The extreme sensitivity of mycobacterium tuberculosis to the front-line antituberculosis drug isoniazid

Nature Biotechnology

Volumn 14, Issue 11, 1996, Pages 1557-1561

  Deretic, V ^a   Pagán Ramos, Eileen ^a   Zhang, Yiqiang ^b   Dhandayuthapani, Subramanian ^b   Via, Laura E ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

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

Author keywords

INH sensitivity; Oxidative stress; Tuberculosis

Indexed keywords

ISONIAZID;

ANTIBIOTIC SENSITIVITY; BACTERIAL MUTATION; FRAMESHIFT MUTATION; GENE DELETION; MACROPHAGE FUNCTION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NONSENSE MUTATION; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; TUBERCULOSIS;

ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; BASE SEQUENCE; DNA-BINDING PROTEINS; ISONIAZID; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; MUTATION; MYCOBACTERIUM TUBERCULOSIS; OXIDOREDUCTASES; PEROXIDASES; PROMOTER REGIONS (GENETICS); REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; ENTERIC BACTERIA; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 0029959745     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt1196-1557     Document Type: Article

References (59)

1. Kochi, A. 1991. The global tuberculosis situation and the new control strategy of the World Health Organization. Tubercle 72:1-6.
2. Bloom, B.R. and Murray, C.J.L. 1994. Tuberculosis: commentary on a reemergent killer. Science 257:1055-1064.
3. Colston, M.J. and Davis, E.O. 1994. The ins and outs of protein splicing elements. Mol. Microbiol. 12:359-363.
4. Dannenberg, A.M.J, and Rook, G.A.W. 1994. Pathogenesis of pulmonary tuberculosis: an interplay of tissue-damaging and macraphage-activating immune responses—dual mechanisms that control bacillary multiplication, pp. 459-483 in Tuberculosis: Pathogenesis, protection and control. Bloom, B.R. (ed.). ASM Press, Washington, D.C.
5. Fenton, M.J. and Vermeulen, M.W. 1996. Immunopathology of tuberculosis: roles of macrophages and monocytes. Infect. Immun. 64:683-690.
6. Jacobs, W.R., Kalpana, G.V., Cirrilo, J.D., Pascopella, L, Snapper, S.B., Udani, R.A., Jones, W., Barletta, R.G., and Bloom, B.R. 1991. Genetic systems for mycobacteria. Methods Enzymol. 204:537-555.
7. Musser, J.M. 1995. Antimicrobial agent resistance in mycobacteria: molecular genetic insights. Clin. Microbiol. Rev. 8:496-514.
8. Russell, D.G. 1995. Mycobacterium and Leishmania: stowaways in the endosomal network. Trends Cell. Biol. 5:125-128.
9. Young, D.B. and Cole, ST. 1993. Leprosy, tuberculosis, and the new genetics. J. Bacteriol. 175:1-6.
10. Zhang, Y. and Young, D.B. 1993. Molecular mechanisms of isoniazid: a drug at the front line of tuberculosis control. Trends Microbiol. 1:109-113.
11. Deretic, V., Philipp, W., Dhandayuthapani, S., Mudd, M.H., Curcic, R., Garbe, T., et al. 1995. Myobacterium tuberculosis is a natural mutant with an inactivated oxidative-stress regulatory gene: implications for sensitivity to isoniazid. Mol. Microbiol. 17:889-900.
12. Dhandayuthapani, S., Via, L.E., Thomas, C.A., Horowitz, P.M., Deretic, D., Deretic, V. 1995. Green fluorescent protein as a marker for gene expression and cell biology of mycobacterial interactions with macrophages. Mol. Microbiol. 17:901-912.
13. Dhandayuthapani, S., Zhang, Y., Mudd, M.H. and Deretic, V. Oxidative stress response and its role in sensitivity to isonicotinic acid hydrazide in Mycobacterium species: characterization and inducibility of ahpC by peroxides in M. smegmatis and lack of expression in M. aurum and M. tuberculosis. J. Bacteriol. 178:12.
14. Sherman, D.R., Sabo, P.J., Hickey, M.J., Arain, T.M., Mahairas, G.G., Yuan, Y., et al. 1995. Disparate resposes to oxidative stress in a saprophytic and pathogenic mycobacteria. Proc. Natl. Acad. Sci. USA 92:6625-6629.
15. Winder, F.G. 1982. Mode of action of the animycobacteral agents and associated aspects of the molecular biology of the mycobacteriaa, pp. 354-438 in The Biology of the Mycobacteria. Ratledge, C. and Stanford, J.S. (eds.). Academic Press, London.
16. Banerjee, A., Dubnau, E., Quemard, A., Balasubramanian, V., Um, K.S., Wilson, T, et al. 1994. inha, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis. Science 263:227-230.
17. Dessen, A., Quemard, A., Blanchard, J.S., Jacobs, W.R., and Sacchettini, J.C. 1995. Crystal structure and function of the isoniazid target of Mycobacterium tuberculosis. Science 267:1638-1641.
18. Johnsson, K., King, D.S., and Schultz, P.G. 1995. Studies on the mechanism of action of isoniazid and ethionamide in the chemotherapy of tuberculosis. J. Am. Chem. Soc. 117:5009-5010
19. Youatt, J. 1969. A review of the action of isoniazid. Am. Rev. Respir. Dis. 99:729-749.
20. Gayathri-Devi, B., Shaila, M.S., Ramakrishnan, T, and Gopinathan, K.P. 1975. The purification and properties of peroxidase in Mycobacterium tuberculosis H37Rv and its possible role in the mechanism of action of isonicotinic acid hydrazide. Biochem. J. 148:187-197.
21. Bekierkunst, A. 1996. Nicotinamide-adenine dinucleotide exposed to isoniazad. Science 152:525-526.
22. Kasarov, L.B. and Moat, A.G. 1972. Metabolism of nicotinamide adenine dinucleotide in human and bovine strains of Mycobacterium tuberculosis. J. Bacteriol. 110:600-603.
23. Kruger-Thiemer, E. 1958. Isonicotinic acid hypothesis of the antituberculous action of isoniazid. Am. Rev. Tubero. 77:364-367.
24. Seydel, J., Schaper, K.-J., Wempe, E., and Cordes, H.P. 1976. Mode of action and quantitative structure-activity correlations of tuberculostatic drugs of the isonicotinic acid hydrazide type. J. Med. Chem. 19:483-492.
25. Herman, D.J. and Weber, M.M. 1980. Isonizaid interaction with tyrosine as a possible mode of action of the drug in mycobacteria. Antimicrob. Agents Chemother. 17:170-178.
26. Long, E.R. 1958. pp. 362-388 in The Chemistry and Chemotherapy of Tuberculosis. Balliere, Tindall & Cox, Ltd., London.
27. Quemard, A., Lacaveand, C, and Laneelle, G. 1991. Isoniazid inhibition of mycolic acid synthesis by cell extracts of sensitive and resistant strains of Mycobacterium aurum. Antibicrob. Agents Chemother. 35:1035-1039.
28. Winder, F.G. 1960. Catalase and peroxidase in Mycobacteria. Am. Rev. Respir. Dis. 81:68-78.
29. Shoeb, H.A., Bowman, B.U., Ottolenghi, A.C., and Merola, A.J. 1985. Enzymatic and nonenzymatic superoxide-generating reactions of isoniazid. Antimicrob. Agents Chemother. 27:408-412.
30. Shoeb, H.A., Bowman, B.U., Ottolenghi, A.C., and Merola, A.J. 1985. Evidence for the generation of active oxygen by isoniazid treatment of extracts of Mycobacterium tuberculosis H37Ra. Antimicrob. Agents Chemother. 27:404-407.
31. Shoeb, H.A., Bowman, B.U., Ottolenghi, A.C., and Merola, A.J. 1985. Peroxidase-mediated oxidation of isoniazid. Antimicrob. Agents Chemother. 27:399-403.
32. Zinner, K., Vidgal, C.C.C., Duran, N., and Cilento, G. 1977. Oxidation of isonicotininc acid hydrazide by the peroxidase system. Arch. Biochem. Biophys. 180:452-458.
33. Christman, M.F., Morgan, R.W., Jacobson, F.S., and Ames, B.N. 1985. Positive control of a regulation for defences against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41:753-762.
34. Christman, M.F., Storz, G., and Ames, B.N. 1989. OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium is homologous to a family of bacterial regulatory proteins. Proc. Natl. Acad. Sci. USA 86:3484-3488.
35. Toledano, M.B., Kulllk, I., Trinh, F., Baird, P.T., Schneider, T.D. and Storz, G. 1994. Redox-dependent shift of OxyR-DNA contacts along an extended DNA-binding site: a mechanism for differential promoter selection. Cell 78:897-909.
36. Farr, S.B. and Kogoma, T. 1991. Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol. Rev. 55:561-585.
37. Middlebrook, G. and Cohn, M.L. 1953. Some observations on the pathogenicity of isoniazid-resistant variants of tubercle bacilli. Science 118:297-299.
38. Middlebrook, G. 1954. Isoniazid-resistance and catalase activity of tubercle bacilli. Am. Rev. Tubero. 69:471-472.
39. Zhang, Y, Heym, B., Allen, B., Young, D., and Cole, S.T. 1992. The catelase-peroxidase gene and isoniazid resistance of Mycobacterium tuberculosis. Nature 358:591-593.
40. Heym, B., Alzari, P.M., Honore, N., and Cole, S.T. 1995. Missense mutations in the catalase-peroxidase gene, katG, are associated with isoniazid resistance in Mycobacterium tuberculosis. Mol. Microbiol. 15:235-245.
41. Cockerill, F.R., UN, J.R., Temesgen, Z., Zhang, Y, Stockman, L, Roberts, G.D., et al. 1995. Rapid identif cation of a point mutation of the Mycobacterium tuberculosis cataJase-per-oxidase associated with isoniazid resistance. J. Infect Dis. 171:240-245.
42. Rouse, DA and Morris, S.L 1995. Molecular mechanisms of isoniazid resistance in Mycobacterium tuberculosis and Mycobacterium bovis. Infect Immun. 63:1427-1433.
43. Pretorius, G.S., Helden, P.D., Sirgel, F., Eisenach, K.D., and victor, T.C. 1995. Mutations in katG gene sequences in isoniazid-resistant clinical isolates of Mycobacterium tuberculosis are rare. Antimicrob. Agents Chemother 39:2276-2281.
44. Rouse, D.A., Li, Z., Bai, G.-H., and Morris, S.L. 1995. Characterization of the katG and inhA genes of isoniazid-resistant clinical isolates of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 39:2472-2477.
45. Bergh, S. and Cole, S.T. 1994. MycDB: an integrated mycobacterial database. Mol. Microbiol. 12:534-574.
46. Zhang, Y., Garbe, T., and Young, D. 1993. Transformation with katG restores isoniazid-sensitivity in Mycobacterium tuberculosis isolates resistant to a range of drug concentrations. Mol. Microbiol. 8:521-524.
47. Milano, A., De Rossi, E., Gusberti, L., Heym, B., Marone, P., and Riccardi, G. 1996. The katE gene, which encodes the catalase HPII of Mycobacterium avium. Mol. Microbiol. 19:113-123.
48. Rosner, J.L. 1993. Susceptibilities of oxyR regulon mutants of Escherichia coli and Salmonella typhimurium to isoniazid. Antimicrob. Agents Chemother. 37:2251-2253.
49. Yamaguchi, R., Mutsuo, K., Yamazaki, A., Takahashi, M., Fukusawa, Y, Wada, M., and Abe, C. 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.
50. Schell, M.A. 1993. Molecular biology of the LysR family of transcriptional regulators. Annu. Rev. Microbiol. 47:597-626.
51. Jacobson, F.S., Morgan, R.W., Christman, M.F., and Ames, B.N. 1989. An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defense of DNA against oxidative damage. J. Biol. Chem. 264:1488-1496.
52. Storz, G.S., Christman, M.F., Sies, H., and Ames, B.N. 1987. Spontanous mutagenesis and oxidative damage to DNA in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 84:8917-8921.
53. Chae, H.Z., Robinson, K., Poole, L.B., Church, G., Storz, G. and Rhee, S.G. 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).
54. Zhang, Y, Dhandayuthapani, S., and Deretic, V. 1996. Molecular basis for the exquisite sensitivity of Mycobacterium tuberculosis to isoniazid. Proc. Natl. Acad. Sci. USA. In press.
55. Le Lirzin, M.J.N., Vivien, J.N., Lepeuple, A., Thibier, R., and Pretet, C. 1971. Rapid microbiological estimation of serum isoniazid. Rev. Tubero. Pneumol. 35:350-356.
56. Heym, B. and Cole, S.T. 1992. Isolation and characterization of isoniazid-resistant mutants of Mycobacterium smegmatis and M. aurum. Res. Microbiol. 143:721-730.
57. Wilson, T.M. and Collins, D.M. 1996. aphC, a gene involved in isoniazid resistance of the Mycobacterium tuberculosis complex. Mol. Microbiol. 19:1025-1034.
58. Sherman, D.R., Mdluli, K., Hickey, M.J., Arain, T.M., Morris, S.L., Barry, C.E., and Stover, OK. 1996. Compensatory ahpC gene expression in isoniazid-resistant Mycobacterium tuberculosis. Science 272:1641-1643.
59. Sreevantsan, S., Zhang, Y, Deretic, V, and Musser, J.M. Analysis of the охуR-ahpC region in isoniazid-resistant and susceptible Mycobacterium tuberculosis complex organisms recovered from diseased humans and animals in diverse localities. Submitted.