Cyclic AMP-mediated inhibition of vesicular stomatitis virus and herpes simplex virus replication in mouse macrophage-like cells Free

Abstract

In this study, we have analysed the effects of cAMP inducers on the multiplication of vesicular stomatis virus (VSV) and herpes simplex virus type 1 (HSV-1) in mouse macrophage-like cells. The addition of dibutyryl cAMP (dB-cAMP) or cholera toxin to resting peritoneal macrophages aged or P388D cells resulted in a 10- to 100-fold reduction of VSV yield compared to control cultures. In contrast, no cAMP-dependent inhibition was found in VSV-infected L929 cells. In macrophage-like cells, the dB-cAMP-induced antiviral state was not inhibited by antibodies to interferon (IFN)-α/β and did not correlate with any increase in the intracellular levels of 2–5 oligo(A) synthetase. Dibutyryl cAMP did not inhibit virus yields in mouse macrophages infected with encephalomyocarditis virus. In P388D cells, the addition of dB-cAMP resulted in an approximately 10-fold inhibition of HSV-1 replication with respect to control cultures, as evaluated both by TCID and plaque assays on Vero cells. Dibutyryl cAMP did not affect VSV binding or entry into mouse macrophages and the cAMP-mediated anti-VSV state was significantly reduced by inhibitors of protein kinase C (i.e. staurosporine and H7). These data suggest that macrophages may acquire resistance to infection by VSV and HSV-1 after treatment with cAMP inducers. This cAMP-mediated antiviral activity does not depend on the modulation of the endogenous IFN system, suggesting that macrophages exhibit multiple resistance mechanisms (i.e. IFN-dependent and IFN-independent) to maintain their intrinsic antiviral activity.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-73-11-2949
1992-11-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/73/11/JV0730112949.html?itemId=/content/journal/jgv/10.1099/0022-1317-73-11-2949&mimeType=html&fmt=ahah

References

  1. Allen L. B., Eagle N. C., Huffman J. H., Shuman D. A., Meyer R. B. Jr, Sidwell R. W. 1974; Enhancement of interferon antiviral action in L-cells by cyclic nucleotides. Proceedings of the Society for Experimental Biology and Medicine 146:580–584
    [Google Scholar]
  2. Belardelli F., Ausiello C., Tomasi M., Rossi G. B. 1980; Cholera toxin and its B subunit inhibit interferon effects on virus production and erythroid differentiation of FLC. Virology 107:109120
    [Google Scholar]
  3. Belardelli F., Vignaux F., Proietti E., Gresser I. 1984; Injection of mice with antibody to interferon renders peritoneal macrophages permissive for vesicular stomatitis and encephalomyo-carditis viruses. Proceedings of the National Academy of Sciences, U. S. A. 81:602–606
    [Google Scholar]
  4. Belardelli F., Gessani S., Proietti E., Locardi C., Borghi P., Watanabe Y., Kawade Y., Gresser I. 1987; Studies on the expression of spontaneous and induced interferons in mouse peritoneal cells by means of monoclonal antibodies to mouse interferons. Journal of General Virology 68:2203–2212
    [Google Scholar]
  5. Benedetto A., Rossi G. B., Amici C., Belardelli F., Cioè L., Carruba G., Carrasco L. 1980; Inhibition of animal virus products by means of translation inhibitors impermeable to normal cells. Virology 106:123–132
    [Google Scholar]
  6. Beushausen S., Narindrasorasak S., Sanwal B. D., Dales S. 1987; In vivo and in vitro models of demyelinating disease: activation of the adenylate cyclase system influences JHM virus expression in explanted rat oligodendrocytes. Journal of Virology 61:3795–3803
    [Google Scholar]
  7. Bravo R., Neuberg M., Burckhardt J., Almendral J., Wallich R., Muller R. 1987; Involvement of common and cell type-specific pathways in c-fos gene control: stable induction by cAMP in macrophages. Cell 48:251–260
    [Google Scholar]
  8. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. 1979; Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294–5299
    [Google Scholar]
  9. Di Marzio P., Gessani S., Locardi C., Borghi P., Baglioni C., Belardelli F. 1990; Effects of different biological response modifiers on interferon expression in bacterial lipopolysaccharide (LPS)-responsive and LPS-hyporesponsive mouse peritoneal macrophages. Journal of General Virology 71:2585–2591
    [Google Scholar]
  10. Friedman R. M., Pastan I. 1969; Interferon and cyclic-3′-5′ adenosine monophosphate: potentiation of antiviral activity. Biochemical and Biophysical Research Communications 36:735–740
    [Google Scholar]
  11. Gessani S., Belardelli F., Pecorelli A., Puddu P., Baglioni C. 1989; Bacterial lipopolysaccharide and interferon gamma induce transcription of interferon-beta mRNA and interferon secretion in murine macrophages. Journal of Virology 63:2785–2789
    [Google Scholar]
  12. Gresser I., Belardelli F., Vignaux F., Maury C., Tovey M. G., Maunoury M. T. 1985; Injection of mice with antibody to mouse interferon alpha/beta decreases the level of 2′-5′ oligo-adenylate synthetase in peritoneal macrophages. Journal of Virology 53:221–227
    [Google Scholar]
  13. Hidaka H., Inagaki M., Kawamoto S., Sasaki Y. 1984; Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry 23:5036–5041
    [Google Scholar]
  14. Katakami Y., Nakao Y., Koizumi T., Katakami N., Ogawa R., Fujita T. 1988; Regulation of tumour necrosis factor production by mouse peritoneal macrophages: the role of cellular cyclic-AMP. Immunology 64:719–724
    [Google Scholar]
  15. Koren H. S., Handwerger B. S., Wunderlich J. R. 1975; Identification of macrophage-like characteristics in a cultured murine tumor line. Journal of Immunology 114:894–897
    [Google Scholar]
  16. Kuno S., Veno R., Hayashi O., Nakashima H., Harada S., Yamamoto N. 1986; Prostaglandin E2, a seminal constituent, facilitates the replication of acquired immune deficiency syndrome virus in vitro. Proceedings of the National Academy of Sciences, U. S. A. 83:3487–3492
    [Google Scholar]
  17. Leary K. R., Connor J. R., Morahan P. S. 1985; Comparison of herpes simplex virus type 1 DNA replication and virus production in murine bone marrow-derived and resident peritoneal macrophages. Journal of General Virology 66:1123–1129
    [Google Scholar]
  18. Mogensen G. C. 1979; Role of macrophages in natural resistance to virus infections. Microbiological Reviews 43:1–26
    [Google Scholar]
  19. Morahan P. S., Connor J. N., Leary K. R. 1985; Viruses and the versatile macrophage. British Medical Bulletin 41:15–21
    [Google Scholar]
  20. Muschel R. J., Rosen N., Rosen O. M., Bloom B. R. 1977; Modulation of Fc-mediated phagocytosis by cyclic-AMP and insulin in a macrophage-like cell line. Journal of Immunology 119:1813–1820
    [Google Scholar]
  21. Ohmori Y., Strassman G., Hamilton T. A. 1990; cAMP differentially regulates expression of mRNA encoding IL-lα and IL-1β in murine peritoneal macrophages. Journal of Immunology 145:3333–3339
    [Google Scholar]
  22. Ongradi J., Telekes A. 1990; Relationship between the prostaglandin cascade and virus infection. Acta virologica 34:380–400
    [Google Scholar]
  23. Robbins S. J., Rapp F. 1980; Inhibition of measles virus replication by cyclic-AMP. Virology 106:317–326
    [Google Scholar]
  24. Roesler W. J., Vandenbark G. R., Hanson R. W. 1988; Cyclic AMP and the induction of eukaryotic gene transcription. Journal of Biological Chemistry 263:9063–9066
    [Google Scholar]
  25. Rosen N., Piscitello J., Schneck J., Muschel R. J., Bloom B. R., Rosen O. M. 1979; Properties of protein kinase and adenylate cyclase-deficient variants of a macrophage-like cell line. Cell Physiology 98:125–136
    [Google Scholar]
  26. Santoro M. G., Garaci E., Amici C. 1991; Induction of heat shock protein synthesis by prostaglandins with anti-neoplastic and antiviral activity. In Advances in Prostaglandin, Thromboxane and Leukotriene Research pp. 867–874 Edited by Samuelsson B., Wong P. Y., Sun F. F. New York: Raven Press;
    [Google Scholar]
  27. Sit M. F., Tenney D. J., Rothstein J. L., Morahan P. S. 1988; Effect of macrophage activation on resistance of mouse peritoneal macrophages to infection with herpes simplex virus types 1 and 2. Journal of General Virology 69:1999–2010
    [Google Scholar]
  28. Taffet S. M., Singhel K. J., Overholtzer J. F., Shurtleff S. A. 1989; Regulation of tumour necrosis factor expression in a macrophage-like cell line by lipopolysaccharide and cyclic AMP. Cellular Immunology 120:291–300
    [Google Scholar]
  29. Tamaoki T., Nomoto H., Takahashi I., Kato Y., Morimoto M., Tomita F. 1986; Staurosporine, a potent inhibitor of phospho-lipid/Ca++ dependent protein kinase. Research Communication 135:397–402
    [Google Scholar]
  30. Tannbnbaum C. S., Hamilton T. A. 1989; Lipopolysaccharide-induced gene expression in murine peritoneal macrophages is selectively suppressed by agents that elevate intracellular cAMP. Journal of Immunology 142:1274–1280
    [Google Scholar]
  31. Weber J. M., Stewart R. B. 1975; Cyclic AMP potentiation of interferon antiviral activity and effect of interferon on cellular cyclic AMP levels. Journal of General Virology 28:363–372
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-73-11-2949
Loading
/content/journal/jgv/10.1099/0022-1317-73-11-2949
Loading

Data & Media loading...

Most cited Most Cited RSS feed