Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1985 Jun;54(3):844–850. doi: 10.1128/jvi.54.3.844-850.1985

Regulation of Moloney murine leukemia virus replication in chronically infected cells arrested at the G0/G1 phase.

I Gloger, G Arad, A Panet
PMCID: PMC254872  PMID: 2582148

Abstract

The replication of Moloney murine leukemia virus (MMuLV) in chronically infected mouse cells arrested at the G0/G1 phase of the cell cycle by different procedures was investigated. MMuLV production was inhibited in glutamine- and isoleucine (Gln-Ile)-deprived G0/G1 cells. In contrast, butyric acid treatment, which efficiently arrested the cells at the G0/G1 phase of the cell cycle, did not inhibit MMuLV production. Furthermore, the inhibition of MMuLV production caused by either Gln-Ile deprivation or by interferon (IFN) treatment was overcome by butyric acid treatment. Thus, the replication of MMuLV could be dissociated from cell proliferation. The inhibition of MMuLV production in Gln-Ile-deprived cell cultures was compared to the inhibitory effect of IFN, which is known to affect budding and release of the virus. Rates of MMuLV protein synthesis were not affected in both the IFN-treated and Gln-Ile-deprived cells. However, processing of the viral polyprotein Pre65gag into p30 was blocked in the Gln-Ile-deprived cells. Furthermore, whereas in IFN-treated cells, MMuLV accumulated on the cell surface and could be released upon treatment with trypsin, in Gln-Ile-deprived cells, no virions were released by such treatment. These results indicate that in cells arrested by Gln-Ile deprivation, MMuLV is inhibited at a posttranslation step. This step appears to precede the anti-MMuLV block induced by IFN.

Full text

PDF
844

Images in this article

847Image
on p.847
848Image
on p.848

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. Altenburg B. C., Via D. P., Steiner S. H. Modification of the phenotype of murine sarcoma virus-transformed cells by sodium butyrate. Effects on morphology and cytoskeletal elements. Exp Cell Res. 1976 Oct 15;102(2):223–231. doi: 10.1016/0014-4827(76)90036-7. [DOI] [PubMed] [Google Scholar]
  3. Balazs I., Caldarella J. Retrovirus gene expression during the cell cycle. I. Virus production, synthesis, and expression of viral proteins in Rauscher murine leukemia virus-infected mouse cells. J Virol. 1981 Sep;39(3):792–799. doi: 10.1128/jvi.39.3.792-799.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bell J. G., Wyke J. A., Macpherson I. A. Transformation by a temperature sensitive mutant of Rous sarcoma virus in the absence of serum. J Gen Virol. 1975 May;27(2):127–134. doi: 10.1099/0022-1317-27-2-127. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. D'Anna J. A., Tobey R. A., Gurley L. R. Concentration-dependent effects of sodium butyrate in Chinese hamster cells: cell-cycle progression, inner-histone acetylation, histone H1 dephosphorylation, and induction of an H1-like protein. Biochemistry. 1980 Jun 10;19(12):2656–2671. doi: 10.1021/bi00553a019. [DOI] [PubMed] [Google Scholar]
  7. Fallon R. J., Cox R. P. Cell cycle analysis of sodium butyrate and hydroxyurea, inducers of ectopic hormone production in HeLa cells. J Cell Physiol. 1979 Aug;100(2):251–262. doi: 10.1002/jcp.1041000206. [DOI] [PubMed] [Google Scholar]
  8. Fan H., Baltimore D. RNA metabolism of murine leukemia virus: detection of virus-specific RNA sequences in infected and uninfected cells and identification of virus-specific messenger RNA. J Mol Biol. 1973 Oct 15;80(1):93–117. doi: 10.1016/0022-2836(73)90235-0. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Guttman-Bass N., Cedar H., Panet A. Quantification of newly synthesized virus RNA in moloney murine leukaemia virus-infected cells. J Gen Virol. 1980 Jun;48(Pt 2):341–350. doi: 10.1099/0022-1317-48-2-341. [DOI] [PubMed] [Google Scholar]
  11. Harel J., Rassart E., Jolicoeur P. Cell cycle dependence of synthesis of unintegrated viral DNA in mouse cells newly infected with murine leukemia virus. Virology. 1981 Apr 15;110(1):202–207. doi: 10.1016/0042-6822(81)90022-2. [DOI] [PubMed] [Google Scholar]
  12. Humphries E. H., Temin H. M. Requirement for cell division for initiation of transcription of Rous sarcoma virus RNA. J Virol. 1974 Sep;14(3):531–546. doi: 10.1128/jvi.14.3.531-546.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kerr I. M., Olshevsky U., Lodish H. F., Baltimore D. Translation of murine leukemia virus RNA in cell-free systems from animal cells. J Virol. 1976 May;18(2):627–635. doi: 10.1128/jvi.18.2.627-635.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kimchi A., Shure H., Lapidot Y., Rapoport S., Panet A., Revel M. Antimitogenic effects of interferon and (2'-5')-oligoadenylate in synchronized 3T3 fibroblasts. FEBS Lett. 1981 Nov 16;134(2):212–216. doi: 10.1016/0014-5793(81)80604-7. [DOI] [PubMed] [Google Scholar]
  15. Kruh J. Effects of sodium butyrate, a new pharmacological agent, on cells in culture. Mol Cell Biochem. 1982 Feb 5;42(2):65–82. doi: 10.1007/BF00222695. [DOI] [PubMed] [Google Scholar]
  16. Leong J. A., Levinson W., Bishop M. J. Synchronization of Rous sarcoma virus production in chick embryo cells. Virology. 1972 Jan;47(1):133–141. doi: 10.1016/0042-6822(72)90246-2. [DOI] [PubMed] [Google Scholar]
  17. Levin J. G., Hu S. C., Rein A., Messer L. I., Gerwin B. I. Murine leukemia virus mutant with a frameshift in the reverse transcriptase coding region: implications for pol gene structure. J Virol. 1984 Aug;51(2):470–478. doi: 10.1128/jvi.51.2.470-478.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lu A. H., Soong M. M., Wong P. K. Maturation of Moloney murine leukemia virus. Virology. 1979 Feb;93(1):269–274. doi: 10.1016/0042-6822(79)90297-6. [DOI] [PubMed] [Google Scholar]
  19. Naso R. B., Brown R. L. Synthesis and cleavage of Rauscher leukemia virus precursor proteins in synchronized cells. Virology. 1977 Oct 1;82(1):247–251. doi: 10.1016/0042-6822(77)90049-6. [DOI] [PubMed] [Google Scholar]
  20. Panem S., Kirsten W. H. Release of mouse leukemia-sarcoma virus from synchronized cells. J Natl Cancer Inst. 1973 Feb;50(2):563–565. doi: 10.1093/jnci/50.2.563. [DOI] [PubMed] [Google Scholar]
  21. Panet A., Kra-Oz Z. A competition immunoassay for characterizing the reverse transcriptase of mammalian RNA tumor viruses. Virology. 1978 Aug;89(1):95–101. doi: 10.1016/0042-6822(78)90043-0. [DOI] [PubMed] [Google Scholar]
  22. Pardee A. B. A restriction point for control of normal animal cell proliferation. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1286–1290. doi: 10.1073/pnas.71.4.1286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Paskind M. P., Weinberg R. A., Baltimore D. Dependence of Moloney murine leukemia virus production on cell growth. Virology. 1975 Sep;67(1):242–248. doi: 10.1016/0042-6822(75)90421-3. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Schwartzberg P., Colicelli J., Goff S. P. Construction and analysis of deletion mutations in the pol gene of Moloney murine leukemia virus: a new viral function required for productive infection. Cell. 1984 Jul;37(3):1043–1052. doi: 10.1016/0092-8674(84)90439-2. [DOI] [PubMed] [Google Scholar]
  26. Sherton C. C., Evans L. H., Polonoff E., Kabat D. Relationship of Friend murine leukemia virus production to growth and hemoglobin synthesis in cultured erythroleukemia cells. J Virol. 1976 Jul;19(1):118–125. doi: 10.1128/jvi.19.1.118-125.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Traktman P., Baltimore D. Protease bypass of temperature-sensitive murine leukemia virus maturation mutants. J Virol. 1982 Dec;44(3):1039–1046. doi: 10.1128/jvi.44.3.1039-1046.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Witte O. N., Baltimore D. Relationship of retrovirus polyprotein cleavages to virion maturation studied with temperature-sensitive murine leukemia virus mutants. J Virol. 1978 Jun;26(3):750–761. doi: 10.1128/jvi.26.3.750-761.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Yen A., Pardee A. B. Arrested states produced by isoleucine deprivation and their relationship to the low serum produced arrested state in Swiss 3T3 cells. Exp Cell Res. 1978 Jul;114(2):389–395. doi: 10.1016/0014-4827(78)90497-4. [DOI] [PubMed] [Google Scholar]

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

RESOURCES