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. 1996 Dec;70(12):8977–8983. doi: 10.1128/jvi.70.12.8977-8983.1996

Apoptosis and T-cell depletion during feline infectious peritonitis.

B L Haagmans 1, H F Egberink 1, M C Horzinek 1
PMCID: PMC190995  PMID: 8971027

Abstract

Cats that have succumbed to feline infectious peritonitis, an immune-mediated disease caused by variants of feline coronaviruses, show apoptosis and T-cell depletion in their lymphoid organs. The ascitic fluid that develops in the course of the condition causes apoptosis in vitro but only in activated T cells. Since feline infectious peritonitis virus does not infect T cells, and viral proteins did not inhibit T-cell proliferation, we postulate that soluble mediators released during the infection cause apoptosis and T-cell depletion.

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Selected References

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  1. Banda N. K., Bernier J., Kurahara D. K., Kurrle R., Haigwood N., Sekaly R. P., Finkel T. H. Crosslinking CD4 by human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis. J Exp Med. 1992 Oct 1;176(4):1099–1106. doi: 10.1084/jem.176.4.1099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cohen J. J., Duke R. C., Fadok V. A., Sellins K. S. Apoptosis and programmed cell death in immunity. Annu Rev Immunol. 1992;10:267–293. doi: 10.1146/annurev.iy.10.040192.001411. [DOI] [PubMed] [Google Scholar]
  3. Dive C., Gregory C. D., Phipps D. J., Evans D. L., Milner A. E., Wyllie A. H. Analysis and discrimination of necrosis and apoptosis (programmed cell death) by multiparameter flow cytometry. Biochim Biophys Acta. 1992 Feb 3;1133(3):275–285. doi: 10.1016/0167-4889(92)90048-g. [DOI] [PubMed] [Google Scholar]
  4. Esolen L. M., Park S. W., Hardwick J. M., Griffin D. E. Apoptosis as a cause of death in measles virus-infected cells. J Virol. 1995 Jun;69(6):3955–3958. doi: 10.1128/jvi.69.6.3955-3958.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Gavrieli Y., Sherman Y., Ben-Sasson S. A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol. 1992 Nov;119(3):493–501. doi: 10.1083/jcb.119.3.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Godfraind C., Holmes K. V., Coutelier J. P. Thymus involution induced by mouse hepatitis virus A59 in BALB/c mice. J Virol. 1995 Oct;69(10):6541–6547. doi: 10.1128/jvi.69.10.6541-6547.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gruber J., Sgonc R., Hu Y. H., Beug H., Wick G. Thymocyte apoptosis induced by elevated endogenous corticosterone levels. Eur J Immunol. 1994 May;24(5):1115–1121. doi: 10.1002/eji.1830240516. [DOI] [PubMed] [Google Scholar]
  8. Hayashi T., Sasaki N., Ami Y., Fujiwara K. Role of thymus-dependent lymphocytes and antibodies in feline infectious peritonitis after oral infection. Nihon Juigaku Zasshi. 1983 Dec;45(6):759–766. doi: 10.1292/jvms1939.45.759. [DOI] [PubMed] [Google Scholar]
  9. Herrewegh A. A., de Groot R. J., Cepica A., Egberink H. F., Horzinek M. C., Rottier P. J. Detection of feline coronavirus RNA in feces, tissues, and body fluids of naturally infected cats by reverse transcriptase PCR. J Clin Microbiol. 1995 Mar;33(3):684–689. doi: 10.1128/jcm.33.3.684-689.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jacobse-Geels H. E., Daha M. R., Horzinek M. C. Isolation and characterization of feline C3 and evidence for the immune complex pathogenesis of feline infectious peritonitis. J Immunol. 1980 Oct;125(4):1606–1610. [PubMed] [Google Scholar]
  11. Jeurissen S. H., Wagenaar F., Pol J. M., van der Eb A. J., Noteborn M. H. Chicken anemia virus causes apoptosis of thymocytes after in vivo infection and of cell lines after in vitro infection. J Virol. 1992 Dec;66(12):7383–7388. doi: 10.1128/jvi.66.12.7383-7388.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lam K. M., Vasconcelos A. C. Newcastle disease virus-induced apoptosis in chicken peripheral blood lymphocytes. Vet Immunol Immunopathol. 1994 Dec;44(1):45–56. doi: 10.1016/0165-2427(94)90168-6. [DOI] [PubMed] [Google Scholar]
  13. Levine B., Huang Q., Isaacs J. T., Reed J. C., Griffin D. E., Hardwick J. M. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature. 1993 Feb 25;361(6414):739–742. doi: 10.1038/361739a0. [DOI] [PubMed] [Google Scholar]
  14. Liu Y., Janeway C. A., Jr Interferon gamma plays a critical role in induced cell death of effector T cell: a possible third mechanism of self-tolerance. J Exp Med. 1990 Dec 1;172(6):1735–1739. doi: 10.1084/jem.172.6.1735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Meyaard L., Otto S. A., Jonker R. R., Mijnster M. J., Keet R. P., Miedema F. Programmed death of T cells in HIV-1 infection. Science. 1992 Jul 10;257(5067):217–219. doi: 10.1126/science.1352911. [DOI] [PubMed] [Google Scholar]
  16. Meyaard L., Otto S. A., Keet I. P., Roos M. T., Miedema F. Programmed death of T cells in human immunodeficiency virus infection. No correlation with progression to disease. J Clin Invest. 1994 Mar;93(3):982–988. doi: 10.1172/JCI117105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mosier D., Sieburg H. Macrophage-tropic HIV: critical for AIDS pathogenesis? Immunol Today. 1994 Jul;15(7):332–339. doi: 10.1016/0167-5699(94)90081-7. [DOI] [PubMed] [Google Scholar]
  18. Moskophidis D., Lechner F., Pircher H., Zinkernagel R. M. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature. 1993 Apr 22;362(6422):758–761. doi: 10.1038/362758a0. [DOI] [PubMed] [Google Scholar]
  19. Muro-Cacho C. A., Pantaleo G., Fauci A. S. Analysis of apoptosis in lymph nodes of HIV-infected persons. Intensity of apoptosis correlates with the general state of activation of the lymphoid tissue and not with stage of disease or viral burden. J Immunol. 1995 May 15;154(10):5555–5566. [PubMed] [Google Scholar]
  20. Pedersen N. C. Virologic and immunologic aspects of feline infectious peritonitis virus infection. Adv Exp Med Biol. 1987;218:529–550. doi: 10.1007/978-1-4684-1280-2_69. [DOI] [PubMed] [Google Scholar]
  21. Razvi E. S., Welsh R. M. Programmed cell death of T lymphocytes during acute viral infection: a mechanism for virus-induced immune deficiency. J Virol. 1993 Oct;67(10):5754–5765. doi: 10.1128/jvi.67.10.5754-5765.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rimstad E., Reubel G. H., Dean G. A., Higgins J., Pedersen N. C. Cloning, expression and characterization of biologically active feline tumour necrosis factor-alpha. Vet Immunol Immunopathol. 1995 Apr;45(3-4):297–310. doi: 10.1016/0165-2427(94)05345-S. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Saha K., Yuen P. H., Wong P. K. Murine retrovirus-induced depletion of T cells is mediated through activation-induced death by apoptosis. J Virol. 1994 Apr;68(4):2735–2740. doi: 10.1128/jvi.68.4.2735-2740.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schijns V. E., Wierda C. M., Vahlenkamp T. W., Horzinek M. C., de Groot R. J. Molecular cloning and expression of cat interferon-gamma. Immunogenetics. 1995;42(5):440–441. doi: 10.1007/BF00179414. [DOI] [PubMed] [Google Scholar]
  25. Shibata S., Kyuwa S., Lee S. K., Toyoda Y., Goto N. Apoptosis induced in mouse hepatitis virus-infected cells by a virus-specific CD8+ cytotoxic T-lymphocyte clone. J Virol. 1994 Nov;68(11):7540–7545. doi: 10.1128/jvi.68.11.7540-7545.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Stoddart C. A., Scott F. W. Intrinsic resistance of feline peritoneal macrophages to coronavirus infection correlates with in vivo virulence. J Virol. 1989 Jan;63(1):436–440. doi: 10.1128/jvi.63.1.436-440.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stoddart M. E., Gaskell R. M., Harbour D. A., Gaskell C. J. Virus shedding and immune responses in cats inoculated with cell culture-adapted feline infectious peritonitis virus. Vet Microbiol. 1988 Feb;16(2):145–158. doi: 10.1016/0378-1135(88)90039-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Surh C. D., Sprent J. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature. 1994 Nov 3;372(6501):100–103. doi: 10.1038/372100a0. [DOI] [PubMed] [Google Scholar]
  29. Terai C., Kornbluth R. S., Pauza C. D., Richman D. D., Carson D. A. Apoptosis as a mechanism of cell death in cultured T lymphoblasts acutely infected with HIV-1. J Clin Invest. 1991 May;87(5):1710–1715. doi: 10.1172/JCI115188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Vennema H., de Groot R. J., Harbour D. A., Dalderup M., Gruffydd-Jones T., Horzinek M. C., Spaan W. J. Early death after feline infectious peritonitis virus challenge due to recombinant vaccinia virus immunization. J Virol. 1990 Mar;64(3):1407–1409. doi: 10.1128/jvi.64.3.1407-1409.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Weller M., Constam D. B., Malipiero U., Fontana A. Transforming growth factor-beta 2 induces apoptosis of murine T cell clones without down-regulating bcl-2 mRNA expression. Eur J Immunol. 1994 Jun;24(6):1293–1300. doi: 10.1002/eji.1830240608. [DOI] [PubMed] [Google Scholar]
  32. Westendorp M. O., Frank R., Ochsenbauer C., Stricker K., Dhein J., Walczak H., Debatin K. M., Krammer P. H. Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature. 1995 Jun 8;375(6531):497–500. doi: 10.1038/375497a0. [DOI] [PubMed] [Google Scholar]
  33. Zheng L., Fisher G., Miller R. E., Peschon J., Lynch D. H., Lenardo M. J. Induction of apoptosis in mature T cells by tumour necrosis factor. Nature. 1995 Sep 28;377(6547):348–351. doi: 10.1038/377348a0. [DOI] [PubMed] [Google Scholar]

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