Induction of Serine Protease Inhibitor 9 by Mycobacterium tuberculosis Inhibits Apoptosis and Promotes Survival of Infected Macrophages

Journal of Infectious Diseases

Volumn 205, Issue 1, 2012, Pages 144-151

  Toossi, Zahra ^a,c   Wu, Mianda ^a   Rojas, Roxana ^a   Kalsdorf, Barbara ^e   Aung, Htin ^a   Hirsch, Christina S ^a,d   Walrath, Jessica ^b,c   Wolbink, Angela ^f   Van Ham, Marieke ^e   Silver, Richard F ^b,c,d,g  

^a Divisions of Infectious Diseases   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c DEPARTMENT OF VETERANS AFFAIRS   (United States)

^d UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^e Research Center Borstel   (Germany)

^f SANQUIN RESEARCH   (Netherlands)

^g Division of Pulmonary Critical Care and Sleep Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; PROTEIN BCL 2; SERINE PROTEINASE INHIBITOR; SERINE PROTEINASE INHIBITOR 9; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ADULT; APOPTOSIS; ARTICLE; BACTERIAL SURVIVAL; CELL SURVIVAL; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME SYNTHESIS; GENE EXPRESSION; HUMAN; HUMAN CELL; LUNG ALVEOLUS MACROPHAGE; MONOCYTE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; TUBERCULOSIS; WESTERN BLOTTING;

APOPTOSIS; CASPASE 3; CELLS, CULTURED; HUMANS; MACROPHAGES, ALVEOLAR; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, SMALL INTERFERING; SERPINS;

EID: 84555189227     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jir697     Document Type: Article

References (27)

1. Molloy A, Laochumroonvorapong P, Kaplan G. Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin. J Exp Med 1994; 180:1499-509.
2. Fratazzi C, Arbeit RD, Carini C, et al. Macrophage apoptosis in mycobacterial infections. J Leukoc Biol 1999; 66:763-4. (Pubitemid 29532037)
3. Keane J, Balcewicz-Sablinska MK, Remold HG, et al. Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect Immun 1997; 65:298-304. (Pubitemid 27008937)
4. Keane J, Remold HG, Kornfeld H. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol 2000; 164:2016-20. (Pubitemid 30108758)
5. Rios-Barrera VA, Campos-Pena V, Aguilar-Leon D, et al. Macrophage and T lymphocyte apoptosis during experimental pulmonary tuberculosis: their relationship to mycobacterial virulence. Eur J Immunol 2006; 36:345-53. (Pubitemid 43257457)
6. Sly LM, Hingley-Wilson SM, Reiner NE, McMaster WR. Survival of Mycobacterium tuberculosis in host macrophages involves resistance to apoptosis dependent upon induction of antiapoptotic Bcl-2 family member Mcl-1. J Immunol 2003; 170:430-7. (Pubitemid 36026168)
7. Spira A, Carroll JD, Liu G, et al. Apoptosis genes in human alveolar macrophages infected with virulent or attenuated Mycobacterium tuberculosis: a pivotal role for tumor necrosis factor. Am J Respir CellMol Biol 2003; 29:545-51. (Pubitemid 37357705)
8. Zhang J, Jiang R, Takayama H, Tanaka Y. Survival of virulent Mycobacterium tuberculosis involves preventing apoptosis induced by Bcl-2 upregulation and release resulting from necrosis in J774 macrophages. Microbiol Immunol 2005; 49:845-52. (Pubitemid 41373935)
9. Wesche DE, Lomas-Neira JL, Perl M, Chung CS, Ayala A. Leukocyte apoptosis and its significance in sepsis and shock. J Leukoc Biol 2005; 78:325-37. (Pubitemid 41061305)
10. Logue SE, Martin SJ. Caspase activation cascades in apoptosis. Biochem Soc Trans 2008; 36:1-9. (Pubitemid 351269611)
11. Silver RF, Walrath J, Lee H, et al. Human alveolar macrophage gene responses to Mycobacterium tuberculosis strains H37Ra and H37Rv. Am J Respir Cell Mol Biol 2009; 40:491-504.
12. Bird CH, Sutton VR, Sun J, et al. Selective regulation of apoptosis: the cytotoxic lymphocyte serpin proteinase inhibitor 9 protects against granzyme B-mediated apoptosis without perturbing the Fas cell death pathway. Mol Cell Biol 1998; 18:6387-98. (Pubitemid 28500528)
13. Walrath J, Zukowski L, Krywiak A, Silver RF. Resident Th1-like effector memory cells in pulmonary recall responses to Mycobacterium tuberculosis. Am J Respir Cell Mol Biol 2005; 33:48-55. (Pubitemid 40961013)
14. Toossi Z, Hirsch CS, Hamilton BD, Knuth CK, FriedlanderMA, Rich EA. Decreased production of TGF-beta 1 by human alveolar macrophages compared with blood monocytes. J Immunol 1996; 156:3461-8. (Pubitemid 26123562)
15. Silver RF, Li Q, Boom WH, Ellner JJ. Lymphocyte-dependent inhibition of growth of virulent Mycobacterium tuberculosis H37Rv within human monocytes: requirement for CD41 T cells in purified protein derivativepositive, but not in purified protein derivative-negative subjects. J Immunol 1998; 160:2408-17. (Pubitemid 28119925)
16. Young JL, Sukhova GK, Foster D, Kisiel W, Libby P, Schonbeck U. The serpin proteinase inhibitor 9 is an endogenous inhibitor of interleukin 1beta-converting enzyme (caspase-1) activity in human vascular smooth muscle cells. J Exp Med 2000; 191:1535-44. (Pubitemid 30257350)
17. Wilkinson RJ, Desjardin LE, Islam N, et al. An increase in expression of a Mycobacterium tuberculosis mycolyl transferase gene (fbpB) occurs early after infection of human monocytes. Mol Microbiol 2001; 39:813-21. (Pubitemid 32158158)
18. Islam N, Kanost AR, Teixeira L, et al. Role of cellular activation and tumor necrosis factor-alpha in the early expression of Mycobacterium tuberculosis 85B mRNA in human alveolar macrophages. J Infect Dis 2004; 190:341-51. (Pubitemid 38951976)
19. Bladergroen BA, Strik MC, Bovenschen N, et al. The granzyme B inhibitor, protease inhibitor 9, is mainly expressed by dendritic cells and at immune-privileged sites. J Immunol 2001; 166:3218-25. (Pubitemid 33117320)
20. Rook GA, Hernandez-Pando R. The pathogenesis of tuberculosis. Annu Rev Microbiol 1996; 50:259-84. (Pubitemid 26337464)
21. Sun J, Bird CH, Sutton V, et al. A cytosolic granzyme B inhibitor related to the viral apoptotic regulator cytokine response modifier A is present in cytotoxic lymphocytes. J Biol Chem 1996; 271: 27802-9. (Pubitemid 26367355)
22. Annand RR, Dahlen JR, Sprecher CA, et al. Caspase-1 (interleukin-1beta- converting enzyme) is inhibited by the human serpin analogue proteinase inhibitor 9. Biochem J 1999; 342:655-65. (Pubitemid 29452651)
23. Kannan-Thulasiraman P, Shapiro DJ. Modulators of inflammation use nuclear factor-kappa B and activator protein-1 sites to induce the caspase-1 and granzyme B inhibitor, proteinase inhibitor 9. J Biol Chem 2002; 277:41230-9. (Pubitemid 35215715)
24. Classen CF, Bird PI, Debatin KM. Modulation of the granzyme B inhibitor proteinase inhibitor 9 (PI-9) by activation of lymphocytes and monocytes in vitro and by Epstein-Barr virus and bacterial infection. Clin Exp Immunol 2006; 143:534-42.
25. Dhiman R, Kathania M, Raje M, Majumdar S. Inhibition of bfl-1/A1 by siRNA inhibits mycobacterial growth in THP-1 cells by enhancing phagosomal acidification. Biochim Biophys Acta 2008; 1780:733-42.
26. Mogga SJ, Mustafa T, Sviland L, Nilsen R. Increased Bcl-2 and reduced Bax expression in infected macrophages in slowly progressive primary murine Mycobacterium tuberculosis infection. Scand J Immunol 2002; 56:383-91.
27. Lee J, Remold HG, Ieong MH, Kornfeld H. Macrophage apoptosis in response to high intracellular burden of Mycobacterium tuberculosis is mediated by a novel caspase-independent pathway. J Immunol 2006; 176:4267-74. (Pubitemid 44264406)