1887

Abstract

Maedi–visna virus (MVV) causes encephalitis, pneumonia and arthritis in sheep. , MVV infection and replication lead to strong cytopathic effects characterized by syncytia formation and subsequent cellular lysis. It was demonstrated previously that MVV infection induces cell death of sheep choroid plexus cells (SCPC) by a mechanism that can be associated with apoptotic cell death. Here, the relative implication of several caspases during acute infection with MVV is investigated by employing diverse and strategies. It was demonstrated using specific pairs of caspase substrates and inhibitors that, during infection of SCPC by MVV, the two major pathways of caspase activation (i.e. intrinsic and extrinsic pathways) were stimulated: significant caspase-9 and -8 activities, as well as caspase-3 activity, were detected. To study the role of caspases during MVV infection , specific, cell-permeable, caspase inhibitors were used. First, these results showed that both z-DEVD-FMK (a potent inhibitor of caspase-3-like activities) and z-VAD-FMK (a broad spectrum caspase inhibitor) inhibit caspase-9, -8 and -3 activities. Second, both irreversible caspase inhibitors, z-DEVD-FMK and z-VAD-FMK, delayed MVV-induced cellular lysis as well as virus growth. Third, during SCPC infection by MVV, cells were positively stained with FITC-VAD-FMK, a probe that specifically stains cells containing active caspases. In conclusion, these data suggest that MVV infection induces SCPC cell death by a mechanism that is strongly dependent on active caspases.

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2002-12-01
2019-10-23
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References

  1. Agol, V. I., Belov, G. A., Bienz, K., Egger, D., Kolesnikova, M. S., Raikhlin, N. T., Romanova, L. I., Smirnova, E. A. & Tolskaya, E. A. ( 1998; ). Two types of death of poliovirus-infected cells: caspase involvement in the apoptosis but not cytopathic effect. Virology 252, 343-353.[CrossRef]
    [Google Scholar]
  2. Alnemri, E. S., Livingston, D. J., Nicholson, D. W., Salvesen, G., Thornberry, N. A., Wong, W. W. & Yuan, J. ( 1996; ). Human ICE/CED-3 protease nomenclature. Cell 87, 171.[CrossRef]
    [Google Scholar]
  3. Antoni, B. A., Sabbatini, P., Rabson, A. B. & White, E. ( 1995; ). Inhibition of apoptosis in human immunodeficiency virus-infected cells enhances virus production and facilitates persistent infection. Journal of Virology 69, 2384-2392.
    [Google Scholar]
  4. Banki, K., Hutter, E., Gonchoroff, N. J. & Perl, A. ( 1998; ). Molecular ordering in HIV-induced apoptosis. Oxidative stress, activation of caspases, and cell survival are regulated by transaldolase. Journal of Biological Chemistry 273, 11944-11953.[CrossRef]
    [Google Scholar]
  5. Bertin, J., Mendrysa, S. M., LaCount, D. J., Gaur, S., Krebs, J. F., Armstrong, R. C., Tomaselli, K. J. & Friesen, P. D. ( 1996; ). Apoptotic suppression of baculovirus P35 involves cleavage by and inhibition of a virus-induced CED-3/ICE-like protease. Journal of Virology 70, 6251-6259.
    [Google Scholar]
  6. Bitzer, M., Prinz, F., Bauer, M., Spiegel, M., Neubert, W. J., Gregor, M., Schulze-Osthoff, K. & Lauer, U. ( 1999; ). Sendai virus infection induces apoptosis through activation of caspase-8 (FLICE) and caspase-3 (CPP32). Journal of Virology 73, 702-708.
    [Google Scholar]
  7. Boulakia, C. A., Chen, G., Ng, F. W., Teodoro, J. G., Branton, P. E., Nicholson, D. W., Poirier, G. G. & Shore, G. C. ( 1996; ). Bcl-2 and adenovirus E1B 19 kDa protein prevent E1A-induced processing of CPP32 and cleavage of poly(ADP-ribose) polymerase. Oncogene 12, 529-535.
    [Google Scholar]
  8. Budihardjo, I., Oliver, H., Lutter, M., Luo, X. & Wang, X. ( 1999; ). Biochemical pathways of caspase activation during apoptosis. Annual Review of Cell and Developmental Biology 15, 269-290.[CrossRef]
    [Google Scholar]
  9. Cain, K., Inayat-Hussain, S. H., Couet, C. & Cohen, M. ( 1996; ). A cleavage-site-directed inhibitor of interleukin-1 β-converting enzyme-like proteases inhibits apoptosis in primary cultures of rat hepatocytes. Biochemical Journal 314, 27-32.
    [Google Scholar]
  10. Chinnaiyan, A. M., Woffendin, C., Dixit, V. M. & Nabel, G. J. ( 1997; ). The inhibition of pro-apoptotic ICE-like proteases enhances HIV replication. Nature Medicine 3, 333-337.[CrossRef]
    [Google Scholar]
  11. Chiou, S. K. & White, E. ( 1998; ). Inhibition of ICE-like proteases inhibits apoptosis and increases virus production during adenovirus infection. Virology 244, 108-118.[CrossRef]
    [Google Scholar]
  12. Chuang, L. F., Killam, K. F.Jr & Chuang, R. Y. ( 1993; ). Increased replication of simian immunodeficiency virus in CEM x174 cells by morphine sulfate. Biochemical and Biophysical Research Communications 195, 1165-1173.[CrossRef]
    [Google Scholar]
  13. Clements, J. E. & Zink, M. C. ( 1996; ). Molecular biology and pathogenesis of animal lentivirus infections. Clinical Microbiology Reviews 9, 100-117.
    [Google Scholar]
  14. Cohen, G. M. ( 1997; ). Caspases: the executioners of apoptosis. Biochemical Journal 326, 1-16.
    [Google Scholar]
  15. Duval, R., Delebassée, S., Cardot, P. J. P. & Bosgiraud, C. ( 2002; ). Visna virus-induced cytopathic effect in vitro is caused by apoptosis. Archives of Virology 147, 943-959.[CrossRef]
    [Google Scholar]
  16. Earnshaw, W. C., Martins, L. M. & Kaufmann, S. H. ( 1999; ). Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annual Review of Biochemistry 68, 383-424.[CrossRef]
    [Google Scholar]
  17. Georgsson, G. ( 1994; ). Neuropathologic aspects of lentiviral infections. Annals of the New York Academy of Sciences 724, 50-67.[CrossRef]
    [Google Scholar]
  18. Georgsson, G., Martin, J. R., Klein, J., Palsson, P. A., Nathanson, N. & Petursson, G. P. ( 1982; ). Primary demyelination in visna. An ultrastructural study of Icelandic sheep with clinical signs following experimental infection. Acta Neuropathologica 57, 171-178.[CrossRef]
    [Google Scholar]
  19. Gougeon, M.-L. & Montagnier, L. ( 1999; ). Programmed cell death as a mechanism of CD4 and CD8 T cell deletion in AIDS. Molecular control and effect of highly active anti-retroviral therapy. Annals of the New York Academy of Sciences 887, 199-212.
    [Google Scholar]
  20. Gougeon, M.-L., Ledru, E., Naora, H., Bocchino, M. & Lecoeur, H. ( 2000; ). HIV, cytokines and programmed cell death. A subtle interplay. Annals of the New York Academy of Sciences 926, 30-45.
    [Google Scholar]
  21. Hengartner, M. O. ( 2000; ). The biochemistry of apoptosis. Nature 407, 770-776.[CrossRef]
    [Google Scholar]
  22. Kerr, J. F., Wyllie, A. H. & Currie, A. R. ( 1972; ). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. British Journal of Cancer 26, 239-257.[CrossRef]
    [Google Scholar]
  23. Kidd, V. J. ( 1998; ). Proteolytic activities that mediate apoptosis. Annual Review of Physiology 60, 533-573.[CrossRef]
    [Google Scholar]
  24. Kroemer, G., Zamzami, N. & Susin, S. A. ( 1997; ). Mitochondrial control of apoptosis. Immunology Today 18, 44-51.[CrossRef]
    [Google Scholar]
  25. McCune, J. M. ( 2001; ). The dynamics of CD4+ T-cell depletion in HIV disease. Nature 410, 974-979.[CrossRef]
    [Google Scholar]
  26. MacFarlane, M., Cain, K., Sun, X. M., Alnemri, E. S. & Cohen, G. M. ( 1997; ). Processing/activation of at least four interleukin-1β converting enzyme-like proteases occurs during the execution phase of apoptosis in human monocytic tumor cells. Journal of Cell Biology 137, 469-479.[CrossRef]
    [Google Scholar]
  27. Meier, P., Finch, A. & Evan, G. ( 2000; ). Apoptosis in development. Nature 407, 796-801.[CrossRef]
    [Google Scholar]
  28. Metzstein, M. M., Stanfield, G. M. & Horvitz, H. R. ( 1998; ). Genetics of programmed cell death in C. elegans: past, present and future. Trends in Genetics 14, 410-416.[CrossRef]
    [Google Scholar]
  29. Narayan, O., Wolinsky, J. S., Clements, J. E., Strandberg, J. D., Griffin, D. E. & Cork, L. C. ( 1982; ). Slow virus replication: the role of macrophages in the persistence and expression of visna viruses of sheep and goats. Journal of General Virology 59, 345-356.[CrossRef]
    [Google Scholar]
  30. Nava, V. E., Rosen, A., Veliuona, M. A., Clem, R. J., Levine, B. & Hardwick, J. M. ( 1998; ). Sindbis virus induces apoptosis through a caspase-dependent, CrmA-sensitive pathway. Journal of Virology 72, 452-459.
    [Google Scholar]
  31. Nicholson, D. W. ( 2000; ). From bench to clinic with apoptosis-based therapeutic agents. Nature 407, 810-816.[CrossRef]
    [Google Scholar]
  32. Nicholson, D. W. & Thornberry, N. A. ( 1997; ). Caspases: killer proteases. Trends in Biochemical Sciences 22, 299-306.[CrossRef]
    [Google Scholar]
  33. Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A., Munday, N. A., Raju, S. M., Smulson, M. E., Yamin, T.-T., Yu, V. L. & Miller, D. K. ( 1995; ). Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376, 37-43.[CrossRef]
    [Google Scholar]
  34. O’Brien, V. ( 1998; ). Viruses and apoptosis. Journal of General Virology 79, 1833-1845.
    [Google Scholar]
  35. Pépin, M., Vitu, C., Russo, P., Mornex, J.-F. & Peterhans, E. ( 1998; ). Maedi–visna virus infection in sheep: a review. Veterinary Research 29, 341-367.
    [Google Scholar]
  36. Petursson, G., Nathanson, N., Georgsson, G., Panitch, H. & Palsson, P. A. ( 1976; ). Pathogenesis of visna. I. Sequential, virologic serologic and pathologic studies. Laboratory Investigation 35, 402-412.
    [Google Scholar]
  37. Petursson, G., Palsson, P. A. & Georgsson, G. ( 1989; ). Maedi–visna in sheep: host–virus interactions and utilization as a model. Intervirology 30, 36-44.
    [Google Scholar]
  38. Pugachev, K. V. & Frey, T. K. ( 1998; ). Rubella virus induces apoptosis in culture cells. Virology 250, 359-370.[CrossRef]
    [Google Scholar]
  39. Reed, L. J. & Muench, H. ( 1938; ). A simple method of estimating fifty percent endpoints. American Journal of Hygiene 27, 493-497.
    [Google Scholar]
  40. Roulston, A., Marcellus, R. C. & Branton, P. E. ( 1999; ). Viruses and apoptosis. Annual Review of Microbiology 53, 577-628.[CrossRef]
    [Google Scholar]
  41. Roy, S. & Nicholson, D. W. ( 2000; ). Cross-talk in cell death signaling. Journal of Experimental Medicine 192, 21-26.[CrossRef]
    [Google Scholar]
  42. Ruggieri, A., Harada, T., Matsuura, Y. & Miyamura, T. ( 1997; ). Sensitization to Fas-mediated apoptosis by hepatitis C virus core protein. Virology 229, 68-76.[CrossRef]
    [Google Scholar]
  43. Salvesen, G. S. & Dixit, V. M. ( 1997; ). Caspases: intracellular signaling by proteolysis. Cell 91, 443-446.[CrossRef]
    [Google Scholar]
  44. Sandstrom, P. A., Pardi, D., Goldsmith, C. S., Chengying, D., Diamond, A. M. & Folks, T. M. ( 1996; ). bc1-2 expression facilitates human immunodeficiency virus type-1 mediated cytopathic effects during acute spreading infections. Journal of Virology 70, 4617-4622.
    [Google Scholar]
  45. Shen, Y. & Shenk, T. E. ( 1995; ). Viruses and apoptosis. Current Opinion in Genetics & Development 5, 105-111.[CrossRef]
    [Google Scholar]
  46. Sigurdsson, B. ( 1954; ). Observations on three slow infections of sheep: Maedi, para tuberculosis, rida, a slow encephalitis of sheep with general remarks on infections which develop slowly, and some of their special characteristics. British Veterinary Journal 110, 225-270.
    [Google Scholar]
  47. Slee, E. A., Zhu, H., Chow, S. C., MacFarlane, M., Nicholson, D. W. & Cohen, G. M. ( 1996; ). Benzyloxylcarbonyl–Val–Ala–Asp (Ome) fluromethylketone (Z–VAD.FMF) inhibits apoptosis by blocking the processing of CPP32. Biochemical Journal 315, 21-24.
    [Google Scholar]
  48. Sonigo, P., Alizon, M., Staskus, K., Klatzmann, D., Cole, S., Danos, O., Retzel, E., Tiollais, P., Haase, A. & Wain-Hobson, S. ( 1985; ). Nucleotide sequence of the visna lentivirus: relationship to the AIDS virus. Cell 42, 369-382.[CrossRef]
    [Google Scholar]
  49. Steller, H. ( 1995; ). Mechanisms and genes of cellular suicide. Science 267, 1445-1449.[CrossRef]
    [Google Scholar]
  50. Taddeo, B., Nickoloff, B. J. & Foreman, K. E. ( 2000; ). Caspase inhibitor blocks human immunodeficiency virus 1-induced T-cell death without enhancement of HIV-1 replication and dimethyl sulfoxide increases HIV-1 replication without influencing T-cell survival. Archives of Pathology and Laboratory Medicine 124, 240-245.
    [Google Scholar]
  51. Takahashi, A. & Earnshaw, W. C. ( 1996; ). ICE-related proteases in apoptosis. Current Opinion in Genetics & Development 6, 50-55.[CrossRef]
    [Google Scholar]
  52. Teodoro, J. G. & Branton, P. E. ( 1997; ). Regulation of apoptosis by viral gene products. Journal of Virology 71, 1739-1746.
    [Google Scholar]
  53. Tollefson, A. E., Scaria, A., Hermiston, T. W., Ryerse, J. S., Wold, L. J. & Wold, W. S. ( 1996; ). The adenovirus death protein (E3-11·6K) is required at very late stages of infection for efficient cell lysis and release of adenovirus from infected cells. Journal of Virology 70, 2296-2306.
    [Google Scholar]
  54. Zhivotovsky, B., Gahm, A., Ankarcrona, M., Nicotera, P. & Orrenius, S. ( 1995; ). Multiple proteases are involved in thymocyte apoptosis. Experimental Cell Research 221, 404-412.[CrossRef]
    [Google Scholar]
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