PhoP: A missing piece in the intricate puzzle of Mycobacterium tuberculosis virulence

PLoS ONE

Volumn 3, Issue 10, 2008, Pages

  Gonzalo Asensio, Jesús ^a,h   Mostowy, Serge ^b,g   Harders Westerveen, Jose ^c   Huygen, Kris ^d   Hernández Pando, Rogelio ^e   Thole, Jelle ^f   Behr, Marcel ^b   Gicquel, Brigitte ^g   Martín, Carlos ^a,h  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b MONTREAL GENERAL HOSPITAL   (Canada)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d PASTEUR INSTITUTE OF BRUSSELS   (Belgium)

^e INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

^f Tubercolosis Vaccine Initiative   (Netherlands)

^g INSTITUT PASTEUR   (France)

^h INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; EARLY SECRETORY ANTIGENIC TARGET 6; ISOCITRATE LYASE; PHOP PROTEIN; SO2 PHOP VACCINE; UNCLASSIFIED DRUG; VACCINE; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; ESAT 6 PROTEIN, MYCOBACTERIUM TUBERCULOSIS; ESAT-6 PROTEIN, MYCOBACTERIUM TUBERCULOSIS; PHOP PROTEIN, BACTERIA; VIRULENCE FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGENICITY; ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; ENZYME INACTIVATION; ENZYME REGULATION; LIPID METABOLISM; LIPOGENESIS; MICROBIAL ATTENUATION; MOUSE; MUTANT; MYCOBACTERIOSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEOMICS; STRESS; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; ANIMAL; ANIMAL DISEASE; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; CELL HYPOXIA; CLUSTER ANALYSIS; COMPARATIVE STUDY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; OXIDATIVE STRESS; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; SECRETION; TUBERCULOSIS;

MYCOBACTERIUM TUBERCULOSIS;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BCG VACCINE; CELL HYPOXIA; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; LIPID METABOLISM; MICE; MICE, INBRED BALB C; MODELS, BIOLOGICAL; MYCOBACTERIUM TUBERCULOSIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; PROTEOMICS; TUBERCULOSIS; VIRULENCE FACTORS;

EID: 55649113699     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003496     Document Type: Article

References (65)

1. Rohde K, Yates RM, Purdy GE, Russell DG (2007) Mycobacterium tuberculosis and the environment within the phagosome. Immunol Rev 219: 37-54.
2. Wayne LG, Sohaskey CD (2001) Nonreplicating persistence of Mycobacterium tuberculosis. Annu Rev Microbiol 55: 139-163.
3. Boshoff HI, Barry CE 3rd (2005) Tuberculosis - metabolism and respiration in the absence of growth. Nat Rev Microbiol 3: 70-80.
4. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, et al. (2003) Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. J Exp Med 198: 693-704.
5. Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, et al. (2001) Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha-crystallin. Proc Natl Acad Sci U S A 98: 7534-7539.
6. Voskuil MI, Visconti KC, Schoolnik GK (2004) Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis (Edinb) 84: 218-227.
7. Rustad TR, Harrell MI, Liao R, Sherman DR (2008) The enduring hypoxic response of Mycobacterium tuberculosis. PLoS ONE 3: e1502.
8. Rohde KH, Abramovitch RB, Russell DG (2007) Mycobacterium tuberculosis invasion of macrophages: linking bacterial gene expression to environmental cues. Cell Host Microbe 2: 352-364.
9. Fontan P, Aris V, Ghanny S, Soteropoulos P, Smith I (2008) Global transcriptional profile of Mycobacterium tuberculosis during THP-1 human macrophage infection. Infect Immun 76: 717-725.
10. 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.
11. Perez E, Samper S, Bordas Y, Guilhot C, Gicquel B, et al. (2001) An essential role for phoP in Mycobacterium tuberculosis virulence. Mol Microbiol 41: 179-187.
12. Martin C, Williams A, Hernandez-Pando R, Cardona PJ, Gormley E, et al. (2006) The live Mycobacterium tuberculosis phoP mutant strain is more attenuated than BCG and confers protective immunity against tuberculosis in mice and guinea pigs. Vaccine 24: 3408-3419.
13. Chesne-Seck ML, Barilone N, Boudou F, Gonzalo Asensio J, Kolattukudy PE, et al. (2008) A point mutation in the two-component regulator PhoP-PhoR accounts for the absence of polyketide-derived acyltrehaloses but not that of phthiocerol dimycocerosates in Mycobacterium tuberculosis H37Ra. J Bacteriol 190: 1329-1334.
14. Frigui W, Bottai D, Majlessi L, Monot M, Josselin E, et al. (2008) Control of M. tuberculosis ESAT-6 Secretion and Specific T Cell Recognition by PhoP. PLoS Pathog 4: e33.
15. Lee JS, Krause R, Schreiber J, Mollenkopf HJ, Kowall J, et al. (2008) Mutation in the transcriptional regulator PhoP contributes to avirulence of Mycobacterium tuberculosis H37Ra strain. Cell Host Microbe 3: 97-103.
16. Gonzalo Asensio J, Maia C, Ferrer NL, Barilone N, Laval F, et al. (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.
17. Gonzalo-Asensio J, Soto CY, Arbues A, Sancho J, Menendez MD, et al. (2008) Mycobacterium tuberculosis phoPR operon is positively autoregulated in the virulent strain H37Rv. J Bacteriol.
18. 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.
19. 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.
20. Kumar A, Toledo JC, Patel RP, Lancaster JR Jr, Steyn AJ (2007) Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc Natl Acad Sci U S A 104: 11568-11573.
21. Shiloh MU, Manzanillo P, Cox JS (2008) Mycobacterium tuberculosis senses host-derived carbon monoxide during macrophage infection. Cell Host Microbe 3: 323-330.
22. Kinger AK, Tyagi JS (1993) Identification and cloning of genes differentially expressed in the virulent strain of Mycobacterium tuberculosis. Gene 131: 113-117.
23. 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.
24. Waddell SJ, Butcher PD (2007) Microarray analysis of whole genome expression of intracellular Mycobacterium tuberculosis. Curr Mol Med 7: 287-296.
25. Velmurugan K, Chen B, Miller JL, Azogue S, Gurses S, et al. (2007) Mycobacterium tuberculosis nuoG Is a Virulence Gene That Inhibits Apoptosis of Infected Host Cells. PLoS Pathog 3: e110.
26. Winau F, Hegasy G, Kaufmann SH, Schaible UE (2005) No life without death-apoptosis as prerequisite for T cell activation. Apoptosis 10: 707-715.
27. Hutter B, Dick T (1998) Increased alanine dehydrogenase activity during dormancy in Mycobacterium smegmatis. FEMS Microbiol Lett 167: 7-11.
28. Wayne LG, Hayes LG (1998) Nitrate reduction as a marker for hypoxic shiftdown of Mycobacterium tuberculosis. Tuber Lung Dis 79: 127-132.
29. Pym AS, Brodin P, Brosch R, Huerre M, Cole ST (2002) Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 46: 709-717.
30. 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.
31. Brodin P, Majlessi L, Marsollier L, de Jonge MI, Bottai D, et al. (2006) Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect Immun 74: 88-98.
32. Guinn KM, Hickey MJ, Mathur SK, Zakel KL, Grotzke JE, et al. (2004) Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis. Mol Microbiol 51: 359-370.
33. Stanley SA, Raghavan S, Hwang WW, Cox JS (2003) Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc Natl Acad Sci U S A 100: 13001-13006.
34. McLaughlin B, Chon JS, MacGurn JA, Carlsson F, Cheng TL, et al. (2007) A Mycobacterium ESX-1-secreted virulence factor with unique requirements for export. PLoS Pathog 3: e105.
35. Xu J, Laine O, Masciocchi M, Manoranjan J, Smith J, et al. (2007) A unique Mycobacterium ESX-1 protein co-secretes with CFP-10/ESAT-6 and is necessary for inhibiting phagosome maturation. Mol Microbiol 66: 787-800.
36. Raghavan S, Manzanillo P, Chan K, Dovey C, Cox JS (2008) Secreted transcription factor controls Mycobacterium tuberculosis virulence. Nature 454: 717-721.
37. Walters SB, Dubnau E, Kolesnikova I, Laval F, Daffe M, et al. (2006) The Mycobacterium tuberculosis PhoPR two-component system regulates genes essential for virulence and complex lipid biosynthesis. Mol Microbiol 60: 312-330.
38. Camacho LR, Ensergueix D, Perez E, Gicquel B, Guilhot C (1999) Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol 34: 257-267.
39. Gao Q, Kripke K, Arinc Z, Voskuil M, Small P (2004) Comparative expression studies of a complex phenotype: cord formation in Mycobacterium tuberculosis. Tuberculosis (Edinb) 84: 188-196.
40. Munoz-Elias EJ, Upton AM, Cherian J, McKinney JD (2006) Role of the methylcitrate cycle in Mycobacterium tuberculosis metabolism, intracellular growth, and virulence. Mol Microbiol 60: 1109-1122.
41. Upton AM, McKinney JD (2007) Role of the methylcitrate cycle in propionate metabolism and detoxification in Mycobacterium smegmatis. Microbiology 153: 3973-3982.
42. McKinney JD, Honer zu Bentrup K, Munoz-Elias EJ, Miczak A, Chen B, et al. (2000) Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406: 735-738.
43. Sharma V, Sharma S, Hoener zu Bentrup K, McKinney JD, Russell DG, et al. (2000) Structure of isocitrate lyase, a persistence factor of Mycobacterium tuberculosis. Nat Struct Biol 7: 663-668.
44. Skeiky YA, Sadoff JC (2006) Advances in tuberculosis vaccine strategies. Nat Rev Microbiol 4: 469-476.
45. 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.
46. Roupie V, Romano M, Zhang L, Korf H, Lin MY, et al. (2007) Immunogenicity of eight dormancy regulon-encoded proteins of Mycobacterium tuberculosis in DNA-vaccinated and tuberculosis-infected mice. Infect Immun 75: 941-949.
47. Honaker RW, Stewart A, Schittone S, Izzo A, Klein MR, et al. (2008) BCG vaccine strains lack narK2 and narX induction and exhibit altered phenotypes during dormancy. Infect Immun.
48. Reed MB, Gagneux S, Deriemer K, Small PM, Barry CE 3rd (2007) The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J Bacteriol 189: 2583-2589.
49. Betts JC, Lukey PT, Robb LC, McAdam RA, Duncan K (2002) Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 43: 717-731.
50. Chan K, Knaak T, Satkamp L, Humbert O, Falkow S, et al. (2002) Complex pattern of Mycobacterium marinum gene expression during long-term granulomatous infection. Proc Natl Acad Sci U S A 99: 3920-3925.
51. Rosenkrands I, Slayden RA, Crawford J, Aagaard C, Barry CE 3rd, et al. (2002) Hypoxic response of Mycobacterium tuberculosis studied by metabolic labeling and proteome analysis of cellular and extracellular proteins. J Bacteriol 184: 3485-3491.
52. Chen JM, Alexander DC, Behr MA, Liu J (2003) Mycobacterium bovis BCG vaccines exhibit defects in alanine and serine catabolism. Infect Immun 71: 708-716.
53. Dubnau E, Fontan P, Manganelli R, Soares-Appel S, Smith I (2002) Mycobacterium tuberculosis genes induced during infection of human macrophages. Infect Immun 70: 2787-2795.
54. Senaratne RH, De Silva AD, Williams SJ, Mougous JD, Reader JR, et al. (2006) 5′-Adenosinephosphosulphate reductase (CysH) protects Mycobacterium tuberculosis against free radicals during chronic infection phase in mice. Mol Microbiol 59: 1744-1753.
55. Senaratne RH, Mougous JD, Reader JR, Williams SJ, Zhang T, et al. (2007) Vaccine efficacy of an attenuated but persistent Mycobacterium tuberculosis cysH mutant. J Med Microbiol 56: 454-458.
56. Lewis KN, Liao R, Guinn KM, Hickey MJ, Smith S, et al. (2003) Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guerin attenuation. J Infect Dis 187: 117-123.
57. Hsu T, Hingley-Wilson SM, Chen B, Chen M, Dai AZ, et al. (2003) The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc Natl Acad Sci U S A 100: 12420-12425.
58. Gao LY, Guo S, McLaughlin B, Morisaki H, Engel JN, et al. (2004) A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 53: 1677-1693.
59. Mattow J, Jungblut PR, Schaible UE, Mollenkopf HJ, Lamer S, et al. (2001) Identification of proteins from Mycobacterium tuberculosis missing in attenuated Mycobacterium bovis BCG strains. Electrophoresis 22: 2936-2946.
60. Hobson RJ, McBride AJ, Kempsell KE, Dale JW (2002) Use of an arrayed promoter-probe library for the identification of macrophage-regulated genes in Mycobacterium tuberculosis. Microbiology 148: 1571-1579.
61. Stewart GR, Wernisch L, Stabler R, Mangan JA, Hinds J, et al. (2002) Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology 148: 3129-3138.
62. Graham JE, Clark-Curtiss JE (1999) 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 96: 11554-11559.
63. Munoz-Elias EJ, McKinney JD (2005) Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat Med 11: 638-644.
64. Asensio JA, Arbues A, Perez E, Gicquel B, Martin C (2008) Live tuberculosis vaccines based on phoP mutants: a step towards clinical trials. Expert Opin Biol Ther 8: 201-211.
65. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.