Apoptosis of macrophages during pulmonary Mycobacterium bovis infection: Correlation with intracellular bacillary load and cytokine levels

Immunology

Volumn 128, Issue 1 PART 2, 2009, Pages

  Rodrigues, Michele F ^a   Barsante, Michele M ^a   Alves, Caio C S ^a   Souza, Maria A ^a   Ferreira, Ana P ^a   Amarante Mendes, Gustavo P ^b   Teixeira, Henrique C ^a  

^a FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Apoptosis; Cytokines; Infection; Macrophages; Mycobacteria

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 12; PROTEIN BCL 2; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL VIRULENCE; BOVINE TUBERCULOSIS; CONTROLLED STUDY; CYTOKINE RELEASE; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOGENESIS; LUNG ALVEOLUS MACROPHAGE; MALE; MOUSE; MYCOBACTERIUM BOVIS; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; INTERLEUKIN-10; INTERLEUKIN-12; LUNG; MACROPHAGES, ALVEOLAR; MALE; MICE; MICE, INBRED BALB C; MYCOBACTERIUM BOVIS; PROTO-ONCOGENE PROTEINS C-BCL-2; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA; VIRULENCE;

EID: 68249136798     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2009.03062.x     Document Type: Article

References (40)

1. Flynn JL, Chan J. Tuberculosis: latency and reactivation. Infect Immun 2001 69 : 4195 201.
2. Kaufmann SH. Tuberculosis: deadly combination. Nature 2008 453 : 295 6.
3. Kaufmann SH. Immunity to intracellular bacteria. Annu Rev Immunol 1993 11 : 129 63.
4. Raja A. Imunology of tuberculosis. Indian J Med Res 2004 120 : 213 32.
5. Russell DG. Phagosomes, fatty acids and tuberculosis. Nat Cell Biol 2003 5 : 776 8.
6. Warner DF, Mizrahi V. The survival kit of Mycobacterium tuberculosis. Nat Med 2007 13 : 282 4.
7. McDonough KA, Kress Y, Bloom BR. Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages. Infect Immun 1993 61 : 2763 73.
8. Fenton MJ, Vermeulen MW. Immunopathology of tuberculosis: roles of macrophages and monocytes. Infect Immun 1996 64 : 683 90.
9. Rojas M, Olivier M, Gros P, Barrera LF, García LF. TNF-α and IL-10 modulate the induction of apoptosis by virulent Mycobacterium tuberculosis in murine macrophages. J Immunol 1999 162 : 6122 31.
10. Molloy A, Laochumroonvorapong P, Kaplan G. Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guérin. J Exp Med 1994 180 : 1499 509.
11. Keane J, Balcewicz-Sablinska MK, Remold HG, Chupp GL, Meek BB, Fenton MJ, Kornfeld H. Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect Immun 1997 65 : 298 304. (Pubitemid 27008937)
12. Fratazzi C, Arbeit RD, Carini C, Balcewicz-Sablinska MK, Keane J, Kornfeld H, Remold HG. Macrophage apoptosis in mycobacterial infections. J Leukoc Biol 1999 66 : 763 4.
13. Keane J, Remold HG, Kornfeld H. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol 2000 164 : 2016 20.
14. Porcelli SA, Jacobs WR Jr. Tuberculosis: unsealing the apoptotic envelope. Nat Immunol 2008 9 : 1101 2.
15. 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.
16. Ríos-Barrera VA, Campos-Penã V, Aguilar-León D, Lascurain LR, Meraz-Ríos MA, Moreno J, Figueroa-Granados V, Hernández-Pando R. Macrophage and T lymphocyte apoptosis during experimental pulmonary tuberculosis: their relationship to mycobacterial virulence. Eur J Immunol 2006 36 : 345 53.
17. 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.
18. Klingler K, Tchou-Wong KM, Brändli O, Aston C, Kim R, Chi C, Rom WN. Effects of mycobacteria on regulation of apoptosis in mononuclear phagocytes. Infect Immun 1997 65 : 5272 8.
19. 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.
20. 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.
21. Keane J, Shurtleff B, Kornfeld H. TNF-dependent BALB/c murine macrophage apoptosis following Mycobacterium tuberculosis infection inhibits bacillary growth in an IFN-gamma independent manner. Tuberculosis 2002 82 : 55 61.
22. Spira A, Carroll JD, Liu G, Aziz Z, Shah V, Kornfeld H, Keane J. Apoptosis genes in human alveolar macrophages infected with virulent or attenuated Mycobacterium tuberculosis. a pivotal role for tumor necrosis factor. Am J Respir Cell Mol Biol 2003 29 : 545 51.
23. Balcewicz-Sablinska MK, Gan H, Remold HG. Interleukin 10 produced by macrophages inoculated with Mycobacterium avium attenuates mycobacteria-induced apoptosis by reduction of TNF-α activity. J Infect Dis 1999 180 : 1230 7.
24. Nigou J, Gilleron M, Rojas M, García LF, Thurnher M, Puzo G. Mycobacterial lipoarabinomannans: modulators of dendritic cell function and the apoptotic response. Microbes Infect 2002 4 : 945 53.
25. Schaible UE, Winau F, Sieling PA et al. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat Med 2003 9 : 1039 46.
26. Winau F, Kaufmann SH, Schaible UE. Apoptosis paves the detour path for CD8 T cell activation against intracellular bacteria. Cell Microbiol 2004 7 : 599 607.
27. Fulton SA, Martin TD, Redline RW, Henry BoomW. Pulmonary immune responses during primary Mycobacterium bovis-Calmette-Guérin bacillus infection in C57BL/6 mice. Am J Respir Cell Mol Biol 2000 22 : 333 43.
28. Bekker LG, Moreira AL, Bergtold A, Freeman S, Ryffel B, Kaplan G. Immunophathologic effects of tumor necrosis factor alpha in murine mycobacterial infection are dose dependent. Infect Immun 2000 68 : 6954 61.
29. Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, LaFace DM, Green DR. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 1995 182 : 1545 56.
30. van Rijt LS, Kuipers H, Vos N, Hijdra D, Hoogsteden HC, Lambrecht BN. A rapid flow cytometric method for determining the cellular composition of bronchoalveolar lavage fluid cells in mouse models of asthma. J Immnunol Methods 2004 288 : 111 21.
31. Winau F, Weber S, Sad S et al. Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity 2006 24 : 105 17.
32. Pan H, Yan BS, Rojas M et al. Ipr1 gene mediates innate immunity to tuberculosis. Nature 2005 434 : 767 72.
33. Savill J, Dransfield I, Gregory C, Haslett C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2002 2 : 965 75.
34. O'Sullivan MP, O'Leary S, Kelly DM, Keane J. A caspase-independent pathway mediates macrophage cell death in response to Mycobacterium tuberculosis infection. Infect Immun 2007 75 : 1984 93.
35. Arcila ML, Sánchez MD, Ortiz B, Barrera LF, García LF, Rojas M. Activation of apoptosis, but not necrosis, during Mycobacterium tuberculosis infection correlated with decreased bacterial growth: role of TNF-α, IL-10, caspases and phospholipase A2. Cell Immunol 2007 249 : 80 93.
36. Balcewicz-Sablinska MK, Keane J, Kornefeld H, Remold HG. Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-α. J Immunol 1998 161 : 2636 41.
37. Cohen SB, Crawlwy JB, Kahan MC, Feldmann M, Foxwell BM. Interleukin-10 rescues T cells from apoptotic cell death: association with an upregulation of Bcl-2. Immunology 1997 92 : 1 5.
38. Levy Y, Brouet JC. Interleukin-10 prevents spontaneous death of germinal center B cells by induction of the Bcl-2 protein. J Clin Invest 1994 93 : 424 8.
39. Hickman SP, Chan J, Salgame P. Mycobacterium tuberculosis induces differential cytokine production from dendritic cells and macrophages with divergent effects on naive T cell polarization. J Immunol 2002 168 : 4636 42.
40. Pompei L, Jang S, Zamlynny B, Ravikumar S, McBride A, Hickman SP, Salgame P. Disparity in IL-12 release in dendritic cells and macrophages in response to Mycobacterium tuberculosis is due to use of distinct TLRs. J Immunol 2007 178 : 5192 9.