Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program

Journal of Experimental Medicine

Volumn 198, Issue 5, 2003, Pages 705-713

  Voskuil, Martin I ^a,b   Schnappinger, Dirk ^a   Visconti, Kevin C ^a   Harrell, Maria I ^c   Dolganov, Gregory M ^d   Sherman, David R ^c   Schoolnik, Gary K ^a,e  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e STANFORD UNIVERSITY   (United States)

Author keywords

Cytochrome oxidase; Latency; M. tuberculosis; Microarray; Nitric oxide

Indexed keywords

CYTOCHROME C OXIDASE; HEME DERIVATIVE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXYGEN;

AEROBIC METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; DNA MICROARRAY; GENE EXPRESSION; GENE REPLICATION; GRANULOMA; HOST; IN VIVO STUDY; MACROPHAGE; MITOCHONDRIAL RESPIRATION; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXYGEN CONCENTRATION; PRIORITY JOURNAL; REGULON; SURVIVAL; TUBERCULOSIS;

MYCOBACTERIUM TUBERCULOSIS; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE; OXYGEN CONSUMPTION; TRIAZENES;

EID: 0042140672     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20030205     Document Type: Article

References (36)

1. Dye, C., S. Scheele, P. Dolin, V. Pathania, and M.C. Raviglione. 1999. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA. 282:677-686.
2. Flynn, J.L., and J. Chan. 2001. Tuberculosis: latency and reactivation. Infect. Immun. 69:4195-4201.
3. McKinney, J.D., K. Honer zu Bentrup, E.J. Munoz-Elias, A. Miczak, B. Chen, W.T. Chan, D. Swenson, J.C. Sacchettini, W.R. Jacobs, Jr., and D.G. Russell. 2000. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature. 406:735-738.
4. Betts, J.C., P.T. Lukey, L.C. Robb, R.A. McAdam, and K. Duncan. 2002. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 43:717-731.
5. Wayne, L.G., and C.D. Sohaskey. 2001. Nonreplicating persistence of mycobacterium tuberculosis. Annu. Rev. Microbiol. 55:139-163.
6. Nathan, C., and S. Ehrt. 2003. Nitric oxide in tuberculosis. In Tuberculosis. 2nd ed. W. Rom and S. Garay, editors. Lippincott, Williams and Wilkins, New York. 215-235.
7. Brown, G.C. 2001. Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim. Biophys. Acta. 1504:46-57.
8. Martin, E., K. Davis, K. Bian, Y.C. Lee, and F. Murad. 2000. Cellular signaling with nitric oxide and cyclic guanosine monophosphate. Semin. Perinatol. 24:2-6.
9. Schoolnik, G.K., M.I. Voskuil, D. Schnappinger, F.H. Yildiz, K. Meidom, N.A. Dolganov, M.A. Wilson, and K.H. Chong. 2001. Whole genomic DNA microarray expression analysis of biofilm development by Vibrio cholerae 01 El Tor. Methods Enzymol. 336:3-18.
10. Rodriguez, G.M., M.I. Voskuil, B. Gold, G.K. Schoolnik, and I. Smith. 2002. ideR, An essential gene in mycobacterium tuberculosis: role of IdeR, in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect. Immun. 70:3371-3381.
11. Manganelli, R., M.I. Voskuil, G.K. Schoolnik, and I. Smith. 2001. The Mycobacterium tuberculosis ECF sigma factor sigmaE: role in global gene expression and survival in macrophages. Mol. Microbiol. 41:423-437.
12. Wayne, L.G., and L.G. Hayes. 1996. An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect. Immun. 64:2062-2069.
13. Sherman, D.R., M. Voskuil, D. Schnappinger, R. Liao, M.I. Harrell, and G.K. Schoolnik. 2001. Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha-crystallin. Proc. Natl. Acad. Sci. USA. 98:7534-7539.
14. Schnappinger, D., S. Ehrt, M.I. Voskuil, Y. Liu, J.A. Mangan, I.M. Monahan, G. Dolganov, B. Efron, P.D. Butcher, C. Nathan, and G. Schoolnik. 2003. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J. Exp. Med. 198:693-704.
15. Shi, L., Y.J. Jung, S. Tyagi, M.L. Gennaro, and R.J. North. 2003. Expression of Th1-mediated immunity in mouse lungs induces a Mycobacterium tuberculosis transcription pattern characteristic of nonreplicating persistence. Proc. Natl. Acad. Sci. USA. 100:241-246.
16. Choi, H.S., P.R. Rai, H.W. Chu, C. Cool, and E.D. Chan. 2002. Analysis of nitric oxide synthase and nitrotyrosine expression in human pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 166:178-186.
17. Lee, B.Y., S.A. Hefta, and P.J. Brennan. 1992. Characterization of the major membrane protein of virulent Mycobacterium tuberculosis. Infect. Immun. 60:2066-2074.
18. Boon, C., and T. Dick. 2002. Mycobacterium bovis BCG response regulator essential for hypoxic dormancy. J. Bacteriol. 184:6760-6767.
19. Park, H.D., K.M. Guinn, M.I. Harrell, R. Liao, M.I. Voskuil, M. Tompa, G.K. Schoolnik, and D.R. Sherman. 2003. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol. Microbiol. 48:833-843.
20. Wayne, L.G., and L.G. Hayes. 1998. Nitrate reduction as a marker for hypoxic shiftdown of Mycobacterium tuberculosis. Tuber. Lung Dis. 79:127-132.
21. Wayne, L.G. 1977. Synchronized replication of Mycobacterium tuberculosis. Infect. Immun. 17:528-530.
22. Diez, A., N. Gustavsson, and T. Nystrom. 2000. The universal stress protein A of Escherichia coli is required for resistance to DNA damaging agents and is regulated by a RecA/ FtsK-dependent regulatory pathway. Mol. Microbiol. 36:1494-1503.
23. Peh, H.L., A. Toh, B. Murugasu-Oei, and T. Dick. 2001. In vitro activities of mitomycin C against growing and hypoxic dormant tubercle bacifli. Antimicrob. Agents Chernother. 45:2403-2404.
24. Crowe, J.H., F.A. Hoekstra, and L.M. Crowe. 1992. Anhydrobiosis. Annu. Rev. Physiol. 54:579-599.
25. Yuan, Y., D.D. Crane, and C.E. Barry III. 1996. Stationary phase-associated protein expression in Mycobacterium tuberculosis: function of the mycobacterial alpha-crystallin homolog. J. Bacteriol. 178:4484-4492.
26. Garbe, T.R., N.S. Hibler, and V. Deretic. 1999. Response to reactive nitrogen intermediates in Mycobacterium tuberculosis: induction of the 16-kilodalton alpha-crystallin homolog by exposure to nitric oxide donors. Infect. Immun. 67:460-465.
27. Narberhaus, F. 2002. Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol. Mol. Biol. Rev. 66:64-93.
28. Bohne, W., J. Heesemann, and U. Gross. 1994. Reduced replication of Toxoplasma gondii is necessary for induction of bradyzoite-specific antigens: a possible role for nitric oxide in triggering stage conversion. Infect. Immun. 62:1761-1767.
29. Hausladen, A., C.T. Privalle, T. Keng, J. DeAngelo, and J.S. Stamler. 1996. Nitrosative stress: activation of the transcription factor OxyR. Cell. 86:719-729.
30. Nunoshiba, T. 1996. Two-stage gene regulation of the superoxide stress response soxRS system in Escherichia coli. Crit. Rev. Eukaryot. Gene Expr. 6:377-389.
31. Poole, R.K., M.F. Anjum, J. Membrillo-Hernandez, S.O. Kim, M.N. Hughes, and V. Stewart. 1996. Nitric oxide, nitrite, and Fnr regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12. J. Bacteriol. 178:5487-5492.
32. Ouellet, H., Y. Ouellet, C. Richard, M. Labarre, B. Wittenberg, J. Wittenberg, and M. Guertin. 2002. Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide. Proc. Natl. Acad. Sci. USA. 99:5902-5907.
33. Kwast, K.E., P.V. Burke, B.T. Staahl, and R.O. Poyton. 1999. Oxygen sensing in yeast: evidence for the involvement of the respiratory chain in regulating the transcription of a subset of hypoxic genes. Proc. Natl. Acad. Sci. USA. 96:5446-5451.
34. Oh, J.I., and S. Kaplan. 2000. Redox signaling: globalization of gene expression. EMBO J. 19:4237-4247.
35. Cole, S.T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, S.V. Gordon, K. Eiglmeier, S. Gas, C.E. Barry III, et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature. 393:537-544.
36. Dolganov, G.M., P.G. Woodruff, A.A. Novikov, Y. Zhang, R.E. Ferrando, R. Szubin, and J.V. Fahy. 2001. A novel method of gene transcript profiling in airway biopsy homogenates reveals increased expression of a Na+-K+-Cl-cotransporter (NKCC1) in asthmatic subjects. Genome Res. 11:1473-1483.