Mycobacterium tuberculosis two-component systems and implications in novel vaccines and drugs

Critical Reviews in Eukaryotic Gene Expression

Volumn 22, Issue 1, 2012, Pages 37-52

  Zhou, Pei Fu ^a   Long, Quan Xin ^a   Zhou, Ye Xin ^a   Wang, Hong Hai ^b   Xie, Jian Ping ^a,b  

^a SOUTHWEST UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

Author keywords

Drug; Mycobacterium tuberculosis; Two component system; Vaccine

Indexed keywords

BACTERIAL PROTEIN; BCG VACCINE; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE;

ANALYTIC METHOD; BACTERIAL VIRULENCE; DNA MICROARRAY; DORMANCY; DRUG SAFETY; DRUG STABILITY; DRUG TARGETING; ENVIRONMENTAL FACTOR; FATTY ACID METABOLISM; HUMAN; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TWO COMPONENT SYSTEM;

EUKARYOTA; MYCOBACTERIUM TUBERCULOSIS;

EID: 84860341809     PISSN: 10454403     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevEukarGeneExpr.v22.i1.30     Document Type: Review

References (123)

1. WHO. GLOBAL TUBERCULOSIS CONTROL: WHO REPORT 2011. 2011.
2. Manganelli R, Provvedi R, Rodrigue S, Beaucher J, Gaudreau L, Smith I. Sigma factors and global gene regulation in Mycobacterium tuberculosis. J Bacteriol. 2004 Feb;186(4):895-902.
3. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature. 1998 Jun 11;393(6685):537-44.
4. Tekaia F, Gordon SV, Garnier T, Brosch R, Barrell BG, Cole ST. Analysis of the proteome of Mycobacterium tuberculosis in silico. Tuber Lung Dis. 1999;79(6):329-42.
5. Patricia A. Fontan SWaIS. Cellular signaling pathways and transcriptional regulation in Mycobacterium tuberculosis Stress control and virulence. CURRENT SCIENCE. 2004;86(01).
6. Daniel J. Bretl CDaTCZ. Adaptation to Environmental Stimuli within the Host: Two-Component Signal Transduction Systems of Mycobacterium tuberculosis. Microbiology and Molecular Biology Reviews. 2011;75(4):566-82.
7. Fol M, Chauhan A, Nair NK, Maloney E, Moomey M, Jagannath C, Madiraju MV, Rajagopalan M. Modulation of Mycobacterium tuberculosis proliferation by MtrA, an essential two-component response regulator. Mol Microbiol. 2006 May;60(3):643-57.
8. Via LE, Curcic R, Mudd MH, Dhandayuthapani S, Ulmer RJ, Deretic V. Elements of signal transduction in Mycobacterium tuberculosis: in vitro phosphorylation and in vivo expression of the response regulator MtrA. J Bacteriol. 1996 Jun;178(11):3314-21.
9. Zahrt TC, Deretic V. An essential two-component signal transduction system in Mycobacterium tuberculosis. J Bacteriol. 2000 Jul;182(13):3832-8.
10. Maha Al Zayer DS, Renata Dziedzic, Krishna Sarva, Murty V. Madiraju,Malini Rajagopalan Mycobacterium tuberculosis mtrA merodiploid strains with point mutations in the signal-receiving domain of MtrA exhibit growth defects in nutrient broth. Plasmid. 2011.
11. Li Y, Zeng J, Zhang H, He ZG. The characterization of conserved binding motifs and potential target genes for M. tuberculosis MtrAB reveals a link between the twocomponent system and the drug resistance of M. smegmatis. BMC Microbiol. 2010;10:242.
12. Rajagopalan M, Dziedzic R, Al Zayer M, Stankowska D, Ouimet MC, Bastedo DP, Marczynski GT, Madiraju MV. The Mycobacterium tuberculosis origin of replication and the promoter for immunodominant secreted antigen 85B are the targets of MtrA, the essential response regulator. J Biol Chem. 2010 Mar 11.
13. Sassetti CM, Boyd DH, Rubin EJ. Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol. 2003 Apr;48(1):77-84.
14. Zhang M, Yue J, Yang YP, Zhang HM, Lei JQ, Jin RL, Zhang XL, Wang HH. Detection of mutations associated with isoniazid resistance in Mycobacterium tuberculosis isolates from China. J Clin Microbiol. 2005 Nov;43(11):5477-82.
15. Colangeli R, Helb D, Sridharan S, Sun J, Varma-Basil M, Hazbon MH, Harbacheuski R, Megjugorac NJ, Jacobs WR, Jr., Holzenburg A, Sacchettini JC, Alland D. The Mycobacterium tuberculosis iniA gene is essential for activity of an efflux pump that confers drug tolerance to both isoniazid and ethambutol. Mol Microbiol. 2005 Mar;55(6):1829-40.
16. Brocker M, Mack C, Bott M. Target genes, consensus binding site, and role of phosphorylation for the response regulator MtrA of Corynebacterium glutamicum. J Bacteriol. 2011 Mar;193(5):1237-49.
17. Nguyen HT, Wolff KA, Cartabuke RH, Ogwang S, Nguyen L. A Lipoprotein Modulates Activity of the MtrAB Two-Component System to Provide Intrinsic Multidrug Resistance, Cytokinetic Control and Cell Wall Homeostasis in Mycobacterium. Mol Microbiol. 2010 Mar 10.
18. Singh KK, Zhang X, Patibandla AS, Chien P, Jr., Laal S. Antigens of Mycobacterium tuberculosis expressed during preclinical tuberculosis: serological immunodominance of proteins with repetitive amino acid sequences. Infect Immun. 2001 Jun;69(6):4185-91.
19. Raghavan S, Manzanillo P, Chan K, Dovey C, Cox JS. Secreted transcription factor controls Mycobacterium tuberculosis virulence. Nature. 2008 Aug 7;454(7205):717-21
20. Ludwiczak P, Gilleron M, Bordat Y, Martin C, Gicquel B, Puzo G. Mycobacterium tuberculosis phoP mutant: lipoarabinomannan molecular structure. Microbiology. 2002 Oct;148(Pt 10):3029-37.
21. Nigou J, Zelle-Rieser C, Gilleron M, Thurnher M, Puzo G. Mannosylated lipoarabinomannans inhibit IL-12 production by human dendritic cells: evidence for a negative signal delivered through the mannose receptor. J Immunol. 2001 Jun 15;166(12):7477-85.
22. Gonzalo Asensio J, Maia C, Ferrer NL, Barilone N, Laval F, Soto CY, Winter N, Daffe M, Gicquel B, Martin C, Jackson M. The virulence-associated two-component PhoP-PhoR system controls the biosynthesis of polyketide-derived lipids in Mycobacterium tuberculosis. J Biol Chem. 2006 Jan 20;281(3):1313-6.
23. Gonzalo-Asensio J, Mostowy S, Harders-Westerveen J, Huygen K, Hernandez-Pando R, Thole J, Behr M, Gicquel B, Martin C. PhoP: a missing piece in the intricate puzzle of Mycobacterium tuberculosis virulence. PLoS One. 2008;3(10):e3496.
24. Xu J, Laine O, Masciocchi M, Manoranjan J, Smith J, Du SJ, Edwards N, Zhu X, Fenselau C, Gao LY. A unique Mycobacterium ESX-1 protein co-secretes with CFP-10/ ESAT-6 and is necessary for inhibiting phagosome maturation. Mol Microbiol. 2007 Nov;66(3):787-800.
25. Glover RT, Kriakov J, Garforth SJ, Baughn AD, Jacobs WR, Jr. The two-component regulatory system senX3regX3 regulates phosphate-dependent gene expression in Mycobacterium smegmatis. J Bacteriol. 2007 Aug;189(15):5495-503.
26. Gebhard S, Cook GM. Differential regulation of highaffinity phosphate transport systems of Mycobacterium smegmatis: identification of PhnF, a repressor of the phnDCE operon. J Bacteriol. 2008 Feb;190(4):1335-43.
27. Rifat D, Bishai WR, Karakousis PC. Phosphate depletion: a novel trigger for Mycobacterium tuberculosis persistence. J Infect Dis. 2009 Oct 1;200(7):1126-35.
28. Jiang X, Zhang W, Gao F, Huang Y, Lv C, Wang H. Comparison of the proteome of isoniazid-resistant and -susceptible strains of Mycobacterium tuberculosis. Microb Drug Resist. 2006 Winter;12(4):231-8.
29. Sureka K, Dey S, Datta P, Singh AK, Dasgupta A, Rodrigue S, Basu J, Kundu M. Polyphosphate kinase is involved in stress-induced mprAB-sigE-rel signalling in mycobacteria. Mol Microbiol. 2007 Jul;65(2):261-76.
30. Primm TP AS, Mizrahi V, Avarbock D, Rubin H, Barry CE 3rd. The stringent response of Mycobacterium tuberculosis is required for long-term survival. J Bacteriol 2000;182(17):4889-98.
31. Dahl JL, Kraus CN, Boshoff HI, Doan B, Foley K, Avarbock D, Kaplan G, Mizrahi V, Rubin H, Barry CE, 3rd. 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. 2003 Aug 19;100(17):10026-31.
32. Wu J, Long Q, Xie J. (p)ppGpp and drug resistance. J Cell Physiol. 2010 Aug;224(2):300-4.
33. Rickman L, Saldanha JW, Hunt DM, Hoar DN, Colston MJ, Millar JB, Buxton RS. 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. 2004 Jan 30;314(1):259-67.
34. Supply P, Magdalena J, Himpens S, Locht C. Identification of novel intergenic repetitive units in a mycobacterial two-component system operon. Mol Microbiol. 1997 Dec;26(5):991-1003.
35. Magdalena J, Vachee A, Supply P, Locht C. Identification of a new DNA region specific for members of Mycobacterium tuberculosis complex. J Clin Microbiol. 1998 Apr;36(4):937-43.
36. Aminian M, Shabbeer A, Bennett KP. Determination of Major Lineages of Mycobacterium tuberculosis Complex using Mycobacterial Interspersed Repetitive Units. Proceedings (IEEE Int Conf Bioinformatics Biomed). 2009 Nov 1;2009:338-43.
37. Shrivastava R, Das DR, Wiker HG, Das AK. Functional insights from the molecular modelling of a novel two component system. Biochem Biophys Res Commun. 2006 Jun 16;344(4):1327-33.
38. Shrivastava R, Ghosh AK, Das AK. Probing the nucleotide binding and phosphorylation by the histidine kinase of a novel three-protein two-component system from Mycobacterium tuberculosis. FEBS Lett. 2007 May 1;581(9):1903-9.
39. Shrivastava R, Ghosh AK, Das AK. Intraand intermolecular domain interactions among novel two-component system proteins coded by Rv0600c, Rv0601c and Rv0602c of Mycobacterium tuberculosis. Microbiology. 2009 Mar;155(Pt 3):772-9.
40. Chao JD, Papavinasasundaram KG, Zheng X, ChavezSteenbock A, Wang X, Lee GQ, Av-Gay Y. Convergence of Ser/Thr and two-component signaling to coordinate expression of the dormancy regulon in Mycobacterium tuberculosis. J Biol Chem. 2010 Sep 17;285(38):29239-46.
41. Dasgupta N, Kapur V, Singh KK, Das TK, Sachdeva S, Jyothisri K, Tyagi JS. Characterization of a two-component system, devR-devS, of Mycobacterium tuberculosis. Tuber Lung Dis. 2000;80(3):141-59.
42. Cho HY, Cho HJ, Kim YM, Oh JI, Kang BS. Structural insight into the heme-based redox sensing by DosS from Mycobacterium tuberculosis. J Biol Chem. 2009 May 8;284(19):13057-67.
43. Podust LM, Ioanoviciu A, Ortiz de Montellano PR. 2.3 A X-ray structure of the heme-bound GAF domain of sensory histidine kinase DosT of Mycobacterium tuberculosis. Biochemistry. 2008 Nov 25;47(47):12523-31.
44. Yukl ET, Ioanoviciu A, Sivaramakrishnan S, Nakano MM, Ortiz de Montellano PR, Moenne-Loccoz P. Nitric oxide dioxygenation reaction in DevS and the initial response to nitric oxide in Mycobacterium tuberculosis. Biochemistry. 2011 Feb 15;50(6):1023-8.
45. Honaker RW, Leistikow RL, Bartek IL, Voskuil MI. Unique roles of DosT and DosS in DosR regulon induction and Mycobacterium tuberculosis dormancy. Infect Immun. 2009 Aug;77(8):3258-63.
46. Kim MJ, Park KJ, Ko IJ, Kim YM, Oh JI. Different roles of DosS and DosT in the hypoxic adaptation of Mycobacteria. J Bacteriol. 2010 Oct;192(19):4868-75.
47. Ioanoviciu A, Meharenna YT, Poulos TL, Ortiz de Montellano PR. DevS oxy complex stability identifies this heme protein as a gas sensor in Mycobacterium tuberculosis dormancy. Biochemistry. 2009 Jun 30;48(25):5839-48.
48. Sousa EH, Tuckerman JR, Gonzalez G, Gilles-Gon-zalez MA. DosT and DevS are oxygen-switched kinases in Mycobacterium tuberculosis. Protein Sci. 2007 Aug;16(8):1708-19.
49. Shiloh MU, Manzanillo P, Cox JS. Mycobacterium tuberculosis senses host-derived carbon monoxide during macrophage infection. Cell Host Microbe. 2008 May 15;3(5):323-30.
50. Taneja NK, Dhingra S, Mittal A, Naresh M, Tyagi JS. Mycobacterium tuberculosis transcriptional adaptation, growth arrest and dormancy phenotype development is triggered by vitamin C. PLoS One. 2010;5(5):e10860.
51. Reed MB, Gagneux S, Deriemer K, Small PM, Barry CE, 3rd. The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J Bacteriol. 2007 Apr;189(7):2583-9.
52. Badillo-Lopez C, Gonzalez-Mejia A, Helguera-Repetto AC, Salas-Rangel LP, Rivera-Gutierrez S, Cerna-Cortes JF, Gonzalez YMJA. Differential expression of dnaA and dosR genes among members of the Mycobacterium tuberculosis complex under oxic and hypoxic conditions. Int Microbiol. 2010 Mar;13(1):9-13.
53. Domenech P, Kolly GS, Leon-Solis L, Fallow A, Reed MB. Massive gene duplication event among clinical isolates of the Mycobacterium tuberculosis W/Beijing family. J Bacteriol. 2010 Sep;192(18):4562-70.
54. Leyten EM, Lin MY, Franken KL, Friggen AH, Prins C, van Meijgaarden KE, Voskuil MI, Weldingh K, Andersen P, Schoolnik GK, Arend SM, Ottenhoff TH, Klein MR. Human T-cell responses to 25 novel antigens encoded by genes of the dormancy regulon of Mycobacterium tuberculosis. Microbes Infect. 2006 Jul;8(8):2052-60.
55. Roupie V, Romano M, Zhang L, Korf H, Lin MY, Franken KL, Ottenhoff TH, Klein MR, Huygen K. Immunogenicity of eight dormancy regulon-encoded proteins of Mycobacterium tuberculosis in DNA-vaccinated and tuberculosis-infected mice. Infect Immun. 2007 Feb;75(2):941-9.
56. Black GF, Thiel BA, Ota MO, Parida SK, Adegbola R, Boom WH, Dockrell HM, Franken KL, Friggen AH, Hill PC, Klein MR, Lalor MK, Mayanja H, Schoolnik G, Stanley K, Weldingh K, Kaufmann SH, Walzl G, Ottenhoff TH. Immunogenicity of novel DosR regulon-encoded candidate antigens of Mycobacterium tuberculosis in three high-burden populations in Africa. Clin Vaccine Immunol. 2009 Aug;16(8):1203-12.
57. Goletti D, Butera O, Vanini V, Lauria FN, Lange C, Franken KL, Angeletti C, Ottenhoff TH, Girardi E. Response to Rv2628 latency antigen associates with cured tuberculosis and remote infection. Eur Respir J. 2010 Jul;36(1):135-42.
58. Chakravorty S, Sen MK, Tyagi JS. Diagnosis of extrapulmonary tuberculosis by smear, culture, and PCR using universal sample processing technology. J Clin Microbiol. 2005 Sep;43(9):4357-62.
59. Chakravorty S, Pathak D, Dudeja M, Haldar S, Hanif M, Tyagi JS. PCR amplification of shorter fragments from the devR (Rv3133c) gene significantly increases the sensitivity of tuberculosis diagnosis. FEMS Microbiol Lett. 2006 Apr;257(2):306-11.
60. Obozova TA AeM, Baranovskiǐ PM, Smetanina SE, Kiselev VI. Correlation between the expression of Rv3286c, Rv2626c, Rv2031c, AND Rv3133c and the tolerance of Mycobacterium bovis BCG to rifampicin and metronidazole in different physiological conditions. Probl Tuberk Bolezn Legk 2005;2:34-6.
61. Roberts DM, Liao RP, Wisedchaisri G, Hol WG, Sherman DR. Two sensor kinases contribute to the hypoxic response of Mycobacterium tuberculosis. J Biol Chem. 2004 May 28;279(22):23082-7.
62. Kumar A, Deshane JS, Crossman DK, Bolisetty S, Yan BS, Kramnik I, Agarwal A, Steyn AJ. Heme oxygenase1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J Biol Chem. 2008 Jun 27;283(26):18032-9.
63. Leistikow RL, Morton RA, Bartek IL, Frimpong I, Wagner K, Voskuil MI. The Mycobacterium tuberculosis DosR regulon assists in metabolic homeostasis and enables rapid recovery from non-respiring dormancy. J Bacteriol. 2009 Dec 18.
64. Zahrt TC, Deretic V. Mycobacterium tuberculosis signal transduction system required for persistent infections. Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12706-11.
65. He H, Zahrt TC. Identification and characterization of a regulatory sequence recognized by Mycobacterium tuberculosis persistence regulator MprA. J Bacteriol. 2005 Jan;187(1):202-12.
66. Clausen T, Southan C, Ehrmann M. The HtrA family of proteases: implications for protein composition and cell fate. Mol Cell. 2002 Sep;10(3):443-55.
67. Pang X, Howard ST. Regulation of the alpha-crystallin gene acr2 by the MprAB two-component system of Mycobacterium tuberculosis. J Bacteriol. 2007 Sep;189(17):6213-21.
68. He H, Hovey R, Kane J, Singh V, Zahrt TC. MprAB is a stress-responsive two-component system that directly regulates expression of sigma factors SigB and SigE in Mycobacterium tuberculosis. J Bacteriol. 2006 Mar;188(6):2134-43.
69. Ohara N, Naito M, Miyazaki C, Matsumoto S, Tabira Y, Yamada T. HrpA, a new ribosome-associated protein which appears in heat-stressed Mycobacterium bovis bacillus Calmette-Guerin. J Bacteriol. 1997 Oct;179(20):6495-8.
70. Tiwari A, Balazsi G, Gennaro ML, Igoshin OA. The interplay of multiple feedback loops with post-translational kinetics results in bistability of mycobacterial stress response. Phys Biol. 2010;7(3):036005.
71. Barik S, Sureka K, Mukherjee P, Basu J, Kundu M. RseA, the SigE specific anti-sigma factor of Mycobacterium tu- berculosis, is inactivated by phosphorylation-dependent ClpC1P2 proteolysis. Mol Microbiol. 2009 Dec 16.
72. Pang X, Vu P, Byrd TF, Ghanny S, Soteropoulos P, Mukamolova GV, Wu S, Samten B, Howard ST. Evidence for complex interactions of stress-associated regulons in an mprAB deletion mutant of Mycobacterium tuberculosis. Microbiology. 2007 Apr;153(Pt 4):1229-42.
73. Sureka K, Ghosh B, Dasgupta A, Basu J, Kundu M, Bose I. Positive feedback and noise activate the stringent response regulator rel in mycobacteria. PLoS One. 2008;3(3):e1771.
74. Dahl JL BD. The wag31 gene of Mycobacterium tuberculosis is positively regulated by the stringent response. FEMS Microbiol Lett. 2011.
75. Kang CM, Abbott DW, Park ST, Dascher CC, Cantley LC, Husson RN. The Mycobacterium tuberculosis serine/threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes Dev. 2005 Jul 15;19(14):1692-704.
76. Kang CM, Nyayapathy S, Lee JY, Suh JW, Husson RN. Wag31, a homologue of the cell division protein DivIVA, regulates growth, morphology and polar cell wall synthesis in mycobacteria. Microbiology. 2008 Mar;154(Pt 3):725-35.
77. Hamasha K, Sahana MB, Jani C, Nyayapathy S, Kang CM, Rehse SJ. The effect of Wag31 phosphorylation on the cells and the cell envelope fraction of wild-type and conditional mutants of Mycobacterium smegmatis studied by visible-wavelength Raman spectroscopy. Biochem Biophys Res Commun. 2010 Jan 1;391(1):664-8.
78. Jani C, Eoh H, Lee JJ, Hamasha K, Sahana MB, Han JS, Nyayapathy S, Lee JY, Suh JW, Lee SH, Rehse SJ, Crick DC, Kang CM. Regulation of polar peptidoglycan biosynthesis by Wag31 phosphorylation in mycobacteria. BMC Microbiol. 2010;10:327.
79. Mukherjee P, Sureka K, Datta P, Hossain T, Barik S, Das KP, Kundu M, Basu J. Novel role of Wag31 in protection of mycobacteria under oxidative stress. Mol Microbiol. 2009 Jul;73(1):103-19.
80. Cao W, Tang S, Yuan H, Wang H, Zhao X, Lu H. Mycobacterium tuberculosis antigen Wag31 induces expression of C-chemokine XCL2 in macrophages. Curr Microbiol. 2008 Sep;57(3):189-94.
81. White MJ, He H, Penoske RM, Twining SS, Zahrt TC. PepD participates in the Mycobacterial stress response mediated through MprAB and SigE. J Bacteriol. 2010 Jan 8.
82. Parish T, Smith DA, Kendall S, Casali N, Bancroft GJ, Stoker NG. Deletion of two-component regulatory systems increases the virulence of Mycobacterium tuberculosis. Infect Immun. 2003 Mar;71(3):1134-40.
83. Steyn AJ, Joseph J, Bloom BR. Interaction of the sensor module of Mycobacterium tuberculosis H37Rv KdpD with members of the Lpr family. Mol Microbiol. 2003 Feb;47(4):1075-89.
84. Haydel SE, Benjamin WH, Jr., Dunlap NE, Clark-Curtiss JE. Expression, autoregulation, and DNA binding properties of the Mycobacterium tuberculosis TrcR response regulator. J Bacteriol. 2002 Apr;184(8):2192-203.
85. Haydel SE, Clark-Curtiss JE. The Mycobacterium tuberculosis TrcR response regulator represses transcription of the intracellularly expressed Rv1057 gene, encoding a seven-bladed beta-propeller. J Bacteriol. 2006 Jan;188(1):150-9.
86. Wernisch L, Kendall SL, Soneji S, Wietzorrek A, Parish T, Hinds J, Butcher PD, Stoker NG. Analysis of wholegenome microarray replicates using mixed models. Bioinformatics. 2003 Jan;19(1):53-61.
87. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, Monahan IM, Dolganov G, Efron B, Butcher PD, Nathan C, Schoolnik GK. Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. J Exp Med. 2003 Sep 1;198(5):693-704.
88. Bhattacharya M, Biswas A, Das AK. Interaction analysis of TcrX/Y two component system from Mycobacterium tuberculosis. Biochimie. 2009 Dec 3.
89. Graham JE, Clark-Curtiss JE. Identification of Mycobacterium tuberculosis RNAs synthesized in response to phagocytosis by human macrophages by selective capture of transcribed sequences (SCOTS). Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11554-9.
90. Haydel SE, Malhotra V, Cornelison GL, Clark-Curtiss JE. The prrAB two-component system is essential for Mycobacterium tuberculosis viability and is induced during nitrogen-limiting conditions. J Bacteriol. 2011 Nov
91. Morth JP, Gosmann S, Nowak E, Tucker PA. A novel two-component system found in Mycobacterium tuberculosis. FEBS Lett. 2005 Aug 1;579(19):4145-8.
92. Morth JP, Feng V, Perry LJ, Svergun DI, Tucker PA. The crystal and solution structure of a putative transcriptional antiterminator from Mycobacterium tuberculosis. Structure. 2004 Sep;12(9):1595-605.
93. Martin C, Williams A, Hernandez-Pando R, Cardona PJ, Gormley E, Bordat Y, Soto CY, Clark SO, Hatch GJ, Aguilar D, Ausina V, Gicquel B. The live Mycobacterium tuberculosis phoP mutant strain is more attenuated than BCG and confers protective immunity against tuberculosis in mice and guinea pigs. Vaccine. 2006 Apr 24;24(17):3408-19.
94. Aguilar D, Infante E, Martin C, Gormley E, Gicquel B, Hernandez Pando R. Immunological responses and protective immunity against tuberculosis conferred by vaccination of Balb/C mice with the attenuated Mycobacterium tuberculosis (phoP) SO2 strain. Clin Exp Immunol. 2007 Feb;147(2):330-8.
95. Cardona PJ, Asensio JG, Arbues A, Otal I, Lafoz C, Gil O, Caceres N, Ausina V, Gicquel B, Martin C. Extended safety studies of the attenuated live tuberculosis vaccine SO2 based on phoP mutant. Vaccine. 2009 Apr 21;27(18):2499-505.
96. Ferrer NL, Gomez AB, Soto CY, Neyrolles O, Gicquel B, Garcia-Del Portillo F, Martin C. Intracellular replication of attenuated Mycobacterium tuberculosis phoP mutant in the absence of host cell cytotoxicity. Microbes Infect. 2009 Jan;11(1):115-22.
97. Verreck FA, Vervenne RA, Kondova I, van Kralingen KW, Remarque EJ, Braskamp G, van der Werff NM, Kersbergen A, Ottenhoff TH, Heidt PJ, Gilbert SC, Gicquel B, Hill AV, Martin C, McShane H, Thomas AW. MVA.85A boosting of BCG and an attenuated, phoP deficient M. tuberculosis vaccine both show protective efficacy against tuberculosis in rhesus macaques. PLoS One. 2009;4(4):e5264.
98. Matsushita M, Janda KD. Histidine kinases as targets for new antimicrobial agents. Bioorg Med Chem. 2002 Apr;10(4):855-67.
99. Gupta RK, Thakur TS, Desiraju GR, Tyagi JS. Structure based design of DevR inhibitor active against nonreplicating Mycobacterium tuberculosis. J Med Chem. 2009 Oct 22;52(20):6324-34.
100. Li Y, Zeng J, He ZG. Characterization of a functional C-terminus of the Mycobacterium tuberculosis MtrA responsible for both DNA binding and interaction with its two-component partner protein, MtrB. J Biochem. 2010 Nov;148(5):549-56.
101. Gupta S, Sinha A, Sarkar D. Transcriptional autoregulation by Mycobacterium tuberculosis PhoP involves recognition of novel direct repeat sequences in the regulatory region of the promoter. FEBS Lett. 2006 Oct 2;580(22):5328-38.
102. Walters SB, Dubnau E, Kolesnikova I, Laval F, Daffe M, Smith I. The Mycobacterium tuberculosis PhoPR two-component system regulates genes essential for virulence and complex lipid biosynthesis. Mol Microbiol. 2006 Apr;60(2):312-30.
103. Frigui W, Bottai D, Majlessi L, Monot M, Josselin E, Brodin P, Garnier T, Gicquel B, Martin C, Leclerc C, Cole ST, Brosch R. Control of M. tuberculosis ESAT-6 secretion and specific T cell recognition by PhoP. PLoS Pathog. 2008 Feb 8;4(2):e33.
104. Ferrer NL, Gomez AB, Neyrolles O, Gicquel B, Martin C. Interactions of attenuated Mycobacterium tuberculosis phoP mutant with human macrophages. PLoS One. 2010;5(9):e12978.
105. Soto CY, Menendez MC, Perez E, Samper S, Gomez AB, Garcia MJ, Martin C. IS6110 mediates increased transcription of the phoP virulence gene in a multidrugresistant clinical isolate responsible for tuberculosis outbreaks. J Clin Microbiol. 2004 Jan;42(1):212-9.
106. Wang S, Engohang-Ndong J, Smith I. Structure of the DNA-binding domain of the response regulator PhoP from Mycobacterium tuberculosis. Biochemistry. 2007 Dec 25;46(51):14751-61.
107. Perez E, Samper S, Bordas Y, Guilhot C, Gicquel B, Martin C. An essential role for phoP in Mycobacterium tuberculosis virulence. Mol Microbiol. 2001 Jul;41(1):179-87.
108. Roberts G, Vadrevu IS, Madiraju MV, Parish T. Control of CydB and GltA1 Expression by the SenX3 RegX3 Two Component Regulatory System of Mycobacterium tuberculosis. PLoS One. 2011;6(6):e21090.
109. Himpens S, Locht C, Supply P. Molecular characterization of the mycobacterial SenX3-RegX3 two-component system: evidence for autoregulation. Microbiology. 2000 Dec;146 Pt 12:3091-8.
110. Parish T, Smith DA, Roberts G, Betts J, Stoker NG. The senX3-regX3 two-component regulatory system of Mycobacterium tuberculosis is required for virulence. Microbiology. 2003 Jun;149(Pt 6):1423-35.
111. Florczyk MA, McCue LA, Purkayastha A, Currenti E, Wolin MJ, McDonough KA. A family of acr-coregulated Mycobacterium tuberculosis genes shares a common DNA motif and requires Rv3133c (dosR or devR) for expression. Infect Immun. 2003 Sep;71(9):5332-43.
112. Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, Tompa M, Schoolnik GK, Sherman DR. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol. 2003 May;48(3):833-43.
113. Vasudeva-Rao HM, McDonough KA. Expression of the Mycobacterium tuberculosis acr-coregulated genes from the DevR (DosR) regulon is controlled by multiple levels of regulation. Infect Immun. 2008 Jun;76(6):2478-89.
114. Chauhan S, Tyagi JS. 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. 2008 Jun;190(12):4301-12.
115. Chauhan S, Tyagi JS. 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. 2009 Oct;191(19):6075-81.
116. Bagchi G, Chauhan S, Sharma D, Tyagi JS. Transcription and autoregulation of the Rv3134c-devR-devS operon of Mycobacterium tuberculosis. Microbiology. 2005 Dec;151(Pt 12):4045-53.
117. Malhotra V, Sharma D, Ramanathan VD, Shakila H, Saini DK, Chakravorty S, Das TK, Li Q, Silver RF, Narayanan PR, Tyagi JS. Disruption of response regulator gene, devR, leads to attenuation in virulence of Mycobacterium tuberculosis. FEMS Microbiol Lett. 2004 Feb 16;231(2):237-45.
118. Converse PJ, Karakousis PC, Klinkenberg LG, Kesavan AK, Ly LH, Allen SS, Grosset JH, Jain SK, Lamichhane G, Manabe YC, McMurray DN, Nuermberger EL, Bishai WR. Role of the dosR-dosS two-component regulatory system in Mycobacterium tuberculosis virulence in three animal models. Infect Immun. 2009 Mar;77(3):1230-7.
119. Zahrt TC, Wozniak C, Jones D, Trevett A. Functional analysis of the Mycobacterium tuberculosis MprAB twocomponent signal transduction system. Infect Immun. 2003 Dec;71(12):6962-70.
120. Pang X, Cao G, Neuenschwander PF, Haydel SE, Hou G, Howard ST. The beta-propeller gene Rv1057 of Mycobacterium tuberculosis has a complex promoter directly regulated by both the MprAB and TrcRS two-component systems. Tuberculosis (Edinb). 2011 Nov 16.
121. Ewann F, Locht C, Supply P. Intracellular autoregulation of the Mycobacterium tuberculosis PrrA response regulator. Microbiology. 2004 Jan;150(Pt 1):241-6.
122. Ewann F, Jackson M, Pethe K, Cooper A, Mielcarek N, Ensergueix D, Gicquel B, Locht C, Supply P. Transient requirement of the PrrA-PrrB two-component system for early intracellular multiplication of Mycobacterium tuberculosis. Infect Immun. 2002 May;70(5):2256-63.
123. Haydel SE, Dunlap NE, Benjamin WH, Jr. In vitro evidence of two-component system phosphorylation between the Mycobacterium tuberculosis TrcR/TrcS proteins. Microb Pathog. 1999 Apr;26(4):195-206.