Nutrient-starved, non-replicating Mycobacterium tuberculosis requires respiration, ATP synthase and isocitrate lyase for maintenance of ATP homeostasis and viability

Microbiology

Volumn 156, Issue 1, 2010, Pages 81-87

  Gengenbacher, Martin ^a   Rao, Srinivasa P S ^a   Pethe, Kevin ^a   Dick, Thomas ^a  

^a NOVARTIS INSTITUTE FOR TROPICAL DISEASES   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

1 (6 BROMO 2 METHOXY 3 QUINOLINYL) 4 DIMETHYLAMINO 2 (1 NAPHTHYL) 1 PHENYL 2 BUTANOL; ISOCITRATE LYASE; ISONIAZID; MOXIFLOXACIN; NITRATE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RIFAMPICIN; STREPTOMYCIN;

ADAPTATION; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL METABOLISM; BACTERIAL SURVIVAL; BACTERIAL VIABILITY; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; ENERGY METABOLISM; HOMEOSTASIS; MICROBIAL RESPIRATION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; STARVATION;

ADAPTATION, PHYSIOLOGICAL; ADENOSINE TRIPHOSPHATE; DRUG RESISTANCE, BACTERIAL; ENERGY METABOLISM; GENE KNOCKOUT TECHNIQUES; HOMEOSTASIS; ISOCITRATE LYASE; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MYCOBACTERIUM TUBERCULOSIS; NITRATES; OXYGEN; PROTON-TRANSLOCATING ATPASES;

BACILLI (CLASS); MYCOBACTERIUM TUBERCULOSIS;

EID: 76849095708     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.033084-0     Document Type: Article

References (34)

1. Amaral, L., Kristiansen, J. E., Abebe, L. S. & Millett, W. (1996). Inhibition of the respiration of multi-drug resistant clinical isolates of Mycobacterium tuberculosis by thioridazine: potential use for initial therapy of freshly diagnosed tuberculosis. J Antimicrob Chemother 38, 1049-1053.
2. Andries, K., Verhasselt, P., Guillemont, J., Göhlmann, H. W., Neefs, J. M., Winkler, H., Van Gestel, J., Timmerman, P., Zhu, M. & other authors (2005). A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 307, 223-227.
3. Bardarov, S., Bardarov, S., Jr, Pavelka, M. S., Jr, Sambandamurthy, V., Larsen, M., Tufariello, J., Chan, J., Hatfull, G. & Jacobs, W. R., Jr (2002). Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology 148, 3007-3017.
4. Betts, J. C., Lukey, P. T., Robb, L. C., McAdam, R. A. & Duncan, K. (2002). Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 43, 717-731.
5. Boshoff, H. I. & Barry, C. E., III (2005). Tuberculosis - metabolism and respiration in the absence of growth. Nat Rev Microbiol 3, 70-80.
6. Cattell, K. J., Lindop, C. R., Knight, I. G. & Beechey, R. B. (1971). The identification of the site of action of N,N'-dicyclohexylcarbodi-imide as a proteolipid in mitochondrial membranes. Biochem J 125, 169-177.
7. Mtb-mediated adaptation to stationary phase in long-term persistence of Mycobacterium tuberculosis in mice. Proc Natl Acad Sci U S A 100, 10026-10031.
8. Dick, T. (2001). Dormant tubercle bacilli: the key to more effective TB chemotherapy? J Antimicrob Chemother 47, 117-118.
9. Fenhalls, G., Stevens, L., Moses, L., Bezuidenhout, J., Betts, J. C., Helden, P. van, Lukey, P. T. & Duncan, K. (2002). In situ detection of Mycobacterium tuberculosis transcripts in human lung granulomas reveals differential gene expression in necrotic lesions. Infect Immun 70, 6330-6338.
10. Gordhan, B. G., Smith, D. A., Kana, B. D., Bancroft, G. & Mizrahi, V. (2006). The carbon starvation-inducible genes Rv2557 and Rv2558 of Mycobacterium tuberculosis are not required for long-term survival under carbon starvation and for virulence in SCID mice. Tuberculosis (Edinb) 86, 430-437.
11. Harries, A. D. & Dye, C. (2006). Tuberculosis. Ann Trop Med Parasitol 100, 415-431.
12. Hinds, J., Mahenthiralingam, E., Kempsell, K. E., Duncan, K., Stokes, R. W., Parish, T. & Stoker, N. G. (1999). Enhanced gene replacement in mycobacteria. Microbiology 145, 519-527.
13. Honer Zu Bentrup, K., Miczak, A., Swenson, D. L. & Russell, D. G. (1999). Characterization of activity and expression of isocitrate lyase in Mycobacterium avium and Mycobacterium tuberculosis. J Bacteriol 181, 7161-7167.
14. Koul, A., Dendouga, N., Vergauwen, K., Molenberghs, B., Vranckx, L., Willebrords, R., Ristic, Z., Lill, H., Dorange, I. & other authors (2007). Diarylquinolines target subunit c of mycobacterial ATP synthase. Nat Chem Biol 3, 323-324.
15. Koul, A., Vranckx, L., Dendouga, N., Balemans, W., Van den Wyngaert, I., Vergauwen, K., Göhlmann, H. W., Willebrords, R., Poncelet, A. & other authors (2008). Diarylquinolines are bactericidal for dormant mycobacteria as a result of disturbed ATP homeostasis. J Biol Chem 283, 25273-25280.
16. Lee, M. H., Pascopella, L., Jacobs, W. R., Jr & Hatfull, G. F. (1991). Site-specific integration of mycobacteriophage L5: integration-proficient vectors for Mycobacterium smegmatis, Mycobacterium tuberculosis, and bacille Calmette-Guerin. Proc Natl Acad Sci U S A 88, 3111-3115.
17. Lim, A., Eleuterio, M., Hutter, B., Murugasu-Oei, B. & Dick, T. (1999). Oxygen depletion-induced dormancy in Mycobacterium bovis BCG. J Bacteriol 181, 2252-2256.
18. Loebel, R. O., Shorr, E. & Richardson, H. B. (1933a). The influence of adverse conditions upon the respiratory metabolism and growth of human tubercle bacilli. J Bacteriol 26, 167-200.
19. Loebel, R. O., Shorr, E. & Richardson, H. B. (1933b). The influence of foodstuffs upon the respiratory metabolism and growth of human tubercle bacilli. J Bacteriol 26, 139-166.
20. McKinney, J. D., Honer zu Bentrup, K., Munoz-Elias, E. J., Miczak, A., Chen, B., Chan, W. T., Swenson, D., Sacchettini, J. C., Jacobs, W. R., Jr & Russell, D. G. (2000). Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406, 735-738.
21. Nyka, W. (1974). Studies on the effect of starvation on mycobacteria. Infect Immun 9, 843-850.
22. Ovchinnikov, Y. A.., Abdulaev, N. G. & Modyanov, N. N. (1982). Structural basis of proton-translocating protein function. Annu Rev Biophys Bioeng 11, 445-463.
23. Parish, T. & Stoker, N. G. (2000). Use of a flexible cassette method to generate a double unmarked Mycobacterium tuberculosis tlyA plcABC mutant by gene replacement. Microbiology 146, 1969-1975.
24. Primm, T. P., Andersen, S. J., Mizrahi, V., Avarbock, D., Rubin, H. & Barry, C. E., III (2000). The stringent response of Mycobacterium tuberculosis is required for long-term survival. J Bacteriol 182, 4889-4898.
25. Rao, S. P., Alonso, S., Rand, L., Dick, T. & 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.
26. Stover, C. K., de la Cruz, V. F., Fuerst, T. R., Burlein, J. E., Benson, L. A., Bennett, L. T., Bansal, G. P., Young, J. F. & Lee, M. H. (1991). New use of BCG for recombinant vaccines. Nature 351, 456-460.
27. Teh, J. S., Yano, T. & Rubin, H. (2007). Type II NADH: menaquinone oxidoreductase of Mycobacterium tuberculosis. Infect Disord Drug Targets 7, 169-181.
28. Via, L. E., Lin, P. L., Ray, S. M., Carrillo, J., Allen, S. S., Eum, S. Y., Taylor, K., Klein, E., Manjunatha, U. & other authors (2008). Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 76, 2333-2340.
29. Wayne, L. G. & Hayes, L. G. (1996). An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 64, 2062-2069.
30. Wayne, L. G. & Sohaskey, C. D. (2001). Nonreplicating persistence of Mycobacterium tuberculosis. Annu Rev Microbiol 55, 139-163.
31. Weinstein, E. A., Yano, T., Li, L. S. & other authors (2005). Inhibitors of type II NADH: menaquinone oxidoreductase represent a class of antitubercular drugs. Proc Natl Acad Sci U S A 102, 4548-4553.
32. Williams, K. J. & Duncan, K. (2007). Current strategies for identifying and validating targets for new treatment-shortening drugs for TB. Curr Mol Med 7, 297-307.
33. Xie, Z., Siddiqi, N. & Rubin, E. J. (2005). Differential antibiotic susceptibilities of starved Mycobacterium tuberculosis isolates. Antimicrob Agents Chemother 49, 4778-4780.
34. Yano, T., Li, L. S., Weinstein, E., Teh, J. S. & Rubin, H. (2006). Steady-state kinetics and inhibitory action of antitubercular phenothiazines on Mycobacterium tuberculosis type-II NADH-menaquinone oxido-reductase (NDH-2). J Biol Chem 281, 11456-11463.