1887

Abstract

Inhibition of vesicular stomatitis virus (VSV) replication in L cells by interferon (IFN) resembles the action of IFN on some retroviruses, in that the incorporation of glycoprotein into virions is defective. Primary amines added between 1 and 2 h post-infection significantly enhanced (five- to 1000-fold) the antiviral activity of IFN against VSV, but no enhancement of the antiviral activity of IFN against encephalomyocarditis virus, a virus with no membrane component, by primary amines was seen. SDS-PAGE and immunofluorescence analysis of viral proteins, and Nycodenz gradient fractionation, suggested that both IFN and primary amines inhibited the transport of VSV glycoprotein (G) to the plasma membrane; instead, G accumulated in the trans-Golgi network (TGN). Using sensitive intracellular pH (pHi) indicators, we found that IFN treatment significantly raised the pHi. A further increase in pHi was seen with a combination of IFN and primary amines; the increase in pHi correlated with an enhancement of the antiviral activity of IFN by primary amines. Amiloride inhibited the IFN-induced increase in pHi and a concomitant increase in the concentration of Na ions; this observation suggested that IFN induced cytoplasmic alkalinization by activating an Na/H antiporter system. These results indicated that the IFN-induced increase in pHi may be responsible for the accumulation of G in the TGN, thereby producing G-deficient virus particles with reduced infectivity.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-72-9-2143
1991-09-01
2022-10-07
Loading full text...

Full text loading...

/deliver/fulltext/jgv/72/9/JV0720092143.html?itemId=/content/journal/jgv/10.1099/0022-1317-72-9-2143&mimeType=html&fmt=ahah

References

  1. Anderson R. G. W., Pathak R. K. 1985; Vesicles and cisternae in the trans Golgi apparatus of human fibroblasts are acidic compartments. Cell 40:635–643
    [Google Scholar]
  2. Bassnett S., Reinisch L., Beebe D. C. 1990; Intracellular pH measurements using single excitation emission fluorescence ratios. American Journal of Physiology 258:171–178
    [Google Scholar]
  3. Branaca A. A., Faltynek C. R., D’Alessandro S. B., Baglioni C. 1982; Interaction of interferon with cellular receptors, internalization and degradation of cell-bound interferon. Journal of Biological Chemistry 257:13291–13296
    [Google Scholar]
  4. Chatterjee S., Hunter E., Whitley R. 1985; Effect of cloned interferon on protein synthesis and morphogenesis of herpes simplex virus. Journal of Virology 56:419–425
    [Google Scholar]
  5. Civitelli R., Teitelbaum S. L., Hruska K. A., Lacey D. L. 1989; IL-I activates the Na+/H+ antiport in a murine T cell. Journal of Immunology 143:4000–4008
    [Google Scholar]
  6. de Curtis I., Howell K. E., Simons K. 1988; Isolation of a fraction enriched in the trans-Golgi network from baby hamster kidney cells. Experimental Cell Research 175:248–265
    [Google Scholar]
  7. Dille B. J., Johnson T. C. 1982; Inhibition of vesicular stomatitis virus glycoprotein expression by chloroquine. Journal of General Virology 62:91–103
    [Google Scholar]
  8. Doms R. W., Russ G., Yewdell J. W. 1989; Brefeldin A redistributes resident and itinerant Golgi proteins to the endoplasmic reticulum. Journal of Cell Biology 109:61–72
    [Google Scholar]
  9. Drebot M. A., Lee S. H. S., Rozee K. R. 1984; Differential effect of interferon on glycoprotein and membrane protein of vesicular stomatitis virus released from murine and simian cells. Journal of Interferon Research 4:167–172
    [Google Scholar]
  10. Esteban M. 1984; Defective vaccinia virus particles in interferon-treated infected cells. Virology 133:220–227
    [Google Scholar]
  11. Frelin C., Vigne P., Barby M., Lazdunski M. 1987; Molecular properties of amiloride action and its Na+ transporting agent. Kidney International 32:782–793
    [Google Scholar]
  12. Friedman R. M., Pitha P. M. 1984; The effect of interferon on membrane-associated viruses. In Interferon 3, Mechanism of Production and Action pp 319–325 Edited by Friedman R. M. Amsterdam: Elsevier;
    [Google Scholar]
  13. Friedman R. M., Chang E. H., Ramseur J. M., Myers M. W. 1975; Interferon-directed inhibition of chronic murine leukemia virus production in cell cultures; lack of effect on intracellular viral markers. Journal of Virology 10:569–574
    [Google Scholar]
  14. Gendelman H. E., Baca L., Turpin J., Kalter D. C., Hansen B., Orenstein J. M., Friedman R. M., Meltzer M. S. 1990; Regulation of HIV replication in infected T cells and monocytes by interferon: mechanisms for viral replication. Journal of Immunology 145:2669–2676
    [Google Scholar]
  15. Harootunian A. T., Kao J. P. Y., Eckert B. K., Tsein R. Y. 1989; Fluorescence ratio imaging of cytosolic free Na+ in individual fibroblasts and lymphocytes. Journal of Biological Chemistry 264:19458–19467
    [Google Scholar]
  16. Helenius A., Kartenbeck J., Simons K., Fries E. 1980; On the entry of Semliki Forest virus into BHK-21 cells. Journal of Cell Biology 84:404–420
    [Google Scholar]
  17. Ho D. D., Hartshom K. L., Rota T. R., Andrew C. A., Kaplan J. C., Scholley R. T., Hirsch M. S. 1985; Recombinant human interferon alpha-A suppresses HTLVIII replication in vitro. Lancet i:602–604
    [Google Scholar]
  18. Jay F. T., Daywood M. R., Friedman R. M. 1983; Interferon induces the production of membrane protein-deficient and infectivity-defective vesicular stomatitis virions through interference in the virion assembly process. Journal of General Virology 64:707–712
    [Google Scholar]
  19. Kerr I. M., Brown R. E. 1978; ppA2′p5′A2′p5′A: an inhibitor of protein synthesis synthesized with an enzyme fraction from interferon-treated cells. Proceedings of the National Academy of Sciences, U.S.A. 75:256–260
    [Google Scholar]
  20. Koldovsky O., Palmieri M. 1971; Cortisone evoked decrease of acid-β-galactosidase, β-glucuroridase, N-acetyl-β-glucosaminidase and asylsulphatase in the ileum of suckling rats. Biochemical Journal 125:697–701
    [Google Scholar]
  21. Koyama A. H., Uchida T. 1989; The effect of ammonium chloride on the multiplication of herpes simplex virus type I in Vero cells. Virus Research 13:271–282
    [Google Scholar]
  22. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227:680–685
    [Google Scholar]
  23. Maheshwari R. K., Friedman R. M. 1979; Production of vesicular stomatitis virus with low infectivity by interferon-treated cells. Journal of General Virology 44:261–264
    [Google Scholar]
  24. Maheshwari R. K., Friedman R. M. 1980; Effect of interferon treatment on vesicular stomatitis virus (VSV); release of unusual particles with low infectivity. Virology 101:399–407
    [Google Scholar]
  25. Maheshwari R. K., Jay F. T., Friedman R. M. 1980a; Selective inhibition of glycoprotein and membrane protein of vesicular stomatitis virus from interferon-treated cells. Science 207:540–541
    [Google Scholar]
  26. Maheshwari R. K., Demsey A. E., Mohanty S. B., Friedman R. M. 1980b; Interferon-treated cells release vesicular stomatitis virus particles lacking glycoprotein spikes: correlation with bio-chemical data. Proceedings of the National Academy of Sciences, U.S.A. 77:2284–2287
    [Google Scholar]
  27. Matlin K. S. 1986; Ammonium chloride slows transport of the influenza virus hemagglutinin but does not cause missorting in a polarized epithelial cell line. Journal of Biological Chemistry 261:15172–15178
    [Google Scholar]
  28. Mounira K. C. A., Thang M. N. 1985; Chloroquine impairs the interferon-induced antiviral state without affecting the 2′-5′-oligoadenylate synthetase. Journal of Biological Chemistry 260:7960–7964
    [Google Scholar]
  29. Munoz A., Carrasco L. 1984; Formation of non-infective herpesvirus particles in cultured cells treated with human interferon. Journal of General Virology 65:1069–1078
    [Google Scholar]
  30. Ohkuma S., Poole B. 1978; Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proceedings of the National Academy of Sciences, U.S.A 75:3327–3331
    [Google Scholar]
  31. Panigrahi P., Mohanty B. 1989; Defective transport of hemagglutinin-neuraminidase glycoprotein of bovine parainfluenza-3 virus in interferon-treated cells. Archives of Virology 109:125–133
    [Google Scholar]
  32. Panigrahi P., Mohanty S. B., Maheshwari R. K., Friedman R. M. 1988; Effect of cloned human interferon a2a on bovine parainfluenza-3 virus. Archives of Virology 98:107–115
    [Google Scholar]
  33. Pennington R. J. 1961; Biochemistry of dystrophic muscle; mitochondrial succinate-tetrazolium reductase and adenosine tri-phosphatase. Biochemical Journal 80:649–654
    [Google Scholar]
  34. Pesonen M., Ansorge W., Simons K. 1984; Transcytosis of the G protein of vesicular stomatitis virus after implantation onto the apical plasma membrane of Madin-Darby canine kidney cells. I. Involvement of endosomes and lysosomes. Journal of Cell Biology 99:796–802
    [Google Scholar]
  35. Pfeffer L. M., Reich N. 1989; The role of protein kinase C activation in signal transduction by IFN expression of interferon-stimulated genes and induction of antiviral activity. Journal of Interferon Research 9:155–157
    [Google Scholar]
  36. Poli G., Orenstein J. M., Kinta A., Folks T. M., Fauci A. S. 1989; Interferon but not AZT suppresses HIV expression in chronically infected cell lines. Science 244:575–577
    [Google Scholar]
  37. Pouyssegur J., Franchi A., Paris S., Sardet C. 1988; Mechanism of activation and molecular genetics of mammalian Na+/H+ antiporter. In pH Homeostasis Mechanism and Control pp 61–78 Edited by Haussinger D. New York; Academic Press.:
    [Google Scholar]
  38. Proietti E., Carpinelli G., Vito M. D., Belardelli F., Gresser I, Podo F. 1986; 31P-Nuclear magnetic resonance analysis of interferon-induced alterations of phospholipid metabolites in interferon-sensitive and interferon-resistant Friend leukemia cell tumours in mice. Cancer Research 46:2849–2857
    [Google Scholar]
  39. Schuldiner S., Rozengurt E. 1982; Na+/H+ antiport in Swiss 3T3 cells; mitogenic stimulation leads to cytoplasmic alkalinization. Proceedings of the National Academy of Sciences, U.S.A. 79:7778–7782
    [Google Scholar]
  40. Seglan P. O. 1983; Inhibition of lysosomal function. Methods in Enzymology 96:737–764
    [Google Scholar]
  41. Singh V. K., Maheshwari R. K., Damewood G. P. IV, Stephenson C. B., Oliver C., Friedman R. M. 1988; Interferon alters intracellular transport of vesicular stomatitis virus glycoprotein.. Journal of Biological Regulators and Homeostatic Agents53–62
    [Google Scholar]
  42. Thomas J. A., Buchsbaum R. N., Zimniak Z., Rackes E. 1979; Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry 81:2210–2218
    [Google Scholar]
  43. Yagi M. J., King N. W. Jr, Bekesi G. 1980; Alterations of a mouse mammory tumour virus glycoprotein with interferon treatment. Journal of Virology 34:225–233
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-72-9-2143
Loading
/content/journal/jgv/10.1099/0022-1317-72-9-2143
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error