Is Mycobacterium tuberculosis stressed out? A critical assessment of the genetic evidence

Microbes and Infection

Volumn 12, Issue 14-15, 2010, Pages 1091-1101

  Stallings, Christina L ^a   Glickman, Michael S ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Mycobacterium tuberculosis; Pathogenesis; Stress responses

Indexed keywords

PHOSPHATE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

ACIDIFICATION; CELL SURFACE; CLINICAL ASSESSMENT; DNA DAMAGE; GENETIC ANALYSIS; HUMAN; MEDICAL INFORMATION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUTRIENT; PHAGOSOME; PRIORITY JOURNAL; SHORT SURVEY; STARVATION; TUBERCULOSIS;

GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; MYCOBACTERIUM TUBERCULOSIS; STRESS, PHYSIOLOGICAL;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

EID: 78649895979     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2010.07.014     Document Type: Short Survey

References (97)

1. Andries K., Verhasselt P., Guillemont J., Gohlmann H.W., Neefs J.M., Winkler H., Van Gestel J., Timmerman P., Zhu M., Lee E., Williams P., de Chaffoy D., Huitric E., Hoffner S., Cambau E., Truffot-Pernot C., Lounis N., Jarlier V. A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 2005, 307:223-227.
2. Medlar E.M., Bernstein S., Steward D.M. A bacteriologic study of resected tuberculous lesions. Am. Rev. Tuberc. 1952, 66:36-43.
3. Efficacy of various durations of isoniazid preventive therapy for tuberculosis: five years of follow-up in the IUAT trial. International Union Against Tuberculosis Committee on Prophylaxis. Bull. World Health Organ 1982, 60:555-564.
4. Flynn J.L., Chan J. Immunology of tuberculosis. Annu. Rev. Immunol. 2001, 19:93-129.
5. Pan H., Yan B.S., Rojas M., Shebzukhov Y.V., Zhou H., Kobzik L., Higgins D.E., Daly M.J., Bloom B.R., Kramnik I. Ipr1 gene mediates innate immunity to tuberculosis. Nature 2005, 434:767-772.
6. Gill W.P., Harik N.S., Whiddon M.R., Liao R.P., Mittler J.E., Sherman D.R. A replication clock for Mycobacterium tuberculosis. Nat. Med. 2009, 15:211-214.
7. Stallings C.L., Stephanou N.C., Chu L., Hochschild A., Nickels B.E., Glickman M.S. CarD is an essential regulator of rRNA transcription required for Mycobacterium tuberculosis persistence. Cell 2009, 138:146-159.
8. Karakousis P.C., Yoshimatsu T., Lamichhane G., Woolwine S.C., Nuermberger E.L., Grosset J., Bishai W.R. Dormancy phenotype displayed by extracellular Mycobacterium tuberculosis within artificial granulomas in mice. J. Exp. Med. 2004, 200:647-657.
9. McCune R.M., Feldmann F.M., McDermott W. Microbial persistence. II. Characteristics of the sterile state of tubercle bacilli. J. Exp. Med. 1966, 123:469-486.
10. Scanga C.A., Mohan V.P., Joseph H., Yu K., Chan J., Flynn J.L. Reactivation of latent tuberculosis: variations on the cornell murine model. Infect. Immun. 1999, 67:4531-4538.
11. Lin P.L., Rodgers M., Smith L., Bigbee M., Myers A., Bigbee C., Chiosea I., Capuano S.V., Fuhrman C., Klein E., Flynn J.L. Quantitative comparison of active and latent tuberculosis in the cynomolgus macaque model. Infect. Immun. 2009, 77:4631-4642.
12. Singh A., Crossman D.K., Mai D., Guidry L., Voskuil M.I., Renfrow M.B., Steyn A.J. Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog. 2009, 5:e1000545.
13. Cunningham A.F., Spreadbury C.L. Mycobacterial stationary phase induced by low oxygen tension: cell wall thickening and localization of the 16-kilodalton alpha-crystallin homolog. J. Bacteriol. 1998, 180:801-808.
14. Alonso S., Pethe K., Russell D.G., Purdy G.E. Lysosomal killing of Mycobacterium mediated by ubiquitin-derived peptides is enhanced by autophagy. Proc. Natl. Acad. Sci. USA 2007, 104:6031-6036.
15. Liu P.T., Stenger S., Tang D.H., Modlin R.L. Cutting edge: vitamin D-mediated human antimicrobial activity against Mycobacterium tuberculosis is dependent on the induction of cathelicidin. J. Immunol. 2007, 179:2060-2063.
16. Martineau A.R., Newton S.M., Wilkinson K.A., Kampmann B., Hall B.M., Nawroly N., Packe G.E., Davidson R.N., Griffiths C.J., Wilkinson R.J. Neutrophil-mediated innate immune resistance to mycobacteria. J. Clin. Invest. 2007, 117:1988-1994.
17. Kisich K.O., Heifets L., Higgins M., Diamond G. Antimycobacterial agent based on mRNA encoding human beta-defensin 2 enables primary macrophages to restrict growth of Mycobacterium tuberculosis. Infect. Immun. 2001, 69:2692-2699.
18. Stenger S., Hanson D.A., Teitelbaum R., Dewan P., Niazi K.R., Froelich C.J., Ganz T., Thoma-Uszynski S., Melian A., Bogdan C., Porcelli S.A., Bloom B.R., Krensky A.M., Modlin R.L. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science 1998, 282:121-125.
19. Bhatt A., Fujiwara N., Bhatt K., Gurcha S.S., Kremer L., Chen B., Chan J., Porcelli S.A., Kobayashi K., Besra G.S., Jacobs W.R. Deletion of kasB in Mycobacterium tuberculosis causes loss of acid-fastness and subclinical latent tuberculosis in immunocompetent mice. Proc. Natl. Acad. Sci. USA 2007, 104:5157-5162.
20. Gao L.Y., Laval F., Lawson E.H., Groger R.K., Woodruff A., Morisaki J.H., Cox J.S., Daffe M., Brown E.J. Requirement for kasB in Mycobacterium mycolic acid biosynthesis, cell wall impermeability and intracellular survival: implications for therapy. Mol. Microbiol. 2003, 49:1547-1563.
21. Maloney E., Stankowska D., Zhang J., Fol M., Cheng Q.J., Lun S., Bishai W.R., Rajagopalan M., Chatterjee D., Madiraju M.V. The two-domain LysX protein of Mycobacterium tuberculosis is required for production of lysinylated phosphatidylglycerol and resistance to cationic antimicrobial peptides. PLoS Pathog. 2009, 5:e1000534.
22. Vandal O.H., Roberts J.A., Odaira T., Schnappinger D., Nathan C.F., Ehrt S. Acid-susceptible mutants of Mycobacterium tuberculosis share hypersusceptibility to cell wall and oxidative stress and to the host environment. J. Bacteriol. 2009, 191:625-631.
23. Cox J.S., Chen B., McNeil M., Jacobs W.R. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 1999, 402:79-83.
24. Dao D.N., Sweeney K., Hsu T., Gurcha S.S., Nascimento I.P., Roshevsky D., Besra G.S., Chan J., Porcelli S.A., Jacobs W.R. Mycolic acid modification by the mmaA4 gene of M. tuberculosis modulates IL-12 production. PLoS Pathog. 2008, 4:e1000081.
25. Glickman M.S., Cox J.S., Jacobs W.R. A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Mol. Cell 2000, 5:717-727.
26. Geiman D.E., Kaushal D., Ko C., Tyagi S., Manabe Y.C., Schroeder B.G., Fleischmann R.D., Morrison N.E., Converse P.J., Chen P., Bishai W.R. Attenuation of late-stage disease in mice infected by the Mycobacterium tuberculosis mutant lacking the SigF alternate sigma factor and identification of SigF-dependent genes by microarray analysis. Infect. Immun. 2004, 72:1733-1745.
27. Makinoshima H., Glickman M.S. Regulation of Mycobacterium tuberculosis cell envelope composition and virulence by intramembrane proteolysis. Nature 2005, 436:406-409.
28. Singh A., Gupta R., Vishwakarma R.A., Narayanan P.R., Paramasivan C.N., Ramanathan V.D., Tyagi A.K. Requirement of the mymA operon for appropriate cell wall ultrastructure and persistence of Mycobacterium tuberculosis in the spleens of guinea pigs. J. Bacteriol. 2005, 187:4173-4186.
29. Rao V., Fujiwara N., Porcelli S.A., Glickman M.S. Mycobacterium tuberculosis controls host innate immune activation through cyclopropane modification of a glycolipid effector molecule. J. Exp. Med. 2005, 201:535-543.
30. Rao V., Gao F., Chen B., Jacobs W.R., Glickman M.S. Trans-cyclopropanation of mycolic acids on trehalose dimycolate suppresses Mycobacterium tuberculosis-induced inflammation and virulence. J. Clin. Invest. 2006, 116:1660-1667.
31. Camacho L.R., Constant P., Raynaud C., Laneelle M.A., Triccas J.A., Gicquel B., Daffe M., Guilhot C. Analysis of the phthiocerol dimycocerosate locus of Mycobacterium tuberculosis. Evidence that this lipid is involved in the cell wall permeability barrier. J. Biol. Chem. 2001, 276:19845-19854.
32. Armstrong J.A., Hart P.D. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J. Exp. Med. 1971, 134:713-740.
33. Russell D.G. Mycobacterium tuberculosis: here today, and here tomorrow. Nat. Rev. Mol. Cell Biol. 2001, 2:569-577.
34. Vandal O.H., Pierini L.M., Schnappinger D., Nathan C.F., Ehrt S. A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat. Med. 2008, 14:849-854.
35. MacGurn J.A., Cox J.S. A genetic screen for Mycobacterium tuberculosis mutants defective for phagosome maturation arrest identifies components of the ESX-1 secretion system. Infect. Immun. 2007, 75:2668-2678.
36. Pethe K., Swenson D.L., Alonso S., Anderson J., Wang C., Russell D.G. Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation. Proc. Natl. Acad. Sci. USA 2004, 101:13642-13647.
37. Rengarajan J., Murphy E., Park A., Krone C.L., Hett E.C., Bloom B.R., Glimcher L.H., Rubin E.J. Mycobacterium tuberculosis Rv2224c modulates innate immune responses. Proc. Natl. Acad. Sci. USA 2008, 105:264-269.
38. Buchmeier N., Blanc-Potard A., Ehrt S., Piddington D., Riley L., Groisman E.A. A parallel intraphagosomal survival strategy shared by Mycobacterium tuberculosis and Salmonella enterica. Mol. Microbiol. 2000, 35:1375-1382.
39. Molle V., Saint N., Campagna S., Kremer L., Lea E., Draper P., Molle G. pH-dependent pore-forming activity of OmpATb from Mycobacterium tuberculosis and characterization of the channel by peptidic dissection. Mol. Microbiol. 2006, 61:826-837.
40. Raynaud C., Papavinasasundaram K.G., Speight R.A., Springer B., Sander P., Bottger E.C., Colston M.J., Draper P. The functions of OmpATb, a pore-forming protein of Mycobacterium tuberculosis. Mol. Microbiol. 2002, 46:191-201.
41. MacMicking J.D., North R.J., LaCourse R., Mudgett J.S., Shah S.K., Nathan C.F. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA 1997, 94:5243-5248.
42. MacMicking J.D., Nathan C., Hom G., Chartrain N., Fletcher D.S., Trumbauer M., Stevens K., Xie Q.W., Sokol K., Hutchinson N., et al. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 1995, 81:641-650.
43. Darwin K.H., Ehrt S., Gutierrez-Ramos J.C., Weich N., Nathan C.F. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 2003, 302:1963-1966.
44. K.E. Burns, K.H. Darwin, Pupylation versus ubiquitylation: tagging for proteasome-dependent degradation, Cell Microbiol. 12 424-431.
45. Darwin K.H., Lin G., Chen Z., Li H., Nathan C.F. Characterization of a Mycobacterium tuberculosis proteasomal ATPase homologue. Mol. Microbiol. 2005, 55:561-571.
46. Gandotra S., Schnappinger D., Monteleone M., Hillen W., Ehrt S. In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat. Med. 2007, 13:1515-1520.
47. Chan J., Xing Y., Magliozzo R.S., Bloom B.R. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J. Exp. Med. 1992, 175:1111-1122.
48. Flesch I.E., Kaufmann S.H. Activation of tuberculostatic macrophage functions by gamma interferon, interleukin-4, and tumor necrosis factor. Infect. Immun. 1990, 58:2675-2677.
49. Cooper A.M., Segal B.H., Frank A.A., Holland S.M., Orme I.M. Transient loss of resistance to pulmonary tuberculosis in p47(phox-/-) mice. Infect. Immun. 2000, 68:1231-1234.
50. Dussurget O., Stewart G., Neyrolles O., Pescher P., Young D., Marchal G. Role of Mycobacterium tuberculosis copper-zinc superoxide dismutase. Infect. Immun. 2001, 69:529-533.
51. Edwards K.M., Cynamon M.H., Voladri R.K., Hager C.C., DeStefano M.S., Tham K.T., Lakey D.L., Bochan M.R., Kernodle D.S. Iron-cofactored superoxide dismutase inhibits host responses to Mycobacterium tuberculosis. Am. J. Respir. Crit. Care Med. 2001, 164:2213-2219.
52. Piddington D.L., Fang F.C., Laessig T., Cooper A.M., Orme I.M., Buchmeier N.A. Cu, Zn superoxide dismutase of Mycobacterium tuberculosis contributes to survival in activated macrophages that are generating an oxidative burst. Infect. Immun. 2001, 69:4980-4987.
53. Ng V.H., Cox J.S., Sousa A.O., MacMicking J.D., McKinney J.D. Role of KatG catalase-peroxidase in mycobacterial pathogenesis: countering the phagocyte oxidative burst. Mol. Microbiol. 2004, 52:1291-1302.
54. Cirillo S.L., Subbian S., Chen B., Weisbrod T.R., Jacobs W.R., Cirillo J.D. Protection of Mycobacterium tuberculosis from reactive oxygen species conferred by the mel2 locus impacts persistence and dissemination. Infect. Immun. 2009, 77:2557-2567.
55. Wayne L.G., Hayes L.G. An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect. Immun. 1996, 64:2062-2069.
56. Wayne L.G., Lin K.Y. Glyoxylate metabolism and adaptation of Mycobacterium tuberculosis to survival under anaerobic conditions. Infect. Immun. 1982, 37:1042-1049.
57. Wayne L.G. Dormancy of Mycobacterium tuberculosis and latency of disease. Eur. J. Clin. Microbiol. Infect. Dis. 1994, 13:908-914.
58. Bloch H., Segal W. Biochemical differentiation of Mycobacterium tuberculosis grown in vivo and in vitro. J. Bacteriol. 1956, 72:132-141.
59. 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., Russell D.G. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 2000, 406:735-738.
60. Via L.E., Lin P.L., Ray S.M., Carrillo J., Allen S.S., Eum S.Y., Taylor K., Klein E., Manjunatha U., Gonzales J., Lee E.G., Park S.K., Raleigh J.A., Cho S.N., McMurray D.N., Flynn J.L., Barry C.E. Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect. Immun. 2008, 76:2333-2340.
61. Kumar A., Toledo J.C., Patel R.P., Lancaster J.R., Steyn A.J. Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc. Natl. Acad. Sci. USA 2007, 104:11568-11573.
62. Kumar A., Deshane J.S., Crossman D.K., Bolisetty S., Yan B.S., Kramnik I., Agarwal A., Steyn A.J. Heme oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J. Biol. Chem. 2008, 283:18032-18039.
63. Shiloh M.U., Manzanillo P., Cox J.S. Mycobacterium tuberculosis senses host-derived carbon monoxide during macrophage infection. Cell Host Microbe 2008, 3:323-330.
64. Park H.D., Guinn K.M., Harrell M.I., Liao R., Voskuil M.I., Tompa M., Schoolnik G.K., Sherman D.R. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol. Microbiol. 2003, 48:833-843.
65. Converse P.J., Karakousis P.C., Klinkenberg L.G., Kesavan A.K., Ly L.H., Allen S.S., Grosset J.H., Jain S.K., Lamichhane G., Manabe Y.C., McMurray D.N., Nuermberger E.L., Bishai W.R. Role of the dosR-dosS two-component regulatory system in Mycobacterium tuberculosis virulence in three animal models. Infect. Immun. 2009, 77:1230-1237.
66. Rustad T.R., Harrell M.I., Liao R., Sherman D.R. The enduring hypoxic response of Mycobacterium tuberculosis. PLoS ONE 2008, 3:e1502.
67. Parish T., Smith D.A., Kendall S., Casali N., Bancroft G.J., Stoker N.G. Deletion of two-component regulatory systems increases the virulence of Mycobacterium tuberculosis. Infect. Immun. 2003, 71:1134-1140.
68. Malhotra V., Sharma D., Ramanathan V.D., Shakila H., Saini D.K., Chakravorty S., Das T.K., Li Q., Silver R.F., Narayanan P.R., Tyagi J.S. Disruption of response regulator gene, devR, leads to attenuation in virulence of Mycobacterium tuberculosis. FEMS Microbiol. Lett. 2004, 231:237-245.
69. Gupta R.K., Thakur T.S., Desiraju G.R., Tyagi J.S. Structure-based design of DevR inhibitor active against nonreplicating Mycobacterium tuberculosis. J. Med. Chem. 2009, 52:6324-6334.
70. Sambandamurthy V.K., Wang X., Chen B., Russell R.G., Derrick S., Collins F.M., Morris S.L., Jacobs W.R. A pantothenate auxotroph of Mycobacterium tuberculosis is highly attenuated and protects mice against tuberculosis. Nat. Med. 2002, 8:1171-1174.
71. Bange F.C., Brown A.M., Jacobs W.R. Leucine auxotrophy restricts growth of Mycobacterium bovis BCG in macrophages. Infect. Immun. 1996, 64:1794-1799.
72. Gordhan B.G., Smith D.A., Alderton H., McAdam R.A., Bancroft G.J., Mizrahi V. Construction and phenotypic characterization of an auxotrophic mutant of Mycobacterium tuberculosis defective in L-arginine biosynthesis. Infect. Immun. 2002, 70:3080-3084.
73. Hondalus M.K., Bardarov S., Russell R., Chan J., Jacobs W.R., Bloom B.R. Attenuation of and protection induced by a leucine auxotroph of Mycobacterium tuberculosis. Infect. Immun. 2000, 68:2888-2898.
74. Dahl J.L., Kraus C.N., Boshoff H.I., Doan B., Foley K., Avarbock D., Kaplan G., Mizrahi V., Rubin H., Barry C.E. The role of RelMtb-mediated adaptation to stationary phase in long-term persistence of Mycobacterium tuberculosis in mice. Proc. Natl. Acad. Sci. USA 2003, 100:10026-10031.
75. Primm T.P., Andersen S.J., Mizrahi V., Avarbock D., Rubin H., Barry C.E. The stringent response of Mycobacterium tuberculosis is required for long-term survival. J. Bacteriol. 2000, 182:4889-4898.
76. Rifat D., Bishai W.R., Karakousis P.C. Phosphate depletion: a novel trigger for Mycobacterium tuberculosis persistence. J. Infect. Dis. 2009, 200:1126-1135.
77. Rengarajan J., Bloom B.R., Rubin E.J. Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc. Natl. Acad. Sci. USA 2005, 102:8327-8332.
78. Collins D.M., Kawakami R.P., Buddle B.M., Wards B.J., de Lisle G.W. Different susceptibility of two animal species infected with isogenic mutants of Mycobacterium bovis identifies phoT as having roles in tuberculosis virulence and phosphate transport. Microbiology 2003, 149:3203-3212.
79. Lamarche M.G., Wanner B.L., Crepin S., Harel J. The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol. Rev. 2008, 32:461-473.
80. Rickman L., Saldanha J.W., Hunt D.M., Hoar D.N., Colston M.J., Millar J.B., Buxton R.S. A two-component signal transduction system with a PAS domain-containing sensor is required for virulence of Mycobacterium tuberculosis in mice. Biochem. Biophys. Res. Commun. 2004, 314:259-267.
81. Parish T., Smith D.A., Roberts G., Betts J., Stoker N.G. The senX3-regX3 two-component regulatory system of Mycobacterium tuberculosis is required for virulence. Microbiology 2003, 149:1423-1435.
82. Darwin K.H., Nathan C.F. Role for nucleotide excision repair in virulence of Mycobacterium tuberculosis. Infect. Immun. 2005, 73:4581-4587.
83. Stephanou N.C., Gao F., Bongiorno P., Ehrt S., Schnappinger D., Shuman S., Glickman M.S. Mycobacterial nonhomologous end joining mediates mutagenic repair of chromosomal double-strand DNA breaks. J. Bacteriol. 2007, 189:5237-5246.
84. Sander P., Papavinasasundaram K.G., Dick T., Stavropoulos E., Ellrott K., Springer B., Colston M.J., Bottger E.C. Mycobacterium bovis BCG recA deletion mutant shows increased susceptibility to DNA-damaging agents but wild-type survival in a mouse infection model. Infect. Immun. 2001, 69:3562-3568.
85. Buchmeier N.A., Lipps C.J., So M.Y., Heffron F. Recombination-deficient mutants of Salmonella typhimurium are avirulent and sensitive to the oxidative burst of macrophages. Mol. Microbiol. 1993, 7:933-936.
86. Gong C., Martins A., Bongiorno P., Glickman M., Shuman S. Biochemical and genetic analysis of the four DNA ligases of mycobacteria. J. Biol. Chem. 2004, 279:20594-20606.
87. Shuman S., Glickman M.S. Bacterial DNA repair by non-homologous end joining. Nat. Rev. Microbiol. 2007, 5:852-861.
88. Gong C., Bongiorno P., Martins A., Stephanou N.C., Zhu H., Shuman S., Glickman M.S. Mechanism of nonhomologous end-joining in mycobacteria: a low-fidelity repair system driven by Ku, ligase D and ligase C. Nat. Struct. Mol. Biol. 2005, 12:304-312.
89. Boshoff H.I., Reed M.B., Barry C.E., Mizrahi V. DnaE2 polymerase contributes to in vivo survival and the emergence of drug resistance in Mycobacterium tuberculosis. Cell 2003, 113:183-193.
90. Kana B.D., Abrahams G.L., Sung N., Warner D.F., Gordhan B.G., Machowski E.E., Tsenova L., Sacchettini J.C., Stoker N.G., Kaplan G., Mizrahi V. Role of the DinB homologs, Rv1537 and Rv3056, in Mycobacterium tuberculosis. J. Bacteriol. 2010, 192:2220-2227.
91. Sachdeva P., Misra R., Tyagi A.K., Singh Y. The sigma factors of Mycobacterium tuberculosis: regulation of the regulators. FEBS J. 2010, 277:605-626.
92. Singh A., Guidry L., Narasimhulu K.V., Mai D., Trombley J., Redding K.E., Giles G.I., Lancaster J.R., Steyn A.J. Mycobacterium tuberculosis WhiB3 responds to O2 and nitric oxide via its [4Fe-4S] cluster and is essential for nutrient starvation survival. Proc. Natl. Acad. Sci. USA 2007, 104:11562-11567.
93. Steyn A.J., Collins D.M., Hondalus M.K., Jacobs W.R., Kawakami R.P., Bloom B.R. Mycobacterium tuberculosis WhiB3 interacts with RpoV to affect host survival but is dispensable for in vivo growth. Proc. Natl. Acad. Sci. USA 2002, 99:3147-3152.
94. Ewann F., Jackson M., Pethe K., Cooper A., Mielcarek N., Ensergueix D., Gicquel B., Locht C., Supply P. Transient requirement of the PrrA-PrrB two-component system for early intracellular multiplication of Mycobacterium tuberculosis. Infect. Immun. 2002, 70:2256-2263.
95. Rustad T.R., Sherrid A.M., Minch K.J., Sherman D.R. Hypoxia: a window into Mycobacterium tuberculosis latency. Cell Microbiol. 2009, 11:1151-1159.
96. Papavinasasundaram K.G., Anderson C., Brooks P.C., Thomas N.A., Movahedzadeh F., Jenner P.J., Colston M.J., Davis E.O. Slow induction of RecA by DNA damage in Mycobacterium tuberculosis. Microbiology 2001, 147:3271-3279.
97. C. Deb, C.M. Lee, V.S. Dubey, J. Daniel, B. Abomoelak, T.D. Sirakova, S. Pawar, L. Rogers, P.E. Kolattukudy, A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS One. 4(6) (2009) e6077.