Antisense RNA to ahpC, an oxidative stress defence gene involved in isoniazid resistance, indicates that AhpC of Mycobacterium bovis has virulence properties

Microbiology

Volumn 144, Issue 10, 1998, Pages 2687-2695

  Wilson, Theresa ^a   De Lisle, Geoffrey W ^a   Marcinkeviciene, Jovita A ^b   Blanchard, John S ^b   Collins, Desmond M ^a  

^a AGRESEARCH   (New Zealand)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

AhpC; Antisense RNA; Mycobacterium tuberculosis complex; Oxidative stress; Virulence

Indexed keywords

COMPLEMENTARY RNA; CUMENE HYDROPEROXIDE; ISONIAZID; TUBERCULOSTATIC AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; IMMUNOBLOTTING; MYCOBACTERIUM BOVIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SYNTHESIS;

ANIMALIA; BACTERIA (MICROORGANISMS); CAVIA; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; POSIBACTERIA;

EID: 0031733825     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/00221287-144-10-2687     Document Type: Article

References (37)

1. Banerjee, A., Dubnau, E., Quemard, A., Balasubramanian, V., Sun Um, K., Wilson, T., Collins, D., de Lisle, G. & Jacobs, W. R. (1994). inhA, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis. Science 263, 227-230.
2. Basso, L. A., Zheng, R. & Blanchard, J. S. (1996). Kinetics of inactivation of WT and C243S mutant of Mycobacterium tuberculosis enoyl reductase by activated isoniazid. J Am Chem Soc 118, 11301-11302.
3. Christman, M. F., Morgan, R. W., Jacobson, F. S. & Ames, B. N. (1985). Positive control of a regulon for defences against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41, 753-762.
4. Collins, D. M., Kawakami, R. P., de Lisle, G. W., Pascopella, L., Bloom, B. R. & Jacobs, W. R. (1995). Mutation of the principal sigma factor causes loss of virulence in a strain of the Mycobacterium tuberculosis complex. Proc Natl Acad Sci USA 92, 8036-8040.
5. Deretic, V., Phillip, W., Dhandayuthapani, S., Mudd, M. H., Curcic, R., Garbe, T., Heym, B., Via, L. E. & Cole, S. T. (1995). Mycobacterium tuberculosis is a natural mutant with an inactivated oxidative-stress regulatory gene: implications for sensitivity to isoniazid. Mol Microbiol 17, 889-900.
6. Dessen, A., Quemard, A., Blanchard, J. S., Jacobs, W. R. & Sacchettini, J. C. (1995). Crystal structure and function of the isoniazid target of Mycobacterium tuberculosis. Science 267, 1638-1641.
7. Dhandayuthapani, S., Zhang, Y., Mudd, M. H. & Deretic, V. (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.
8. Heym, B., Alzara, P., Honore, N. & 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.
9. Heym, B., Stavropoulos, E., Honore, N., Domenechi, P., Saint-Joanis, B., Wilson, T., Collins, D. M., Colston, M. J. & Cole, S. T. (1997). Effects of overexpression of the alkyl hydroperoxide reductase AhpC on the virulence and isoniazid resistance of Mycobacterium tuberculosis. Infect Immun 65, 1395-1401.
10. Johnsson, K. & Schultz, P. G. (1994). Mechanistic studies of the oxidation of isoniazid by the catalase peroxidase from Mycobacterium tuberculosis. J Am Chem Soc 116, 7425-7426.
11. Kapur, V., Li, L. L, Hamrick, M. R. & 10 other authors (1995). Rapid Mycobacterium species assignment and unambiguous identification of mutations associated with antimicrobial resistance in Mycobacterium tuberculosis by automated DNA sequencing. Arch Pathol Lab Med 119, 131-138.
12. Kent, P. T. & Kubica, G. P. (1985). Public Health Mycobacteriology, A Guide for the Level III Laboratory. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control.
13. Kernodle, D. S., Voladri, R. K. R., Menzies, B. E., Hager, C. C. & Edwards, K. M. (1997). Expression of an antisense hla fragment in Staphylococcus aureus reduces alpha-toxin production in vitro and attenuates lethal activity in a murine model. Infect Immun 65, 179-184.
14. Mdluli, K., Sherman, D. R., Hickey, M. J., Kreiswirth, B. N., Morris, S., Stover, C. K. & Barry, C. E. (1996). Biochemical and genetic data suggest that InhA is not the primary target for activated isoniazid in Mycobacterium tuberculosis. J Infect Dis 174, 1085-1090.
15. Middlebrook, G. (1954). Isoniazid resistance and catalase activity of tubercle bacilli. Am Rev Tuberc 69, 471-472.
16. Musser, J. M., Kapur, V., Williams, D. L, Kreiswirth, B. N., van Soolingen, D. & van Embden, J. D. A. (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.
17. Parish, T. & Stoker, N. G. (1997). Development and use of a conditional antisense mutagenesis system in mycobacteria. FEMS Microbiol Lett 154, 151-157.
18. Pascopella, L, Collins, F. M., Martin, J. M., Lee, M. H., Hatfull, G. F., Stover, C. K., Bloom, B. R. & Jacobs, W. R. (1994). Use of in vivo complementation in Mycobacterium tuberculosis to identify a genomic fragment associated with virulence. Infect Immun 62, 1313-1319.
19. Quemard, A., Sacchettini, J. C., Dessen, A., Vilcheze, C., Bittman, R., Jacobs, W. R. & Blanchard, J. S. (1995). Enzymatic characterization of the target for isoniazid in Mycobacterium tuberculosis. Biochemistry 34, 8235-8241.
20. Quemard, A., Dessen, A., Sugantino, M., Jacobs, W. R., Sacchettini, J. C. & Blanchard, J. S. (1996). Binding of catalaseperoxidase-activated isoniazid to wild-type and mutant Mycobacterium tuberculosis enoyl-ACP reductases. J Am Chem Soc 118, 1561-1562.
21. Rapaport, E., Levina, A., Metelev, V. & Zamecnik, P. C. (1996). Antimycobacterial activities of antisense oligodeoxynucleotide. phosphorothioates in drug-resistant strains. Proc Natl Acad Sci USA 93, 709-713.
22. Reyrat, J., Berthet, F. & Gicquel, B. (1995). The urease locus of Mycobacterium tuberculosis and its utilization for the demonstration of allelic exchange in Mycobacterium bovis bacillus Calmette-Guerin. Proc Natl Acad Sci USA 92, 8768-8772.
23. Rouse, D. A., Li, Z., Bai, G. & 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.
24. Sherman, D. R., Sabo, P. J., Hickey, M. J., Arain, T. M., Mahairas, G. G., Yuan, Y., Barry, C. E., III & Stover, C. K. (1995). Disparate responses to oxidative stress in saprophytic and pathogenic mycobacteria. Proc Natl Acad Sci USA 92, 6625-6629.
25. Sherman, D. R., Mdluli, K., Hickey, M. J., Arain, T. M., Morris, S. L. & Barry, C. E. (1996). Compensatory ahpC gene expression in isoniazid-resistant Mycobacterium tuberculosis. Science 272, 1641-1643.
26. van Soolingen, D., Hermans, P. W. M., de Haas, P. E. W., Soll, D. R. & van Embden, J. D. A. (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.
27. Sreevatsan, S., Pan, X., Zhang, Y., Deretic, V. & Musser, J. M. (1997). Analysis of the oxyR-ahpC region in isoniazid-resistant and -susceptible Mycobacterium tuberculosis complex organisms recovered from diseased humans and animals in diverse localities. Antimicrob Agents Chemother 41, 600-606.
28. Steenken, W. & Wolinsky, E. (1955). Studies on the pathogenicity of several INH-resistant cultures in mice, guinea pigs and rabbits. In Transactions of the 14th Veterans Administration Conference on the Chemotherapy of Tuberculosis, pp. 210-217. Washington, DC: US Veterans Administration.
29. Storz, G., Jacobson, F. S., Tartaglia, L. A., Morgan, R. W., Silveira, L A. & Ames, B. N. (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.
30. Telenti, A., Honore, N., Bernasconi, C., March, J., Ortega, A., Heym, B., Takiff, H. E. & Cole, S. T. (1997). Genotype assessment of isoniazid and rifampin resistance in Mycobacterium tuberculosis: a blind study at reference laboratory level. J Clin Microbiol 35, 719-723.
31. Wagner, E. G. H. & Simons, R. W. (1994). Antisense RNA control in bacteria, phages and plasmids. Annu Rev Microbiol 48, 713-742.
32. Wards, B. J. & Collins, D. M. (1996). Electroporation at elevated temperatures substantially improves transformation efficiency of slow growing mycobacteria. FEMS Microbiol Lett 145, 101-105.
33. Wilson, T. M. & Collins, D. M. (1996). ahpC, a gene involved in isoniazid resistance of the Mycobacterium tuberculosis complex. Mol Microbiol 19, 1025-1034.
34. Wilson, T. M., de Lisle, G. W. & Collins, D. M. (1995). Effect of inhA and katG on isoniazid resistance and virulence of Mycobacterium bovis. Mol Microbiol 15, 1009-1015.
35. Zhang, Y. & Young, D. (1994). Strain variation in the katG region of Mycobacterium tuberculosis. Mol Microbiol 14, 301-308.
36. Zhang, Y., Garbe, T. & 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.
37. Zhang, Y., Dhandayuthapani, S. & Deretic, V. (1996). Molecular basis for the exquisite sensitivity of Mycobacterium tuberculosis to isoniazid. Proc Natl Acad Sci USA 93, 13212-13216.