A complex regulatory network controlling intrinsic multidrug resistance in Mycobacterium smegmatis

Molecular Microbiology

Volumn 91, Issue 1, 2014, Pages 121-134

  Bowman, Joshua ^a,b   Ghosh, Pallavi ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b Cook MyoSite Inc ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BACTERIAL PROTEIN; CHLORAMPHENICOL; ERYTHROMYCIN; ISONIAZID; PROTEIN MSMEG; PROTEIN SERINE THREONINE KINASE; RNA POLYMERASE; SIGMA FACTOR; SPECTINOMYCIN; TETRACYCLINE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; CATALASE; HYDROGEN PEROXIDE; MITOMYCIN; TRANSCRIPTION FACTOR;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULON; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION; UPREGULATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; SEQUENCE ALIGNMENT;

CORYNEBACTERINEAE; EUKARYOTA; MYCOBACTERIUM SMEGMATIS;

ANTI-BACTERIAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; CATALASE; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; HYDROGEN PEROXIDE; MITOMYCIN; MYCOBACTERIUM SMEGMATIS; PHENOTYPE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; REGULON; SEQUENCE ALIGNMENT; SIGMA FACTOR; TRANSCRIPTION FACTORS;

EID: 84891151501     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12448     Document Type: Article

References (41)

1. Ainsa, J.A., Blokpoel, M.C., Otal, I., Young, D.B., De Smet, K.A., and Martin, C. (1998) Molecular cloning and characterization of Tap, a putative multidrug efflux pump present in Mycobacterium fortuitum and Mycobacterium tuberculosis. J Bacteriol 180: 5836-5843.
2. Av-Gay, Y., and Everett, M. (2000) The eukaryotic-like Ser/Thr protein kinases of Mycobacterium tuberculosis. Trends Microbiol 8: 238-244.
3. Barik, S., Sureka, K., Mukherjee, P., Basu, J., and Kundu, M. (2010) RseA, the SigE specific anti-sigma factor of Mycobacterium tuberculosis, is inactivated by phosphorylation-dependent ClpC1P2 proteolysis. Mol Microbiol 75: 592-606.
4. Baulard, A.R., Betts, J.C., Engohang-Ndong, J., Quan, S., McAdam, R.A., Brennan, P.J., etal. (2000) Activation of the pro-drug ethionamide is regulated in mycobacteria. J Biol Chem 275: 28326-28331.
5. Beaucher, J., Rodrigue, S., Jacques, P.E., Smith, I., Brzezinski, R., and Gaudreau, L. (2002) Novel Mycobacterium tuberculosis anti-sigma factor antagonists control sigmaF activity by distinct mechanisms. Mol Microbiol 45: 1527-1540.
6. Bishai, W. (1998) The Mycobacterium tuberculosis genomic sequence: anatomy of a master adaptor. Trends Microbiol 6: 464-465.
7. Burian, J., Ramon-Garcia, S., Howes, C.G., and Thompson, C.J. (2012) WhiB7, a transcriptional activator that coordinates physiology with intrinsic drug resistance in Mycobacterium tuberculosis. Expert Rev Anti Infect Ther 10: 1037-1047.
8. Burian, J., Yim, G., Hsing, M., Axerio-Cilies, P., Cherkasov, A., Spiegelman, G.B., and Thompson, C.J. (2013) The mycobacterial antibiotic resistance determinant WhiB7 acts as a transcriptional activator by binding the primary sigma factor SigA (RpoV). Nucleic Acids Res; Epub ahead of print on 28 Aug 2013.
9. Buroni, S., Manina, G., Guglierame, P., Pasca, M.R., Riccardi, G., and De Rossi, E. (2006) LfrR is a repressor that regulates expression of the efflux pump LfrA in Mycobacterium smegmatis. Antimicrob Agents Chemother 50: 4044-4052.
10. Chouchane, S., Lippai, I., and Magliozzo, R.S. (2000) Catalase-peroxidase (Mycobacterium tuberculosis KatG) catalysis and isoniazid activation. Biochemistry 39: 9975-9983.
11. Dainese, E., Rodrigue, S., Delogu, G., Provvedi, R., Laflamme, L., Brzezinski, R., etal. (2006) Posttranslational regulation of Mycobacterium tuberculosis extracytoplasmic-function sigma factor sigma L and roles in virulence and in global regulation of gene expression. Infect Immun 74: 2457-2461.
12. Engohang-Ndong, J., Baillat, D., Aumercier, M., Bellefontaine, F., Besra, G.S., Locht, C., and Baulard, A.R. (2004) EthR, a repressor of the TetR/CamR family implicated in ethionamide resistance in mycobacteria, octamerizes cooperatively on its operator. Mol Microbiol 51: 175-188.
13. Gebhard, S., Humpel, A., McLellan, A.D., and Cook, G.M. (2008) The alternative sigma factor SigF of Mycobacterium smegmatis is required for survival of heat shock, acidic pH and oxidative stress. Microbiology 154: 2786-2795.
14. Greenstein, A.E., Macgurn, J.A., Baer, C.E., Falick, A.M., Cox, J.S., and Alber, T. (2007) M.tuberculosis Ser/Thr protein kinase D phosphorylates an anti-anti-sigma factor homolog. PLoS Pathog 3: e49.
15. Gruber, T.M., and Gross, C.A. (2003) Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57: 441-466.
16. Helmann, J.D. (1999) Anti-sigma factors. Curr Opin Microbiol 2: 135-141.
17. Hingley-Wilson, S.M., Sambandamurthy, V.K., and Jacobs, W.R., Jr. (2003) Survival perspectives from the world's most successful pathogen, Mycobacterium tuberculosis. Nat Immunol 4: 949-955.
18. Hofmann, K., and Stoffel, W. (1993) TMbase - A database of membrane spanning proteins segment. Biol Chem Hoppe Seyler 374: 166.
19. Hughes, K.T., and Mathee, K. (1998) The anti-sigma factors. Annu Rev Microbiol 52: 231-286.
20. van Kessel, J.C., and Hatfull, G.F. (2007) Recombineering in Mycobacterium tuberculosis. Nat Methods 4: 147-152.
21. van Kessel, J.C., and Hatfull, G.F. (2008) Mycobacterial recombineering. Methods Mol Biol 435: 203-215.
22. Kroos, L., Zhang, B., Ichikawa, H., and Yu, Y.T. (1999) Control of sigma factor activity during Bacillus subtilis sporulation. Mol Microbiol 31: 1285-1294.
23. Larsen, M.H., Vilcheze, C., Kremer, L., Besra, G.S., Parsons, L., Salfinger, M., etal. (2002) Overexpression of inhA, but not kasA, confers resistance to isoniazid and ethionamide in Mycobacterium smegmatis, M.bovis BCG and M.tuberculosis. Mol Microbiol 46: 453-466.
24. Lee, J.H., Ammerman, N.C., Nolan, S., Geiman, D.E., Lun, S., Guo, H., and Bishai, W.R. (2012) Isoniazid resistance without a loss of fitness in Mycobacterium tuberculosis. Nat Commun 3: 753.
25. McDermott, P.F., White, D.G., Podglajen, I., Alekshun, M.N., and Levy, S.B. (1998) Multidrug resistance following expression of the Escherichia coli marA gene in Mycobacterium smegmatis. J Bacteriol 180: 2995-2998.
26. McKinney, J.D. (2000) In vivo veritas: the search for TB drug targets goes live. Nat Med 6: 1330-1333.
27. McKinney, J.D., Honer zu Bentrup, K., Munoz-Elias, E.J., Miczak, A., Chen, B., Chan, W.T., etal. (2000) Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406: 735-738.
28. Malik, S.S., Luthra, A., and Ramachandran, R. (2009) Interactions of the M.tuberculosis UsfX with the cognate sigma factor SigF and the anti-anti sigma factor RsfA. Biochim Biophys Acta 1794: 541-553.
29. Missiakas, D., and Raina, S. (1998) The extracytoplasmic function sigma factors: role and regulation. Mol Microbiol 28: 1059-1066.
30. Morris, R.P., Nguyen, L., Gatfield, J., Visconti, K., Nguyen, K., Schnappinger, D., etal. (2005) Ancestral antibiotic resistance in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 102: 12200-12205.
31. Murry, J.P., Sassetti, C.M., Lane, J.M., Xie, Z., and Rubin, E.J. (2008) Transposon site hybridization in Mycobacterium tuberculosis. Methods Mol Biol 416: 45-59.
32. Park, S.T., Kang, C.M., and Husson, R.N. (2008) Regulation of the SigH stress response regulon by an essential protein kinase in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 105: 13105-13110.
33. Raman, S., Song, T., Puyang, X., Bardarov, S., Jacobs, W.R., Jr, and Husson, R.N. (2001) The alternative sigma factor SigH regulates major components of oxidative and heat stress responses in Mycobacterium tuberculosis. J Bacteriol 183: 6119-6125.
34. Ramos, J.L., Martinez-Bueno, M., Molina-Henares, A.J., Teran, W., Watanabe, K., Zhang, X., etal. (2005) The TetR family of transcriptional repressors. Microbiol Mol Biol Rev 69: 326-356.
35. Rodrigue, S., Provvedi, R., Jacques, P.E., Gaudreau, L., and Manganelli, R. (2006) The sigma factors of Mycobacterium tuberculosis. FEMS Microbiol Rev 30: 926-941.
36. Rustad, T.R., Sherrid, A.M., Minch, K.J., and Sherman, D.R. (2009) Hypoxia: a window into Mycobacterium tuberculosis latency. Cell Microbiol 11: 1151-1159.
37. Sassetti, C.M., Boyd, D.H., and Rubin, E.J. (2001) Comprehensive identification of conditionally essential genes in mycobacteria. Proc Natl Acad Sci USA 98: 12712-12717.
38. da Silva, P.E., Von Groll, A., Martin, A., and Palomino, J.C. (2011) Efflux as a mechanism for drug resistance in Mycobacterium tuberculosis. FEMS Immunol Med Microbiol 63: 1-9.
39. Song, T., Dove, S.L., Lee, K.H., and Husson, R.N. (2003) RshA, an anti-sigma factor that regulates the activity of the mycobacterial stress response sigma factor SigH. Mol Microbiol 50: 949-959.
40. Wolff, K.A., Nguyen, H.T., Cartabuke, R.H., Singh, A., Ogwang, S., and Nguyen, L. (2009) Protein kinase G is required for intrinsic antibiotic resistance in mycobacteria. Antimicrob Agents Chemother 53: 3515-3519.
41. Zahrt, T.C., and Deretic, V. (2002) Reactive nitrogen and oxygen intermediates and bacterial defenses: unusual adaptations in Mycobacterium tuberculosis. Antioxid Redox Signal 4: 141-159.