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

Journal of Bacteriology

Volumn 178, Issue 12, 1996, Pages 3641-3649

  Dhandayuthapani, S ^a   Zhang, Y ^a   Mudd, M H ^a   Deretic, V ^a,b  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORYNEBACTERINEAE; MYCOBACTERIUM AURUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

HYDROGEN PEROXIDE; HYDROPEROXIDE; ISONIAZID; NUCLEASE S1; OXIDOREDUCTASE; PEROXIDE;

ARTICLE; DRUG SENSITIVITY; IMMUNOBLOTTING; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATIVE STRESS; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; REGULATOR GENE;

AMINO ACID SEQUENCE; BASE SEQUENCE; DRUG RESISTANCE, MICROBIAL; ENZYME INDUCTION; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, BACTERIAL; ISONIAZID; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS; OXIDATION-REDUCTION; OXIDOREDUCTASES; PEROXIDASES; PEROXIDES; PLASMIDS; PROMOTER REGIONS (GENETICS); RNA, MESSENGER;

EID: 0029888258     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.178.12.3641-3649.1996     Document Type: Article

References (43)

1. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1989. Current protocols in molecular biology. John Wiley & Sons, New York.
2. Banerjee, A., E. Dubnau, A. Quemard, V. Balasubramanian, K. S. Um, T. Wilson, D. Collins, G. de Lisle, and W. R. Jacobs, Jr. 1994. inhA, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis. Science 263:227-230.
3. Chae, H. Z., K. Robison, L. B. Poole, G. Church, G. Storz, and S. G. Rhee. 1994. Cloning and sequencing of thiol-specific antioxidant from mammalian brain: alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc. Natl. Acad. Sci. USA 91:7017-7021.
4. Christman, M. F., R. W. Morgan, F. S. Jacobson, and B. N. Ames. 1985. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41:753-762.
5. Curcic, R., S. Dhandayuthapani, and V. Deretic. 1994. Gene expression in mycobacteria: transcriptional fusions based on xylE and analysis of the promoter region of the response regulator mtrA from Mvcobacterium tuberculosis. Mol. Microbiol. 13:1057-1064.
6. Dannenberg, A, M., Jr., and G. A. W. Rook. 1994. Pathogenesis of pulmonary tuberculosis: an interplay of tissue-damaging and macrophage-activating immune responses - dual mechanisms that control bacillary multiplication, p. 459-483. In B. R. Bloom (ed.). Tuberculosis: pathogenesis, protection, and control. ASM Press, Washington, D.C.
7. Deretic, V., N. S. Hibler, and S. C. Holt. 1992. Immunochemical analysis of AlgP(Hpl), a histonelike element participating in control of mucoidy in Pseudomonas aeruginosa. J. Bacteriol. 174:824-831.
8. 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.
9. Dhandayuthapani, S. L. E. Via, C. A. Thomas, P. M. Horowitz, D. Deretic, and V. Deretic. 1995. Green fluorescent protein as a marker for gene expression and cell biology of mycobacterial with macrophages. Mol. Microbiol. 17:901-912.
10. Farr, S. B., and T. Kogoma. 1991. Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol. Rev. 55:561-585.
11. Ferrante, A. A., J. Augliera, K. Lewis, and A. M. Klibanov. 1995. Cloning of an organic solvent-resistance gene in Escherichia coli: the unexpected role of alkylhydroperoxide reductase. Proc. Natl. Acad. Sci. USA 92:7617-7621.
12. Garbe, T., N. S. Hibler, and V. Deretic. 1996. Response of Mycobacterium tuberculosis to reactive oxygen and nitrogen intermediates. Mol. Med. 2:134-142.
13. Heym, B., P. M. Alzari, N. Honore, and S. T. Cole. 1995. Missense mutations in the catalase-peroxidase gene, katG, are associated with isoniazid resistance in Mycobacterium tuberculosis. Mol. Microbiol. 15:235-245.
14. Heym, B., and S. T. Cole. 1992. Isolation and characterization of isoniazid-resistant mutants of Mycobacterium smegmatis and M. aurum. Res. Microbiol. 143:721-730.
15. Jacobs, W. R., Jr., G. V. Kalpana, J. D. Cirrilo, L. Pascopella, S. B. Snapper, R. A. Udani, W. Jones, R. G. Barletta, and B. R. Bloom. 1991. Genetic systems for mycobacteria. Methods Enzymol. 204:537-555.
16. Jacobson, F. S., R. W. Morgan, M. F. Christman, and B. N. Ames. 1989. An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defense of DNA against oxidative damage. J. Biol. Chem. 264:1488-1496.
17. Kruger-Thiemer, E. 1958. Isonicotinic acid hypothesis of the antituberculous action of isoniazid. Am. Rev. Tuberc. 78:364-367.
18. 17a.Lacave, C. Personal communication.
19. Lirzin, M. L., J. N. Vivien, A. Lepeuple, R. Thibier, and C. Pretet. 1971. Rapid microbiological estimation of serum isoniazid. Rev. Tuberc. Pneumol. 35:350-356.
20. Loewen, P. C., B. L. Trigs, C. S. Geroge, and B. Hrabarchuk. 1185. Genetic mapping of karG, a locus that affects synthesis of the bifunctional catalascperoxidase hydroperoxidase I in Escherichia coli. J. Bacteriol. 162:661-667.
21. Middlebrook, G. 1954. Isoniazid-resistance and catalase activity of tubercle bacilli. Am. Rev. Tuberc. 69:471-472.
22. Mudd, M., Y. Zhang, S. Dhandayuthapani, and V. Deretic. Unpublished results.
23. Musser, J. M. 1995. Antimicrobial agent resistance in mycobacteria: molecular genetic insights. Clin. Microbiol. Rev. 8:496-514.
24. Rosner, J. L. 1993. Susceptibilities of oxyR regulon mutants of Escherichia coli and Salmonella typhimurium to isoniazid. Antimicrob. Agents Chemother. 37:2251-2253.
25. Rosner, J. L., and G. Storz. 1994. Effects of peroxides on susceptibilities of Escherichia coli and Mycobacterium smegmatis to isoniazid. Antimicrob. Agents Chemothcr. 38:1829-1833.
26. Rouse, D. A., and S. L. Morris. 1995. Molecular mechanisms of isoniazid resistance in Mycobacterium tuberculosis and Mycobacterium bovis. Infect. Immun. 63:1427-1433.
27. Schell, M. A. 1993. Molecular biology of the LysR family of transcriptional regulators. Annu. Rev. Microbiol. 47:597-626.
28. E) which controls mucoidy in cystic fibrosis isolates of Pseudomonas aeruginosa. J. Bacteriol. 177:5670-5679.
29. Sherman, D. R., P. J. Sabo, M. J. Hickey, T. M. Arain, G. G. Maharias, 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.
30. Shoeb, H. A., B. U. Bowman, Jr., A. C. Ottolenghi, and A. J. Merola. 1985. Evidence for the generation of active oxygen by isoniazid treatment of extracts of Mycobacterium tuberculosis H37Ra. Antimicrob. Agents Chemother. 27:404-407.
31. Snapper, S. B., R. E. Melton, S. Mustafa, T. Kieser, and W. R. Jacobs. 1990. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol. Microbiol. 4:1911-1919.
32. Storz, G., M. F. Christman, H. Sies, and B. N. Ames. 1987. Spontaneous mutagenesis and oxidative damage to DNA in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 84:8917-8921.
33. Storz, G., F. J. Jacobson, L. A. Tartaglia, R. W. Morgan, L. A. Silveira, and B. N. Ames. 1989. An alkyl hydroperoxide reductase induced by oxidative stress in Salmonella typhimurium and Escherichia coli: genetic characterization and cloning of ahp. J. Bacteriol. 171:2049-2055.
34. Tai, S. S., and Y. Y. Zhu. 1995. Cloning of a Corynebacterium diphtheriae iron-repressible gene that shares sequence homology with the AhpC subunit of alkyl hydroperoxide reductase of Salmonella typhimurium. J. Baeteriol. 177:3512-3517.
35. Tartaglia, L. A., G. Storz, M. H. Brodsky, A. Lai, and B. N. Ames. 1990. Alkyl hydroperoxide reductase from Salmonella typhimrium. Sequence and homology to thioredoxin reductase and other flavoprotein disulfide oxidoreductases. J. Biol. Chem. 265:10535-10540.
36. Toledano, M. B., I. Kullik, F. Trinh, P. T. Baird, T. D. Schneider, and G. Storz. 1994. Redox-dependent shift of OxyR-DNA contacts along an extended DNA-binding site: a mechanism for differential promoter selection. Cell 78:897-909.
37. Winder, F. 1959. Catalase and peroxidase in mycobacteria. Am. Rev. Respir. Dis. 81:68-78.
38. Winder, F. G. 1982. Mode of action of the antimycobacteral agents and associated aspects of the molecular biology of The mycobactcria, p. 351-438. In C. Ratledge and J. L. Stanford (ed.), The biology of the mycobacteria, vol. I. Academic Press, London.
39. Yamaguchi, R., K. Matsuo, A. Yamazaki, M. Takahashi, Y. Fukusawa, M. Wada, and C. Abe. 1992. Cloning and expression of the gene for the Avi-3 antigen of Mycobacterium avium and mapping of its epitopes. Infect. Immun. 60:1210-1216.
40. Youatt, J. 1969. A review of the action of isoniazid. Am. Rev. Respir. Dis. 99:729-749.
41. Zhang, Y., S. Dhandayuthapani, and V. Deretic. Unpublished results.
42. Zhang, Y., B. Heym, B. Allen, D. Young, and S. Cole. 1992. The catalaseperoxidase gene and isoniazid resistance of Mycobacterium tuberculosis. Nature (London) 358:591-593.
43. Zhang, Y., and D. B. Young. 1993. Molecular mechanisms of isoniazid: a drug at the front line of tuberculosis control. Trends Microbiol. 1:109-113.