NADH dehydrogenase defects confer isoniazid resistance and conditional- lethality in Mycobacterium smegmatis

Journal of Bacteriology

Volumn 180, Issue 9, 1998, Pages 2459-2467

  Miesel, Lynn ^a   Weisbrod, Torin R ^a   Marcinkeviciene, Jovita A ^a   Bittman, Robert ^b   Jacobs Jr , William R ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISONIAZID; NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL MUTATION; BACTERIAL VIRULENCE; DNA SEQUENCE; ENZYME ACTIVITY; ENZYME CONFORMATION; MOLECULAR CLONING; MYCOBACTERIUM SMEGMATIS; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 0031980127     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.180.9.2459-2467.1998     Document Type: Article

References (57)

1. Ad Hoc Committee of the Scientific Assembly on Microbiology, Tuberculosis, and Pulmonary Infections. 1995. Treatment of tuberculosis and tuberculosis infection in adults and children. Clin. Infect. Dis. 21:9-27.
2. 1a. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Balasubramanian, V., M. S. Pavelka, Jr., S. S. Bardarov, J. Martin, T. R. Weisbrod, R. A. McAdam, B. R. Bloom, and W. R. Jacobs, Jr. 1996. Allelic exchange in Mycobacterium tuberculosis with long linear recombination substrates. J. Bacteriol. 178:273-279.
4. Banerjee, A., E. Dubnau, A. Quémard, 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. Sience 263:227-230.
5. Bardorov, S. Unpublished data.
6. Basso, L. A., R. Zheng, and J. S. Blanchard. 1996. Kinetics of inactivation of WT and C243S mutant of Mycobacterium tuberculosis enoyl reductase by activated isoniazid. J. Am. Chem. Soc. 118:11301-11302.
7. Bergh, S., and S. T. Cole. 1994. MycDB: an integrated mycobacterial database. Mol. Microbiol. 12:517-534.
8. Bongaerts, J., S. Zoske, U. Weidner, and G. Unden. 1995. Transcriptional regulation of the proton translocating NADH dehydrogenase genes (nuoA-nuoN) of Escherichia coli by electron acceptors, electron donors and gene regulators. Mol. Microbiol. 16:521-534.
9. Calhoun, M. W., and R. B. Gennis. 1993. Demonstration of separate genetic loci encoding distinct membrane-bound respiratory NADH dehydrogenases in Escherichia coli. J. Bacteriol. 175:3013-3019.
10. Cirillo, J. D., T. R. Weisbrod, and W. R. Jacobs, Jr. 1993. Efficient electrotransformation of Mycobacterium smegmatis. Technical bulletin no. 1360, Bio-Rad Laboratories, Richmond, Calif.
11. Cohn, D. L., F. Bustreo, and M. C. Raviglione. 1997. Drug-resistant tuberculosis: review of the worldwide situation and the WHO/IUATLD global surveillance project. Clin. Infect. Dis. 24(Suppl. 1):S121-S130.
12. Davis, W. B., and M. M. Weber. 1977. Specificity of isoniazid on growth inhibition and competition for an oxidized nicotinamide adenine dinucleotide regulatory site on the electron transport pathway in Mycobacterium phlei. Antimicrob. Agents Chemother. 12:213-218.
13. Gennis, R. B., and V. Stewart. 1996. Respiration, p. 217-261. In F. C. Niedhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, D.C.
14. Gillespie, J., L. L. Barton, and E. W. Rypka. 1988. Influence of oxygen tension on the respiratory activity of Mycobacterium phlei. J. Gen. Microbiol. 134:247-252.
15. Gonzalez, B. F., and B. Demple. 1995. Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J. Biol. Chem. 270:13681-13687.
16. Heym, B., N. Honoré, C. Truffot-Pernot, A. Banerjee, C. Schurra, W. R. Jacobs, Jr., J. D. A. van Embden, J. H. Grosset, and S. T. Cole. 1994. Implications of multidrug resistance for the future of short-course chemotherapy of tuberculosis: a molecular study. Lancet 344:293-298.
17. Heym, B., E. Stavropoulos, N. Honoré, P. Domenech, B. Saint-Joanis, T. M. Wilson, D. M. Collins, M. J. Colston, and S. T. Cole. 1997. Effects of overexpression of the alkyl hydroperoxide reductase AhpC on the virulence and isoniazid resistance of Mycobacterium tuberculosis. Infect. Immun. 65: 1395-1401.
18. Jacobs, W. R., Jr., G. V. Kalpana, J. D. Cirillo, L. Pascopella, R. A. Udani, W. D. Jones, Jr., R. Barletta, and B. R. Bloom. 1991. Genetic systems for the mycobacteria. Methods Enzymol. 204:537-555.
19. Johnsson, K., and P. G. Schultz. 1994. Mechanistic studies of the oxidation of isoniazid by the catalase peroxidase from Mycobacterium tuberculosis. J. Am. Chem. Soc. 116:7425-7426.
20. Johnsson, K., D. S. King, and P. G. Shultz. 1995. Studies on the mechanism of action of isoniazid and ethionamide in the chemotherapy of tuberculosis. J. Am. Chem. Soc. 117:5009-5010.
21. Magliozzo, R. S., and J. A. Marcinkeviciene. 1996. Evidence for isoniazid oxidation by oxyferrous mycobacterial catalase-peroxidase. J. Am. Chem. Soc. 118:11303-11304.
22. Marcinkeviciene, J. A., R. S. Magliozzo, and J. S. Blanchard. 1995. Purification and characterization of the Mycobacterium smegmatis catalase-peroxidase involved in isoniazid activation. J. Biol. Chem. 270:22290-22295.
23. Matsushita, K., T. Ohnishi, and H. R. Kaback. 1987. NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain. Biochemistry 26:7732-7737.
24. McKie, J. H., and K. T. Douglas. 1991. Evidence for gene duplication forming similar binding folds for NAD(P)H and FAD in pyridine nucleotide-dependent flavoenzymes. FEBS Lett. 279:5-8.
25. Mdluli, K., D. Sherman, M. J. Hickey, B. N. Kreiswirth, S. Morris, C. K. Stover, and C. E. Barry III. 1996. Biochemical and genetic data suggest that InhA is not a primary target for activated isoniazid in Mycobacterium tuberculosis. J. Infect. Dis. 174:1085-1090.
26. Middlebrook, G. 1952. Sterilization of tubercle bacilli by isonicotinic acid hydrazide and the incidence of variants resistant to the drug in vitro. Am. Rev. Tuberc. 65:765-767.
27. Middlebrook, G., and M. L. Cohn. 1953. Some observations on the pathgenicity of isoniazid-resistant variants of tubercle bacilli. Science 118:297-299.
28. Middlebrook, G. 1954. Isoniazid resistance and catalase activity of tubercle bacilli. Am. Rev. Tuberc. 69:471-472.
29. Miller, J. H. 1992. A short course in bacterial genetics. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
30. Morris, S., G. H. Bai, P. Suffys, L. Portillo-Gomez, M. Fairchok, and D. Rouse. 1995. Molecular mechanisms of multiple drug resistance in clinical isolates of Mycobacterium tuberculosis. J. Infect. Dis. 171:954-960.
31. Musser, J. Unpublished data.
32. Musser, J. M., V. Kapur, D. L. Williams, B. N. Kreiswirth, D. van Soolingen, and J. D. A. van Embden. 1996. Characterization of the catalase-peroxidase gene (katG) and inhA locus in isoniazid-resistant and -susceptible strains of Mycobacterium tuberculosis by automated DNA sequencing: restricted array of mutations associated with drug resistance. J. Infect. Dis. 173:196-202.
33. Nicholls, D. J., T. K. Sundaram, T. Atkinson, and N. P. Minton. 1990. Cloning and nucleotide sequences of the mdh and sucD genes from Thermus aquaticus B. FEMS Microbiol. Lett. 70:7-14.
34. Pavelka, M. S., Jr., and W. R. Jacobs, Jr. 1996. Biosynthesis of diaminopimelate, the precursor of lysine and a component of peptidoglycan, is an essential function of Mycobacterium smegmatis. J. Bacteriol. 178:6496-6507.
35. Poole, L. B., and H. R. Ellis. 1996. Flavin-dependent alkyl hydroperoxide reductase from Salmonella typhimurium. 1. Purification and enzymatic activities of overexpressed AhpF and AhpC proteins. Biochemistry 35:56-64.
36. Prasada Reddy, T. L., R. S. Murthy, and T. A. Venkitasubramanian. 1975. Variations in the pathways of malate oxidation and phosphorylation in different species of mycobacteria. Biochim. Biophys. Acta 376:210-218.
37. Quémard, A., J. C. Sacchettini, A Dessen, C. Vilcheze, R. Bittman, W. R. Jacobs, Jr., and J. S. Blanchard. 1995. Enzymatic characterization of the target for isoniazid in Mycobacterium tuberculosis. Biochemistry 34:8235-8241.
38. Robitzek, E. H., and I. J. Selikoff. 1952. Hydrazine derivative of isonicotinic acid (rimifon, marsilid) in the treatment of active progressive caseous-pneumonic tuberculosis. Am. Rev. Tuberc. 65:402-428.
39. Rosner, J. L., and G. Storz. 1994. Effects of peroxides on susceptibilities of Escherichia coli and Mycobacterium smegmatis to isoniazid. Antimicrob. Agents Chemother. 38:1829-1833.
40. Rozwarski, D. A., G. A. Grant, D. H. R. Barton, W. R. Jacobs, Jr., and J. C. Sacchettini. 1998. Modification of the NADH of the isoniazid target (InhA) from Mycobacterium tuberculosis. Science 279:98-102.
41. 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.
42. Shoeb, H. A., B. U. Bowman, Jr., A. C. Ottolenghi, and A. J. Merola. 1985. Peroxidase-mediated oxidation of isoniazid. Antimicrob. Agents Chemother. 27:399-403.
43. 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.
44. Spiro, S., R. E. Roberts, and J. R. Guest. 1989. FNR-dependent repression of the ndh gene of Escherichia coli and metal ion requirement for FNR-regulated gene expression. Mol. Microbiol. 3:601-608.
45. Stover, C. K., V. F. de la Cruz, T. R. Fuerst, J. E. Burlein, L. A. L. T. Bennett, G. P. Bansal, J. F. Young, M. H. Lee, G. F. Hatfull, S. B. Snapper, R. G. Barletta, W. R. Jacobs, Jr., and B. R. Bloom. 1991. New use of BCG for recombinant vaccines. Nature 351:456-460.
46. Sugimoto, E., and L. I. Pizer. 1968. The mechanism of end product inhibition of serine biosynthesis. J. Biol. Chem. 243:2081-2089.
47. Szybalski, W., and V. Bryson. 1952. Bacterial resistance studies with derivatives of isonicotinic acid. Am. Rev. Tuberc. 65:768-770.
48. Takayama, K., L. Wang, and H. L. David. 1972. Effect of isoniazid on the in vivo mycolic acid synthesis, cell growth, and viability of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 2:29-35.
49. Takayama, K., H. K. Schnoes, E. L. Armstrong, and R. W. Boyle. 1975. Site of inhibitory action of isoniazid in the synthesis of mycolic acids in Mycobacterium tuberculosis. J. Lipid Res. 16:308-317.
50. Telenti, A., N. Honoré, C. Bernasconi, J. March, A. Ortega, B. Heym, H. E. Takiff, and S. T. Cole. 1997. Genotypic assessment of isoniazid and rifampin resistance in Mycobacterium tuberculosis: a blind study at reference laboratory level. J. Clin. Microbiol. 35:719-723.
51. Wilson, T. M., and D. M. Collins. 1996. ahpC, a gene involved in isoniazid resistance of the Mycobacterium tuberculosis complex. Mol. Microbiol. 19: 1025-1034.
52. Winder, F. 1960. Catalase and peroxidase in mycobacteria. Am. Rev. Respir. Dis. 81:68-78.
53. Winder, F. G. 1982. Mode of action of the antimycobacterial agents and associated aspects of the molecular biology of the mycobacteria, p. 353-438. In C. Ratledge and J. Stanford (ed.), The biology of the mycobacteria. Academic Press, New York, N.Y.
54. Young, I. G., and B. J. Wallace. 1976. Mutations affecting the reduced nicotinamide adenine dinucleotide dehydrogenase complex of Escherichia coli. Biochim. Biophys. Acta 449:376-385.
55. Young, I. G., A. Jaworowski, and M. I. Poulis. 1978. Amplification of the respiratory NADH dehydrogenase of Escherichia coli by gene cloning. Gene 4:25-36.
56. Zhang, Y., B. Heym, B. Allen, D. Young, and S. Cole. 1992. The catalase-peroxidase gene and isoniazid resistance of Mycobacterium tuberculosis. Nature 358:591-593.
57. Zhang, Y., S. Dhandayuthapani, and V. Deretic. 1996. Molecular basis for the exquisite sensitivity of Mycobacterium tuberculosis to isoniazid. Proc. Natl. Acad. Sci. USA 93:13212-13216.