Structure analysis of the extracellular domain reveals disulfide bond forming-protein properties of Mycobacterium tuberculosis Rv2969c

Protein and Cell

Volumn 4, Issue 8, 2013, Pages 628-640

  Wang, Lu ^a,b   Li, Jun ^a,b   Wang, Xiangxi ^a,b   Liu, Wu ^a   Zhang, Xuejun C ^a   Li, Xuemei ^a   Rao, Zihe ^a,c  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c NANKAI UNIVERSITY   (China)

Author keywords

disulfide bond forming protein; Mycobacterium tuberculosis; X ray crystallography

Indexed keywords

BACTERIAL ENZYME; BACTERIAL PROTEIN; DISULFIDE BOND FORMING PROTEIN; DSBA PROTEIN; INSULIN; OXIDOREDUCTASE; PERIPLASMIC PROTEIN; RIBONUCLEASE; THIOREDOXIN; UNCLASSIFIED DRUG; VITAMIN K EPOXIDE REDUCTASE;

ACIDITY; ALPHA HELIX; ARTICLE; BINDING SITE; CALCIUM BINDING; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ESCHERICHIA COLI; HYDROPHOBICITY; IN VITRO STUDY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MYCOBACTERIUM TUBERCULOSIS; POSIBACTERIA;

EID: 84880799849     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-013-3033-x     Document Type: Article

References (47)

1. Alphey, M. S., Gabrielsen, M., Micossi, E., Leonard, G. A., McSweeney, S. M., Ravelli, R. B., Tetaud, E., Fairlamb, A. H., Bond, C. S., and Hunter, W. N. (2003). Tryparedoxins from Crithidia fasciculata and Trypanosoma brucei: photoreduction of the redox disulfide using synchrotron radiation and evidence for a conformational switch implicated in function. J Biol Chem 278, 25919-25925.
2. Chim, N., Riley, R., The, J., Im, S., Segelke, B., Lekin, T., Yu, M., Hung, L. W., Terwilliger, T., Whitelegge, J. P., et al. (2010). An extracellular disulfide bond forming protein (DsbF) from Mycobacterium tuberculosis: structural, biochemical, and gene expression analysis. J Mol Biol 396, 1211-1226.
3. Comas, I., and Gagneux, S. (2009). The past and future of tuberculosis research. PLoS Pathog 5, e1000600.
4. Crow, A., Lewin, A., Hecht, O., Carlsson Moller, M., Moore, G. R., Hederstedt, L., and Le Brun, N. E. (2009a). Crystal structure and biophysical properties of Bacillus subtilis BdbD. An oxidizing thiol: disulfide oxidoreductase containing a novel metal site. J Biol Chem 284, 23719-23733.
5. Crow, A., Liu, Y., Moller, M. C., Le Brun, N. E., and Hederstedt, L. (2009b). Structure and functional properties of Bacillus subtilis en dospore biogenesis factor StoA. J Biol Chem 284, 10056-10066.
6. Daniels, R., Mellroth, P., Bernsel, A., Neiers, F., Normark, S., von Heijne, G., and Henriques-Normark, B. (2010). Disulfide bond formation and cysteine exclusion in gram-positive bacteria. J Biol Chem 285, 3300-3309.
7. DeLano, W. L. (2002). The PyMOL Molecular Graphics System. De-Lano Scientific, San Carlos, CA, USA.
8. Denoncin, K., and Collet, J. F. (2012). Disulfide bond formation in the bacterial periplasm: major achievements and challenges ahead. Antioxid Redox Signal 19, 63-71.
9. Depuydt, M., Messens, J., and Collet, J. F. (2011). How proteins form disulfide bonds. Antioxid Redox Signal 15, 49-66.
10. Dorenbos, R., Stein, T., Kabel, J., Bruand, C., Bolhuis, A., Bron, S., Quax, W. J., and van Dijl, J. M. (2002). Thiol-disulfide oxidoreductases are essential for the production of the lantibiotic sublancin 168. J Biol Chem 277, 16682-16688.
11. Dumoulin, A., Grauschopf, U., Bischoff, M., Thony-Meyer, L., and Berger-Bachi, B. (2005). Staphylococcus aureus DsbA is a membranebound lipoprotein with thiol-disulfide oxidoreductase activity. Arch Microbiol 184, 117-128.
12. Dutton, R. J., Boyd, D., Berkmen, M., and Beckwith, J. (2008). Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc Natl Acad Sci U S A 105, 11933-11938.
13. Dutton, R. J., Wayman, A., Wei, J. R., Rubin, E. J., Beckwith, J., and Boyd, D. (2010). Inhibition of bacterial disulfide bond formation by the anticoagulant warfarin. Proc Natl Acad Sci U S A 107, 297-301.
14. Emsley, P., and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132.
15. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010). Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66, 486-501.
16. Ericsson, U. B., Hallberg, B. M., DeTitta, G. T., Dekker, N., and Nordlund, P. (2006). Thermofluor-based high-throughput stability optimization of proteins for structural studies. Anal Biochem 357, 289-298.
17. Erlendsson, L. S., Acheson, R. M., Hederstedt, L., and Le Brun, N. E. (2003). Bacillus subtilis ResA is a thiol-disulfide oxidoreductase involved in cytochrome c synthesis. J Biol Chem 278, 17852-17858.
18. Erlendsson, L. S., and Hederstedt, L. (2002). Mutations in the thiol-disulfide oxidoreductases BdbC and BdbD can suppress cytochrome c deficiency of CcdA-defective Bacillus subtilis cells. J Bacteriol 184, 1423-1429.
19. Goldstone, D., Baker, E. N., and Metcalf, P. (2005). Crystallization and preliminary diffraction studies of the C-terminal domain of the DipZ homologue from Mycobacterium tuberculosis. Acta Crystallogr Sect F Struct Biol Cryst Commun 61, 243-245.
20. Goulding, C. W., Apostol, M., Anderson, D. H., Gill, H. S., Smith, C. V., Kuo, M. R., Yang, J. K., Waldo, G. S., Suh, S. W., Chauhan, R., et al. (2002). The TB structural genomics consortium: providing a structural foundation for drug discovery. Curr Drug Targets Infect Disord 2, 121-141.
21. Goulding, C. W., Apostol, M. I., Gleiter, S., Parseghian, A., Bardwell, J., Gennaro, M., and Eisenberg, D. (2004). Gram-positive DsbE proteins function differently from Gram-negative DsbE homologs. A structure to function analysis of DsbE from Mycobacterium tuberculosis. J Biol Chem 279, 3516-3524.
22. Goulding, C. W., Perry, L. J., Anderson, D., Sawaya, M. R., Cascio, D., Apostol, M. I., Chan, S., Parseghian, A., Wang, S. S., Wu, Y., et al. (2003). Structural genomics of Mycobacterium tuberculosis: a preliminary report of progress at UCLA. Biophys Chem 105, 361-370.
23. Hennecke, J., Sebbel, P., and Glockshuber, R. (1999). Random circular permutation of DsbA reveals segments that are essential for protein folding and stability. J Mol Biol 286, 1197-1215.
24. Heras, B., Kurz, M., Jarrott, R., Shouldice, S. R., Frei, P., Robin, G., Cemazar, M., Thony-Meyer, L., Glockshuber, R., and Martin, J. L. (2008). Staphylococcus aureus DsbA does not have a destabilizing disulfide. A new paradigm for bacterial oxidative folding. J Biol Chem 283, 4261-4271.
25. Hu, Y., Dong, X., Wu, A., Cao, Y., Tian, L., and Jiang, T. (2011). Incorporation of local structural preference potential improves fold recognition. PLoS One 6, e17215.
26. Inaba, K., and Ito, K. (2008). Structure and mechanisms of the DsbBDsbA disulfide bond generation machine. Biochim Biophys Acta 1783, 520-529.
27. Inaba, K., Murakami, S., Suzuki, M., Nakagawa, A., Yamashita, E., Okada, K., and Ito, K. (2006). Crystal structure of the DsbB-DsbA complex reveals a mechanism of disulfide bond generation. Cell 127, 789-801.
28. Kadokura, H., Tian, H., Zander, T., Bardwell, J. C., and Beckwith, J. (2004). Snapshots of DsbA in action: detection of proteins in the process of oxidative folding. Science 303, 534-537.
29. Krissinel, E., and Henrick, K. (2007). Inference of macromolecular assemblies from crystalline state. J Mol Biol 372, 774-797.
30. Kurz, M., Iturbe-Ormaetxe, I., Jarrott, R., Shouldice, S. R., Wouters, M. A., Frei, P., Glockshuber, R., O'Neill, S. L., Heras, B., and Martin, J. L. (2009). Structural and functional characterization of the oxidoreductase alpha-DsbA1 from Wolbachia pipientis. Antioxid Redox Signal 11, 1485-1500.
31. Li, W., Schulman, S., Dutton, R. J., Boyd, D., Beckwith, J., and Rapoport, T. A. (2010). Structure of a bacterial homologue of vitamin K epoxide reductase. Nature 463, 507-512.
32. Martin, J. L., Bardwell, J. C., and Kuriyan, J. (1993). Crystal structure of the DsbA protein required for disulphide bond formation in vivo. Nature 365, 464-468.
33. Matthews, B. W. (1968). Solvent content of protein crystals. J Mol Biol 33, 491-497.
34. McCarthy, A. A., Haebel, P. W., Torronen, A., Rybin, V., Baker, E. N., and Metcalf, P. (2000). Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli. Nat Struct Biol 7, 196-199.
35. Meima, R., Eschevins, C., Fillinger, S., Bolhuis, A., Hamoen, L. W., Dorenbos, R., Quax, W. J., van Dijl, J. M., Provvedi, R., Chen, I., et al. (2002). The bdbDC operon of Bacillus subtilis encodes thioldisulfide oxidoreductases required for competence development. J Biol Chem 277, 6994-7001.
36. Messens, J., and Collet, J. F. (2006). Pathways of disulfide bond formation in Escherichia coli. Int J Biochem Cell Biol 38, 1050-1062.
37. Otwinowski, Z., and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Method Enzymol 276, 307-326.
38. Paxman, J. J., Borg, N. A., Horne, J., Thompson, P. E., Chin, Y., Sharma, P., Simpson, J. S., Wielens, J., Piek, S., Kahler, C. M., et al. (2009). The structure of the bacterial oxidoreductase enzyme DsbA in complex with a peptide reveals a basis for substrate specificity in the catalytic cycle of DsbA enzymes. J Biol Chem 284, 17835-17845.
39. Reid, E., Cole, J., and Eaves, D. J. (2001). The Escherichia coli CcmG protein fulfils a specific role in cytochrome c assembly. Biochem J 355, 51-58.
40. Shao, F., Bader, M. W., Jakob, U., and Bardwell, J. C. (2000). DsbG, a protein disulfide isomerase with chaperone activity. J Biol Chem 275, 13349-13352.
41. Shouldice, S. R., Heras, B., Walden, P. M., Totsika, M., Schembri, M. A., and Martin, J. L. (2011). Structure and function of DsbA, a key bacterial oxidative folding catalyst. Antioxid Redox Signal 14, 1729-1760.
42. Stewart, E. J., Katzen, F., and Beckwith, J. (1999). Six conserved cysteines of the membrane protein DsbD are required for the transfer of electrons from the cytoplasm to the periplasm of Escherichia coli. EMBO J 18, 5963-5971.
43. Trott, O., and Olson, A. J. (2010). AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31, 455-461.
44. Wang, C., Chen, S., Wang, X., Wang, L., Wallis, A. K., Freedman, R. B., and Wang, C. C. (2010). Plasticity of human protein disulfide isomerase: evidence for mobility around the X-linker region and its functional significance. J Biol Chem 285, 26788-26797.
45. Wang, X., Dutton, R. J., Beckwith, J., and Boyd, D. (2011). Membrane topology and mutational analysis of Mycobacterium tuberculosis VKOR, a protein involved in disulfide bond formation and a homologue of human vitamin K epoxide reductase. Antioxid Redox Signal 14, 1413-1420.
46. Weik, M., Ravelli, R. B., Kryger, G., McSweeney, S., Raves, M. L., Harel, M., Gros, P., Silman, I., Kroon, J., and Sussman, J. L. (2000). Specific chemical and structural damage to proteins produced by synchrotron radiation. Proc Natl Acad Sci U S A 97, 623-628.
47. Yang, Q., Yu, K., Yan, L., Li, Y., Chen, C., and Li, X. (2011). Structural view of the regulatory subunit of aspartate kinase from Mycobacterium tuberculosis. Protein Cell 2, 745-754.