucanase CelC by grafting the duplicated segment of endoglucanase CelD, Protein Eng. 6, 947-52.
18. Fujino, T., Beguin, P., and Aubert, J. P. (1993) Organization of a Clostridium thermocellum gene cluster encoding the cellulosomal scaffolding protein CipA and a protein possibly involved in attachment of the cellulosome to the cell surface, J. Bacteriol. 175, 1891-9.
19. Gerngross, U. T., Romaniec, M. P., Kobayashi, T., Huskisson, N. S., and Demain, A. L. (1993) Sequencing of a Clostridium thermocellum gene (cipA) encoding the cellulosomal SL-protein reveals an unusual degree of internal homology, Mol. Microbiol. 8, 325-34.
20. Fujino, T., Beguin, P., and Aubert, J. P. (1992) Cloning of a Clostridium thermocellum DNA fragment encoding polypeptides that bind the catalytic components of the cellulosome, FEMS Microbiol. Lett. 73, 165-70.
21. Salamitou, S., Raynaud, O., Lemaire, M., Coughlan, M., Beguin, P., and Aubert, J. P. (1994) Recognition specificity of the duplicated segments present in Clostridium thermocellum endoglucanase CelD and in the cellulosome- integrating protein CipA, J. Bacteriol. 176, 2822-7.
22. Yaron, S., Morag, E., Bayer, E. A., Lamed, R., and Shoham, Y. (1995) Expression, purification and subunit-binding properties of cohesins 2 and 3 of the Clostridium thermocellum cellulosome, FEBS Lett. 360, 121-4.
23. Lytle, B., Myers, C., Kruus, K., and Wu, J. H. (1996) Interactions of the CelS binding ligand with various receptor domains of the Clostridium thermocellum cellulosomal scaffolding protein, CipA, J. Bacteriol. 178, 1200-3.
24. Jindou, S., Soda, A., Karita, S., Kajino, T., Beguin, P., Wu, J. H., Inagaki, M., Kimura, T., Sakka, K., and Ohmiya, K. (2004) Cohesin-dockerin interactions within and between Clostridium josui and Clostridium thermocellum: binding selectivity between cognate dockerin and cohesin domains and species specificity, J. Biol. Chem. 279, 9867-74.
25. Leibovitz, E., and Beguin, P. (1996) A new type of cohesin domain that specifically binds the dockerin domain of the Clostridium thermocellum cellulosome-integrating protein CipA, J. Bacteriol. 178, 3077-84.
26. Leibovitz, E., Ohayon, H., Gounon, P., and Beguin, P. (1997) Characterization and subcellular localization of the Clostridium thermocellum scaffoldin dockerin binding protein SdbA, J. Bacteriol. 179, 2519-23.
27. Pages, S., Belaich, A., Belaich, J. P., Morag, E., Lamed, R., Shoham, Y., and Bayer, E. A. (1997) Species-specificity of the cohesin-dockerin interaction between Clostridium thermocellum and Clostridium cellulolyticum: prediction of specificity determinants of the dockerin domain, Proteins: Struct., Funct., Genet. 29, 517-27.
28. Lytle, B. L., Volkman, B. F., Westler, W. M., and Wu, J. H. (2000) Secondary structure and calcium-induced folding of the Clostridium thermocellum dockerin domain determined by NMR spectroscopy, Arch. Biochem. Biophys. 379, 237-44.
29. Lytle, B. L., Volkman, B. F., Westler, W. M., Heckman, M. P., and Wu, J. H. (2001) Solution structure of a type I dockerin domain, a novel prokaryotic, extracellular calcium-binding domain, J. Mol. Biol. 307, 745-53.
30. Carvalho, A. L., Dias, F. M., Prates, J. A., Nagy, T., Gilbert, H. J., Davies, G. J., Ferreira, L. M., Romao, M. J., and Fontes, C. M. (2003) Cellulosome assembly revealed by the crystal structure of the cohesin-dockerin complex, Proc. Natl. Acad. Sci. U.S.A. 100, 13809-14.
31. Lytle, B., and Wu, J. H. (1998) Involvement of both dockerin subdomains in assembly of the Clostridium thermocellum cellulosome, J. Bacteriol. 180, 6581-5.
32. Mechaly, A., Yaron, S., Lamed, R., Fierobe, H. P., Belaich, A., Belaich, J. P., Shoham, Y., and Bayer, E. A. (2000) Cohesin-dockerin recognition in cellulosome assembly: experiment versus hypothesis, Proteins: Struct., Funct., Genet. 39, 170-7.
33. Mechaly, A., Fierobe, H. P., Belaich, A., Belaich, J. P., Lamed, R., Shoham, Y., and Bayer, E. A. (2001) Cohesin-dockerin interaction in cellulosome assembly: a single hydroxyl group of a dockerin domain distinguishes between nonrecognition and high affinity recognition, J. Biol. Chem. 276, 9883-8.
34. Schaeffer, F., Matuschek, M., Guglielmi, G., Miras, I., Alzari, P. M., and Beguin, P. (2002) Duplicated dockerin subdomains of Clostridium thermocellum endoglucanase CelD bind to a cohesin domain of the scaffolding protein CipA with distinct thermodynamic parameters and a negative cooperativity, Biochemistry 41, 2106-14.
35. Jindou, S., Kajino, T., Inagaki, M., Karita, S., Beguin, P., Kimura, T., Sakka, K., and Ohmiya, K. (2004) Interaction between a type-II dockerin domain and a type-II cohesin domain from Clostridium thermocellum cellulosome, Biosci. Biotechnol. Biochem. 68, 924-6.
36. Garcia-Campayo, V., and Beguin, P. (1997) Synergism between the cellulosome-integrating protein CipA and endoglucanase CelD of Clostridium thermocellum, J. Biotechnol. 57, 39-47.
37. 15N NMR sequence-specific resonance assignment of a Clostridium thermocellum type II cohesin module, J. Biomol. NMR 23, 73-4.
38. Bohm, G., Muhr, R., and Jaenicke, R. (1992) Quantitative analysis of protein far UV circular dichroism spectra by neural networks, Protein Eng. 5, 191-195.
39. Kay, L. E., Keiffer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity, J. Am. Chem. Soc. 114, 10663-10665.
40. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-93.
41. Johnson, B. A., and Blevins, R. A. (1994) NMRVIEW: a computer program for the visualization and analysis of NMR data, J. Biomol. NMR 4, 603-614.
42. Wyatt, P. J. (1993) Light scattering and the absolute characterization of macromolecules, Anal. Chim. Acta 272, 1-40.
43. Schuck, P., Perugini, M. A., Gonzales, N. R., Howlett, G. J., and Schubert, D. (2002) Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems, Biophys. J. 82, 1096-111.
44. Adams, J. J., Jang, C. J., Spencer, H. L., Elliott, M., and Smith, S. P. (2004) Expression, purification and structural characterization of the scaffoldin hydrophilic X-module from the cellulosome of Clostridium thermocellum, Protein Expression Purif. 38, 258-263.
45. Zhang, M., Tanaka, T., and Ikura, M. (1995) Calcium-induced conformational transition revealed by the solution structure of apo calmodulin, Nat. Struct. Biol. 2, 758-67.
46. Gagne, S. M., Tsuda, S., Li, M. X., Smillie, L. B., and Sykes, B. D. (1995) Structures of the troponin C regulatory domains in the apo and calcium-saturated states, Nat. Struct. Biol. 2, 784-9.
47. Smith, S. P., and Shaw, G. S. (1998) A novel calcium-sensitive switch revealed by the structure of human S100B in the calcium-bound form, Structure 6, 211-22.
48. Smith, S. P., and Shaw, G. S. (1998) A change-in-hand mechanism for S100 signaling, Biochem. Cell Biol. 76, 324-33.
49. Fierobe, H. P., Pages, S., Belaich, A., Champ, S., Lexa, D., and Belaich, J. P. (1999) Cellulosome from Clostridium cellulolyticum: molecular study of the Dockerin/Cohesin interaction, Biochemistry 38, 12822-32.
50. Murashima, K., Kosugi, A., and Doi, R. H. (2003) Solubilization of cellulosomal cellulases by fusion with cellulose-binding domain of noncellulosomal cellulase engineered from Clostridium cellulovorans, Proteins: Struct., Funct., Genet. 50, 620-8.
51. Slupsky, C. M., Reinach, F. C., Smillie, L. B., and Sykes, B. D. (1995) Solution secondary structure of calcium-saturated troponin C monomer determined by multidimensional heteronuclear NMR spectroscopy, Protein Sci. 4, 1279-90.
52. 15N spectra of proteins: heteronuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin, Biochemistry 29, 4659-67.
53. Smith, S. P., Barber, K. R., Dunn, S. D., and Shaw, G. S. (1996) Structural influence of cation binding to recombinant human brain S100b: evidence for calcium-induced exposure of a hydrophobic surface, Biochemistry 35, 8805-14.
54. Smith, S. P., and Shaw, G. S. (1997) Assignment and secondary structure of calcium-bound human S100B, J. Biomol. NMR 10, 77-88.
55. Slupsky, C. M., Kay, C. M., Reinach, F. C., Smillie, L. B., and Sykes, B. D. (1995) Calcium-induced dimerization of troponin C: mode of interaction and use of trifluoroethanol as a denaturant of quaternary structure, Biochemistry 34, 7365-75.
56. Shimon, L. J., Bayer, E. A., Morag, E., Lamed, R., Yaron, S., Shoham, Y., and Frolow, F. (1997) A cohesin domain from Clostridium thermocellum: the crystal structure provides new insights into cellulosome assembly, Structure 5, 381-90.
57. Tavares, G. A., Beguin, P., and Alzari, P. M. (1997) The crystal structure of a type I cohesin domain at 1.7 A resolution, J. Mol. Biol. 273, 701-13.
58. Spinelli, S., Fierobe, H. P., Belaich, A., Belaich, J. P., Henrissat, B., and Cambillau, C. (2000) Crystal structure of a cohesin module from Clostridium cellulolyticum: implications for dockerin recognition, J. Mol. Biol. 304, 189-200.
59. Miras, I., Schaeffer, F., Beguin, P., and Alzari, P. M. (2002) Mapping by site-directed mutagenesis of the region responsible for cohesin-dockerin interaction on the surface of the seventh cohesin domain of Clostridium thermocellum CipA, Biochemistry 47, 2115-9.
60. Nakar, D., Handelsman, T., Shoham, Y., Fierobe, H. P., Belaich, J. P., Morag, E., Lamed, R., and Bayer, E. A. (2004) Pinpoint mapping of recognition residues on the cohesin surface by progressive homologue swapping, J. Biol. Chem. 279, 42881-8.