The transcriptional regulator Rv0485 modulates the expression of a pe and ppe gene pair and is required for Mycobacterium tuberculosis virulence

Infection and Immunity

Volumn 77, Issue 10, 2009, Pages 4654-4667

  Goldstone, Rachael M ^a   Goonesekera, Sunali D ^b   Bloom, Barry R ^b   Sampson, Samantha L ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CONTROLLED STUDY; FEMALE; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE MUTATION; IMMUNE RESPONSE; IMMUNOMODULATION; IN VIVO STUDY; MACROPHAGE; MICROARRAY ANALYSIS; MOUSE; MUTAGENESIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PE GENE; PHENOTYPE; PPE GENE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REGULON; SURVIVAL TIME; TRANSCRIPTION REGULATION; TRANSPOSON; TUBERCULOSIS;

AMINO ACID SEQUENCE; ANIMAL STRUCTURES; ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; COLONY COUNT, MICROBIAL; DNA TRANSPOSABLE ELEMENTS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; LUNG; MICE; MICE, INBRED BALB C; MICE, SCID; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MYCOBACTERIUM TUBERCULOSIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SURVIVAL ANALYSIS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TUBERCULOSIS; VIRULENCE FACTORS;

EID: 70349429749     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01495-08     Document Type: Article

References (67)

1. Abdallah, A. M., T. Verboom, F. Hannes, M. Safi, M. Strong, D. Eisenberg, R. J. Musters, C. M. Vandenbroucke-Grauls, B. J. Appelmelk, J. Luirink, and W. Bitter. 2006. A specific secretion system mediates PPE41 transport in pathogenic mycobacteria. Mol. Microbiol. 62:667-679.
2. Ando, M., T. Yoshimatsu, C. Ko, P. J. Converse, and W. R. Bishai. 2003. Deletion of Mycobacterium tuberculosis sigma factor E results in delayed time to death with bacterial persistence in the lungs of aerosol-infected mice. Infect. Immun. 71:7170-7172.
3. Bacon, J., L. G. Dover, K. A. Hatch, Y. Zhang, J. M. Gomes, S. Kendall, L. Wernisch, N. G. Stoker, P. D. Butcher, G. S. Besra, and P. D. Marsh. 2007. Lipid composition and transcriptional response of Mycobacterium tuberculosis grown under iron-limitation in continuous culture: identification of a novel wax ester. Microbiology 153:1435-1444.
4. Balaji, K. N., G. Goyal, Y. Narayana, M. Srinivas, R. Chaturvedi, and S. Mohammad. 2007. Apoptosis triggered by Rv1818c, a PE family gene from Mycobacterium tuberculosis is regulated by mitochondrial intermediates in T cells. Microbes Infect. 9:271-281.
5. Banu, S., N. Honore, B. Saint-Joanis, D. Philpott, M. C. Prevost, and S. T. Cole. 2002. Are the PE-PGRS proteins of Mycobacterium tuberculosis variable surface antigens? Mol. Microbiol. 44:9-19.
6. Basu, S., S. K. Pathak, A. Banerjee, S. Pathak, A. Bhattacharyya, Z. Yang, S. Talarico, M. Kundu, and J. Basu. 2007. Execution of macrophage apoptosis by PE-PGRS33 of Mycobacterium tuberculosis is mediated by Toll-like receptor 2-dependent release of tumor necrosis factor-alpha. J. Biol. Chem. 282:1039-1050.
7. Belisle, J. T., and M. G. Sonnenberg. 1998. Isolation of genomic DNA from mycobacteria. Methods Mol. Biol. 101:31-44.
8. Berg, T., S. Schild, and J. Reidl. 2007. Regulation of the chitobiose-phosphotransferase system in Vibrio cholerae. Arch. Microbiol. 187:433-439.
9. Bonanni, D., L. Rindi, N. Lari, and C. Garzelli. 2005. Immunogenicity of mycobacterial PPE44 (Rv2770c) in Mycobacterium bovis BCG-infected mice. J. Med. Microbiol. 54:443-448.
10. Brennan, M. J., and G. Delogu. 2002. The PE multigene family: a 'molecular mantra' for mycobacteria. Trends Microbiol. 10:246-249.
11. Brennan, M. J., G. Delogu, Y. Chen, S. Bardarov, J. Kriakov, M. Alavi, and W. R. Jacobs, Jr. 2001. Evidence that mycobacterial PE-PGRS proteins are cell surface constituents that influence interactions with other cells. Infect. Immun. 69:7326-7333.
12. Camacho, L. R., D. Ensergueix, E. Perez, B. Gicquel, and C. Guilhot. 1999. Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol. Microbiol. 34:257-267.
13. Chaitra, M. G., M. S. Shaila, N. R. Chandra, and R. Nayak. 2008. HLAA* 0201-restricted cytotoxic T-cell epitopes in three PE/PPE family proteins of Mycobacterium tuberculosis. Scand. J. Immunol. 67:411-417.
14. Choudhary, R. K., S. Mukhopadhyay, P. Chakhaiyar, N. Sharma, K. J. Murthy, V. M. Katoch, and S. E. Hasnain. 2003. PPE antigen Rv2430c of Mycobacterium tuberculosis induces a strong B-cell response. Infect. Immun. 71:6338-6343.
15. Cole, S. T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, S. V. Gordon, K. Eiglmeier, S. Gas, C. E. Barry III, F. Tekaia, K. Badcock, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. Davies, K. Devlin, T. Feltwell, S. Gentles, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, A. Krogh, J. McLean, S. Moule, L. Murphy, K. Oliver, J. Osborne, M. A. Quail, M. A. Rajandream, J. Rogers, S. Rutter, K. Seeger, J. Skelton, R. Squares, S. Squares, J. E. Sulston, K. Taylor, S. Whitehead, and B. G. Barrell. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
16. Consaul, S. A., and M. S. Pavelka, Jr. 2004. Use of a novel allele of the Escherichia coli aacC4 aminoglycoside resistance gene as a genetic marker in mycobacteria. FEMS Microbiol. Lett. 234:297-301.
17. Delogu, G., and M. J. Brennan. 2001. Comparative immune response to PE and PE-PGRS antigens of Mycobacterium tuberculosis. Infect. Immun. 69:5606-5611.
18. Delogu, G., C. Pusceddu, A. Bua, G. Fadda, M. J. Brennan, and S. Zanetti. 2004. Rv1818c-encoded PE-PGRS protein of Mycobacterium tuberculosis is surface exposed and influences bacterial cell structure. Mol. Microbiol. 52:725-733.
19. Demangel, C., P. Brodin, P. J. Cockle, R. Brosch, L. Majlessi, C. Leclerc, and S. T. Cole. 2004. Cell envelope protein PPE68 contributes to Mycobacterium tuberculosis RD1 immunogenicity independently of a 10-kilodalton culture filtrate protein and ESAT-6. Infect. Immun. 72:2170-2176.
20. Dheenadhayalan, V., G. Delogu, and M. J. Brennan. 2006. Expression of the PE-PGRS 33 protein in Mycobacterium smegmatis triggers necrosis in macrophages and enhanced mycobacterial survival. Microbes Infect. 8:262-272.
21. Dheenadhayalan, V., G. Delogu, M. Sanguinetti, G. Fadda, and M. J. Brennan. 2006. Variable expression patterns of Mycobacterium tuberculosis PE-PGRS genes: evidence that PE-PGRS16 and PE-PGRS26 are inversely regulated in vivo. J. Bacteriol. 188:3721-3725.
22. Dillon, D. C., M. R. Alderson, C. H. Day, D. M. Lewinsohn, R. Coler, T. Bement, A. Campos-Neto, Y. A. Skeiky, I. M. Orme, A. Roberts, S. Steen, W. Dalemans, R. Badaro, and S. G. Reed. 1999. Molecular characterization and human T-cell responses to a member of a novel Mycobacterium tuberculosis mtb39 gene family. Infect. Immun. 67:2941-2950.
23. Dodd, I. B., and J. B. Egan. 1988. The prediction of helix-turn-helix DNA-binding regions in proteins. A reply to Yudkin. Protein Eng. 2:174-176.
24. Espitia, C., J. P. Laclette, M. Mondragon-Palomino, A. Amador, J. Campuzano, A. Martens, M. Singh, R. Cicero, Y. Zhang, and C. Moreno. 1999. The PE-PGRS glycine-rich proteins of Mycobacterium tuberculosis: a new family of fibronectin-binding proteins? Microbiology 145:3487-3495.
25. Flores, J., and C. Espitia. 2003. Differential expression of PE and PE-PGRS genes in Mycobacterium tuberculosis strains. Gene 318:75-81.
26. Fortune, S. M., A. Jaeger, D. A. Sarracino, M. R. Chase, C. M. Sassetti, D. R. Sherman, B. R. Bloom, and E. J. Rubin. 2005. Mutually dependent secretion of proteins required for mycobacterial virulence. Proc. Natl. Acad. Sci. USA 102:10676-10681.
27. Geiman, D. E., D. Kaushal, C. Ko, S. Tyagi, Y. C. Manabe, B. G. Schroeder, R. D. Fleischmann, N. E. Morrison, P. J. Converse, P. Chen, and W. R. Bishai. 2004. Attenuation of late-stage disease in mice infected by the Mycobacterium tuberculosis mutant lacking the SigF alternate sigma factor and identification of SigF-dependent genes by microarray analysis. Infect. Immun. 72:1733-1745.
28. Gey Van Pittius, N. C., J. Gamieldien, W. Hide, G. D. Brown, R. J. Siezen, and A. D. Beyers. 2001. The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Gram-positive bacteria. Genome Biol. 2:RESEARCH0044.
29. Gey van Pittius, N. C., S. L. Sampson, H. Lee, Y. Kim, P. D. van Helden, and R. M. Warren. 2006. Evolution and expansion of the Mycobacterium tuberculosis PE and PPE multigene families and their association with the duplication of the ESAT-6 (esx) gene cluster regions. BMC Evol. Biol. 6:95.
30. Hahn, M. Y., S. Raman, M. Anaya, and R. N. Husson. 2005. The Mycobacterium tuberculosis extracytoplasmic-function sigma factor SigL regulates polyketide synthases and secreted or membrane proteins and is required for virulence. J. Bacteriol. 187:7062-7071.
31. Hsu, T., S. M. Hingley-Wilson, B. Chen, M. Chen, A. Z. Dai, P. M. Morin, C. B. Marks, J. Padiyar, C. Goulding, M. Gingery, D. Eisenberg, R. G. Russell, S. C. Derrick, F. M. Collins, S. L. Morris, C. H. King, and W. R. Jacobs, Jr. 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. USA 100:12420-12425.
32. Kaushal, D., B. G. Schroeder, S. Tyagi, T. Yoshimatsu, C. Scott, C. Ko, L. Carpenter, J. Mehrotra, Y. C. Manabe, R. D. Fleischmann, and W. R. Bishai. 2002. Reduced immunopathology and mortality despite tissue persistence in a Mycobacterium tuberculosis mutant lacking alternative sigma factor, SigH. Proc. Natl. Acad. Sci. USA 99:8330-8335.
33. Khan, N., K. Alam, S. Nair, V. L. Valluri, K. J. Murthy, and S. Mukhopadhyay. 2008. Association of strong immune responses to PPE protein Rv1168c with active tuberculosis. Clin. Vaccine Immunol. 15:974-980.
34. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
35. Lee, J. H., P. C. Karakousis, and W. R. Bishai. 2008. Roles of SigB and SigF in the Mycobacterium tuberculosis sigma factor network. J. Bacteriol. 190:699-707.
36. Lewis, K. N., R. Liao, K. M. Guinn, M. J. Hickey, S. Smith, M. A. Behr, and D. R. Sherman. 2003. Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guerin attenuation. J. Infect. Dis. 187:117-123.
37. Li, Y., E. Miltner, M. Wu, M. Petrofsky, and L. E. Bermudez. 2005. A Mycobacterium avium PPE gene is associated with the ability of the bacterium to grow in macrophages and virulence in mice. Cell Microbiol. 7:539-548.
38. Mehta, P. K., A. K. Pandey, S. Subbian, S. H. El-Etr, S. L. Cirillo, M. M. Samrakandi, and J. D. Cirillo. 2006. Identification of Mycobacterium marinum macrophage infection mutants. Microb. Pathog. 40:139-151.
39. Mustafa, A. S., P. J. Cockle, F. Shaban, R. G. Hewinson, and H. M. Vordermeier. 2002. Immunogenicity of Mycobacterium tuberculosis RD1 region gene products in infected cattle. Clin. Exp. Immunol. 130:37-42.
40. Mustafa, A. S., Y. A. Skeiky, R. Al-Attiyah, M. R. Alderson, R. G. Hewinson, and H. M. Vordermeier. 2006. Immunogenicity of Mycobacterium tuberculosis antigens in Mycobacterium bovis BCG-vaccinated and M. bovis-infected cattle. Infect. Immun. 74:4566-4572.
41. Pallen, M. J. 2002. The ESAT-6/WXG100 superfamily - and a new Grampositive secretion system? Trends Microbiol. 10:209-212.
42. Parra, M., N. Cadieux, T. Pickett, V. Dheenadhayalan, and M. J. Brennan. 2006. A PE protein expressed by Mycobacterium avium is an effective T-cell immunogen. Infect. Immun. 74:786-789.
43. Pfaffl, M. W., G. W. Horgan, and L. Dempfle. 2002. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30:e36.
44. Plumbridge, J. 1999. Expression of the phosphotransferase system both mediates and is mediated by Mlc regulation in Escherichia coli. Mol. Microbiol. 33:260-273. (Pubitemid 29322513)
45. Pym, A. S., P. Brodin, R. Brosch, M. Huerre, and S. T. Cole. 2002. Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol. Microbiol. 46:709-717.
46. Rachman, H., M. Strong, U. Schaible, J. Schuchhardt, K. Hagens, H. Mollenkopf, D. Eisenberg, and S. H. Kaufmann. 2006. Mycobacterium tuberculosis gene expression profiling within the context of protein networks. Microbes Infect. 8:747-757.
47. Raghavan, S., P. Manzanillo, K. Chan, C. Dovey, and J. S. Cox. 2008. Secreted transcription factor controls Mycobacterium tuberculosis virulence. Nature 454:717-721.
48. Ramakrishnan, L., N. A. Federspiel, and S. Falkow. 2000. Granuloma-specific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 288:1436-1439. (Pubitemid 30366332)
49. Raman, S., R. Hazra, C. C. Dascher, and R. N. Husson. 2004. Transcription regulation by the Mycobacterium tuberculosis alternative sigma factor SigD and its role in virulence. J. Bacteriol. 186:6605-6616.
50. Raman, S., X. Puyang, T. Y. Cheng, D. C. Young, D. B. Moody, and R. N. Husson. 2006. Mycobacterium tuberculosis SigM positively regulates Esx secreted protein and nonribosomal peptide synthetase genes and down regulates virulence-associated surface lipid synthesis. J. Bacteriol. 188:8460-8468.
51. Rodriguez, G. M., B. Gold, M. Gomez, O. Dussurget, and I. Smith. 1999. Identification and characterization of two divergently transcribed iron regulated genes in Mycobacterium tuberculosis. Tuber. Lung Dis. 79:287-298.
52. Roupie, V., M. Romano, L. Zhang, H. Korf, M. Y. Lin, K. L. Franken, T. H. Ottenhoff, M. R. Klein, and K. Huygen. 2007. Immunogenicity of eight dormancy regulon-encoded proteins of Mycobacterium tuberculosis in DNA-vaccinated and tuberculosis-infected mice. Infect. Immun. 75:941-949.
53. Sampson, S. L., P. Lukey, R. M. Warren, P. D. van Helden, M. Richardson, and M. J. Everett. 2001. Expression, characterization and subcellular localization of the Mycobacterium tuberculosis PPE gene Rv1917c. Tuberculosis (Edinburgh) 81:305-317.
54. Sassetti, C. M., D. H. Boyd, and E. J. Rubin. 2001. Comprehensive identification of conditionally essential genes in mycobacteria. Proc. Natl. Acad. Sci. USA 98:12712-12717.
55. 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.
56. Sassetti, C. M., and E. J. Rubin. 2003. Genetic requirements for mycobacterial survival during infection. Proc. Natl. Acad. Sci. USA 100:12989-12994.
57. Senaratne, R. H., A. D. De Silva, S. J. Williams, J. D. Mougous, J. R. Reader, T. Zhang, S. Chan, B. Sidders, D. H. Lee, J. Chan, C. R. Bertozzi, and L. W. Riley. 2006. 5′-Adenosinephosphosulphate reductase (CysH) protects Mycobacterium tuberculosis against free radicals during chronic infection phase in mice. Mol. Microbiol. 59:1744-1753.
58. Skeiky, Y. A., M. R. Alderson, P. J. Ovendale, J. A. Guderian, L. Brandt, D. C. Dillon, A. Campos-Neto, Y. Lobet, W. Dalemans, I. M. Orme, and S. G. Reed. 2004. Differential immune responses and protective efficacy induced by components of a tuberculosis polyprotein vaccine, Mtb72F, delivered as naked DNA or recombinant protein. J. Immunol. 172:7618-7628.
59. Smialowski, P., A. J. Martin-Galiano, A. Mikolajka, T. Girschick, T. A. Holak, and D. Frishman. 2007. Protein solubility: sequence based prediction and experimental verification. Bioinformatics 23:2536-2542. (Pubitemid 350048355)
60. Stewart, G. R., J. Patel, B. D. Robertson, A. Rae, and D. B. Young. 2005. Mycobacterial mutants with defective control of phagosomal acidification. PLoS Pathog. 1:269-278.
61. Stewart, G. R., L. Wernisch, R. Stabler, J. A. Mangan, J. Hinds, K. G. Laing, D. B. Young, and P. D. Butcher. 2002. Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology 148:3129-3138.
62. Steyn, A. J., D. M. Collins, M. K. Hondalus, W. R. Jacobs, Jr., R. P. Kawakami, and B. R. Bloom. 2002. Mycobacterium tuberculosis WhiB3 interacts with RpoV to affect host survival but is dispensable for in vivo growth. Proc. Natl. Acad. Sci. USA 99:3147-3152.
63. Sun, R., P. J. Converse, C. Ko, S. Tyagi, N. E. Morrison, and W. R. Bishai. 2004. Mycobacterium tuberculosis ECF sigma factor sigC is required for lethality in mice and for the conditional expression of a defined gene set. Mol. Microbiol. 52:25-38.
64. Tsenova, L., R. Harbacheuski, A. L. Moreira, E. Ellison, W. Dalemans, M. R. Alderson, B. Mathema, S. G. Reed, Y. A. Skeiky, and G. Kaplan. 2006. Evaluation of the Mtb72F polyprotein vaccine in a rabbit model of tuberculous meningitis. Infect. Immun. 74:2392-2401.
65. Voskuil, M. I., D. Schnappinger, R. Rutherford, Y. Liu, and G. K. Schoolnik. 2004. Regulation of the Mycobacterium tuberculosis PE/PPE genes. Tuberculosis (Edinburgh) 84:256-262.
66. Voskuil, M. I., D. Schnappinger, K. C. Visconti, M. I. Harrell, G. M. Dolganov, D. R. Sherman, and G. K. Schoolnik. 2003. Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J. Exp. Med. 198:705-713.
67. Zhang, H., J. Wang, J. Lei, M. Zhang, Y. Yang, Y. Chen, and H. Wang. 2007. PPE protein (Rv3425) from DNA segment RD11 of Mycobacterium tuberculosis: a potential B-cell antigen used for serological diagnosis to distinguish vaccinated controls from tuberculosis patients. Clin. Microbiol. Infect. 13:139-145.