Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1982 Jul;43(1):213–222. doi: 10.1128/jvi.43.1.213-222.1982

Effect of interferon on the replication of mink cell focus-inducing virus in murine cells: synthesis, processing, assembly, and release of viral proteins.

J A Bilello, N A Wivel, P M Pitha
PMCID: PMC256112  PMID: 6180173

Abstract

Treatment of mink cell focus-inducing (MCF) virus (isolate AK-13) producing SC-1 cells with mouse fibroblast interferon (150 to 600 U/ml) led to a 100-fold decrease in the release of infectious virus, whereas there was a 2.5- to 10-fold decrease in various parameters of virus particle release. Analysis of labeled virion proteins indicated that a temporal change in virion protein composition occurred after interferon treatment. After a 24-h exposure of chronically infected cells to interferon, the virions produced contained a 85,000-dalton glycoprotein (apparently of nonviral origin) which was in excess of the virus envelope glycoprotein gp70. Particles produced from cells treated with interferon for 32 to 48 h were nearly devoid of gp70 and contained substantially lower quantities of p30. Intracellular processing of viral precursor polyproteins to the mature virion structural proteins was not altered in the presence of interferon. However, an accumulation of the viral p30 and p12E proteins was observed in interferon-treated cells, consistent with an increase in cell-associated virions. Immunoprecipitation analysis of the tissue culture fluids from [35S]methionine-labeled control and interferon-treated cells revealed marked decrease in p30 and p15E/p12E released after interferon treatment. In contrast, gp70 did not accumulate in interferon-treated cells, but was released into the culture medium in a form that was neither pelletable nor associated with p15E/p12E.

Full text

PDF
213

Images in this article

216Image
on p.216
216Image
on p.216
217Image
on p.217
217Image
on p.217
218Image
on p.218
219Image
on p.219
220Image
on p.220
220Image
on p.220

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aboud M., Kimchi R., Bakhanashvili M., Salzberg S. Intracellular production of virus particles and viral components in NIH/3T3 cells chronically infected with Moloney murine leukemia virus: effect of interferon. J Virol. 1981 Dec;40(3):830–838. doi: 10.1128/jvi.40.3.830-838.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bilello J. A., Colletta G., Warnecke G., Koch G., Frisby D., Pragnell I. B., Ostertag W. Analysis of the expression of spleen focus-forming virus (SFFV)-related RNA and gp55, a Friend and Rauscher virus-specific protein. Virology. 1980 Dec;107(2):331–344. doi: 10.1016/0042-6822(80)90301-3. [DOI] [PubMed] [Google Scholar]
  3. Billiau A. Effect of interferon on RNA tumor viruses. Tex Rep Biol Med. 1977;35:406–419. [PubMed] [Google Scholar]
  4. 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. Virology. 1976 Sep;73(2):537–542. doi: 10.1016/0042-6822(76)90416-5. [DOI] [PubMed] [Google Scholar]
  5. Bolognesi D. P., Langlois A. J., Schäfer W. Polypeptides of mammalian oncornaviruses. IV. Structural components of murine leukemia virus released as soluble antigens in cell culture. Virology. 1975 Dec;68(2):550–555. doi: 10.1016/0042-6822(75)90297-4. [DOI] [PubMed] [Google Scholar]
  6. Bolognesi D. P., Montelaro R. C., Frank H., Schäfer W. Assembly of type C oncornaviruses: a model. Science. 1978 Jan 13;199(4325):183–186. doi: 10.1126/science.202022. [DOI] [PubMed] [Google Scholar]
  7. Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  8. Chang E. H., Friedman R. M. A large glycoprotein of Moloney leukemia virus derived from interferon-treated cells. Biochem Biophys Res Commun. 1977 Jul 11;77(1):392–398. doi: 10.1016/s0006-291x(77)80210-6. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Chatterjee S., Cheung H. C., Hunter E. Interferon inhibits Sendai virus-induced cell fusion: an effect on cell membrane fluidity. Proc Natl Acad Sci U S A. 1982 Feb;79(3):835–839. doi: 10.1073/pnas.79.3.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Famulari N. G., Jelalian K. Cell surface expression of the env gene polyprotein of dual-tropic mink cell focus-forming murine leukemia virus. J Virol. 1979 Jun;30(3):720–728. doi: 10.1128/jvi.30.3.720-728.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Friedman R. M., Maheshwari R. K., Jay F. T., Czarniecki C. Mechanism of interferon inhibition of viruses that bud from the plasma membrane. Ann N Y Acad Sci. 1980;350:533–544. doi: 10.1111/j.1749-6632.1980.tb20655.x. [DOI] [PubMed] [Google Scholar]
  13. Friedman R. M., Ramseur J. M. Inhibition of murine leukemia virus production in chronically infected AKR cells: a novel effect of interferon. Proc Natl Acad Sci U S A. 1974 Sep;71(9):3542–3544. doi: 10.1073/pnas.71.9.3542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gordon J., Minks M. A. The interferon renaissance: molecular aspects of induction and action. Microbiol Rev. 1981 Jun;45(2):244–266. doi: 10.1128/mr.45.2.244-266.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Green N., Shinnick T. M., Witte O., Ponticelli A., Sutcliffe J. G., Lerner R. A. Sequence-specific antibodies show that maturation of Moloney leukemia virus envelope polyprotein involves removal of a COOH-terminal peptide. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6023–6027. doi: 10.1073/pnas.78.10.6023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gresser I., Coppey J., Bourali C. Interferon and murine leukemia. VI. Effect of interferon preparations on the lymphoid leukemia of AKR mice. J Natl Cancer Inst. 1969 Nov;43(5):1083–1089. [PubMed] [Google Scholar]
  17. Hartley J. W., Wolford N. K., Old L. J., Rowe W. P. A new class of murine leukemia virus associated with development of spontaneous lymphomas. Proc Natl Acad Sci U S A. 1977 Feb;74(2):789–792. doi: 10.1073/pnas.74.2.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hovi T., Saksela O., Vaheri A. Increased secretion of plasminogen activator by human macrophages after exposure to leukocyte interferon. FEBS Lett. 1981 Jul 6;129(2):233–236. doi: 10.1016/0014-5793(81)80172-x. [DOI] [PubMed] [Google Scholar]
  19. Joklik W. K., Merigan T. C. Concerning the mechanism of action of interferon. Proc Natl Acad Sci U S A. 1966 Aug;56(2):558–565. doi: 10.1073/pnas.56.2.558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jungwirth C., Horak I., Bodo G., Lindner J., Schultze B. The synthesis of poxvirus-specific RNA in interferon-treated cells. Virology. 1972 Apr;48(1):59–70. doi: 10.1016/0042-6822(72)90114-6. [DOI] [PubMed] [Google Scholar]
  21. Karshin W. L., Arcement L. J., Naso R. B., Arlinghaus R. B. Common precursor for Rauscher leukemia virus gp69/71, p15(E), and p12(E). J Virol. 1977 Sep;23(3):787–798. doi: 10.1128/jvi.23.3.787-798.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  23. Lodish H. F., Porter M. Specific incorporation of host cell surface proteins into budding vesicular stomatitis virus particles. Cell. 1980 Jan;19(1):161–169. doi: 10.1016/0092-8674(80)90397-9. [DOI] [PubMed] [Google Scholar]
  24. Maheshwari R. K., Banerjee D. K., Waechter C. J., Olden K., Friedman R. M. Interferon treatment inhibits glycosylation of a viral protein. Nature. 1980 Oct 2;287(5781):454–456. doi: 10.1038/287454a0. [DOI] [PubMed] [Google Scholar]
  25. Maheshwari R. K., Demsey A. E., Mohanty S. B., Friedman R. M. Interferon-treated cells release vesicular stomatitis virus particles lacking glycoprotein spikes: correlation with biochemical data. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2284–2287. doi: 10.1073/pnas.77.4.2284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Metz D. H., Esteban M. Interferon inhibits viral protein synthesis in L cells infected with vaccinia virus. Nature. 1972 Aug 18;238(5364):385–388. doi: 10.1038/238385a0. [DOI] [PubMed] [Google Scholar]
  27. Pfeffer L. M., Landsberger F. R., Tamm I. Beta-interferon-induced time-dependent changes in the plasma membrane lipid bilayer of cultured cells. J Interferon Res. 1981;1(4):613–620. doi: 10.1089/jir.1981.1.613. [DOI] [PubMed] [Google Scholar]
  28. Pinter A., Fleissner E. The presence of disulfide-linked gp70-p15(E) complexes in AKR murine leukemia virus. Virology. 1977 Dec;83(2):417–422. doi: 10.1016/0042-6822(77)90187-8. [DOI] [PubMed] [Google Scholar]
  29. Pitha P. M., Fernie B., Maldarelli F., Hattman T., Wivel N. A. Effect of interferon on mouse leukaemia virus (MuLV). V. Abnormal proteins in virions of Rauscher MuLV produced in the presence of interferon. J Gen Virol. 1980 Jan;46(1):97–110. doi: 10.1099/0022-1317-46-1-97. [DOI] [PubMed] [Google Scholar]
  30. Pitha P. M., Rowe W. P., Oxman M. N. Effect of interferon on exogenous, endogenous, and chroniv murine leukemia virus infection. Virology. 1976 Apr;70(2):324–338. doi: 10.1016/0042-6822(76)90275-0. [DOI] [PubMed] [Google Scholar]
  31. 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. Virology. 1977 Jun 1;79(1):1–13. doi: 10.1016/0042-6822(77)90329-4. [DOI] [PubMed] [Google Scholar]
  32. Pitha P. M. The effects of interferon in mouse cells infected with MuLV. Ann N Y Acad Sci. 1980;350:301–313. doi: 10.1111/j.1749-6632.1980.tb20630.x. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Reading C. L., Brunson K. W., Torrianni M., Nicolson G. L. Malignancies of metastatic murine lymphosarcoma cell lines and clones correlate with decreased cell surface display of RNA tumor virus envelope glycoprotein gp70. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5943–5947. doi: 10.1073/pnas.77.10.5943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schroder E. W., Chou I. N., Jaken S., Black P. H. Interferon inhibits the release of plasminogen activator from SV3T3 cells. Nature. 1978 Dec 21;276(5690):828–829. doi: 10.1038/276828a0. [DOI] [PubMed] [Google Scholar]
  36. Shinnick T. M., Lerner R. A., Sutcliffe J. G. Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981 Oct 15;293(5833):543–548. doi: 10.1038/293543a0. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES