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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1982 Feb;79(3):835–839. doi: 10.1073/pnas.79.3.835

Interferon inhibits Sendai virus-induced cell fusion: an effect on cell membrane fluidity.

S Chatterjee, H C Cheung, E Hunter
PMCID: PMC345847  PMID: 6174982

Abstract

Interferon can affect several cellular functions, in addition to its antiviral activity. We report here that pretreatment of human cells with homologous interferon significantly inhibits cell fusion induced by Sendai virus and that this refractory state is accompanied by a decrease in cell plasma membrane fluidity. Multinucleate cell formation induced by beta-propiolactone-inactivated Sendai virus in human fibroblast cells (a system in which fusion results from an interaction of the viral glycoprotein with the cell membrane) was inhibited by more than 90% after addition of human interferon for 18-24 hr. This inhibition could be neutralized by antiserum to interferon. Furthermore, inhibitor studies with cycloheximide and actinomycin D clearly indicated that synthesis of protein and RNA is necessary to establish the resistant state. To determine whether the inhibition of Sendai virus-induced cell fusion resulted from interferon-induced changes at the cell plasma membrane, experiments were carried out using the fluorescence probe 1,6-diphenyl-1,3,5-hexatriene, which is capable of sensing molecular motions in the hydrocarbon core of the bilayer structure. A significant decrease in the membrane fluidity of interferon-treated cells was observed. It is likely, therefore, that the inhibitory effect on Sendai virus-induced cell fusion observed in interferon-treated cells results from an increased rigidity of the target cell membrane.

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Selected References

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  1. Baglioni C. Interferon-induced enzymatic activities and their role in the antriviral state. Cell. 1979 Jun;17(2):255–264. doi: 10.1016/0092-8674(79)90151-x. [DOI] [PubMed] [Google Scholar]
  2. 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 Cancer. 1975 Jun 15;15(6):947–953. doi: 10.1002/ijc.2910150610. [DOI] [PubMed] [Google Scholar]
  3. Bourgeade M. F., Rousset S., Paulin D., Chany C. Reorganization of the cytoskeleton by interferon in MSV-transformed cells. J Interferon Res. 1981 Feb;1(2):323–332. doi: 10.1089/jir.1981.1.323. [DOI] [PubMed] [Google Scholar]
  4. Bratt M. A., Gallaher W. R. Preliminary analysis of the requirements for fusion from within and fusion from without by Newcastle disease virus. Proc Natl Acad Sci U S A. 1969 Oct;64(2):536–543. doi: 10.1073/pnas.64.2.536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brouty-Boyé D., Zetter B. R. Inhibition of cell motility by interferon. Science. 1980 May 2;208(4443):516–518. doi: 10.1126/science.6154315. [DOI] [PubMed] [Google Scholar]
  6. Chang E. H., Jay F. T., Friedman R. M. Physical, morphological, and biochemical alterations in the membrane of AKR mouse cells after interferon treatment. Proc Natl Acad Sci U S A. 1978 Apr;75(4):1859–1863. doi: 10.1073/pnas.75.4.1859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chang E. H., Mims S. J., Triche T. J., Friedman R. M. Interferon inhibits mouse leukaemia virus release: an electron microscope study. J Gen Virol. 1977 Feb;34(2):363–367. doi: 10.1099/0022-1317-34-2-363. [DOI] [PubMed] [Google Scholar]
  8. Chatterjee S., Hunter E. Fusion of normal primate cells: a common biological property of the D-type retroviruses. Virology. 1980 Nov;107(1):100–108. doi: 10.1016/0042-6822(80)90276-7. [DOI] [PubMed] [Google Scholar]
  9. Chatterjee S., Hunter E. Inhibition of Mason-Pfizer monkey virus-induced syncytium formation in normal human cells by homologous interferon. Virology. 1980 Jul 30;104(2):487–490. doi: 10.1016/0042-6822(80)90351-7. [DOI] [PubMed] [Google Scholar]
  10. Chatterjee S., Hunter E. The characterization of Mason-Pfizer monkey virus-induced cell fusion. Virology. 1979 Jun;95(2):421–433. doi: 10.1016/0042-6822(79)90497-5. [DOI] [PubMed] [Google Scholar]
  11. Cheung H. C., Almira E. C., Kansal P. C., Reddy W. J. A membrane abnormality in lymphocytes from diabetic subjects. Endocr Res Commun. 1980;7(3):145–156. doi: 10.3109/07435808009065968. [DOI] [PubMed] [Google Scholar]
  12. Djeu J. Y., Huang K. Y., Herberman R. B. Augmentation of mouse natural killer activity and induction of interferon by tumor cells in vivo. J Exp Med. 1980 Apr 1;151(4):781–789. doi: 10.1084/jem.151.4.781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Farrell P. J., Sen G. C., Dubois M. F., Ratner L., Slattery E., Lengyel P. Interferon action: two distinct pathways for inhibition of protein synthesis by double-stranded RNA. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5893–5897. doi: 10.1073/pnas.75.12.5893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Friedman R. M. Antiviral activity of interferons. Bacteriol Rev. 1977 Sep;41(3):543–567. doi: 10.1128/br.41.3.543-567.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Garland F., Graves D. E., Yielding L. W., Cheung H. C. Comparative studies of the binding of ethidium bromide and its photoreactive analogues to nucleic acids by fluorescence and rapid kinetics. Biochemistry. 1980 Jul 8;19(14):3221–3226. doi: 10.1021/bi00555a019. [DOI] [PubMed] [Google Scholar]
  16. Gresser I. On the varied biologic effects of interferon. Cell Immunol. 1977 Dec;34(2):406–415. doi: 10.1016/0008-8749(77)90262-3. [DOI] [PubMed] [Google Scholar]
  17. KOHN A. POLYKARYOCYTOSIS INDUCED BY NEWCASTLE DISEASE VIRUS IN MONOLAYERS OF ANIMAL CELLS. Virology. 1965 Jun;26:228–245. doi: 10.1016/0042-6822(65)90050-4. [DOI] [PubMed] [Google Scholar]
  18. Lindahl P., Gresser I., Leary P., Tovey M. Interferon treatment of mice: enhanced expression of histocompatibility antigens on lymphoid cells. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1284–1287. doi: 10.1073/pnas.73.4.1284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pfeffer L. M., Murphy J. S., Tamm I. Interferon effects on the growth and division of human fibroblasts. Exp Cell Res. 1979 Jun;121(1):111–120. doi: 10.1016/0014-4827(79)90450-6. [DOI] [PubMed] [Google Scholar]
  20. Pfeffer L. M., Wang E., Tamm I. Interferon effects on microfilament organization, cellular fibronectin distribution, and cell motility in human fibroblasts. J Cell Biol. 1980 Apr;85(1):9–17. doi: 10.1083/jcb.85.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pitha P. M., Wivel N. A., Fernie B. F., Harper H. P. Effect of interferon on murine leukaemia virus infection. IV. Formation of non-infectious virus in chronically infected cells. J Gen Virol. 1979 Mar;42(3):467–480. doi: 10.1099/0022-1317-42-3-467. [DOI] [PubMed] [Google Scholar]
  22. Raj N. B., Pitha P. M. Synthesis of new proteins associated with the induction of interferon in human fibroblast cells. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4918–4922. doi: 10.1073/pnas.77.8.4918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rice-Evans C., Bruckdorfer K. R., Dootson G. Studies on the altered membrane characteristics of sickle cells. FEBS Lett. 1978 Oct 1;94(1):81–86. doi: 10.1016/0014-5793(78)80911-9. [DOI] [PubMed] [Google Scholar]
  24. Roberts W. K., Hovanessian A., Brown R. E., Clemens M. J., Kerr I. M. Interferon-mediated protein kinase and low-molecular-weight inhibitor of protein synthesis. Nature. 1976 Dec 2;264(5585):477–480. doi: 10.1038/264477a0. [DOI] [PubMed] [Google Scholar]
  25. Sen G. C., Lebleu B., Brown G. E., Kawakita M., Slattery E., Lengyel P. Interferon, double-stranded RNA and mRNA degradation. Nature. 1976 Nov 25;264(5584):370–373. doi: 10.1038/264370a0. [DOI] [PubMed] [Google Scholar]
  26. Shinitzky M., Inbar M. Difference in microviscosity induced by different cholesterol levels in the surface membrane lipid layer of normal lymphocytes and malignant lymphoma cells. J Mol Biol. 1974 Jan 5;85(4):603–615. doi: 10.1016/0022-2836(74)90318-0. [DOI] [PubMed] [Google Scholar]
  27. Taylor J. Inhibition of interferon action by actinomycin. Biochem Biophys Res Commun. 1964;14:447–451. doi: 10.1016/0006-291x(64)90084-1. [DOI] [PubMed] [Google Scholar]
  28. Tomita Y., Kuwata T. Suppressive effects of interferon on cell fusion by Sendai virus. J Gen Virol. 1981 Aug;55(Pt 2):289–295. doi: 10.1099/0022-1317-55-2-289. [DOI] [PubMed] [Google Scholar]
  29. Vignaux F., Gresser I. Differential effects of interferon on the expression of H-2K, H-2D, and Ia antigens on mouse lymphocytes. J Immunol. 1977 Feb;118(2):721–723. [PubMed] [Google Scholar]

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