Differential regulation of the two-component regulatory system senX3-regX3 in Mycobacterium tuberculosis

Microbiology (United Kingdom)

Volumn 160, Issue PART 6, 2014, Pages 1125-1133

  Rifat, Dalin ^a   Karakousis, Petros C ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA GALACTOSIDASE; REGX3 PROTEIN; SENX3 PROTEIN; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; BACTERIAL GROWTH; DNA FLANKING REGION; DNA SEQUENCE; GENE EXPRESSION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

EID: 84901712265     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.077180-0     Document Type: Article

References (47)

1. Ahmad, Z., Nuermberger, E. L., Tasneen, R., Pinn, M. L., Williams, K. N., Peloquin, C. A., Grosset, J. H. & Karakousis, P. C. (2010). Comparison of the 'Denver regimen' against acute tuberculosis in the mouse and guinea pig. J Antimicrob Chemother 65, 729-734.
2. Baek, J. H. & Lee, S. Y. (2007). Transcriptome analysis of phosphate starvation response in Escherichia coli. J Microbiol Biotechnol 17, 244-252.
3. Barletta, R. G., Kim, D. D., Snapper, S. B., Bloom, B. R. & Jacobs, W. R., Jr (1992). Identification of expression signals of the mycobacteriophages Bxb1, L1 and TM4 using the Escherichia-Mycobacterium shuttle plasmids pYUB75 and pYUB76 designed to create translational fusions to the lacZ gene. J Gen Microbiol 138, 23-30.
4. Barry, G., Squires, C. L. & Squires, C. (1979). Control features within the rplJL-rpoBC transcription unit of Escherichia coli. Proc Natl Acad Sci U S A 76, 4922-4926.
5. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S. & other authors (1998). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544.
6. Converse, P. J., Karakousis, P. C., Klinkenberg, L. G., Kesavan, A. K., Ly, L. H., Allen, S. S., Grosset, J. H., Jain, S. K., Lamichhane, G. & other authors (2009). Role of the dosR-dosS two-component regulatory system in Mycobacterium tuberculosis virulence in three animal models. Infect Immun 77, 1230-1237.
7. Dahl, J. L., Kraus, C. N., Boshoff, H. I., Doan, B., Foley, K., Avarbock, D., Kaplan, G., Mizrahi, V., Rubin, H. & Barry, C. E., III (2003). The role of RelMtb-mediated adaptation to stationary phase in long-term persistence of Mycobacterium tuberculosis in mice. Proc Natl Acad Sci U S A 100, 10026-10031.
8. Delihas, N. (2011). Impact of small repeat sequences on bacterial genome evolution. Genome Biol Evol 3, 959-973.
9. Dorman, C. J. (1995). 1995 Flemming Lecture. DNA topology and the global control of bacterial gene expression: implications for the regulation of virulence gene expression. Microbiology 141, 1271-1280.
10. Fornwald, J. A., Schmidt, F. J., Adams, C. W., Rosenberg, M. & Brawner, M. E. (1987). Two promoters, one inducible and one constitutive, control transcription of the Streptomyces lividans galactose operon. Proc Natl Acad Sci U S A 84, 2130-2134.
11. Glover, R. T., Kriakov, J., Garforth, S. J., Baughn, A. D. & Jacobs, W. R., Jr (2007). The two-component regulatory system senX3-regX3 regulates phosphate-dependent gene expression in Mycobacterium smegmatis. J Bacteriol 189, 5495-5503.
12. Gomez, J. E. & McKinney, J. D. (2004). M. tuberculosis persistence, latency, and drug tolerance. Tuberculosis (Edinb) 84, 29-44.
13. Gonzalo Asensio, J., Maia, C., Ferrer, N. L., Barilone, N., Laval, F., Soto, C. Y., Winter, N., Daffé, M., Gicquel, B. & other authors (2006). The virulence-associated two-component PhoP-PhoR system controls the biosynthesis of polyketide-derived lipids in Mycobacterium tuberculosis. J Biol Chem 281, 1313-1316.
14. Grosset, J. (2003). Mycobacterium tuberculosis in the extracellular compartment: an underestimated adversary. Antimicrob Agents Chemother 47, 833-836.
15. Haapanen, J. H., Kass, I., Gensini, G. & Middlebrook, G. (1959). Studies on the gaseous content of tuberculous cavities. Am Rev Respir Dis 80, 1-5.
16. Haydel, S. E., Malhotra, V., Cornelison, G. L. & Clark-Curtiss, J. E. (2012). The prrAB two-component system is essential for Mycobacterium tuberculosis viability and is induced under nitrogenlimiting conditions. J Bacteriol 194, 354-361.
17. He, H., Hovey, R., Kane, J., Singh, V. & Zahrt, T. C. (2006). MprAB is a stress-responsive two-component system that directly regulates expression of sigma factors SigB and SigE in Mycobacterium tuberculosis. J Bacteriol 188, 2134-2143.
18. Himpens, S., Locht, C. & Supply, P. (2000). Molecular characterization of the mycobacterial SenX3-RegX3 two-component system: evidence for autoregulation. Microbiology 146, 3091-3098.
19. James, J. N., Hasan, Z. U., Ioerger, T. R., Brown, A. C., Personne, Y., Carroll, P., Ikeh, M., Tilston-Lunel, N. L., Palavecino, C. & other authors (2012). Deletion of SenX3-RegX3, a key two-component regulatory system of Mycobacterium smegmatis, results in growth defects under phosphate-limiting conditions. Microbiology 158, 2724-2731.
20. Karakousis, P. C., Yoshimatsu, T., Lamichhane, G., Woolwine, S. C., Nuermberger, E. L., Grosset, J. & Bishai, W. R. (2004). Dormancy phenotype displayed by extracellular Mycobacterium tuberculosis within artificial granulomas in mice. J Exp Med 200, 647-657.
21. Karakousis, P. C., Williams, E. P. & Bishai, W. R. (2008). Altered expression of isoniazid-regulated genes in drug-treated dormant Mycobacterium tuberculosis. J Antimicrob Chemother 61, 323-331.
22. Klinkenberg, L. G., Lee, J. H., Bishai, W. R. & Karakousis, P. C. (2010). The stringent response is required for full virulence of Mycobacterium tuberculosis in guinea pigs. J Infect Dis 202, 1397-1404.
23. Lamichhane, G., Zignol, M., Blades, N. J., Geiman, D. E., Dougherty, A., Grosset, J., Broman, K. W. & Bishai, W. R. (2003). A postgenomic method for predicting essential genes at subsaturation levels of mutagenesis: application to Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 100, 7213-7218.
24. MacArthur, I., Parreira, V. R., Lepp, D., Mutharia, L. M., Vazquez-Boland, J. A. & Prescott, J. F. (2011). The sensor kinase MprB is required for Rhodococcus equi virulence. Vet Microbiol 147, 133-141.
25. Magdalena, J., Vachée, A., Supply, P. & Locht, C. (1998a). Identification of a new DNA region specific for members of Mycobacteriumtuberculosis complex. J Clin Microbiol 36, 937-943.
26. Magdalena, J., Vachée, A., Supply, P. & Locht, C. (1998b). Identification of a new DNA region specific for members of Mycobacteriumtuberculosis complex. J Clin Microbiol 36, 937-943.
27. Manganelli, R., Dubnau, E., Tyagi, S., Kramer, F. R. & Smith, I. (1999). Differential expression of 10 sigma factor genes in Mycobacterium tuberculosis. Mol Microbiol 31, 715-724.
28. Mayuri, B., Bagchi, G., Das, T. K. & Tyagi, J. S. (2002). Molecular analysis of the dormancy response in Mycobacterium smegmatis: expression analysis of genes encoding the DevR-DevS two-component system, Rv3134c and chaperone alpha-crystallin homologues. FEMS Microbiol Lett 211, 231-237.
29. Miller, J. F., Mekalanos, J. J. & Falkow, S. (1989). Coordinate regulation and sensory transduction in the control of bacterial virulence. Science 243, 916-922.
30. Millet, J., Miyagi-Shiohira, C., Yamane, N., Sola, C. & Rastogi, N. (2007). Assessment of mycobacterial interspersed repetitive unit-QUB markers to further discriminate the Beijing genotype in a populationbased study of the genetic diversity of Mycobacterium tuberculosis clinical isolates from Okinawa, Ryukyu Islands, Japan. J Clin Microbiol 45, 3606-3615.
31. Newbury, S. F., Smith, N. H. & Higgins, C. F. (1987). Differential mRNA stability controls relative gene expression within a polycistronic operon. Cell 51, 1131-1143.
32. Ohno, H., Zhu, G., Mohan, V. P., Chu, D., Kohno, S., Jacobs, W. R., Jr & Chan, J. (2003). The effects of reactive nitrogen intermediates on gene expression in Mycobacterium tuberculosis. Cell Microbiol 5, 637-648.
33. Parish, T., Smith, D. A., Roberts, G., Betts, J. & Stoker, N. G. (2003). The senX3-regX3 two-component regulatory system of Mycobacterium tuberculosis is required for virulence. Microbiology 149, 1423-1435.
34. Rao, N. N., Liu, S. & Kornberg, A. (1998). Inorganic polyphosphate in Escherichia coli: the phosphate regulon and the stringent response. J Bacteriol 180, 2186-2193.
35. Rengarajan, J., Bloom, B. R. & Rubin, E. J. (2005). Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci U S A 102, 8327-8332.
36. Rickman, L., Saldanha, J. W., Hunt, D. M., Hoar, D. N., Colston, M. J., Millar, J. B. & Buxton, R. S. (2004). A two-component signal transduction system with a PAS domain-containing sensor is required for virulence of Mycobacterium tuberculosis in mice. Biochem Biophys Res Commun 314, 259-267.
37. Rifat, D., Bishai, W. R. & Karakousis, P. C. (2009). Phosphate depletion: a novel trigger for Mycobacterium tuberculosis persistence. J Infect Dis 200, 1126-1135.
38. Sanyal, S., Banerjee, S. K., Banerjee, R., Mukhopadhyay, J. & Kundu, M. (2013). Polyphosphate kinase 1, a central node in the stress response network of Mycobacterium tuberculosis, connects the twocomponent systems MprAB and SenX3-RegX3 and the extracytoplasmic function sigma factor, sigma E. Microbiology 159, 2074-2086.
39. Sun, R., Converse, P. J., Ko, C., Tyagi, S., Morrison, N. E. & Bishai, W. R. (2004). Mycobacterium tuberculosis ECF sigma factor sigC is required for lethality in mice and for the conditional expression of a defined gene set. Mol Microbiol 52, 25-38.
40. Supply, P., Magdalena, J., Himpens, S. & Locht, C. (1997). Identification of novel intergenic repetitive units in a mycobacterial two-component system operon. Mol Microbiol 26, 991-1003.
41. Sureka, K., Dey, S., Datta, P., Singh, A. K., Dasgupta, A., Rodrigue, S., Basu, J. & Kundu, M. (2007). Polyphosphate kinase is involved in stress-induced mprAB-sigE-rel signalling in mycobacteria. Mol Microbiol 65, 261-276.
42. Taylor, W. E., Straus, D. B., Grossman, A. D., Burton, Z. F., Gross, C. A. & Burgess, R. R. (1984). Transcription from a heat-inducible promoter causes heat shock regulation of the sigma subunit of E. coli RNA polymerase. Cell 38, 371-381.
43. Thayil, S. M., Morrison, N., Schechter, N., Rubin, H. & Karakousis, P. C. (2011). The role of the novel exopolyphosphatase MT0516 in Mycobacterium tuberculosis drug tolerance and persistence. PLoS ONE 6, e28076.
44. Tischler, A. D., Leistikow, R. L., Kirksey, M. A., Voskuil, M. I. & McKinney, J. D. (2013). Mycobacterium tuberculosis requires phosphate-responsive gene regulation to resist host immunity. Infect Immun 81, 317-328.
45. Unniraman, S., Chatterji, M. & Nagaraja, V. (2002). DNA gyrase genes in Mycobacterium tuberculosis: a single operon driven by multiple promoters. J Bacteriol 184, 5449-5456.
46. Via, L. E., Curcic, R., Mudd, M. H., Dhandayuthapani, S., Ulmer, R. J. & Deretic, V. (1996). Elements of signal transduction in Mycobacterium tuberculosis: in vitro phosphorylation and in vivo expression of the response regulator MtrA. J Bacteriol 178, 3314-3321.
47. Zahrt, T. C. & Deretic, V. (2000). An essential two-component signal transduction system in Mycobacterium tuberculosis. J Bacteriol 182, 3832-3838.