Components of the Rv0081-Rv0088 Locus, which encodes a predicted formate hydrogenlyase complex, are coregulated by Rv0081, MprA, and DosR in Mycobacterium tuberculosis

Journal of Bacteriology

Volumn 193, Issue 19, 2011, Pages 5105-5118

  He, Hongjun ^a   Bretl, Daniel J ^a   Penoske, Renee M ^a   Anderson, David M ^a   Zahrt, Thomas C ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; FORMIC ACID; GENOMIC DNA; HYDROGENASE; PLASMID DNA; RECOMBINANT PROTEIN;

ADAPTATION; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIUM CULTURE; BINDING SITE; CULTURE MEDIUM; DELETION MUTANT; DNA SEQUENCE; DOSR GENE; ENZYME ASSAY; ESCHERICHIA COLI; GENE LOCUS; LIQUID CHROMATOGRAPHY; MPRA GENE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PERSISTENT INFECTION; POLYMERASE CHAIN REACTION; PREDICTION; PRIORITY JOURNAL; PROTEIN PURIFICATION; REGULON; RV0081 GENE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUBERCULOSIS;

BACTERIAL PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FORMATE DEHYDROGENASES; GENE EXPRESSION REGULATION, BACTERIAL; MULTIENZYME COMPLEXES; MUTATION; MYCOBACTERIUM TUBERCULOSIS; PROTAMINE KINASE; PROTEIN KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

MYCOBACTERIUM TUBERCULOSIS;

EID: 80053603928     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.05562-11     Document Type: Article

References (70)

1. Allen, B. W. 1998. Mycobacteria: general culture methodology and safety considerations, p. 15-30. In T. Parish and N. G. Stoker (ed.), Mycobacteria protocols, vol. 101. Humana Press Inc., Totowa, NJ.
2. Anonymous. 2010. Global tuberculosis control 2010. World Health Organization, Geneva, Switzerland.
3. Anonymous. 2010. Treatment of tuberculosis guidelines. World Health Organization, Geneva, Switzerland.
4. Bardarov, S., et al. 2002. Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology 148:3007- 3017.
5. Barik, S., K. Sureka, P. Mukherjee, J. Basu, and M. Kundu. 2010. RseA, the SigE specific anti-sigma factor of Mycobacterium tuberculosis, is inactivated by phosphorylation-dependent ClpC1P2 proteolysis. Mol. Microbiol. 75: 592-606.
6. Betts, J. C., P. T. Lukey, L. C. Robb, R. A. McAdam, and K. Duncan. 2002. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 43: 717-731.
7. Birkmann, A., F. Zinoni, G. Sawers, and A. Bock. 1987. Factors affecting transcriptional regulation of the formate-hydrogen-lyase pathway of Escherichia coli. Arch. Microbiol. 148:44-51.
8. Black, G. F., et al. 2009. Immunogenicity of novel DosR regulon-encoded candidate antigens of Mycobacterium tuberculosis in three high-burden populations in Africa. Clin. Vaccine Immunol. 16:1203-1212.
9. Boon, C., and T. Dick. 2002. Mycobacterium bovis BCG response regulator essential for hypoxic dormancy. J. Bacteriol. 184:6760-6767.
10. Busenlehner, L. S., M. A. Pennella, and D. P. Giedroc. 2003. The SmtB/ArsR family of metalloregulatory transcriptional repressors: structural insights into prokaryotic metal resistance. FEMS Microbiol. Rev. 27:131-143.
11. Campbell, D. R., et al. 2007. Mycobacterial cells have dual nickel-cobalt sensors: sequence relationships and metal sites of metal-responsive repressors are not congruent. J. Biol. Chem. 282:32298-32310.
12. Cavet, J. S., A. I. Graham, W. Meng, and N. J. Robinson. 2003. A cadmiumlead-sensing ArsR-SmtB repressor with novel sensory sites. Complementary metal discrimination by NmtR AND CmtR in a common cytosol. J. Biol. Chem. 278:44560-44566.
13. Cavet, J. S., et al. 2002. A nickel-cobalt-sensing ArsR-SmtB family repressor. Contributions of cytosol and effector binding sites to metal selectivity. J. Biol. Chem. 277:38441-38448.
14. Chauhan, S., A. Kumar, A. Singhal, J. S. Tyagi, and H. Krishna Prasad. 2009. CmtR, a cadmium-sensing ArsR-SmtB repressor, cooperatively interacts with multiple operator sites to autorepress its transcription in Mycobacterium tuberculosis. FEBS J. 276:3428-3439.
15. Chauhan, S., and J. S. Tyagi. 2008. Cooperative binding of phosphorylated DevR to upstream sites is necessary and sufficient for activation of the Rv3134c-devRS operon in Mycobacterium tuberculosis: implication in the induction of DevR target genes. J. Bacteriol. 190:4301-4312.
16. Chauhan, S., and J. S. Tyagi. 2008. Interaction of DevR with multiple binding sites synergistically activates divergent transcription of narK2-Rv1738 genes in Mycobacterium tuberculosis. J. Bacteriol. 190:5394-5403.
17. Chauhan, S., and J. S. Tyagi. 2009. Powerful induction of divergent tgs1-Rv3131 genes in Mycobacterium tuberculosis is mediated by DevR interaction with a high-affinity site and an adjacent cryptic low-affinity site. J. Bacteriol. 191:6075-6081.
18. Cole, S. T., et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
19. Converse, P. J., et al. 2009. Role of the dosR-dosS two-component regulatory system in Mycobacterium tuberculosis virulence in three animal models. Infect. Immun. 77:1230-1237.
20. Dasgupta, N., et al. 2000. Characterization of a two-component system, devR-devS, of Mycobacterium tuberculosis. Tuber. Lung Dis. 80:141-159.
21. Domenech, P., G. S. Kolly, L. Leon-Solis, A. Fallow, and M. B. Reed. 2010. Massive gene duplication event among clinical isolates of the Mycobacterium tuberculosis W/Beijing family. J. Bacteriol. 192:4562-4570.
22. Dona, V., et al. 2008. Evidence of complex transcriptional, translational, and posttranslational regulation of the extracytoplasmic function sigma factor E in Mycobacterium tuberculosis. J. Bacteriol. 190:5963-5971.
23. Estorninho, M., et al. 2010. ClgR regulation of chaperone and protease systems is essential for Mycobacterium tuberculosis parasitism of the macrophage. Microbiology 156:3445-3455.
24. Fallow, A., P. Domenech, and M. B. Reed. 2010. Strains of the East Asian (W/Beijing) lineage of Mycobacterium tuberculosis are DosS/DosT-DosR two-component regulatory system natural mutants. J. Bacteriol. 192:2228- 2238.
25. Fisher, M. A., B. B. Plikaytis, and T. M. Shinnick. 2002. Microarray analysis of the Mycobacterium tuberculosis transcriptional response to the acidic conditions found in phagosomes. J. Bacteriol. 184:4025-4032.
26. Florczyk, M. A., et al. 2003. A family of acr-coregulated Mycobacterium tuberculosis genes shares a common DNA motif and requires Rv3133c (dosR or devR) for expression. Infect. Immun. 71:5332-5343.
27. Haydel, S. E., and J. E. Clark-Curtiss. 2004. Global expression analysis of two-component system regulator genes during Mycobacterium tuberculosis growth in human macrophages. FEMS Microbiol. Lett. 236:341-347.
28. He, H., R. Hovey, J. Kane, V. Singh, and T. C. Zahrt. 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.
29. He, H., and T. C. Zahrt. 2005. Identification and characterization of a regulatory sequence recognized by Mycobacterium tuberculosis persistence regulator MprA. J. Bacteriol. 187:202-212.
30. Honaker, R. W., R. K. Dhiman, P. Narayanasamy, D. C. Crick, and M. I. Voskuil. 2010. DosS responds to a reduced electron transport system to induce the Mycobacterium tuberculosis DosR regulon. J. Bacteriol. 192: 6447-6455.
31. Hopper, S., et al. 1994. Regulated expression in vitro of genes coding for formate hydrogenlyase components of Escherichia coli. J. Biol. Chem. 269: 19597-19604.
32. Hopper, S., and A. Bock. 1995. Effector-mediated stimulation of ATPase activity by the sigma 54-dependent transcriptional activator FHLA from Escherichia coli. J. Bacteriol. 177:2798-2803.
33. Jacobs, W. R., Jr., et al. 1991. Genetic systems for mycobacteria. Methods Enzymol. 204:19.
34. Karakousis, P. C., et al. 2004. Dormancy phenotype displayed by extracellular Mycobacterium tuberculosis within artificial granulomas in mice. J. Exp. Med. 200:647-657.
35. Kumar, A., et al. 2008. Heme oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J. Biol. Chem. 283: 18032-18039.
36. Leistikow, R. L., et al. 2010. The Mycobacterium tuberculosis DosR regulon assists in metabolic homeostasis and enables rapid recovery from nonrespiring dormancy. J. Bacteriol. 192:1662-1670.
37. Leonhartsberger, S., I. Korsa, and A. Bock. 2002. The molecular biology of formate metabolism in enterobacteria. J. Mol. Microbiol. Biotechnol. 4:269- 276.
38. Lucarelli, D., et al. 2007. Crystal structure and function of the zinc uptake regulator FurB from Mycobacterium tuberculosis. J. Biol. Chem. 282:9914- 9922.
39. Malhotra, V., et al. 2004. Disruption of response regulator gene, devR, leads to attenuation in virulence of Mycobacterium tuberculosis. FEMS Microbiol. Lett. 231:237-245.
40. Manganelli, R., M. I. Voskuil, G. K. Schoolnik, and I. Smith. 2001. The Mycobacterium tuberculosis ECF sigma factor E: role in global gene expression and survival in macrophages. Mol. Microbiol. 41:423-437.
41. Mehra, S., N. K. Dutta, H. J. Mollenkopf, and D. Kaushal. 2010. Mycobacterium tuberculosis MT2816 encodes a key stress-response regulator. J. Infect. Dis. 202:943-953.
42. Morby, A. P., J. S. Turner, J. W. Huckle, and N. J. Robinson. 1993. SmtB is a metal-dependent repressor of the cyanobacterial metallothionein gene smtA: identification of a Zn inhibited DNA-protein complex. Nucleic Acids Res. 21:921-925.
43. Pang, X., et al. 2007. Evidence for complex interactions of stress-associated regulons in an mprAB deletion mutant of Mycobacterium tuberculosis. Microbiology 153:1229-1242.
44. Parish, T., et al. 2003. Deletion of two-component regulatory systems increases the virulence of Mycobacterium tuberculosis. Infect. Immun. 71: 1134-1140.
45. Park, H. D., et al. 2003. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol. Microbiol. 48: 833-843.
46. Pecher, A., et al. 1983. On the redox control of synthesis of anaerobically induced enzymes in enterobacteriaceae. Arch. Microbiol. 136:131-136.
47. Riley, L. 1996. Phagocytosis of M. tuberculosis, p. 281-289. In W. Rom and S. Garay (ed.), Tuberculosis. Little Brown, Boston, MA.
48. Rosentel, J. K., F. Healy, J. A. Maupin-Furlow, J. H. Lee, and K. T. Shanmugam. 1995. Molybdate and regulation of mod (molybdate transport), fdhF, and hyc (formate hydrogenlyase) operons in Escherichia coli. J. Bacteriol. 177:4857-4864.
49. Rossmann, R., G. Sawers, and A. Bock. 1991. Mechanism of regulation of the formate-hydrogenlyase pathway by oxygen, nitrate, and pH: definition of the formate regulon. Mol. Microbiol. 5:2807-2814.
50. Rustad, T. R., M. I. Harrell, R. Liao, and D. R. Sherman. 2008. The enduring hypoxic response of Mycobacterium tuberculosis. PLoS One 3:e1502.
51. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
52. Sassetti, C. M., D. H. Boyd, and E. J. Rubin. 2003. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48:77-84.
53. Sauter, M., R. Bohm, and A. Bock. 1992. Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. Mol. Microbiol. 6:1523-1532.
54. Sawers, R. G. 2005. Formate and its role in hydrogen production in Escherichia coli. Biochem. Soc. Trans. 33:42-46.
55. Schlensog, V., S. Lutz, and A. Bock. 1994. Purification and DNA-binding properties of FHLA, the transcriptional activator of the formate hydrogenlyase system from Escherichia coli. J. Biol. Chem. 269:19590-19596.
56. Schnappinger, D., et al. 2003. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J. Exp. Med. 198:693-704.
57. Skibinski, D. A., et al. 2002. Regulation of the hydrogenase-4 operon of Escherichia coli by the 54-dependent transcriptional activators FhlA and HyfR. J. Bacteriol. 184:6642-6653.
58. Stover, C. K., et al. 1991. New use of BCG for recombinant vaccines. Nature 351:456-460.
59. Sureka, K., et al. 2007. Polyphosphate kinase is involved in stress-induced mprAB-sigE-rel signalling in mycobacteria. Mol. Microbiol. 65:261-276.
60. Talaat, A. M., R. Lyons, S. T. Howard, and S. A. Johnston. 2004. The temporal expression profile of Mycobacterium tuberculosis infection in mice. Proc. Natl. Acad. Sci. U. S. A. 101:4602-4607.
61. Taneja, N. K., S. Dhingra, A. Mittal, M. Naresh, and J. S. Tyagi. 2010. Mycobacterium tuberculosis transcriptional adaptation, growth arrest and dormancy phenotype development is triggered by vitamin C. PLoS One 5:e10860.
62. Timm, J., E. M. Lim, and B. Gicquel. 1994. Escherichia coli-mycobacteria shuttle vectors for operon and gene fusions to lacZ: the pJEM series. J. Bacteriol. 176:6749-6753.
63. Tottey, S., D. R. Harvie, and N. J. Robinson. 2005. Understanding how cells allocate metals using metal sensors and metallochaperones. ACC Chem. Res. 38:775-783.
64. Vasudeva-Rao, H. M., and K. A. McDonough. 2008. Expression of the Myco-bacterium tuberculosis acr-coregulated genes from the DevR (DosR) regulon is controlled by multiple levels of regulation. Infect. Immun. 76:2478-2489.
65. Vignais, P. M., and A. Colbeau. 2004. Molecular biology of microbial hydrogenases. Curr. Issues Mol. Biol. 6:159-188.
66. Voskuil, M. I., et al. 2003. Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J. Exp. Med. 198:705-713.
67. Wang, Y., L. Hemmingsen, and D. P. Giedroc. 2005. Structural and functional characterization of Mycobacterium tuberculosis CmtR, a PbII/CdII-sensing SmtB/ArsR metalloregulatory repressor. Biochemistry 44:8976-8988.
68. White, M. J., H. He, R. M. Penoske, S. S. Twining, and T. C. Zahrt. 2010. PepD participates in the mycobacterial stress response mediated through MprAB and SigE. J. Bacteriol. 192:1498-1510.
69. Zahrt, T. C., and V. Deretic. 2001. Mycobacterium tuberculosis signal transduction system required for persistent infections. Proc. Natl. Acad. Sci. U. S. A. 98:12706-12711.
70. Zahrt, T. C., C. Wozniak, D. Jones, and A. Trevett. 2003. Functional analysis of the Mycobacterium tuberculosis MprAB two-component signal transduction system. Infect. Immun. 71:6962-6970.