A novel antioxidant gene from Mycobacterium tuberculosis

Journal of Experimental Medicine

Volumn 186, Issue 11, 1997, Pages 1885-1896

  Ehrt, Sabine ^a,b   Shiloh, Michael U ^a   Ruan, Jia ^a   Choi, Michael ^a   Gunzburg, Stuart ^a   Nathan, Carl ^a   Xie, Qiao Wen ^a   Riley, Lee W ^a,b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE NITROGEN METABOLITE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; MOLECULAR CLONING; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR GENE; STRAIN DIFFERENCE; SURVIVAL RATE; TUBERCULOSIS CONTROL;

AMINO ACID SEQUENCE; ANIMALS; ANTIOXIDANTS; BACTERIAL PROTEINS; BASE SEQUENCE; CLONING, MOLECULAR; DNA, BACTERIAL; ESCHERICHIA COLI; GENES, BACTERIAL; HYDROGEN PEROXIDE; MACROPHAGES; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS; NITRITES; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; RECOMBINANT FUSION PROTEINS; TRANSFECTION; TUBERCULOSIS;

EID: 0030782719     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.186.11.1885     Document Type: Article

References (61)

1. Raviglione, M.C., D.E. Snider, Jr., and A. Kochi. 1995. Global epidemiology of tuberculosis. Morbidity and mortality of a worldwide epidemic. JAMA (J. Am. Med. Assoc.). 273:220-226.
2. Chan, J., Y. Tian, K.E. Tanaka, M.S. Tsang, K. Yu, P. Salgame, D. Carroll, Y. Kress, R. Teitelbaum, and B.R. Bloom. 1996. Effects of protein malnutrition on tuberculosis in mice. Proc. Natl. Acad. Sci. USA. 93:14857-14861.
3. Daley, C.L., P.M. Small, G.F. Schecter, G.K. Schoolnik, R.A. McAdam, W.R. Jacobs, Jr., and P.C. Hopewell. 1992. An outbreak of tuberculosis with accelerated progression among persons infected with the human immunodeficiency virus. An analysis using restriction-fragment-length polymorphisms. N. Engl. J. Med. 326:231-235.
4. Nathan, C.F. 1983. Mechanisms of macrophage antimicrobial activity. Trans. R. Soc. Trop. Med. Hyg. 77:620-630.
5. Nathan, C.F., and J.B. Hibbs, Jr. 1991. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 3:65-70.
6. Butler, A.R., F.W. Flitney, and D.L. Williams. 1995. NO, nitrosonium ions, nitroxide ions, nitrosothiols and iron-nitrosyls in biology: a chemist's perspective. Trends Pharmacol. Sci. 16: 18-22.
7. De Groote, M.A., and F.C. Fang. 1995. NO inhibitions: antimicrobial properties of nitric oxide. Clin. Infect. Dis. 21: 162-165.
8. Neill, M.A., and S.J. Klebanoff. 1988. The effect of phenolic glycolipid-1 from Mycobacterium leprae on the antimicrobial activity of human macrophages. J. Exp. Med. 167:30-42.
9. Sherman, D.R., P.J. Sabo, M.J. Mickey, T.M. Arain, G.G. Mahairas, Y. Yuan, C.E. Barry III, and C.K. Stover. 1995. Disparate responses to oxidative stress in saprophytic and pathogenic mycobacteria. Proc. Natl. Acad. Sci. USA. 92: 6625-6629.
10. Sherman, D.R., K. Mdluli, M.J. Hickey, T.M. Arain, S.L. Morris, C.E. Barry III, and C.K. Stover. 1996. Compensatory ahpC gene expression in isoniazid-resistant Mycobacterium tuberculosis. Science. 272:1641-1643.
11. Dumarey, C.H., V. Labrousse, N. Rastogi, B.B. Vargaftig, and M. Bachelet. 1994. Selective Mycobacterium avium-induced production of nitric oxide by human monocyte-derived macrophages. J. Leukocyte Biol. 56:36-40.
12. Zhang, Y., M.J. Garcia, R. Lathigra, B. Allen, C. Moreno, J.D. van Embden, and D. Young. 1992. Alterations in the superoxide dismutase gene of an isoniazid-resistant strain of Mycobacterium tuberculosis. Infect. Immun. 60:2160-2165.
13. Chan, J., and S.H.E. Kaufmann. 1994. Immune mechanisms of protection. In Tuberculosis: Pathogenesis, Protection and Control. B.R. Bloom, editor. American Society for Microbiology, Washington. 389-415.
14. Schlesinger, L.S., C.G. Bellinger-Kawahara, N.R. Payne, and M.A. Horwitz. 1990. Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J. Immunol. 144:2771-2780.
15. Wright, S.D., and S.C. Silverstein. 1983. Receptors for C3b and C3bi promote phagocytosis but not the release of toxic oxygen from human phagocytes. J. Exp. Med. 158:2016-2023.
16. Chan, J., Y. Xing, R.S. Magliozzo, and B.R. Bloom. 1992. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J. Exp. Med. 175:1111-1122.
17. MacMicking, J.D., R.J. North, R. LaCourse, J.S. Mudgett, S.K. Shah, and C.F. Nathan. 1997. Identification of NOS2 as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA. 94:5243-5248.
18. Nicholson, S., M. da G. Bonecini-Almeida, J.R. Lapa e Silva, C. Nathan, Q.W. Xie, R. Mumford, J.R. Weidner, J. Calaycay, J. Geng, N. Boechat, et al. 1996. Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis J. Exp. Med. 183:2293-2302.
19. Nozaki, Y., Y. Hasegawa, S. Ichiyama, I. Nakashima, and K. Shimokata. 1997. Mechanism of nitric oxide-dependent killing of Mycobacterium bovis BCG in human alveolar macrophages. Infect. Immun. 65:3644-3647.
20. Doi, T., M. Ando, T. Akaike, M. Suga, K. Sato, and H. Maeda. 1993. Resistance to nitric oxide in Mycobacterium avium complex and its implication in pathogenesis. Inject. Immun. 61:1980-1989.
21. O'Brien, L., J. Carmichael, D.B. Lowrie, and P.W. Andrew. 1994. Strains of Mycobacterium tuberculosis differ in susceptibility to reactive nitrogen intermediates in vitro. Infect. Immun. 62:5187-5190.
22. Friedman, C.R., M.Y. Stoeckle, B.N. Kreiswirth, W.D. Johnson, Jr., S.M. Manoach, J. Berger, K. Sathianathan, A. Hafner, and L.W. Riley. 1995. Transmission of multidrug-resistant tuberculosis in a large urban setting. Am. J. Respir. Crit. Care Med. 152:355-359.
23. Friedman, C., G.C. Quinn, B.N. Kreiswirth, D.C. Perlman, N. Salomon, N. Schluger, M. Lutfey, J. Berger, N. Poltoratskaia, and L.W. Riley. 1997. Widespread dissemination of a single drug-susceptible strain of Mycobacterium tuberculosis. J. Infect. Dis. 176:478-484.
24. Snapper, S.B. R.E. Melton, S. Mustafa, T. Kieser, and W.R. Jacobs, Jr. 1990. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol. Microbiol. 4:1911-1919.
25. Greenberg, J.T., P. Monach, J.H. Chou, P.D. Josephy, and B. Demple. 1990. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc. Natl. Acad. Sci. USA. 87:6181-6185.
26. Greenberg, J.T., and B. Demple. 1988. Overproduction of peroxide-scavenging enzymes in Escherichia coli suppresses spontaneous mutagenesis and sensitivity to redox-cycling agents in oxyR-mutants. EMBO (Eur. Mol. Biol. Organ.) J. 7: 2611-2617.
27. Garbe, T.R., J. Barathi, S. Barnini, Y. Zhang, C. Abou-Zeid, D. Tang, R. Mukherjee, and D.B. Young. 1994. Transformation of mycobacterial species using hygromycin resistance as selectable marker. Microbiology (Reading). 140:133-138.
28. van Soolingen, D., P.W. Hermans, P.E. de Haas, D.R. Soll, and J.D. van Embden. 1991. Occurrence and stability of insertion sequences in Mycobacterium tuberculosis complex strains: evaluation of an insertion sequence-dependent DNA polymorphism as a tool in the epidemiology of tuberculosis. J. Clin. Microbiol. 29:2578-2586.
29. Shiloh, M.U., J. Ruan, and C. Nathan. 1997. Evaluation of bacterial numbers and phagocyte function with a fluorescence-based microplate assay. Infect. Immun. 65:3193-3197.
30. Buchmeier, N., and F. Heffron. 1989. Intracellular survival of wild-type Salmonella typhimurium and macrophage-sensitive mutants in diverse populations of macrophages. Inject. Immun. 57:1-7.
31. MacMicking, J.D., C. Nathan, G. Horn, N. Chartrain, D.S. Fletcher, M. Trumbauer, K. Stevens, Q.W. Xie, K. Sokol, N. Hutchinson, et al. 1995. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell. 81:641-650 (see erratum Cell. 1995. 81: 1171).
32. Pollock, J.D., D.A. Williams, M.A. Gifford, L.L. Li, X. Du, J. Fisherman, S.H. Orkin, C.M. Doerschuk, and M.C. Dinauer. 1995. Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat. Genet. 9:202-209.
33. Ding, A.H., C.F. Nathan, and D.J. Stuehr. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages: comparison of activating cytokines and evidence for independent production. J. Immunol. 141:2407-2412.
34. 2 release by human blood monocytes and mouse peritoneal macrophages. J. Immunol. Methods. 78:323-336.
35. Stuehr, D.J., and C.F. Nathan. 1989. Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells. J. Exp. Med. 169:1543-1555.
36. Taylor, T.W.J., E.W. Wignall, and J.F. Cowley. 1927. The decomposition of nitrous acid in aqueous solutions. J. Chem. Soc. (Lond.). 11:1923.
37. Morris, S.L., and J.N. Hansen. 1981. Inhibition of Bacillus cereus spore outgrowth by covalent modification of a sulfhydryl group by nitrosothiol and iodoacetate. J. Bacteriol. 148: 465-471.
38. Stamler, J.S. 1995. S-nitrosothiols and bioregulatory actions of nitrogen oxides through reactions with thiol groups. Curr. Topics Microbiol. Immunol. 196:19-36.
39. Stamler, J.S., D.J. Singel, and J. Loscalzo. 1992. Biochemistry of nitric oxide and its redox-activated forms. Science. 258: 1898-1902.
40. Dykhiuzen, R.S., R. Frazer, C. Duncan, C.C. Smith, M. Golden, N. Benjamin, and C. Leifert. 1996. Antimicrobial effect of acidified nitrite on gut pathogens: importance of dietary nitrate in host defense. Antimicrob. Agents Chemother. 40: 1422-1425.
41. Sturgill-Koszycki, S., P.H. Schlesinger, P. Chakraborty, P.L. Haddix, H.L. Collins, A.K. Fok, R.D. Allen, S.L. Gluck, J. Heuser, and D.G. Russell. 1994. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science. 263:678-681.
42. Burnett, W.V., J. Henner, and T. Eckhardt. 1987. The nucleotide sequence of the gene coding for XP55, a major secreted protein from Streptomyces lividans. Nucleic Acids Res. 15: 3926.
43. De Groote, M.A., D. Granger, Y. Xu, G. Campbell, R. Prince, and F.C. Fang. 1995. Genetic and redox determinants of nitric oxide cytotoxicity in a Salmonella typhimurium model. Proc. Natl. Acad. Sci. USA. 92:6399-6403.
44. De Groote, M.A., T. Testerman, Y. Xu, G. Stauffer, and F.C. Fang. 1996. Homocysteine antagonism of nitric oxide-related cytostasis in Salmonella typhimurium. Science. 272:414-417.
45. Lewis, R.S., S. Tamir, S.R. Tannenbaum, and W.M. Deen. 1995. Kinetic analysis of the fate of nitric oxide synthesized by macrophages in vitro. J. Biol. Chem. 270:29350-29355.
46. Ohkuma, S., and B. Poole. 1978. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc. Natl. Acad. Sci. USA. 75:3327-3331.
47. 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.
48. Nunoshiba, T., T. DeRojas-Walker, S.R. Tannenbaum, and B. Demple. 1995. Roles of nitric oxide in inducible resistance of Escherichia coli to activated macrophages. Infect. Immun. 63:794-798.
49. Nunoshiba, T., T. DeRojas-Walker, J.S. Wishnok, S.R. Tannenbaum, and B. Demple. 1993. Activation by nitric oxide of an oxidative-stress response that defends Escherichia coli against activated macrophages. Proc. Natl. Acad. Sci. USA 90: 9993-9997.
50. Dhandayuthapani, S., Y. Zhang, M.H. Mudd, and V. Deretic. 1996. Oxidative stress response and its role in sensitivity to isoniazid in mycobacteria: characterization and inducibility of ahpC by peroxides in Mycobacterium smegmatis and lack of expression in M. aurum and M. tuberculosis. J. Bacteriol 178: 3641-3649.
51. Zhang, Y., S. Dhandayuthapani, and V. Heretic. 1996. Molecular basis for the exquisite sensitivity of Mycobacterium tuberculosis to isoniazid. Proc. Natl. Acad. Sci. USA 93:13212-13216.
52. 4-treated cells. J. Reticuloendothel. Soc. 26:283-293.
53. Novogrodsky, A. 1974. Selective activation of mouse T and B lymphocytes by penodate, galactose oxidase and soybean agglutinin. Eur. J. Immunol. 4:646-648.
54. Nathan, C.F., and R.K. Root. 1977. Hydrogen peroxide release from mouse peritoneal macrophages: dependence on sequential activation and triggering. J. Exp. Med. 146:1648-1662.
55. Nathan, C.F., H.W. Murray, M.E. Wiebe, and B.Y. Rubin. 1983. Identification of interferon-γ as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med. 158:670-689.
56. Adams, L.B., S.G. Franzblau, Z. Vavrin, J.B.J. Hibbs, and J.L. Krahenbuhl. 1991. L-Arginine-dependent macrophage effector functions inhibit metabolic activity of Mycobacterium leprae. J. Immunol. 147:1642-1646.
57. Schwarz, M.A., J.S. Lazo, J.C. Yalowich, W.P. Allen, M. Whitemore, H.A. Bergonia, E. Tzeng, T.R. Billiar, P.D. Robbins, J.R.J. Lancaster, and B.R. Pitt. 1995. Metallothionein protects against the cytotoxic and DNA-damaging effects of nitric oxide. Proc. Natl. Acad. Sci. USA. 92:4452-4456.
58. Almiron, M., A.J. Link, D. Furlong, and R. Kolter. 1992. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 6:2646-2654.
59. Altuvia, S., M. Almiron, G. Huisman, R. Kolter, and G. Storz. 1994. The dps promoter is activated by OxyR during growth and by IHF and sigma S in stationary phase. Mol. Microbiol. 13:265-272.
60. Deretic, V., W. Philipp, S. Dhandayuthapani, M.H. Mudd, R. Curcic, T. Garbe, B. Heym, L.E. Via, and S.T. Cole. 1995. Mycobacterium tuberculosis is a natural mutant with an inactivated oxidative-stress regulatory gene: implications for sensitivity to isoniazid. Mol. Microbiol. 17:889-900.
61. Nikitovic, D., and A. Holmgren. 1996. S-nitrosogluthathione is cleaved by thioredoxin system with liberation of glutathione and redox regulating nitric oxide. J. Biol. Chem. 271:19180-19185.