Co-expression of DevR and DevRN-Aph proteins is associated with hypoxic adaptation defect and virulence attenuation of Mycobacterium tuberculosis

PLoS ONE

Volumn 5, Issue 2, 2010, Pages

  De Majumdar, Shyamasree ^a   Sharma, Deepak ^a,d   Vashist, Atul ^a   Kaur, Kohinoor ^a   Taneja, Neetu Kumra ^a   Chauhan, Santosh ^a   Challu, Vijay K ^b   Ramanathan, V D ^c   Balasangameshwara, V ^b   Kumar, Prahlad ^b   Tyagi, Jaya Sivaswami ^a  

^a ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

^b NATIONAL TUBERCULOSIS INSTITUTE   (India)

^c NATIONAL INSTITUTE FOR RESEARCH IN TUBERCULOSIS   (India)

^d NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

APHI PROTEIN; BACTERIAL PROTEIN; COMP 1 PROTEIN; DEVR PROTEIN; HYBRID PROTEIN; MUT 1 PROTEIN; UNCLASSIFIED DRUG; MUTANT PROTEIN; TRANSACTIVATOR PROTEIN;

ADAPTATION; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GUINEA PIG; HYPOXIA; MUTANT; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPLEEN; SURVIVAL; WILD TYPE; ANAEROBIC GROWTH; ANIMAL; CELL LINE; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; HUMAN; LUNG; MICROBIAL VIABILITY; MICROBIOLOGY; MUTATION; PATHOGENICITY; PHYSIOLOGY; REGULON; TUBERCULOSIS; VIRULENCE;

BACILLI (CLASS); BACTERIA (MICROORGANISMS); CAVIA; MYCOBACTERIUM TUBERCULOSIS;

ADAPTATION, PHYSIOLOGICAL; ANAEROBIOSIS; ANIMALS; BACTERIAL PROTEINS; CELL LINE; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; GUINEA PIGS; HUMANS; LUNG; MICROBIAL VIABILITY; MUTANT PROTEINS; MUTATION; MYCOBACTERIUM TUBERCULOSIS; REGULON; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TUBERCULOSIS; VIRULENCE;

EID: 77949729415     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009448     Document Type: Article

References (32)

1. Cole ST, Barrell BG (1998) Analysis of the genome of Mycobacterium tuberculosis H37Rv. Novartis Found Symp 217: 160-172; discussion 172-167.
2. Tyagi JS, Sharma D (2004) Signal transduction systems of mycobacteria with special reference to M. tuberculosis. Curr Sci 86: 93-102.
3. Av-Gay Y, Deretic V (2005) Two-component systems, protein kinases and signal transduction in Mycobacterium tuberculosis. In: Cole ST, Eisenach KD, McMurray DN, Jacobs WR, Jr., eds. Tuberculosis and the tubercle bacillus. Washington DC: ASM Press. pp 359-367.
4. Kinger AK, Tyagi JS (1993) Identification and cloning of genes differentially expressed in the virulent strain of Mycobacterium tuberculosis. Gene 131: 113-117.
5. Dasgupta N, Kapur V, Singh KK, Das TK, Sachdeva S, et al. (2000) Characterization of a two-component system, devR-devS, of Mycobacterium tuberculosis. Tuber Lung Dis 80: 141-159.
6. Roberts DM, Liao RP, Wisedchaisri G, Hol WG, Sherman DR (2004) Two sensor kinases contribute to the hypoxic response of Mycobacterium tuberculosis. J Biol Chem 279: 23082-23087.
7. Saini DK, Malhotra V, Dey D, Pant N, Das TK, et al. (2004a) DevR-DevS is a bona fide two-component system of Mycobacterium tuberculosis that is hypoxia-responsive in the absence of the DNA-binding domain of DevR. Microbiology 150: 865-875.
8. Saini DK, Malhotra V, Tyagi JS (2004b) Cross talk between DevS sensor kinase homologue, Rv2027c, and DevR response regulator of Mycobacterium tuberculosis. FEBS Lett 565: 75-80.
9. Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, et al. (2001) Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding α-crystallin. Proc Natl Acad Sci U S A 98: 7534-7539.
10. Boon C, Dick T (2002) Mycobacterium bovis BCG response regulator essential for hypoxic dormancy. J Bacteriol 184: 6760-6767.
11. Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, et al. (2003) Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 48: 833-843.
12. Parish T, Smith DA, Kendall S, Casali N, Bancroft GJ, et al. (2003) Deletion of two-component regulatory systems increases the virulence of Mycobacterium tuberculosis. Infect Immun 71: 1134-1140.
13. Malhotra V, Sharma D, Ramanathan VD, Shakila H, Saini DK, et al. (2004) Disruption of response regulator gene, devR, leads to attenuation in virulence of Mycobacterium tuberculosis. FEMS Microbiol Lett 231: 237-245.
14. Rustad TR, Harrell MI, Liao R, Sherman DR (2008) The enduring hypoxic response of Mycobacterium tuberculosis. PLoS One 3: e1502.
15. Converse PJ, Karakousis PC, Klinkenberg LG, Kesavan AK, Ly LH, 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.
16. Shi L, Jung YJ, Tyagi S, Gennaro ML, North RJ (2003) Expression of Th1-mediated immunity in mouse lungs induces a Mycobacterium tuberculosis transcription pattern characteristic of nonreplicating persistence. Proc Natl Acad Sci U S A 100: 241-246.
17. Voskuil MI, Schnappinger D, Visconti KC, Harrell MI, Dolganov GM, et al. (2003) Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198: 705-713.
18. Karakousis PC, Yoshimatsu T, Lamichhane G, Woolwine SC, Nuermberger EL, et al. (2004) Dormancy phenotype displayed by extracellular Mycobacterium tuberculosis within artificial granulomas in mice. J Exp Med 200: 647-657.
19. Sharma D, Bose A, Shakila H, Das TK, Tyagi JS, et al. (2006) Expression of mycobacterial cell division protein, FtsZ, and dormancy proteins, DevR and Acr, within lung granulomas throughout guinea pig infection. FEMS Immunol Med Microbiol 48: 329-336.
20. Tailleux L, Waddell SJ, Pelizzola M, Mortellaro A, Withers M, et al. (2008) Probing host pathogen cross-talk by transcriptional profiling of both Mycobacterium tuberculosis and infected human dendritic cells and macrophages. PLoS One 3: e1403.
21. Chauhan S, Tyagi JS (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.
22. Chauhan S, Tyagi JS (2008) Interaction of DevR with multiple binding sites synergistically activates divergent transcription of narK2-Rv1738 genes in Mycobacterium tuberculosis. J Bacteriol 190: 5394-5403.
23. Chauhan S, Tyagi JS (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.
24. Mitchison DA, Wallace JG, Bhatia AL, Selkon JB, Subbaiah TV, et al. (1960) A comparison of the virulence in guinea-pigs of South Indian and British tubercle bacilli. Tubercle 41: 1-22.
25. Mitchison DA, Bhatia AL, Radhakrishna S, Selkon JB, Subbaiah TV, et al. (1961) The virulence in the guinea-pig of tubercle bacilli isolated before treatment from South Indian patients with pulmonary tuberculosis. I. Homogeneity of the investigation and a critique of the virulence test. Bull World Health Organ 25: 285-312.
26. Behr MA, Wilson MA, Gill WP, Salamon H, Schoolnik GK, et al. (1999) Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 284: 1520-1523.
27. Rodrigue S, Brodeur J, Jacques PE, Gervais AL, Brzezinski R, et al. (2007) Identification of mycobacterial σ factor binding sites by chromatin immunoprecipitation assays. J Bacteriol 189: 1505-1513.
28. Bagchi G, Chauhan S, Sharma D, Tyagi JS (2005) Transcription and autoregulation of the Rv3134c-devR-devS operon of Mycobacterium tuberculosis. Microbiology 151: 4045-4053.
29. Saini DK, Pant N, Das TK, Tyagi JS (2002) Cloning, overexpression, purification, and matrix-assisted refolding of DevS (Rv 3132c) histidine protein kinase of Mycobacterium tuberculosis. Protein Expr Purif 25: 203-208.
30. Ramanathan VD, Jawahar MS, Paramasivan CN, Rajaram K, Chandrasekar K, et al. (1999) A histological spectrum of host responses in tuberculous lymphadenitis. Indian J Med Res 109: 212-220.
31. Lukey PT, Hooker EU (2001) Macrophage virulence assays. In: Parish T, Stoker NG, eds. Mycobacterium tuberculosis Protocols. Totowa, NJ: Humana Press. pp 271-280.
32. Chauhan A, Madiraju MV, Fol M, Lofton H, Maloney E, et al. (2006) Mycobacterium tuberculosis cells growing in macrophages are filamentous and deficient in FtsZ rings. J Bacteriol 188: 1856-1865.