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Apoptosis

, Volume 11, Issue 10, pp 1695–1707 | Cite as

Modulation of eukaryotic cell apoptosis by members of the bacterial order Actinomycetales

  • Daniel P. Barry
  • Blaine L. BeamanEmail author
Review

Abstract

Apoptosis, or programmed cell death, is normally responsible for the orderly elimination of aged or damaged cells, and is a necessary part of the homeostasis and development of multicellular organisms. Some pathogenic bacteria can disrupt this process by triggering excess apoptosis or by preventing it when appropriate. Either event can lead to disease. There has been extensive research into the modulation of host cell death by microorganisms, and several reviews have been published on the phenomenon. Rather than covering the entire field, this review focuses on the dysregulation of host cell apoptosis by members of the order Actinomycetales, containing the genera Corynebacterium, Mycobacterium, Rhodococcus, and Nocardia.

Keywords

Apoptosis Bacteria Mycobacterium tuberculosis Nocardia asteroides Caspases Lipoarabinomannan 

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References

  1. 1.
    DeLeo FR (2004) Modulation of phagocyte apoptosis by bacterial pathogens. Apoptosis 9:399–413PubMedGoogle Scholar
  2. 2.
    Gao L, Abu Kwaik Y (2000) Hijacking of apoptotic pathways by bacterial pathogens. Microbes Infect 2:1705–1719PubMedGoogle Scholar
  3. 3.
    Moss JE, Aliprantis AO, Zychlinsky A (1999) The regulation of apoptosis by microbial pathogens. Int Rev Cytol 187:203–259PubMedGoogle Scholar
  4. 4.
    Weinrauch Y, Zychlinsky A (1999) The induction of apoptosis by bacterial pathogens. Annu Rev Microbiol 53:155–187PubMedGoogle Scholar
  5. 5.
    Raffray M, Cohen GM (1997) Apoptosis and necrosis in toxicology: a continuum or distinct modes of cell death? Pharmacol Ther 75:153–177PubMedGoogle Scholar
  6. 6.
    Edinger AL, Thompson CB (2004) Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 16:663–669PubMedGoogle Scholar
  7. 7.
    Rossi D, Gaidano G (2003) Messengers of cell death: apoptotic signaling in health and disease. Haematologica 88:212–218PubMedGoogle Scholar
  8. 8.
    Cande C, Cecconi F, Dessen P, Kroemer G (2002) Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J Cell Sci 115:4727–4734PubMedGoogle Scholar
  9. 9.
    Schwartz DA, Wharton M. Diphtheria. (1998) In: Horsburgh CR, Nelson AM, (eds) Pathology of emerging infections 2. ASM Press, Washington D.C., pp 145–166Google Scholar
  10. 10.
    Chen Y, Zychlinsky A (1994) Apoptosis induced by bacterial pathogens. Microb Pathog 17:203–212PubMedGoogle Scholar
  11. 11.
    Kusano I, Kageyama A, Tamura T, Oda T, Muramatsu T (2001) Enhancement of diphtheria toxin-induced apoptosis in Vero cells by combination treatment with brefeldin A and okadaic acid. Cell Struct Funct 26:279–288PubMedGoogle Scholar
  12. 12.
    Lesieur C, Vecsey-Semjen B, Abrami L, Fivaz M, Gisou van der Goot F (1997) Membrane insertion: the strategies of toxins (review). Mol Membr Biol 14:45–64PubMedCrossRefGoogle Scholar
  13. 13.
    Komatsu N, Oda T, Muramatsu T (1998) Involvement of both caspase-like proteases and serine proteases in apoptotic cell death induced by ricin, modeccin, diphtheria toxin, and pseudomonas toxin. J Biochem (Tokyo) 124:1038–1044Google Scholar
  14. 14.
    Brinkmann U, Mansfield E, Pastan I (1997) Effects of BCL-2 overexpression on the sensitivity of MCF-7 breast cancer cells to ricin, diphtheria and Pseudomonas toxin and immunotoxins. Apoptosis 2:192–198PubMedGoogle Scholar
  15. 15.
    Thorburn J, Frankel AE, Thorburn A (2003) Apoptosis by leukemia cell-targeted diphtheria toxin occurs via receptor-independent activation of Fas-associated death domain protein. Clin Cancer Res 9:861–865PubMedGoogle Scholar
  16. 16.
    Kochi SK, Collier RJ (1993) DNA fragmentation and cytolysis in U937 cells treated with diphtheria toxin or other inhibitors of protein synthesis. Exp Cell Res 208:296–302PubMedGoogle Scholar
  17. 17.
    Chang MP, Bramhall J, Graves S, Bonavida B, Wisnieski BJ (1989) Internucleosomal DNA cleavage precedes diphtheria toxin-induced cytolysis. Evidence that cell lysis is not a simple consequence of translation inhibition. J Biol Chem 264:15261–15267PubMedGoogle Scholar
  18. 18.
    Morimoto H, Bonavida B (1992) Diphtheria toxin- and Pseudomonas A toxin-mediated apoptosis. ADP ribosylation of elongation factor-2 is required for DNA fragmentation and cell lysis and synergy with tumor necrosis factor-alpha. J Immunol 149:2089–2094PubMedGoogle Scholar
  19. 19.
    Sandvig K, van Deurs B (1992) Toxin-induced cell lysis: protection by 3-methyladenine and cycloheximide. Exp Cell Res 200:253–262PubMedGoogle Scholar
  20. 20.
    Brinkmann U, Brinkmann E, Gallo M, Pastan I (1995) Cloning and characterization of a cellular apoptosis susceptibility gene, the human homologue to the yeast chromosome segregation gene CSE1. Proc Natl Acad Sci USA 92:10427–10431PubMedGoogle Scholar
  21. 21.
    Brinkmann U, Brinkmann E, Gallo M, Scherf U, Pastan I (1996) Role of CAS, a human homologue to the yeast chromosome segregation gene CSE1, in toxin and tumor necrosis factor mediated apoptosis. Biochemistry 35:6891–6899PubMedGoogle Scholar
  22. 22.
    Kageyama A, Kusano I, Tamura T, Oda T, Muramatsu T (2002) Comparison of the apoptosis-inducing abilities of various protein synthesis inhibitors in U937 cells. Biosci Biotechnol Biochem 66:835–839PubMedGoogle Scholar
  23. 23.
    Chang MP, Baldwin RL, Bruce C, Wisnieski BJ (1989) Second cytotoxic pathway of diphtheria toxin suggested by nuclease activity. Science 246:1165–1168PubMedGoogle Scholar
  24. 24.
    Brinkmann U, Brinkmann E, Pastan I (1995) Expression cloning of cDNAs that render cancer cells resistant to Pseudomonas and diphtheria toxin and immunotoxins. Mol Med 1:206–216PubMedGoogle Scholar
  25. 25.
    Oddo M, Renno T, Attinger A et al. (1998) Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. J Immunol 160:5448–5454PubMedGoogle Scholar
  26. 26.
    Duan L, Gan H, Golan DE, Remold HG (2002) Critical role of mitochondrial damage in determining outcome of macrophage infection with Mycobacterium tuberculosis. J Immunol 169:5181–5187PubMedGoogle Scholar
  27. 27.
    Keane J, Shurtleff B, Kornfeld H (2002) TNF-dependent BALB/c murine macrophage apoptosis following Mycobacterium tuberculosis infection inhibits bacillary growth in an IFN-gamma independent manner. Tuberculosis (Edinb) 82:55–61Google Scholar
  28. 28.
    Lopez M, Sly LM, Luu Y et al. (2003) The 19-kDa Mycobacterium tuberculosis protein induces macrophage apoptosis through Toll-like receptor-2. J Immunol 170:2409–2416PubMedGoogle Scholar
  29. 29.
    Sly LM, Hingley-Wilson SM, Reiner NE, McMaster WR (2003) Survival of Mycobacterium tuberculosis in host macrophages involves resistance to apoptosis dependent upon induction of antiapoptotic Bcl-2 family member Mcl-1. J Immunol 170:430–437PubMedGoogle Scholar
  30. 30.
    Keane J, Balcewicz-Sablinska MK, Remold HG et al. (1997) Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect Immun 65:298–304PubMedGoogle Scholar
  31. 31.
    Balcewicz-Sablinska MK, Keane J, Kornfeld H, Remold HG (1998) Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-alpha. J Immunol 161:2636–2641PubMedGoogle Scholar
  32. 32.
    Keane J, Remold HG, Kornfeld H (2000) Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol 164:2016–2020PubMedGoogle Scholar
  33. 33.
    Danelishvili L, McGarvey J, Li YJ, Bermudez LE (2003) Mycobacterium tuberculosis infection causes different levels of apoptosis and necrosis in human macrophages and alveolar epithelial cells. Cell Microbiol 5:649–660PubMedGoogle Scholar
  34. 34.
    Riendeau CJ, Kornfeld H (2003) THP-1 cell apoptosis in response to mycobacterial infection. Infect Immun 71:254–259PubMedGoogle Scholar
  35. 35.
    Spira A, Carroll JD, Liu G et al. (2003) 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 29:545–551PubMedGoogle Scholar
  36. 36.
    Rojas M, Barrera LF, Puzo G, Garcia LF (1997) Differential induction of apoptosis by virulent Mycobacterium tuberculosis in resistant and susceptible murine macrophages: role of nitric oxide and mycobacterial products. J Immunol 159:1352–1361PubMedGoogle Scholar
  37. 37.
    Abarca-Rojano E, Rosas-Medina P, Zamudio-Cortez P, Mondragon-Flores R, Sanchez-Garcia FJ (2003) Mycobacterium tuberculosis virulence correlates with mitochondrial cytochrome c release in infected macrophages. Scand J Immunol 58:419–427PubMedGoogle Scholar
  38. 38.
    Perskvist N, Long M, Stendahl O, Zheng L (2002) Mycobacterium tuberculosis promotes apoptosis in human neutrophils by activating caspase-3 and altering expression of Bax/Bcl-xL via an oxygen-dependent pathway. J Immunol 168:6358–6365PubMedGoogle Scholar
  39. 39.
    Watson VE, Hill LL, Owen-Schaub LB et al. (2000) Apoptosis in Mycobacterium tuberculosis infection in mice exhibiting varied immunopathology. J Pathol 190:211–220PubMedGoogle Scholar
  40. 40.
    Placido R, Mancino G, Amendola A et al. (1997) Apoptosis of human monocytes/macrophages in Mycobacterium tuberculosis infection. J Pathol 181:31–38PubMedGoogle Scholar
  41. 41.
    Ragno S, Estrada-Garcia I, Butler R, Colston MJ (1998) Regulation of macrophage gene expression by Mycobacterium tuberculosis: down-regulation of mitochondrial cytochrome c oxidase. Infect Immun 66:3952–3958PubMedGoogle Scholar
  42. 42.
    Nuzzo I, Galdiero M, Bentivoglio C, Galdiero R, Romano Carratelli C (2002) Apoptosis modulation by mycolic acid, tuberculostearic acid and trehalose 6,6’-dimycolate. J Infect 44:229–235PubMedGoogle Scholar
  43. 43.
    Klingler K, Tchou-Wong KM, Brandli O et al. (1997) Effects of mycobacteria on regulation of apoptosis in mononuclear phagocytes. Infect Immun 65:5272–5278PubMedGoogle Scholar
  44. 44.
    Das SD, Subramanian D, Prabha C (2004) Cell proliferation and apoptosis: dual-signal hypothesis tested in tuberculous pleuritis using mycobacterial antigens. FEMS Immunol Med Microbiol 41:85–92PubMedGoogle Scholar
  45. 45.
    Rojas M, Olivier M, Garcia LF (2002) Activation of JAK2/STAT1-alpha-dependent signaling events during Mycobacterium tuberculosis-induced macrophage apoptosis. Cell Immunol 217:58–66PubMedGoogle Scholar
  46. 46.
    Aleman M, Schierloh P, de la Barrera SS et al. (2004) Mycobacterium tuberculosis triggers apoptosis in peripheral neutrophils involving toll-like receptor 2 and p38 mitogen protein kinase in tuberculosis patients. Infect Immun 72:5150–5158PubMedGoogle Scholar
  47. 47.
    Ciaramella A, Cavone A, Santucci MB et al. (2004) Induction of apoptosis and release of interleukin-1 beta by cell wall-associated 19-kDa lipoprotein during the course of mycobacterial infection. J Infect Dis 190:1167–1176PubMedGoogle Scholar
  48. 48.
    Ozeki Y, Kaneda K, Fujiwara N et al. (1997) in vivo induction of apoptosis in the thymus by administration of mycobacterial cord factor (trehalose 6,6’-dimycolate). Infect Immun 65:1793–1799PubMedGoogle Scholar
  49. 49.
    Hamasaki N, Isowa K, Kamada K et al. (2000) in vivo administration of mycobacterial cord factor (Trehalose 6, 6’-dimycolate) can induce lung and liver granulomas and thymic atrophy in rabbits. Infect Immun 68:3704–3709PubMedGoogle Scholar
  50. 50.
    Ciaramella A, Martino A, Cicconi R, Colizzi V, Fraziano M (2000) Mycobacterial 19-kDa lipoprotein mediates Mycobacterium tuberculosis-induced apoptosis in monocytes/macrophages at early stages of infection. Cell Death Differ 7:1270–1272PubMedGoogle Scholar
  51. 51.
    Vivekanandhan A, Das S (2001) in vivo study on dual-signal hypothesis of apoptosis using mycobacterial antigen. Curr Sci 81:301–304Google Scholar
  52. 52.
    Rojas M, Olivier M, Gros P, Barrera LF, Garcia LF (1999) TNF-alpha and IL-10 modulate the induction of apoptosis by virulent Mycobacterium tuberculosis in murine macrophages. J Immunol 162:6122–6131PubMedGoogle Scholar
  53. 53.
    Gil DP, Leon LG, Correa LI et al. (2004) Differential induction of apoptosis and necrosis in monocytes from patients with tuberculosis and healthy control subjects. J Infect Dis 189:2120–2128PubMedGoogle Scholar
  54. 54.
    Dao DN, Kremer L, Guerardel Y et al. (2004) Mycobacterium tuberculosis lipomannan induces apoptosis and interleukin-12 production in macrophages. Infect Immun 72:2067–2074PubMedGoogle Scholar
  55. 55.
    Rojas M, Garcia LF, Nigou J, Puzo G, Olivier M (2000) Mannosylated lipoarabinomannan antagonizes Mycobacterium tuberculosis-induced macrophage apoptosis by altering Ca+2-dependent cell signaling. J Infect Dis 182:240–251PubMedGoogle Scholar
  56. 56.
    Maiti D, Bhattacharyya A, Basu J (2001) Lipoarabinomannan from Mycobacterium tuberculosis promotes macrophage survival by phosphorylating Bad through a phosphatidylinositol 3-kinase/Akt pathway. J Biol Chem 276:329–333PubMedGoogle Scholar
  57. 57.
    Guerardel Y, Maes E, Briken V et al. (2003) Lipomannan and lipoarabinomannan from a clinical isolate of Mycobacterium kansasii: novel structural features and apoptosis-inducing properties. J Biol Chem 278:36637–36651PubMedGoogle Scholar
  58. 58.
    Ghosh S, Pal S, Das S, Dasgupta SK, Majumdar S (1998) Lipoarabinomannan induced cytotoxic effects in human mononuclear cells. FEMS Immunol Med Microbiol 21:181–188PubMedGoogle Scholar
  59. 59.
    Cree IA, Nurbhai S, Milne G, Beck JS (1987) Cell death in granulomata: the role of apoptosis. J Clin Pathol 40:1314–1319PubMedGoogle Scholar
  60. 60.
    Mustafa T, Bjune TG, Jonsson R, Pando RH, Nilsen R (2001) Increased expression of fas ligand in human tuberculosis and leprosy lesions: a potential novel mechanism of immune evasion in mycobacterial infection. Scand J Immunol 54:630–639PubMedGoogle Scholar
  61. 61.
    Hirsch CS, Toossi Z, Vanham G et al. (1999) Apoptosis and T cell hyporesponsiveness in pulmonary tuberculosis. J Infect Dis 179:945–953PubMedGoogle Scholar
  62. 62.
    Hirsch CS, Toossi Z, Johnson JL et al. (2001) Augmentation of apoptosis and interferon-gamma production at sites of active Mycobacterium tuberculosis infection in human tuberculosis. J Infect Dis 183:779–788PubMedGoogle Scholar
  63. 63.
    Mustafa T, Phyu S, Nilsen R, Bjune G, Jonsson R (1999) Increased expression of Fas ligand on Mycobacterium tuberculosis infected macrophages: a potential novel mechanism of immune evasion by Mycobacterium tuberculosis ? Inflammation 23:507–521PubMedGoogle Scholar
  64. 64.
    Ciaramella A, Cavone A, Santucci MB et al. (2002) Proinflammatory cytokines in the course of Mycobacterium tuberculosis-induced apoptosis in monocytes/macrophages. J Infect Dis 186:1277–1282PubMedGoogle Scholar
  65. 65.
    Duan L, Gan H, Arm J, Remold HG (2001) Cytosolic phospholipase A2 participates with TNF-alpha in the induction of apoptosis of human macrophages infected with Mycobacterium tuberculosis H37Ra. J Immunol 166:7469–7476PubMedGoogle Scholar
  66. 66.
    Santucci MB, Ciaramella A, Mattei M, Sumerska T, Fraziano M (2003) Batimastat reduces Mycobacterium tuberculosis-induced apoptosis in macrophages. Int Immunopharmacol 3:1657–1665PubMedGoogle Scholar
  67. 67.
    Means TK, Jones BW, Schromm AB et al. (2001) Differential effects of a Toll-like receptor antagonist on Mycobacterium tuberculosis-induced macrophage responses. J Immunol 166:4074–4082PubMedGoogle Scholar
  68. 68.
    Li B, Bassiri H, Rossman MD et al. (1998) Involvement of the Fas/Fas ligand pathway in activation-induced cell death of mycobacteria-reactive human gamma delta T cells: a mechanism for the loss of gamma delta T cells in patients with pulmonary tuberculosis. J Immunol 161:1558–1567PubMedGoogle Scholar
  69. 69.
    Durrbaum-Landmann I, Gercken J, Flad HD, Ernst M (1996) Effect of in vitro infection of human monocytes with low numbers of Mycobacterium tuberculosis bacteria on monocyte apoptosis. Infect Immun 64:5384–5389PubMedGoogle Scholar
  70. 70.
    McGarvey JA, Wagner D, Bermudez LE (2004) Differential gene expression in mononuclear phagocytes infected with pathogenic and non-pathogenic mycobacteria. Clin Exp Immunol 136:490–500PubMedGoogle Scholar
  71. 71.
    Mogga SJ, Mustafa T, Sviland L, Nilsen R (2002) Increased Bcl-2 and reduced Bax expression in infected macrophages in slowly progressive primary murine Mycobacterium tuberculosis infection. Scand J Immunol 56:383–391PubMedGoogle Scholar
  72. 72.
    Briken V, Porcelli SA, Besra GS, Kremer L (2004) Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response. Mol Microbiol 53:391–403PubMedGoogle Scholar
  73. 73.
    Rojas M, Barrera LF, Garcia LF (1998) Induction of apoptosis in murine macrophages by Mycobacterium tuberculosis is reactive oxygen intermediates-independent. Biochem Biophys Res Commun 247:436–442PubMedGoogle Scholar
  74. 74.
    Toossi Z, Hamilton BD, Phillips MH et al. (1997) Regulation of nuclear factor-kappa B and its inhibitor I kappa B-alpha/MAD-3 in monocytes by Mycobacterium tuberculosis and during human tuberculosis. J Immunol 159:4109–4116PubMedGoogle Scholar
  75. 75.
    Kornfeld H, Mancino G, Colizzi V (1999) The role of macrophage cell death in tuberculosis. Cell Death Differ 6:71–78PubMedGoogle Scholar
  76. 76.
    Ahmad A, Khan M, Raykundalia C, Catty D (1999) Study of the mechanisms of killing of Mycobacterium bovis BCG by apoptosis in J774 murine macrophages. J Pak Med Assoc 49:273–278PubMedGoogle Scholar
  77. 77.
    Kremer L, Estaquier J, Wolowczuk I et al. (2000) Ineffective cellular immune response associated with T-cell apoptosis in susceptible Mycobacterium bovis BCG-infected mice. Infect Immun 68:4264–4273PubMedGoogle Scholar
  78. 78.
    Gutierrez-Pabello JA, McMurray DN, Adams LG (2002) Upregulation of thymosin beta-10 by Mycobacterium bovis infection of bovine macrophages is associated with apoptosis. Infect Immun 70:2121–2127PubMedGoogle Scholar
  79. 79.
    van Faassen H, Dudani R, Krishnan L, Sad S (2004) Prolonged antigen presentation, APC-, and CD8+ T cell turnover during mycobacterial infection: comparison with Listeria monocytogenes. J Immunol 172:3491–3500PubMedGoogle Scholar
  80. 80.
    Tokunaga T, Yamamoto H, Shimada S et al. (1984) Antitumor activity of deoxyribonucleic acid fraction from Mycobacterium bovis BCG. I. Isolation, physicochemical characterization, and antitumor activity. J Natl Cancer Inst 72:955–962PubMedGoogle Scholar
  81. 81.
    Lee CF, Chang SY, Hsieh DS, Yu DS (2004) Treatment of bladder carcinomas using recombinant BCG DNA vaccines and electroporative gene immunotherapy. Cancer Gene Ther 11:194–207PubMedGoogle Scholar
  82. 82.
    Hersh D, Weiss J, Zychlinsky A (1998) How bacteria initiate inflammation: aspects of the emerging story. Curr Opin Microbiol 1:43–48PubMedGoogle Scholar
  83. 83.
    Kremer L, Estaquier J, Brandt E, Ameisen JC, Locht C (1997) Mycobacterium bovis Bacillus Calmette Guerin infection prevents apoptosis of resting human monocytes. Eur J Immunol 27:2450–2456PubMedGoogle Scholar
  84. 84.
    Hall AK (1995) Thymosin beta-10 accelerates apoptosis. Cell Mol Biol Res 41:167–180PubMedGoogle Scholar
  85. 85.
    Molloy A, Laochumroonvorapong P, Kaplan G. (1994) Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin. J Exp Med 180:1499–1509PubMedGoogle Scholar
  86. 86.
    Horsburgh CR, Nelson AM (1998) Mycobacterium avium. In: Horsburgh CR, Nelson AM, (eds) Pathology of emerging infections 2. ASM Press, Washington D.C., pp 193–216Google Scholar
  87. 87.
    Gan H, Newman GW, Remold HG (1995) Plasminogen activator inhibitor type 2 prevents programmed cell death of human macrophages infected with Mycobacterium avium, serovar 4. J Immunol 155:1304–1315PubMedGoogle Scholar
  88. 88.
    Fratazzi C, Arbeit RD, Carini C, Remold HG (1997) Programmed cell death of Mycobacterium avium serovar 4-infected human macrophages prevents the mycobacteria from spreading and induces mycobacterial growth inhibition by freshly added, uninfected macrophages. J Immunol 158:4320–4327PubMedGoogle Scholar
  89. 89.
    Balcewicz-Sablinska MK, Gan H, Remold HG(1999) Interleukin 10 produced by macrophages inoculated with Mycobacterium avium attenuates mycobacteria-induced apoptosis by reduction of TNF-alpha activity. J Infect Dis 180:1230–1237PubMedGoogle Scholar
  90. 90.
    Bermudez LE, Parker A, Petrofsky M (1999) Apoptosis of Mycobacterium avium-infected macrophages is mediated by both tumour necrosis factor (TNF) and Fas, and involves the activation of caspases. Clin Exp Immunol 116:94–99PubMedGoogle Scholar
  91. 91.
    Mohagheghpour N, van Vollenhoven A, Goodman J, Bermudez LE (2000) Interaction of Mycobacterium avium with human monocyte-derived dendritic cells. Infect Immun 68:5824–5829PubMedGoogle Scholar
  92. 92.
    Allen S, Sotos J, Sylte MJ, Czuprynski CJ (2001) Use of Hoechst 33342 staining to detect apoptotic changes in bovine mononuclear phagocytes infected with Mycobacterium avium subsp. paratuberculosis. Clin Diagn Lab Immunol 8:460–464PubMedGoogle Scholar
  93. 93.
    Bhattacharyya A, Pathak S, Basak C et al. (2003) Execution of macrophage apoptosis by Mycobacterium avium through apoptosis signal-regulating kinase 1/p38 mitogen-activated protein kinase signaling and caspase 8 activation. J Biol Chem 278:26517–26525PubMedGoogle Scholar
  94. 94.
    Weiss DJ, Evanson OA, Deng M, Abrahamsen MS (2004) Sequential patterns of gene expression by bovine monocyte-derived macrophages associated with ingestion of mycobacterial organisms. Microb Pathog 37:215–224PubMedGoogle Scholar
  95. 95.
    Weiss DJ, Evanson OA, Deng M, Abrahamsen MS (2004) Gene expression and antimicrobial activity of bovine macrophages in response to Mycobacterium avium subsp. paratuberculosis. Vet Pathol 41:326–337PubMedGoogle Scholar
  96. 96.
    Hayashi T, Catanzaro A, Rao SP (1997) Apoptosis of human monocytes and macrophages by Mycobacterium avium sonicate. Infect Immun 65:5262–5271PubMedGoogle Scholar
  97. 97.
    Gilbertson B, Zhong J, Cheers C (1999) Anergy, IFN-gamma production, and apoptosis in terminal infection of mice with Mycobacterium avium. J Immunol 163:2073–2080PubMedGoogle Scholar
  98. 98.
    Zhong J, Gilbertson B, Cheers C (2003) Apoptosis of CD4+ and CD8+ T cells during experimental infection with Mycobacterium avium is controlled by Fas/FasL and Bcl-2-sensitive pathways, respectively. Immunol Cell Biol 81:480–486PubMedGoogle Scholar
  99. 99.
    Cree IA, Gardiner CA, Beck JS, Mehta J (1986) Studies of cell death (apoptosis) and cell division in leprosy granulomas. Int J Lepr Other Mycobact Dis 54:607–613PubMedGoogle Scholar
  100. 100.
    Walsh DS, Lane JE, Abalos RM, Myint KS (2004) TUNEL and limited immunophenotypic analyses of apoptosis in paucibacillary and multibacillary leprosy lesions. FEMS Immunol Med Microbiol 41:265–269PubMedGoogle Scholar
  101. 101.
    Hernandez MO, Neves I, Sales JS et al. (2003) Induction of apoptosis in monocytes by Mycobacterium leprae in vitro: a possible role for tumour necrosis factor-alpha. Immunology 109:156–164PubMedGoogle Scholar
  102. 102.
    Rambukkana A, Zanazzi G, Tapinos N, Salzer JL (2002) Contact-dependent demyelination by Mycobacterium leprae in the absence of immune cells. Science 296:927–931PubMedGoogle Scholar
  103. 103.
    Oliveira RB, Ochoa MT, Sieling PA et al. (2003) Expression of Toll-like receptor 2 on human Schwann cells: a mechanism of nerve damage in leprosy. Infect Immun 71:1427–1433PubMedGoogle Scholar
  104. 104.
    Filion MC, Lepicier P, Morales A, Phillips NC (1999) Mycobacterium phlei cell wall complex directly induces apoptosis in human bladder cancer cells. Br J Cancer 79:229–235PubMedGoogle Scholar
  105. 105.
    Filion MC, Phillips NC (2001) Therapeutic potential of mycobacterial cell wall-DNA complexes. Expert Opin Investig Drugs 10:2157–2165PubMedGoogle Scholar
  106. 106.
    Reader S, Menard S, Filion B, Filion MC, Phillips NC (2001) Pro-apoptotic and immunomodulatory activity of a mycobacterial cell wall-DNA complex towards LNCaP prostate cancer cells. Prostate 49:155–165PubMedGoogle Scholar
  107. 107.
    George KM, Pascopella L, Welty DM, Small PL (2000) A Mycobacterium ulcerans toxin, mycolactone, causes apoptosis in guinea pig ulcers and tissue culture cells. Infect Immun 68:877–883PubMedGoogle Scholar
  108. 108.
    Trebichavsky I, Barot-Ciorbaru R, Charley B, Splichal I (1993) Induction of inflammatory cytokines by Nocardia fractions. Folia Biol (Praha) 39:243–249Google Scholar
  109. 109.
    Tam S, Barry DP, Beaman L, Beaman BL (2002) Neuroinvasive Nocardia asteroides GUH-2 induces apoptosis in the substantia nigra in vivo and dopaminergic cells in vitro. Exp Neurol 177:453–460PubMedGoogle Scholar
  110. 110.
    Camp DM, Loeffler DA, Razoky BA et al. (2003) Nocardia asteroides culture filtrates cause dopamine depletion and cytotoxicity in PC12 cells. Neurochem Res 28:1359–1367PubMedGoogle Scholar
  111. 111.
    Loeffler DA, Camp DM, Qu S, Beaman BL, LeWitt PA (2004) Characterization of dopamine-depleting activity of Nocardia asteroides strain GUH-2 culture filtrate on PC12 cells. Microb Pathog 37:73–85PubMedGoogle Scholar
  112. 112.
    Sinkora M, Mandel L, Sinkora J et al. (1997) Bacterial immunomodulators affect programmed cell death of mouse spleen lymphocytes. Ann N Y Acad Sci 815:492–495PubMedGoogle Scholar
  113. 113.
    Luhrmann A, Mauder N, Sydor T et al. (2004) Necrotic death of Rhodococcus equi-infected macrophages is regulated by virulence-associated plasmids. Infect Immun 72:853–862PubMedGoogle Scholar

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© Springer Science + Business Media, LLC 2006

Authors and Affiliations

  1. 1.Department of Medical Microbiology and Immunology, School of MedicineUniversity of CaliforniaDavisUSA

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