Isolation and characterization of a hybrid respiratory supercomplex consisting of mycobacterium tuberculosis cytochrome bcc and mycobacterium smegmatis cytochrome aa3

Journal of Biological Chemistry

Volumn 290, Issue 23, 2015, Pages 14350-14360

  Kim, Mi Sun ^a,d   Jang, Jichan ^b   AB Rahman, Nurlilah Binte ^c   Pethe, Kevin ^b,c   Berry, Edward A ^a   Huang, Li Shar ^a  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

^b Institute Pasteur Korea   (South Korea)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d Ewha Womans University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; PURIFICATION; TUBES (COMPONENTS);

CRYSTALLOGRAPHIC STUDIES; DIRECT ELECTRON TRANSFER; EXTRACTION AND PURIFICATIONS; ISOLATION AND CHARACTERIZATION; MULTIDRUG-RESISTANT TUBERCULOSIS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PURIFICATION PROCEDURES;

CRYSTAL STRUCTURE;

CYTOCHROME BCC CYTOCHROME AA3 COMPLEX; DIMER; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CYTOCHROME C OXIDASE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; COMPLEX FORMATION; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME PURIFICATION; ENZYME STABILITY; GEL FILTRATION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN EXPRESSION; CHEMISTRY; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; MYCOBACTERIOSIS;

CORYNEBACTERINEAE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

BACTERIAL PROTEINS; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX III; ELECTRON TRANSPORT COMPLEX IV; HUMANS; MYCOBACTERIUM INFECTIONS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 84930655571     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.624312     Document Type: Article

References (32)

1. Lechartier, B., Rybniker, J., Zumla, A., and Cole, S. T. (2014) Tuberculosis drug discovery in the post-post-genomic era. EMBO Mol. Med. 6, 158-168
2. Rao, S. P., Alonso, S., Rand, L., Dick, T., and Pethe, K. (2008) The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 105, 11945-11950
3. Berney, M., and Cook, G. M. (2010) Unique flexibility in energy metabolism allows mycobacteria to combat starvation and hypoxia. PLoS One 5, e8614
4. Mak, P. A., and Rao, S. P., Ping Tan, M., Lin, X., Chyba, J., Tay, J., Ng, S.H., Tan, B. H., Cherian, J., Duraiswamy, J., Bifani, P., Lim, V., Lee, B.H., Ling Ma, N., Beer, D., Thayalan, P., Kuhen, K., Chatterjee, A., Supek, F., Glynne, R., Zheng, J., Boshoff, H. I., Barry, C. E., 3rd, Dick, T., Pethe, K., and Camacho, L. R. (2012) A high-throughput screen to identify inhibitors of ATP homeostasis in non-replicating Mycobacterium tuberculosis. ACS Chem. Biol. 7, 1190-1197
5. Berney, M., and Cook, G. M. (2014) in Advances in Photosynthesis and Respiration (Hohmann-Marriott, M. F., ed) pp. 277-293, Springer Science + Business Media, Dordrecht, The Netherlands
6. Kakkar, A. K., and Dahiya, N. (2014) Bedaquiline for the treatment of resistant tuberculosis: promises and pitfalls. Tuberculosis 94, 357-362
7. Moraski, G. C, Markley, L. D., and Hipskind, P. A., Boshoff, H., Cho, S., Franzblau, S. G., and Miller, M. J. (2011) Advent of imidazo[1, 2-a]pyridine-3-carboxamides with potent multi- and extended drug resistant antituberculosis activity. ACS Med. Chem. Lett. 2, 466-470
8. Abrahams, K. A., and Cox, J. A., Spivey, V. L., Loman, N. J., and Pallen, M. J., Constantinidou, C, Fernandez, R., Alemparte, C, Remuinán, M. J., Barros, D., Ballell, L., and Besra, G. S. (2012) Identification of novel imidazo[1, 2-a]pyridine inhibitors targetingM. tuberculosis QcrB. PLoS One 7, e52951
9. Pethe, K., Bifani, P., Jang, J., Kang, S., Park, S., Ahn, S., Jiricek, J., Jung, J., Jeon, H. K., Cechetto, J., Christophe, T., Lee, H., Kempf, M., Jackson, M., Lenaerts, A. J., Pham, H., Jones, V., Seo, M. J., Kim, Y. M., Seo, M., Seo, J. J., Park, D., Ko, Y., Choi, I., Kim, R., Kim, S. Y., Lim, S., Yim, S. A., Nam, J., Kang, H., Kwon, H., Oh, C. T., Cho, Y., Jang, Y., Kim, J., Chua, A., Tan, B. H., Nanjundappa, M. B., Rao, S. P., Barnes, W. S., Wintjens, R., Walker, J. R., Alonso, S., Lee, S., Oh, S., Oh, T., Nehrbass, U., Han, S. J., No, Z., Lee, J., Brodin, P., Cho, S. N., and Nam, K. (2013) Discovery of Q203, a potent clinical candidate for the treatment of tuberculosis. Nat. Med. 19, 1157-1160
10. Arora, K., Ochoa-Montano, B., Tsang, P. S., and Blundell, T. L., Dawes, S. S., Mizrahi, V., Bayliss, T., Mackenzie, C. J., Cleghorn, L. A., Ray, P. C, Wyatt, P. G., Uh, E., Lee, J., Barry, C. E., 3rd, and Boshoff, H. I. (2014) Respiratory flexibility in response to inhibition of cytochrome C oxidase in Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 58, 6962-6965
11. Sone, N, Nagata, K., Kojima, H., Tajima, J., Kodera, Y., Kanamaru, T., Noguchi, S., and Sakamoto, J. (2001) A novel hydrophobic diheme c-type cytochrome. Purification from Corynebacteriumglutamicum and analysis of the QcrCBA operon encoding three subunit proteins of a putative cytochrome reductase complex. Biochim. Biophys. Acta 1503, 279-290
12. Cheng, Y., Moraski, G.C, Cramer, J., and Miller, M. J., and Schorey, J.S. (2014) Bactericidal activity of an imidazo[1, 2-a]pyridine using a mouse M. tuberculosis infection model. PLoS One 9, e87483
13. Berry, E. A., Guergova-Kuras, M., Huang, L. S., and Crofts, A. R. (2000) Structure and function of cytochrome bc complexes. Annu. Rev. Biochem. 69, 1005-1075
14. 1 of quinol-cytochrome c reductase. J. Biol. Chem. 271, 12457-12462
15. 1. Arch. Microbiol. 175, 282-294
16. 1. J. Biol. Chem. 278, 4339-4346
17. 3 interaction in the respiratory chain of Mycobacterium smegmatis. Microbiology 152, 823-829
18. Sassetti, C. M., and Boyd, D. H., and Rubin, E. J. (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48, 77-84
19. Griffin, J. E., and Gawronski, J. D., Dejesus, M. A., Ioerger, T. R., and Akerley, B. J., and Sassetti, C. M. (2011) High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog. 7, e1002251
20. 3 branch of the respiratory network in mycobacteria and network adaptation occurring in response to its disruption. J. Bacteriol. 187, 6300-6308
21. Hao, H. X., Khalimonchuk, O., Schraders, M., Dephoure, N., and Bayley, J. P., Kunst, H., Devilee, P., Cremers, C. W., Schiffman, J. D., Bentz, B. G., Gygi, S. P., Winge, D. R., Kremer, H., and Rutter, J. (2009) SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science 325, 1139-1142
22. Thomas, P. E., Ryan, D., and Levin, W. (1976) An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal. Biochem. 75, 168-176
23. Berry, E. A., and Trumpower, B. L. (1987) Simultaneous determination of hemes a,b, and cfrom pyridine hemochrome spectra. Anal. Biochem. 161, 1-15
24. Borisov, V. B., and Gennis, R. B., Hemp, J., and Verkhovsky, M. I. (2011) The cytochrome bd respiratory oxygen reductases. Biochim. Biophys. Acta 1807, 1398-1413
25. Kusumoto, K., Sakiyama, M., Sakamoto, J., Noguchi, S., and Sone, N. (2000) Menaquinol oxidase activity and primary structure of cytochrome bd from the amino-acid fermenting bacterium Corynebacterium glutamicum. Arch. Microbiol. 173, 390-397
26. Hägerhäll, C. (1997) Succinate: quinone oxidoreductases: variations on a conserved theme. Biochim. Biophys. Acta 1320, 107-141
27. Pecsi, I., Hards, K., Ekanayaka, N., Berney, M., Hartman, T., Jacobs, W. R., Jr., and Cook, G. M. (2014) Essentiality of succinate dehydrogenase in Mycobacterium smegmatis and its role inthe generation of the membrane potential under hypoxia. mBio 5, 01093-14
28. Hasan, S. S., Yamashita, E., Ryan, C. M., and Whitelegge, J. P., and Cramer, W. A. (2011) Conservation of lipid functions in cytochrome bc complexes. J. Mol. Biol. 414, 145-162
29. 1. Nature 392, 677-684
30. Marres, C. M., and Slater, E.C. (1977) Polypeptide composition ofpurified QH2:cytochrome c oxidoreductase from beef-heart mitochondria. Biochim. Biophys. Acta 462, 531-548
31. Horváth, A., and Berry, E. A., and Maslov, D. A. (2000) Translation of the edited mRNA for cytochrome b in trypanosome mitochondria. Science 287, 1639-1640
32. 3"-type terminal oxidase derived from Nitrobacter agilis. J. Biochem. 89, 265-273