1887

Abstract

Exposure of cells infected with Semliki Forest virus (SFV; ) to mildly acidic pH (5.6) results in a dramatic increase in the host cell membrane permeability due to pore formation by the virus spike proteins. Identical results were obtained when the cells were infected with two other viruses, Sindbis virus (SIN, ) and vesicular stomatitis virus (VSV, ). This permeability change could also be observed on isolated virions of SFV, SIN and VSV by measuring the influx of propidium iodide, a nucleic acid-specific fluorescent marker, into the virions. This influx was dependent on the presence of the ectodomains of the viral spikes and could be hampered by zinc ions. Furthermore, haemagglutinin, a membrane protein of influenza A virus (), expressed in Aedes cells induced a change in membrane permeability identical to that induced by the spike proteins of SFV, SIN and VSV when exposed to low pH. Thus acid-induced membrane permeability changes produced by spike proteins of three different virus families could be demonstrated in infected cells as well as in virions. Therefore, the low pH-induced pore formation by viral spike proteins seems to be more than an event specific for togaviruses and might well be an inherent property of enveloped viruses that use the endocytotic pathway to infect a cell.

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1996-12-01
2024-04-25
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References

  1. Bashford C. L., Alder G. L., Menestrina G., Micklem K. J., Murphy J. J., Pasternak C. A. 1986; Membrane damage by hemolytic viruses, toxins, complement, and other cytotoxic agents. Journal of Biological Chemistry 261:9300–9308
    [Google Scholar]
  2. Bashford C. L., Alder G. M., Graham J. M., Menestrina G., Pasternak C. A. 1988; Ion modulation of membrane permeability: effect of cations on intact cells and on cells and phospholipid bilayers treated with pore-forming agents. Journal of Membrane Biology 103:79–94
    [Google Scholar]
  3. Bhakdi S., Martin E. 1991; Superoxide generation by human neutrophils induced by low doses of Escherichia coli hemolysin. Infection and Immunity 59:2955–2962
    [Google Scholar]
  4. Ciampor F., Bayley P. M., Nermut M. V., Hirst E. M. A., Sugrue R. J., Hay A. J. 1992; Evidence that the amantadine-induced, M2- mediated conversion of influenza-A virus hemagglutinin to the low pH conformation occurs in an acidic trans Golgi compartment. Virology 188:14–24
    [Google Scholar]
  5. Dick M., Barth B. U., Kempf C. 1996; The El protein is mandatory for pore formation by Semliki Forest virus spikes. Virology 220:204–207
    [Google Scholar]
  6. Gaudin Y., Ruigrok R. W. H., Brunner J. 1995; Low-pH induced conformational changes in viral fusion proteins: implication for the fusion mechanism. Journal of General Virology 76:1541–1556
    [Google Scholar]
  7. Grambas S., Hay A. J. 1992; Maturation of influenza-A virus hemagglutinin − estimates of the pH encountered during transport and its regulation by the M2 protein. Virology 190:11–18
    [Google Scholar]
  8. Hay A. J., Zambon M. C. 1984; Multiple actions of amantadine against influenza viruses. In Antiviral Drugs and Interferon: The Molecular Basis of their Activity pp 301–315 Edited by Becker Y. Boston: Martinus Nijhoff;
    [Google Scholar]
  9. Helenius A. 1992; Unpacking the incoming influenza virus. Cell 69:577–578
    [Google Scholar]
  10. Igarashi A. 1978; Isolation of a Singh’s Aedes albopichts cell clone sensitive to Dengue and Chikungunya viruses. Journal of General Virology 40:531–544
    [Google Scholar]
  11. Justman J., Klimjack M. R., Kielian M. 1993; Role of spike protein conformational changes in fusion of Semliki Forest virus. Journal of Virology 67:7597–7607
    [Google Scholar]
  12. Kärber G. 1931; Beitrag zur kollektiven Behandlung pharmako- logischer Reihenversuche. Archives of Experimental Pathology and Pharmacology 162:480–483
    [Google Scholar]
  13. Kempf C., Michel M. R., Kohler U., Koblet H. 1987; Can viral envelope proteins act as or induce proton channels?. Bioscience Reports 7:761–769
    [Google Scholar]
  14. Kobrinskij E. M., Philippov A. K., Curupa G. P., Sokolov N. I., Heider A. M., Markushin S. G., Klimov A. I. 1992; Changes of ion current induced by influenza-virus in oocytes Xenopus laevis . Biologicheskie Membrany 9:233–235
    [Google Scholar]
  15. Kondor-Koch C., Burke B., Garoff H. 1983; Expression of Semliki Forest virus protein from cloned complementary DNA. I. The fusion activity of the spike glycoprotein. Journal of Cell Biology 97:644–651
    [Google Scholar]
  16. Lanzrein M., Käsermann N., Kempf C. 1992; Changes in membrane permeability during Semliki Forest virus induced cell fusion. Bioscience Reports 12:221–236
    [Google Scholar]
  17. Lanzrein M., Weingart R., Kempf C. 1993; pH-dependent pore formation in Semliki Forest virus-infected Aedes albopictus cells. Virology 193:296–302
    [Google Scholar]
  18. Lanzrein M., Schlegel A., Kempf C. 1994a; Entry and uncoating of enveloped viruses. Biochemistry Journal 302:313–320
    [Google Scholar]
  19. Lanzrein M., Spycher-Burger M., Kempf C. 1994b; Semliki Forest virus induced cell cell fusion and pore formation. In Structure, Biogenesis and Dynamics pp 341–348 NATO ASI Series vol H82 Edited by den Kamp J. Op. Wien & New York: Springer-Verlag;
    [Google Scholar]
  20. Liljeström P., Garoff H. 1991; A new generation of animal cell expression vectors based on the Semliki Forest virus replicon. BioTechnology 9:1356–1361
    [Google Scholar]
  21. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J. 1951; Protein determination with the Folin reagent. Journal of Biological Chemistry 193:265–275
    [Google Scholar]
  22. Marsh M., Helenius A. 1989; Virus entry into animal cells. Advances in Virus Research 36:107–151
    [Google Scholar]
  23. Mellman I., Fuchs R., Helenius A. 1986; Acidification of the endocytic and exocytic pathways. Annual Review of Biochemistry 55:663–700
    [Google Scholar]
  24. Ni J., Watson V. W., Cox H., Karpas A. 1993; Multiparameter flow cytometric analysis of a novel cytotoxin (factor 2) induced tumor cell membrane permeability. Cytometry 14:281–286
    [Google Scholar]
  25. Patel K., Pasternak C. A. 1983; Ca2+-sensitive permeability changes caused by influenza virus. Bioscience Reports 3:749–755
    [Google Scholar]
  26. Pinto L. H., Holsinger L. J., Lamb R. A. 1992; Influenza virus M2 protein has ion channel activity. Cell 69:517–528
    [Google Scholar]
  27. Sanz M. A., Pérez L., Carrasco L. 1994; Semliki Forest virus 6K protein modifies membrane permeability after inducible expression in Escherichia coli cells. Journal of Biological Chemistry 269:12106–12110
    [Google Scholar]
  28. Sarkar D. P., Morris S. J., Eidelman O., Zimmerberg J., Blumenthal R. 1989; Initial stages of influenza hemagglutinin-induced cell fusion monitored simultaneously by two fluorescent events: cytoplasmic continuity and lipid mixing. Journal of Cell Biology 109:113–122
    [Google Scholar]
  29. Sato S. B., Kawasaki K., Ohnishi S. 1983; Hemolytic activity of influenza virus hemagglutinin glycoproteins activated in mildly acidic environments. Proceedings of the National Academy of Sciences, USA 80:3153–3157
    [Google Scholar]
  30. Schlegel A., Omar A., Jentsch P., Morell A., Kempf C. 1991; Semliki Forest virus envelope proteins function as proton channels. Bioscience Reports 11:243–255
    [Google Scholar]
  31. Spearman C. 1908; The method of rightand wrong cases (constant stimuli) without Gauss’s formulae. British Journal of Psychology 2:227–242
    [Google Scholar]
  32. Spyr C. A., Käsermann F., Kempf C. 1995; Identification of the pore forming element of Semliki Forest virus spikes. FEBS Letters 375:134–136
    [Google Scholar]
  33. Steinhauer D. A., Wharton S. A., Skehel J. J., Wiley D. C., Hay A. J. 1991; Amantadine selection of a mutant influenza virus containing an acid-stable hemagglutinin glycoprotein: evidence for virus-specific regulation of the pH of glycoprotein transport vesicles. Proceedings of the National Academy of Sciences, USA 88:11525–11529
    [Google Scholar]
  34. Strauss J. H., Strauss E. G. 1994; The alphaviruses: gene expression, replication, and evolution. Microbiological Reviews 58:491–562
    [Google Scholar]
  35. Sugrue R. J., Bahadur G., Zambon M. C., Hall Smith M., Douglas A. R., Hay A. J. 1990; Specific structural alteration of the influenza haemagglutinin by amantadine. EMBO Journal 9:3469–3476
    [Google Scholar]
  36. Young J. D. E., Young G. P. H., Cohn Z. A., Lenard J. 1983; Interaction of enveloped viruses with planar bilayer membranes: observations on Sendai, influenza, vesicular stomatitis, and Semliki Forest viruses. Virology 128:186–194
    [Google Scholar]
  37. Zebedee S. L., Lamb R. A. 1988; Influenza A virus M2 protein: monoclonal antibody restriction of virus growth and detection of M2 in virions. Journal of Virology 62:2762–2772
    [Google Scholar]
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