1887

Abstract

has been shown to induce apoptosis within macrophages, monocytic cell lines and alveolar epithelial cells. The mechanisms and significance of -associated apoptosis are not well understood. It has been speculated that may induce apoptosis through ligation of death receptors by bacterial surface components or by secreted bacterial factors. Translocation of apoptotic factor(s) through the Dot/Icm secretion machinery followed by direct activation of caspases within the cytosol is discussed as another possible mechanism of apoptosis induction by . Here, it is shown that induced the mitochondrial release of cytochrome in CD95 (Fas/Apo-1)-negative monocytic Mono Mac 6 cells, indicating that -induced apoptosis is mediated via the mitochondrial signalling pathway. In addition, blocking of the death receptor pathway at distinct stages using CD95-, FADD- or caspase-8-deficient Jurkat cells did not affect induction of apoptosis by . Conversely, inhibition of the mitochondrial death pathway by overexpression of the anti-apoptotic protein Bcl-2 potently inhibited the processing of caspases and the induction of apoptosis. Therefore, these findings support a model in which the induction of apoptosis by is mediated by activation of the intrinsic mitochondrial death pathway in the absence of external death receptor signalling.

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2002-11-01
2021-10-27
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References

  1. Bantel H, Engels I. H, Voelter W, Schulze-Osthoff K., Wesselborg S. 1999; Mistletoe lectin activates caspase-8/FLICE independently of death receptor signaling and enhances anticancer drug-induced apoptosis. Cancer Res 59:2083–2090
    [Google Scholar]
  2. Baran J, Weglarczyk K, Mysiak M, Guzik K, Ernst M, Flad H. D., Pryjma J. 2001; Fas (CD95)-Fas ligand interactions are responsible for monocyte apoptosis occurring as a result of phagocytosis and killing of Staphylococcus aureus . Infect Immun 69:1287–1297
    [Google Scholar]
  3. Barnett-Foster D, Abul-Milh M, Huesca M., Lingwood C. A. 2000; Enterohemorrhagic Escherichia coli induces apoptosis which augments bacterial binding and phosphatidylethanolamine exposure on the plasma membrane outer leaflet. Infect Immun 68:3108–3115
    [Google Scholar]
  4. Belka C, Rudner J, Wesselborg S. 7 other authors 2000; Differential role of caspase-8 and BID activation during radiation-and CD95-induced apoptosis. Oncogene 19:1181–1190
    [Google Scholar]
  5. Chinnaiyan A. M, O’Rourke K, Lane B. R., Dixit V. M. 1997; Interaction of CED-4 with CED-3 and CED-9: a molecular framework for cell death. Science 275:1122–1126
    [Google Scholar]
  6. Ciancotto N. P., Fields B. S. 1992; Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc Natl Acad Sci USA 89:5188–5191
    [Google Scholar]
  7. Ciancotto N. P, Eisenstein B. I, Mody C. H., Engleberg N. C. 1990; A mutation in the mip gene results in an attenuation of Legionella pneumophila virulence. J Infect Dis 162:121–126
    [Google Scholar]
  8. Durrbaum-Landmann I, Gercken J, Flad H. D., Ernst M. 1996; Effect of in vitro infection of human monocytes with low numbers of Mycobacterium tuberculosis bacteria on monocyte apoptosis. Infect Immun 64:5384–5389
    [Google Scholar]
  9. Engels I. H, Stepczynska A, Stroh C. 10 other authors 2000; Caspase-8/FLICE functions as an executioner caspase in anticancer drug-induced apoptosis. Oncogene 19:4563–4573
    [Google Scholar]
  10. Fearnhead H. O, Rodriguez J, Govek E. E, Guo W, Kobayashi R, Hannon G., Lazebnik Y. A. 1998; Oncogene-dependent apoptosis is mediated by caspase-9. Proc Natl Acad Sci USA 95:13664–13669
    [Google Scholar]
  11. Ferrari D, Stepczynska A, Los M, Wesselborg S., Schulze-Osthoff K. 1998; Differential regulation and ATP requirement for caspase-8 and caspase-3 activation during CD95- and anticancer drug-induced apoptosis. J Exp Med 188:979–984
    [Google Scholar]
  12. Gao L. Y., Abu-Kwaik Y. 1999a; Apoptosis in macrophages and alveolar epithelial cells during early stages of infection by Legionella pneumophila and its role in cytopathogenicity. Infect Immun 67:862–870
    [Google Scholar]
  13. Gao L. Y., Abu-Kwaik Y. 1999b; Activation of caspase-3 during Legionella pneumophila -induced apoptosis. Infect Immun 67:4886–4894
    [Google Scholar]
  14. Gross A, Terraza A, Ouahrani-Bettache S, Liautard J. P., Dornand J. 2000; In vitro Brucella suis infection prevents the programmed cell death of human monocytic cells. Infect Immun 68:342–351
    [Google Scholar]
  15. Hagele S, Hacker J., Brand B. 1998; Legionella pneumophila kills human phagocytes but not protozoan host cells by inducing apoptotic cell death. FEMS Microbiol Lett 169:51–58
    [Google Scholar]
  16. Hersh D, Monack D. M, Smith M. R, Ghori N, Falkow S., Zychlinsky A. 1999; The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA 96:2396–2401
    [Google Scholar]
  17. Hilbi H, Moss J. E, Hersh D. 7 other authors 1998; Shigella -induced apoptosis is dependent on caspase-1 which binds to IpaB. J Biol Chem 273:32895–32900
    [Google Scholar]
  18. Hutchison M. L, Poxton I. R., Govan J. R. 1998; Burkholderia cepacia produces a hemolysin that is capable of inducing apoptosis and degranulation of mammalian phagocytes. Infect Immun 66:2033–2039
    [Google Scholar]
  19. Jendro M. C, Deutsch T, Korber B, Kohler L, Kuipers J. G, Krausse-Opatz B, Westermann J, Raum E., Zeidler H. 2000; Infection of human monocyte-derived macrophages with Chlamydia trachomatis induces apoptosis of T cells: a potential mechanism for persistent infection. Infect Immun 68:6704–6711
    [Google Scholar]
  20. Jendrossek V, Grassmé H, Mueller I, Lang F., Gulbins E. 2001; Pseudomonas aeruginosa -induced apoptosis involves mitochondria and stress-activated protein kinases. Infect Immun 69:2675–2683
    [Google Scholar]
  21. Jonas D, Walev I, Berger T, Liebetrau M, Palmer M., Bhakdi S. 1994; Novel path to apoptosis: small transmembrane pores created by staphylococcal α-toxin in T lymphocytes evoke internucleosomal DNA degradation. Infect Immun 62:1304–1312
    [Google Scholar]
  22. Juo P, Kuo C. J, Yuan J., Blenis J. 1998; Essential requirement for caspase-8/FLICE in the initiation of the Fas-induced apoptotic cascade. Curr Biol 8:1001–1008
    [Google Scholar]
  23. Juo P, Woo M. S, Kuo C. J, Signorelli P, Biemann H. P, Hannun Y. A., Blenis J. 1999; FADD is required for multiple signaling events downstream of the receptor Fas. Cell Growth Differ 10:797–804
    [Google Scholar]
  24. Kirby J. E, Vogel J. P, Andrews H. L., Isberg R. R. 1998; Evidence for pore-forming ability by Legionella pneumophila . Mol Microbiol 27:323–336
    [Google Scholar]
  25. Klingler K, Tchou-Wong K. M, Brandli O, Aston C, Kim R, Chi C., Rom W. N. 1997; Effects of mycobacteria on regulation of apoptosis in mononuclear phagocytes. Infect Immun 65:5272–5278
    [Google Scholar]
  26. Kohler J. R, Maiwald M, Lueck P. C, Helbig J. H, Hingst V., Sonntag H. G. 1999; Detecting legionellosis by unselected culture of respiratory tract secretions and developing links to hospital water strains. J Hosp Infect 41:301–311
    [Google Scholar]
  27. Monack D. M, Mecsas J, Bouley D., Falkow S. 1998; Yersinia -induced apoptosis in vivo aids in the establishment of a systemic infection of mice. J Exp Med 188:2127–2137
    [Google Scholar]
  28. Muller A, Hacker J., Brand B. C. 1996; Evidence for apoptosis of human macrophage-like HL-60 cells by Legionella pneumophila infection. Infect Immun 64:4900–4906
    [Google Scholar]
  29. Muller A, Gunther D, Dux F, Naumann M, Meyer T. F., Rudel T. 1999; Neisserial porin (PorB) causes rapid calcium influx in target cells and induces apoptosis by the activation of cysteine proteases. EMBO J 18:339–352
    [Google Scholar]
  30. Muller A, Gunther D, Brinkmann V, Hurwitz R, Meyer T. F., Rudel T. 2000; Targeting of the pro-apoptotic VDAC-like porin (PorB) of Neisseria gonorrhoeae to mitochondria of infected cells. EMBO J 19:5332–5343
    [Google Scholar]
  31. Nicoletti I, Migliorati G, Pagliacci M. C, Grignani F., Riccardi C. 1991; A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods 139:271–279
    [Google Scholar]
  32. Palmer L. E, Hobbie S, Galan J. E., Bliska J. B. 1998; YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNF-α production and downregulation of the MAP kinases p38 and JNK. Mol Microbiol 27:953–965
    [Google Scholar]
  33. Quinn F. D, Keen M. G., Tompkins L. S. 1989; Genetic, immunological, and cytotoxic comparisons of Legionella proteolytic activities. Infect Immun 57:2719–2725
    [Google Scholar]
  34. Rajalingam K, Al-Younes H, Muller A, Meyer T. F, Szczepek A. J., Rudel T. 2001; Epithelial cells infected with Chlamydophila pneumoniae ( Chlamydia pneumoniae ) are resistant to apoptosis. Infect Immun 69:7880–7888
    [Google Scholar]
  35. Schemer K, Spiik A. K, Dukuzumuremyi J. M, Neurath M. F, Pettersson S., Wolf-Watz H. 1998; The yopJ locus is required for Yersinia -mediated inhibition of NF-κB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity. Mol Microbiol 28:1067–1079
    [Google Scholar]
  36. Schulze-Osthoff K, Ferrari D, Los M, Wesselborg S., Peter M. E. 1998; Apoptosis signaling by death receptors. Eur J Biochem 254:439–459
    [Google Scholar]
  37. Slee E. A, Harte M. T, Kluck R. M. 9 other authors 1999; Ordering the cytochrome c -initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 144:281–292
    [Google Scholar]
  38. Slee E. A, Keogh S. A., Martin S. J. 2000; Cleavage of BID during cytotoxic drug and UV radiation-induced apoptosis occurs downstream of the point of Bcl-2 action and is catalysed by caspase-3: a potential feedback loop for amplification of apoptosis-associated mitochondrial cytochrome c release. Cell Death Differ 7:556–565
    [Google Scholar]
  39. Stevens P. K., Czuprynski C. J. 1996; Pasteurella haemolytica leukotoxin induces bovine leukocytes to undergo morphologic changes consistent with apoptosis in vitro . Infect Immun 64:2687–2694
    [Google Scholar]
  40. Voll R. E, Herrmann M, Roth E. A, Stach C, Kalden J. R., Girkontaite I. 1997; Immunosuppressive effects of apoptotic cells. Nature 390:350–351
    [Google Scholar]
  41. Walz J. M, Gerhardt H, Faigle M, Wolburg H., Neumeister B. 2000; Legionella species of different human prevalence induce different rates of apoptosis in human monocytic cells. APMIS 108:398–408
    [Google Scholar]
  42. Wang J, Fan X, Lindholm C, Bennett M, O’Connoll J, Shanahan F, Brooks E. G, Reyes V. E., Ernst P. B. 2000; Helicobacter pylori modulates lymphoepithelial cell interactions leading to epithelial cell damage through Fas/Fas ligand interactions. Infect Immun 68:4303–4311
    [Google Scholar]
  43. Wesselborg S, Engels I. H, Rossmann E, Los M., Schulze-Osthoff K. 1999; Anticancer drugs induce caspase-8/FLICE activation and apoptosis in the absence of CD95 receptor/ligand interaction. Blood 93:3053–3063
    [Google Scholar]
  44. Yang J, Liu X, Bhalla K, Kim C. N, Ibrado A. M, Cai J, Peng T. I, Jones D. P., Wang X. 1997; Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129–1132
    [Google Scholar]
  45. Yoshiie K, Kim H. Y, Mott J., Rikihisa Y. 2000; Intracellular infection by the human granulocytic ehrlichiosis agent inhibits human neutrophil apoptosis. Infect Immun 68:1125–1133
    [Google Scholar]
  46. Yrlid U., Wick M. J. 2000; Salmonella -induced apoptosis of infected macrophages results in presentation of a bacteria-encoded antigen after uptake by bystander dendritic cells. J Exp Med 191:613–624
    [Google Scholar]
  47. Ziegler-Heitbrock H. W. L, Thiel E, Futterer A, Herzog V, Wirtz A., Riethmuller G. 1988; Establishment of a human cell line (Mono Mac 6) with characteristics of mature monocytes. Int J Cancer 41:456–461
    [Google Scholar]
  48. Zink S. D, Pedersen L, Cianciotto N. P., Abu-Kwaik Y. 2002; The Dot/Icm typeIV secretion system of Legionella pneumophila is essential for the induction of apoptosis in human macrophages. Infect Immun 70:1657–1663
    [Google Scholar]
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