Expression of the PE_PGRS 33 protein in Mycobacterium smegmatis triggers necrosis in macrophages and enhanced mycobacterial survival

Microbes and Infection

Volumn 8, Issue 1, 2006, Pages 262-272

  Dheenadhayalan, Veerabadran ^a   Delogu, Giovanni ^b   Brennan, Michael J ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b CATHOLIC UNIVERSITY   (Italy)

Author keywords

Mycobacterium smegmatis; PE_PGRS genes; Tuberculosis; Tumor necrosis factor

Indexed keywords

BACTERIAL PROTEIN; LACTATE DEHYDROGENASE; PROTEIN PE PGRS 33; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; CELL AGGREGATION; CELL CULTURE; CELL DEATH; CONTROLLED STUDY; CYTOLYSIS; FEMALE; GENE EXPRESSION; MACROPHAGE; MOUSE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; L-LACTATE DEHYDROGENASE; LIVER; LUNG; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MYCOBACTERIUM INFECTIONS, ATYPICAL; MYCOBACTERIUM SMEGMATIS; NECROSIS; SPLEEN; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA; BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 31344463710     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2005.06.021     Document Type: Article

References (44)

1. M.J. Brennan, C. Espitia, and N. Gey Von Pittius The PE and PPE Multigene Families of Mycobacterium tuberculosis S. Cole D.N. McMurray K. Eisenach B. Gicquel W.R. Jacobs Jr. Tuberculosis, second ed 2004 ASM Press Washington, DC 513 525
2. S.T. Cole, 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, and B.G. Barrell Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence Nature 393 1998 537 544
3. A.S. Pym, P. Brodin, R. Brosch, M. Huerre, and S.T. Cole Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti Mol. Microbiol. 46 2002 709 717
4. S.T. Cole Comparative and functional genomics of the Mycobacterium tuberculosis complex Microbiol. 148 2002 2919 2928
5. S. Poulet, and S.T. Cole Characterization of the highly abundant polymorphic GC-rich-repetitive sequence (PGRS) present in Mycobacterium tuberculosis Microbiol. 163 1995 87 95
6. L. Ramakrishnan, N.A. Federspiel, and S. Falkow Granuloma-specific expression of mycobacterium virulence proteins from the glycine-rich PE-PGRS family Science 288 2000 1436 1439
7. S. Banu, N. Honore, B. Saint-Joanis, D. Philpott, M.C. Prevost, and S.T. Cole Are the PE-PGRS proteins of Mycobacterium tuberculosis variable surface antigens? Mol. Microbiol. 44 2002 9 19
8. G. Delogu, C. Pusceddu, A. Bua, G. Fadda, M.J. Brennan, and S. Zanetti Rv1818c-encoded PE_PGRS protein of Mycobacterium tuberculosis is surface exposed and influences bacterial cell structure Mol. Microbiol. 52 2004 725 733
9. J. Flores, and C. Espitia Differential expression of PE and PE-PGRS genes in Mycobacterium tuberculosis strains Gene 318 2003 75 81
10. J.C. Betts, P.T. Lukey, L.C. Robb, R.A. McAdam, and K. Duncan Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling Mol. Microbiol. 43 2002 717 731
11. M.A. Fisher, B.B. Plikaytis, and T.M. Shinnick Microarray analysis of the Mycobacterium tuberculosis transcriptional response to the acidic conditions found in phagosomes J Bacteriol 184 2002 4025 4032
12. G.M. Rodriguez, M.I. Voskuil, B. Gold, G.K. Schoolnik, I. Smith, and R. Ide An essential gene in Mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response Infect. Immun. 70 2002 3371 3381
13. B. Saviola, S.C. Woolwine, and W.R. Bishai Isolation of acid-inducible genes of Mycobacterium tuberculosis with the use of recombinase-based in vivo expression technology Infect. Immun. 71 2003 1379 1388
14. M.I. Voskuil, D. Schnappinger, R. Rutherford, Y. Liu, and G.K. Schoolnik Regulation of the PE/PPE genes Tuberculosis (Edinb.) 84 2004 256 262
15. M.J. Brennan, G. Delogu, Y. Chen, S. Bardarov, J. Kriakov, M. Alavi, and W.R. Jacobs Jr. Evidence that mycobacterial PE_PGRS proteins are cell surface constituents that influence interactions with other cells Infect. Immun. 69 2001 7326 7333
16. G. Delogu, and M.J. Brennan Comparative immune response to PE and PE_PGRS antigens of Mycobacterium tuberculosis Infect. Immun. 69 2001 5606 5611
17. F.M. Collins Protection to mice afforded by BCG vaccines against an aerogenic challenge by three mycobacteria of decreasing virulence Tubercle 66 1995 267 276
18. K.M. Dobos, E.A. Spotts, F.D. Quinn, and C.H. King Necrosis of lung epithelial cells during infection with Mycobacterium tuberculosis is preceded by cell permeation Infect Immun 68 2000 6300 6310
19. K.A. McDonough, and Y. Kress Cytotoxicity for lung epithelial cells is a virulence-associated phenotype of Mycobacterium tuberculosis Infect. Immun. 63 1995 4802 4811
20. J.L. Flynn, M.M. Goldstein, J. Chan, K.J. Triebold, K. Pfeffer, C.J. Lowenstein, R. Schreiber, T.W. Mak, and B.R. Bloom Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice Immunity 2 1995 561 572
21. V. Kindler, A.P. Sappino, G.E. Grau, P.F. Piguet, and P. Vassalli The inducing role of tumor necrosis factor in the development of bactericidal granulomas during BCG infection Cell 56 1989 731 740
22. L.G. Bekker, A.L. Moreira, A. Bergtold, S. Freeman, B. Ryffel, and G. Kaplan Immunopathologic effects of tumor necrosis factor alpha in murine mycobacterial infection are dose-dependent Infect. Immun. 68 2000 6954 6961
23. G.M. Taylor, G.R. Stewart, M. Cooke, S. Chaplin, S. Ladva, J. Kirkup, S. Palmer, and D.B. Young Koch's bacillus - a look at the first isolate of Mycobacterium tuberculosis from a modern perspective Microbiol. 149 2003 3213 3220
24. D.R. Roach, A.G. Bean, C. Demangel, M.P. France, H. Briscoe, and W.J. Britton TNF regulates chemokine induction essential for cell recruitment, granuloma formation, and clearance of mycobacterial infection J. Immunol. 168 2002 4620 4627
25. C. Sanoc, K. Sato, T. Shimizu, H. Kajitani, H. Kawauchi, and H. Tomioka The modulating effects of proinflammatory cytokines interferon-gamma (IFN-gamma) and tumour necrosis factor-alpha (TNF-alpha), and immunoregulating cytokines IL-10 and transforming growth factor-beta (TGF-beta), on anti-microbial activity of murine peritoneal macrophages against Mycobacterium avium-intracellulare complex Clin. Exp. Immunol. 115 1999 435 442
26. R.D. Fleischmann, D. Alland, J.A. Eisen, L. Carpenter, O. White, J. Peterson, R. DeBoy, R. Dodson, M. Gwinn, D. Haft, E. Hickey, J.F. Kolonay, W.C. Nelson, L.A. Umayam, M. Ermolaeva, S.L. Salzberg, A. Delcher, T. Utterback, J. Weidman, H. Khouri, J. Gill, A. Mikula, W. Bishai, W.R. Jacobs Jr., J.C. Venter, and C.M. Fraser Whole-genome comparison of Mycobacterium tuberculosis clinical and laboratory strains J. Bacteriol. 184 2002 5479 5490
27. M.J. Brennan, and G. Delogu The PE multigene family: a 'molecular mantra' for mycobacteria Trends Microbiol. 10 2002 246 249
28. G. Lamichhane, M. Zignol, N.J. Blades, D.E. Geiman, A. Dougherty, J. Grosset, K.W. Broman, and W.R. Bishai A postgenomic method for predicting essential genes at subsaturation levels of mutagenesis: application to Mycobacterium tuberculosis Proc. Natl. Acad. Sci. USA 100 2003 7213 7218
29. F.A. Post, C. Manca, O. Neyrolles, B. Ryffel, D.B. Young, and G. Kaplan Mycobacterium tuberculosis 19-kDa lipoprotein inhibits Mycobacterium smegmatis-induced cytokine production by human macrophages in vitro Infect. Immun. 69 2001 1433 1439
30. L. Danelishvili, J. McGarvey, Y.J. Li, and L.E. Bermudez Mycobacterium tuberculosis infection causes different levels of apoptosis and necrosis in human macrophages and alveolar epithelial cells Cell. Microbiol. 5 2003 649 660
31. T.F. Byrd Tumor necrosis factor- (TNF-) promotes growth of virulent Mycobacterium tuberculosis in human monocytes iron-mediated growth suppression is correlated with decreased release of TNF- from iron-treated infected monocytes J. Clin. Invest. 99 1997 2518 2529
32. R.F. Silver, Q. Li, W.H. Boom, and J.J. Ellner Lymphocyte-dependent inhibition of growth of virulent Mycobacterium tuberculosis H37Rv within human monocytes: requirement for CD4+ T cells in purified protein derivative-positive, but not in purified protein derivative-negative subjects J. Immunol. 160 1998 2408 2417
33. M. Engele, E. Stossel, K. Castiglione, N. Schwerdtner, M. Wagner, P. Bolcskei, M. Rollinghoff, and S. Stenger Induction of TNF in human alveolar macrophages as a potential evasion mechanism of virulent Mycobacterium tuberculosis J. Immunol. 168 2002 1328 1337
34. E.A. Filley, and G.A.W. Rook Effect of mycobacteria on sensitivity to the cytotoxic effects of tumor necrosis factor Infect Immun 59 1991 2567 2572
35. T.K. Means, B.W. Jones, A.B. Schromm, B.A. Shurtleff, J.A. Smith, J. Keane, D.T. Golenbock, S.N. Vogel, and M.J. Fenton Differential effects of a Toll-like receptor antagonist on Mycobacterium tuberculosis-induced macrophage responses J. Immunol. 166 2001 4074 4082
36. D.M. Underhill, A. Ozinsky, K.D. Smith, and A. Aderem Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages Proc. Natl. Acad. Sci. USA 96 1999 14459 14463
37. D. Chatterjee, A.D. Roberts, K. Lowell, P.J. Brennan, and I.M. Orme Structural basis of capacity of lipoarabinomannan to induce secretion of tumor necrosis factor Infect Immun 60 1992 1249 1253
38. L.Y. Gao, S. Guo, B. McLaughlin, H. Morisaki, J.N. Engel, and E.J. Brown A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion Mol. Microbiol. 53 2004 1677 1693
39. T. Hsu, 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. 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 2003 12420 12425
40. C. Espitia, J.P. Laclette, M. Mondragon-Palomino, A. Amador, J. Campuzano, A. Martens, M. Singh, R. Cicero, Y. Zhang, and C. Moreno The PE-PGRS glycine-rich proteins of Mycobacterium tuberculosis: a new family of fibronectin-binding proteins? Microbiol. 145 1999 3487 3495
41. L.R. Camacho, D. Ensergueix, E. Perez, B. Gicquel, and C. Guilhot Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis Mol. Microbiol. 34 1999 257 267
42. F.-C. Bange, F.M. Collins, and W.R. Jacobs Jr. Survival of mice infected with Mycobacterium smegmatis containing large DNA fragments from Mycobacerium tuberculosis Tuber. Lung Dis. 79 1999 171 180
43. M.S. Glickman, J.S. Cox, and W.R. Jacobs Jr. A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis Mol. Cell 5 2000 717 727
44. S.E. Converse, and J.S. Cox A protein secretion pathway critical for Mycobacterium tuberculosis virulence is conserved and functional in Mycobacterium smegmatis J. Bacteriol. 187 2005 1238 1245