1887

Abstract

The process of cell death caused by influenza virus infection in cultured MDCK and HeLa cells was analysed. This infection gave rise to nuclear fragmentation and chromatin condensation accompanied by chromosomal DNA fragmentation into oligonucleosomes. Chromosomal DNA fragmentation progressed concomitantly with cell lysis of MDCK cells and HeLa cells, producing high and low yields of virus particles, respectively, indicating that the extent of cell lysis was not proportional to the virus production. The endonuclease inhibitor zinc blocked DNA fragmentation in MDCK cells. Cycloheximide inhibited DNA fragmentation as well as cell lysis. Inhibition occurred when the drug was added to the medium within 2 h after infection but not efficiently at 4 h or later. Infection induced the Fas Ag gene, which encodes a possible apoptosis-mediating molecule, in the early infectious stage followed by the expression of Fas Ag on the cell surface. These results suggested that influenza virus infection causes apoptotic death of cultured cells, and their fate might be determined at an early stage of the infection by induction of an apoptotic gene.

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1993-11-01
2021-11-29
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References

  1. Bell D. A., Morrison B., Vandenbygaart P. 1990; Immunogenic DNA-related factors. Nucleosomes spontaneously released from normal murine lymphoid cells stimulate proliferation and immunoglobulin synthesis of normal mouse lymphocytes. Journal of Clinical Investigation 85:1487–1496
    [Google Scholar]
  2. Blakely A., Gorman K., Ostergaard H., Svobovda K., Liu C. C., Young J. D. -E., Clark W. R. 1987; Resistance of cloned cytotoxic T lymphocytes to cell-mediated cytotoxicity. Journal of Experimental Medicine 166:1070–1083
    [Google Scholar]
  3. Clifford L. H., Masur H., Edgar L. C., Whalen G., Rook A. H., Fauci A. S. 1983; Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. New England Journal of Medicine 309:453–458
    [Google Scholar]
  4. Cohen J. J., Duke R. C. 1984; Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death. Journal of Immunology 132:38–42
    [Google Scholar]
  5. Duke R. C., Chervenak R., Cohen J. J. 1983; Endogenous endonuclease–induced DNA fragmentation: an early event in cell-mediated cytolysis. Proceedings of the National Academy of Sciences, U,. S,. A. 80:6361–6365
    [Google Scholar]
  6. Duvall E., Wyllie A. H. 1986; Death and the cell. Immunology Today 7:115–119
    [Google Scholar]
  7. Falk M. H., Trauth B. C., Debatin K. -M., Klas C., Gregory C. D., Rickinson A. B., Calender A., Lenoir G. M., Ellwart J. W., Krammer P. H., Bornkamm G. W. 1992; Expression of the APO-1 antigen in Burkitt lymphoma cell lines correlates with a shift towards a lymphoblastoid phenotype. Blood 79:3300–3306
    [Google Scholar]
  8. Gaido M. L., Cidlowski J. A. 1991; Identification, purification, and characterization of a calcium-dependent endonuclease (NUC 18) from apoptotic rat thymocytes. Journal of Biological Chemistry 266:18580–18585
    [Google Scholar]
  9. Gooding L. R. 1992; Virus proteins that counteract host immune defences. Cell 71:5–7
    [Google Scholar]
  10. Hatada E., Hasegawa M., Mukaigawa J., Shimizu K., Fukuda R. 1989; Control of influenza virus gene expression: quantitative analysis of each viral RNA species in infected cells. Journal of Biochemistry 105:537–546
    [Google Scholar]
  11. Henle G., Girardi A., Henle W. 1955; A non-transmissible cytopathogenic effect of influenza virus in tissue culture accompanied by formation of non–infectious hemagglutinins. Journal of Experimental Medicine 101:25–41
    [Google Scholar]
  12. Itoh N., Yonehara S., Ishii A., Yonehara M., Mizushima S. -L., Sameshima M., Hase A., Seto Y., Nagata S. 1991; The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 66:233–243
    [Google Scholar]
  13. Jones D. P., Mcconkey D. J., Nicotera P., Orrenius S. 1989; Calcium-activated DNA fragmentation in rat liver nuclei. Journal of Biological Chemistry 264:6398–6403
    [Google Scholar]
  14. Kerr J. F. R., Harmon B. V. 1991; Definition and incidence of apoptosis: an historical perspective. In Apoptosis: The Molecular Basis of Cell Death pp 5–29 Edited by Tomei L. D., Cope F. O. New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  15. Kimura-takeuchi M., Majde J. A., Toth L. A., Krueger J. M. 1992; The role of double–stranded RNA in induction of the acute– phase response in an abortive influenza virus infection model. Journal of Infectious Diseases 166:1266–1275
    [Google Scholar]
  16. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227:680–685
    [Google Scholar]
  17. Laurent-crawford A. G., Krust B., Muller S., Riviere Y., Rey-cuille M.-A., Bechet J.-M., Montagnier L., Hovanessian A. 1991; The cytopathic effect of HIV is associated with apoptosis. Virology 185:829–839
    [Google Scholar]
  18. Mcconkey D. J., Nicotera P., Hartzell P., Bellomo G., Wyllie A. H., Orrenius S. 1989; Glucocorticoids activate a suicide process in thymocytes through an elevation of cytosolic Ca2+ concentration. Archives of Biochemistry and Biophysics 269:365–370
    [Google Scholar]
  19. Majde J. A., Brown R. K., Jones M. W., Dieffenbach C. W., Maitra N., Krueger J. M., Cady A. B., Smitka C. W., Maassab H. F. 1991; Detection of toxic viral-associated doublestranded RNA (dsRNA) in influenza-infected lung. Microbial Pathogenesis 10:105–115
    [Google Scholar]
  20. Minor P. D., Dimmock N. J. 1975; Inhibition of synthesis of influenza virus proteins: evidence for two host-cell-dependent events during multiplication. Virology 61:114–123
    [Google Scholar]
  21. Miyawaki T., Uehara T., Nibu R., Tsuji T., Yachie A., Yonehara S., Taniguchi N. 1992; Differential expression of apoptosis–related Fas antigen on lymphocyte subpopulations in human peripheral blood. Journal of Immunology 149:3753–3758
    [Google Scholar]
  22. Murphy B. R., Webster R. G. 1990; Orthomyxoviruses. In Virology 2nd edn, pp 1091–1152 Edited by Fields B. N., Knipe D. M. New York: Raven Press;
    [Google Scholar]
  23. Oehm A., Behrmann I., Falk W., Pawlita M., Maier G., Klas C., Li-weber M., Richards S., Dhein J., Trauth B. C., Ponstingl H., Krammer P. H. 1992; Purification and molecular cloning of the APO-1 cell surface antigen, a member of the tumor necrosis factor/nerve growth factor receptor superfamily. Journal of Biological Chemistry 267:10709–10715
    [Google Scholar]
  24. Rubin B. Y., Smith L. J., Hellermann G. R., Lunn R. M., Richardson N. K., Anderson S. L. 1988; Correlation between the anti-cellular and DNA fragmentation activities of tumor necrosis factor. Cancer Research 48:6006–6010
    [Google Scholar]
  25. Stricker R. B., Mchugh T. M., Moody D. J., Morrow W. J. W., Stites D. P., Shuman M. A., Levy J. A. 1987; An AIDS-related cytotoxic autoantibody reacts with a specific antigen on stimulated CD4+ T cells. Nature, London 327:710–713
    [Google Scholar]
  26. Sweet C., Smith H. 1980; Pathogenicity of influenza virus. Microbiological Reviews 44:303–330
    [Google Scholar]
  27. Trauth B. C., Klas C., Peters A. M. J., Matzku S., Moller P., Falk W., Debatin K. -M., Krammer P. H. 1989; Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 245:301–305
    [Google Scholar]
  28. Uehara T., Miyawaki T., Ohta K., Tamaru Y., Yokoi T., Nakamura S., Taniguchi N. 1992; Apoptotic cell death of primed CD45RCF T lymphocytes in Epstein-Barr virus-induced infectious mononucleosis. Blood 80:452–458
    [Google Scholar]
  29. Umansky S. R. 1991; Apoptotic process in the radiation-induced death of lymphocytes. In Apoptosis: The Molecular Basis of Cell Death pp 193–208 Edited by Tomei L. D., Cope F. O. New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  30. Visvanathan K. V., Goodbourn S. 1989; Double-stranded RNA activates binding of nf–kb to an inducible element in the human β-interferon promoter. EMBO Journal 8:1129–1138
    [Google Scholar]
  31. Webster R. G., Rott R. 1987; Influenza virus A pathogenicity: the pivotal role of hemagglutinin. Cell 50:665–666
    [Google Scholar]
  32. Wyllie A. H., Kerr J. f. R., Currie A. R. 1980; Cell death: the significance of apoptosis. International Review of Cytology 68:251–306
    [Google Scholar]
  33. Wyllie A. H., Morris R. G., Smith A. L., Dunlop D. 1984; Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. Journal of Pathology 142:67–77
    [Google Scholar]
  34. Yonehara S., Ishii A., Yonehara M. 1989; A cell–killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. Journal of Experimental Medicine 169:1747–1756
    [Google Scholar]
  35. Zheng L. M., Zychlinsky A., Liu C. -C., Ojcius D. M., Young J. D. -E. 1991; Extracellular ATP as a trigger for apoptosis or programmed cell death. Journal of Cell Biology 112:279–288
    [Google Scholar]
  36. Zinn K., Keller A., Whittemore L. -A., Maniatis T. 1988; 2-Aminopurine selectively inhibits the induction of β-interferon, c–fos, and c–myc gene expression. Science 240:210–213
    [Google Scholar]
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