The oxidation-sensing regulator (MosR) is a new redoxdependent transcription factor in Mycobacterium tuberculosis

Journal of Biological Chemistry

Volumn 287, Issue 45, 2012, Pages 37703-37712

  Brugarolas, Pedro ^a   Movahedzadeh, Farahnaz ^b   Wang, Yuehong ^b   Zhang, Nan ^b   Bartek, Iona L ^c   Gao, Yihe N ^a   Voskuil, Martin I ^c   Franzblau, Scott G ^b   He, Chuan ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL OXIDATION; INTRACELLULAR PATHOGENS; M. TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; OXIDATIVE ENVIRONMENT;

OXIDATION; SENSORS; TRANSCRIPTION FACTORS;

TUBES (COMPONENTS);

BACTERIAL PROTEIN; CYSTEINE; DNA; MGRA PROTEIN; ORGANIC HYDROPEROXIDE RESISTANCE PROTEIN; OXIDATION SENSING REGULATOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL SURVIVAL; BINDING AFFINITY; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISULFIDE BOND; GENE EXPRESSION PROFILING; HYDROGEN BOND; MACROPHAGE; MOLECULAR DYNAMICS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION REGULATION; UPREGULATION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; DISULFIDES; DNA; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN PEROXIDE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; MYCOBACTERIUM TUBERCULOSIS; NUCLEIC ACID CONFORMATION; NUCLEOTIDE MOTIFS; OXIDANTS; OXIDATION-REDUCTION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

EID: 84868334611     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.388611     Document Type: Article

References (55)

1. World Health Organization (2011) Global Tuberculosis Control, WHO Report 2011, pp. 1-27, World Health Organization, Geneva, Switzerlandd
2. Ehrt, S., and Schnappinger, D. (2009)Mycobacterial survival strategies in the phagosome: defense against host stresses. Cell. Microbiol. 11, 1170-11788
3. Flynn, J. L., and Chan, J. (2001) Tuberculosis: latency and reactivation. Infect. Immun. 69, 4195-42011
4. Buchmeier, N., and Fahey, R. C. (2006) The mshA gene encoding the glycosyltransferase of mycothiol biosynthesis is essential in Mycobacterium tuberculosis Erdman. FEMS Microbiol. Lett. 264, 74-799
5. Buchmeier, N. A., Newton, G. L., and Fahey, R. C. (2006) A mycothiol synthase mutant of Mycobacterium tuberculosis has an altered thiol-disulfide content and limited tolerance to stress. J. Bacteriol. 188, 6245-62522
6. Manca, C., Paul, S., Barry, C. E., 3rd, Freedman, V. H., and Kaplan, G. (1999)Mycobacterium tuberculosis catalase and peroxidase activities and resistance to oxidative killing in human monocytes in vitro. Infect. Immun. 67, 74-799
7. Jackett, P. S., Aber, V. R., and Lowrie, D. B. (1978) Virulence and resistance to superoxide, low pH, and hydrogen peroxide among strains of Mycobacterium tuberculosis. J. Gen. Microbiol. 104, 37-455
8. Piddington, D. L., Fang, F. C., Laessig, T., Cooper, A. M., Orme, I. M., and Buchmeier, N. A. (2001) Cu, Zn-superoxide dismutase of Mycobacterium tuberculosis contributes to survival in activated macrophages that are generating an oxidative burst. Infect. Immun. 69, 4980-49877
9. Bryk, R., Griffin, P., and Nathan, C. (2000) Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407, 211-2155
10. Bryk, R., Lima, C. D., Erdjument-Bromage, H., Tempst, P., and Nathan, C. (2002) Metabolic enzymes of mycobacteria linked to antioxidant defense by a thioredoxin-like protein. Science 295, 1073-10777
11. Colangeli, R., Haq, A., Arcus, V. L., Summers, E., Magliozzo, R. S., McBride, A., Mitra, A. K., Radjainia, M., Khajo, A., Jacobs, W. R., Jr., Salgame, P., and Alland, D. (2009)The multifunctional histone-like protein Lsr2 protects mycobacteria against reactive oxygen intermediates. Proc. Natl. Acad. Sci. U.S.A. 106, 4414-44188
12. McCann, J. R., McDonough, J. A., Sullivan, J. T., Feltcher, M. E., and Braunstein, M. (2011) Genome-wide identification of Mycobacterium tuberculosis exported proteins with roles in intracellular growth. J. Bacteriol. 193, 854-8611
13. Green, J., and Paget, M. S. (2004) Bacterial redox sensors. Nat. Rev. Microbiol. 2, 954-9666
14. den Hengst, C. D., and Buttner, M. J. (2008)Redox control in actinobacteria. Biochim. Biophys. Acta 1780, 1201-12166
15. Chen, P. R., Brugarolas, P., and He, C. (2011) Redox signaling in human pathogens. Antioxid. Redox Signal. 14, 1107-11188
16. Chen, P. R., Bae, T., Williams, W. A., Duguid, E. M., Rice, P. A., Schneewind, O., and He, C. (2006) An oxidation-sensing mechanism is used by the global regulator MgrA in Staphylococcus aureus. Nat. Chem. Biol. 2, 591-5955
17. Luong, T. T., Dunman, P. M., Murphy, E., Projan, S. J., and Lee, C. Y. (2006) Transcription profiling of the mgrA Regulon in Staphylococcus aureus. J. Bacteriol. 188, 1899-19100
18. Luong, T. T., Newell, S. W., and Lee, C. Y. (2003) Mgr, a novel global regulator in Staphylococcus aureus. J. Bacteriol. 185, 3703-37100
19. Ha, U., and Jin, S. (1999)Expression of the soxR gene of Pseudomonas aeruginosa is inducible during infection of burn wounds in mice and is required to cause efficient bacteremia. Infect. Immun. 67, 5324-53311
20. Kobayashi, K., and Tagawa, S. (2004) Activation of SoxR-dependent transcription in Pseudomonas aeruginosa. J. Biochem. 136, 607-6155
21. Ochsner, U. A., Vasil, M. L., Alsabbagh, E., Parvatiyar, K., and Hassett, D. J. (2000) Role of the Pseudomonas aeruginosa oxyR-recG operon in oxidative stress defense andDNArepair: OxyR-dependent regulation of katB-ankB, ahpB, and ahpC-ahpF. J. Bacteriol. 182, 4533-45444
22. Singh, A., Crossman, D. K., Mai, D., Guidry, L., Voskuil, M. I., Renfrow, M. B., and Steyn, A. J. (2009)Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog. 5, e10005455
23. Singh, A., Guidry, L., Narasimhulu, K. V., Mai, D., Trombley, J., Redding, K. E., Giles, G. I., Lancaster, J. R., Jr., and Steyn, A. J. (2007) Mycobacterium tuberculosis WhiB3 responds toO2 and nitric oxide via its [4Fe-4S] cluster and is essential for nutrient starvation survival. Proc. Natl. Acad. Sci. U.S.A. 104, 11562-115677
24. Voskuil, M. I., Bartek, I. L., Visconti, K., and Schoolnik, G. K. (2011) The response of Mycobacterium tuberculosis to reactive oxygen and nitrogen species. Front. Microbiol. 2, 1055
25. Zahrt, T. C., Song, J., Siple, J., and Deretic, V. (2001) Mycobacterial FurA is a negative regulator of catalase-peroxidase gene katG. Mol. Microbiol. 39, 1174-11855
26. Rodriguez, G. M., Voskuil, M. I., Gold, B., Schoolnik, G. K., and Smith, I. (2002) ideR, An essential gene in Mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect. Immun. 70, 3371-33811
27. Fernandes, N. D., Wu, Q. L., Kong, D., Puyang, X., Garg, S., and Husson, R. N. (1999)A mycobacterial extracytoplasmic sigma factor involved in survival following heat shock and oxidative stress. J. Bacteriol. 181, 4266-42744
28. Wu, Q. L., Kong, D., Lam, K., and Husson, R. N. (1997) A mycobacterial extracytoplasmic function sigma factor involved in survival following stress. J. Bacteriol. 179, 2922-29299
29. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-3266
30. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-6744
31. Hong, M., Fuangthong, M., Helmann, J. D., and Brennan, R. G. (2005) Structure of an OhrR-ohrA operator complex reveals the DNA binding mechanism of the MarR family. Mol. cell 20, 131-1411
32. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-2211
33. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-5011
34. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, version 1.3r1, Schrödinger, LLC, New Yorkk
35. Leblanc, B., and Moss, T. (1994) DNase I footprinting. Methods Mol. Biol. 30, 1-100
36. Parish, T., and Stoker, N. G. (2000) Use of a flexible cassette method to generate a double unmarked Mycobacterium tuberculosis tlyA plcABC mutant by gene replacement. Microbiology 146, 1969-19755
37. Wilson, M., Voskuil, M., Schnappinger, D., and Schoolnik, G. K. (2001) Functional genomics of Mycobacterium tuberculosis using DNA microarrays. Methods Mol. Med. 54, 335-3577
38. Ta, P., Buchmeier, N., Newton, G. L., Rawat, M., and Fahey, R. C. (2011) Organic hydroperoxide resistance protein and ergothioneine compensate for loss of mycothiol in Mycobacterium smegmatis mutants. J. Bacteriol. 193, 1981-19900
39. Poole, L. B., and Nelson, K. J. (2008)Discovering mechanisms of signalingmediated cysteine oxidation. Curr. Opin. Chem. Biol. 12, 18-244
40. Panmanee, W., Vattanaviboon, P., Poole, L. B., and Mongkolsuk, S. (2006) Novel organic hydroperoxide-sensing and responding mechanisms for OhrR, a major bacterial sensor and regulator of organic hydroperoxide stress. J. Bacteriol. 188, 1389-13955
41. Målen, H., Berven, F. S., Fladmark, K. E., and Wiker, H. G. (2007) Comprehensive analysis of exported proteins from Mycobacterium tuberculosis H37Rv. Proteomics 7, 1702-17188
42. Sherman, D. R., Voskuil, M., Schnappinger, D., Liao, R., Harrell, M. I., and Schoolnik, G. K. (2001) Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding-crystallin. Proc. Natl. Acad. Sci. U.S.A. 98, 7534-75399
43. Voskuil, M. I., Schnappinger, D., Visconti, K. C., Harrell, M. I., Dolganov, G. M., Sherman, D. R., and Schoolnik, G. K. (2003) Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J. Exp. Med. 198, 705-7133
44. Dolan, K. T., Duguid, E. M., and He, C. (2011) Crystal structures of SlyA protein, a master virulence regulator of Salmonella, in free and DNAbound states. J. Biol. Chem. 286, 22178-221855
45. Petrova, T., Ginell, S., Mitschler, A., Kim, Y., Lunin, V. Y., Joachimiak, G., Cousido-Siah, A., Hazemann, I., Podjarny, A., Lazarski, K., and Joachimiak, A. (2010) X-ray-induced deterioration of disulfide bridges at atomic resolution. Acta Crystallogr. D Biol. Crystallogr. 66, 1075-10911
46. Antelmann, H., and Helmann, J. D. (2011) Thiol-based redox switches and gene regulation. Antioxid. Redox Signal 14, 1049-10633
47. Lee, J. W., Soonsanga, S., and Helmann, J. D. (2007) A complex thiolate switch regulates the Bacillus subtilis organic peroxide sensor OhrR. Proc. Natl. Acad. Sci. U.S.A. 104, 8743-87488
48. Poor, C. B., Chen, P. R., Duguid, E., Rice, P. A., and He, C. (2009)Crystal structures of the reduced, sulfenic acid, and mixed disulfide forms of SarZ, a redox active global regulator in Staphylococcus aureus. J. Biol. Chem. 284, 23517-235244
49. Newberry, K. J., Fuangthong, M., Panmanee, W., Mongkolsuk, S., and Brennan, R. G. (2007) Structural mechanism of organic hydroperoxide induction of the transcription regulator OhrR. Mol. Cell 28, 652-6644
50. Mahenthiralingam, E., Marklund, B. I., Brooks, L. A., Smith, D. A., Bancroft, G. J., and Stokes, R. W. (1998) Site-directed mutagenesis of the 19-kilodalton lipoprotein antigen reveals no essential role for the protein in the growth and virulence of Mycobacterium intracellulare. Infect Immun. 66, 3626-36344
51. Fontán, P. A., Voskuil, M. I., Gomez, M., Tan, D., Pardini, M., Manganelli, R., Fattorini, L., Schoolnik, G. K., and Smith, I. (2009)The Mycobacterium tuberculosis sigma factor-B is required for full response to cell envelope stress and hypoxia in vitro, but it is dispensable for in vivo growth. J. Bacteriol. 191, 5628-56333
52. Divangahi, M., Desjardins, D., Nunes-Alves, C., Remold, H. G., and Behar, S. M. (2010) Eicosanoid pathways regulate adaptive immunity to Mycobacterium tuberculosis. Nat. Immunol. 11, 751-7588
53. Schnappinger, D., Ehrt, S., Voskuil, M. I., Liu, Y., Mangan, J. A., Monahan, I. M., Dolganov, G., Efron, B., Butcher, P. D., Nathan, C., and Schoolnik, G. K. (2003) Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J. Exp. Med. 198, 693-7044
54. Rengarajan, J., Bloom, B. R., and Rubin, E. J. (2005) Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc. Natl. Acad. Sci. U.S.A. 102, 8327-83322
55. Chen, M., Divangahi, M., Gan, H., Shin, D. S., Hong, S., Lee, D. M., Serhan, C. N., Behar, S. M., and Remold, H. G. (2008)Lipid mediators in innate immunity against tuberculosis: opposing roles of PGE2 and LXA4 in the induction of macrophage death. J. Exp. Med. 205, 2791-28011