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Interferon inhibits C-type virus at a posttranscriptional, prerelease step

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Summary

The mode of action of interferon in JLSV 5-cells, chronically infected with Rauscher murine leukemia virus (MLV), was studied by examining the fate of preexisting labelled viral RNA in interferon-treated cells and by determining the infectivity/physical particle ratio of cell-associated and extracellular virus.

Interferon added together with3H-uridine inhibited the production of labelled virus particles even when it was only allowed to act after all viral RNA synthesis had been stopped by actinomycin D. This indicated that the interferon-induced antiviral state primarily functions at a posttranscriptional step. When interferon was given after a3H-uridine pulse label and arrest of label incorporation by glucosamine and unlabelled uridine, it prevented a portion of the preexisting radioactive RNA from occurring in extracellular particles. However, part of the labelled viral RNA had reached a stage beyond which interferon could not prevent it from occurring in extracellular virus particles.

The notion that interferon primarily affects release of fully assembled and enveloped MLV particles may be eliminated: interferon-treatment did not affect the release of particle-bound reverse transcriptase in cells treated with cycloheximide after the antiviral state had been established.

It was confirmed that interferon-treated JLSV 5-cells contained an increased number of virus particles associated with the cell membrane. However, these particles were found to have a reduced infectivity compared to those associated with control cells, thus confirming the view that virions produced by interferon-treated cells are defective; perhaps lacking in certain components.

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References

  1. Allen, P. T., Schellekens, H., van Griensven, L. J. L. D., Billiau, A.: Differential sensitivity of Rauscher murine leukaemia virus (MuLV-R) to interferons in two interferon-responsive cell lines. J. gen. Virol.31, 429–435 (1976).

    Google Scholar 

  2. Baron, S., Buckler, C. E., Dianzani, F.: Some determinants of the interferon-induced antiviral state. In:Wolstenholme, G. E. W., O'Conner, M. (eds.), Ciba Foundation Symposium on Interferon, 186–200. London: J. & A. Churchill Ltd. 1967.

    Google Scholar 

  3. Bassin, R. H., Tuttle, N., Fischinger, P. J.: Rapid culture assay technique for murine leukemia viruses. Nature229, 564–566 (1971).

    Google Scholar 

  4. Billiau, A., Sobis, H., de Somer, P.: Influence of interferon on virus particle formation in different oncornavirus carrier cell lines. Int. J. Cancer12, 646–653 (1973).

    Google Scholar 

  5. Billiau, A., Edy, V. G., Sobis, H., de Somer, P.: Influence of interferon on virusparticle synthesis in oncornavirus-carrier lines. II. Evidence for a direct effect on particle release. Int. J. Cancer14, 335–340 (1974).

    Google Scholar 

  6. Billiau, A., Edy, V. G., de Clercq, E., Heremans, H., de Somer, P.: Influence of interferon on the synthesis of virus particles in oncornavirus carrier cell lines. III. Survey of effects on A-, B- and C-type oncornaviruses. Int. J. Cancer15, 947–953 (1975).

    Google Scholar 

  7. Billiau, A., Heremans, H., Allen, P. T., de Somer, P.: Influence of interferon on the synthesis of virus particles in oncornavirus carrier cell lines. IV. Relevance to the potential application of interferon in natural infectious diseases. J. inf. Dis.133 (suppl.), A 51-A 55 (1976).

    Google Scholar 

  8. Billiau, A., Heremans, H., Allen, P. T., de Maeyer-Guignard, J., de Somer, P.: Trapping of oncornavirus particles at the surface of interferon-treated cells. Virology73, 537–542 (1976).

    Google Scholar 

  9. Chang, E. H., Friedman, R. M.: A large glycoprotein of Moloney leukemia virus derived from interferon-treated cells. Biochem. biophys. Res. Commun.77, 392–398 (1977).

    Google Scholar 

  10. Chang, E. H., Myers, M. W., Wong, P. K. Y., Friedman, R. M.: The inhibitory effect of interferon on a temperature-sensitive mutant of Moloney murine leukemia virus. Virology77, 625–636 (1977).

    Google Scholar 

  11. Chang, E. H., Mims, S. J., Triche, T. J., Friedman, R. M.: Interferon inhibits mouse leukemia virus release: an electron microscope study. J. gen. Virol.34, 363–368 (1977).

    Google Scholar 

  12. Dianzani, F., Baron, S., Buckler, C. E.: Effect of metabolic inhibitors on the antiviral action of the interferon system. In:Rita, G. (ed.), The Interferons, 147–159. New York: Academic Press 1968.

    Google Scholar 

  13. Friedman, R. M.: Inhibition of arbovirus protein synthesis by interferon. J. Virol.2, 1081–1085 (1968).

    Google Scholar 

  14. Friedman, R. M., Ramseur, J. M.: Inhibition of murine leukemia virus production in chronically infected AKR cells: a novel effect of interferon. Proc. Nat. Acad. Sci. U.S.A.71, 3542–3544 (1974).

    Google Scholar 

  15. Friedman, R. M., Chang, E. H., Ramseur, J. M., Myers, M. W.: Interferondirected inhibition of chronic murine leukemia virus production in cell cultures: lack of effect on intracellular viral markers. J. Virol.16, 569–574 (1975).

    Google Scholar 

  16. Friedman, R. M., Costa, J. C., Ramseur, J. M., Myers, M. W., Jay, F. T., Chang, E. H.: Persistence of the viral genome in interferon-treated cells infected with oncogenic or nononcogenic viruses. J. inf. Dis.133 (suppl.), A 43-A 50 (1976).

    Google Scholar 

  17. Miller, M. F., Allen, P. T., Dmochowski, L.: Quantitative studies of oncornaviruses in thin sections. J. gen. Virol.21, 57–68 (1973).

    Google Scholar 

  18. Pitha, P. M., Rowe, W. P., Oxman, M. N.: Effect of interferon on exogenous, endogenous, and chronic murine leukemia virus infection. Virology70, 324–338 (1976).

    Google Scholar 

  19. Pitha, P. M., Staal, S. P., Bolognesi, D. P., Denny, T. P., Rowe, W. P.: Effect of interferon on murine leukemia virus infection. II. Synthesis of viral components in exogenous infection. Virology79, 1–13 (1977).

    Google Scholar 

  20. Russell, W. C., Newman, C., Williamson, D. H.: A simple cytochemical technique for demonstration of DNA in cells infected with mycoplasmas and viruses. Nature253, 461–462 (1975).

    Google Scholar 

  21. Samuel, C. E., Joklik, W. K.: A protein synthesizing system from interferontreated cells that discriminates between cellular and viral messenger RNAs. Virology58, 476–491 (1974).

    Google Scholar 

  22. Scholtissek, C.: Detection of an unstable RNA in chick fibroblasts after reduction of the UTP pool by glucosamine. Europ. J. Biochem.24, 358–365 (1971).

    Google Scholar 

  23. Shapiro, S. Z., Strand, M., Billiau, A.: Synthesis and cleavage processing of oncornavirus proteins during interferon inhibition of virus particle release. Infect. Immun.16, 742–747 (1977).

    Google Scholar 

  24. van Griensven, L. J. L. D., Baudelaire, M. F., Peries, J., Emanoil-Ravicovitch, R., Boiron, M.: Studies on the biosynthesis of murine leukemia virus RNA. I. Some properties of Rauscher leukemia virus isolated from interferon treated JLSV 5 cells (Proc. of the second Lepetit Colloquium), 145–153. Amsterdam: North Holland Publishing Company 1970.

    Google Scholar 

  25. Williams Wertz, G.: Method of examining viral RNA metabolism in cells in culture: metabolism of vesicular stomatitis RNA. J. Virol.16, 1340–1344 (1975).

    Google Scholar 

  26. Wright, B. S., Lasfargues, J. C.: Long-term propagation of the Rauscher murine leukemia virus in tissue culture. J. Nat. Cancer Inst.35, 319–327 (1965).

    Google Scholar 

  27. Wong, P. K. Y., Yuen, P. H., Mac Leod, R., Chang, E. H., Myers, M. W., Friedman, R. M.: The effect of interferon onde novo infection of Moloney murine leukemia virus. Cell10, 245–252 (1977).

    Google Scholar 

  28. Wu, A. M., Reitz, M. S., Paran, M., Gallo, R. C.: Mechanism of stimulation of murine type-C RNA tumor virus production by gluco-corticoids: post-transcriptional effects. J. Virol.14, 802–812 (1974).

    Google Scholar 

  29. Wu, A. M., Schultz, A., Gallo, R. C.: Synthesis of type C virus particles from murine cultured cells induced by iododeoxyuridine. V. Effect of interferon and its interaction with dexamethasone. J. Virol.19, 108–117 (1976).

    Google Scholar 

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Authors and Affiliations

  1. Department of Human Biology, Division of Microbiology, Rega Institute, University of Leuven, Leuven, Belgium

    A. Billiau, H. Heremans & P. de Somer

  2. National Cancer Institute, Frederick Cancer Research Center, Frederick, Maryland, USA

    P. T. Allen

  3. Medical Branch, Department of Microbiology, The University of Texas, Galveston, Texas, USA

    S. Baron

Authors
  1. A. Billiau
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  2. H. Heremans
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  3. P. T. Allen
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  4. S. Baron
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  5. P. de Somer
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Billiau, A., Heremans, H., Allen, P.T. et al. Interferon inhibits C-type virus at a posttranscriptional, prerelease step. Archives of Virology 57, 205–220 (1978). https://doi.org/10.1007/BF01315085

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  • DOI: https://doi.org/10.1007/BF01315085

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