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. 1976 Jul;19(1):118–125. doi: 10.1128/jvi.19.1.118-125.1976

Relationship of Friend murine leukemia virus production to growth and hemoglobin synthesis in cultured erythroleukemia cells.

C C Sherton, L H Evans, E Polonoff, D Kabat
PMCID: PMC354838  PMID: 1065778

Abstract

The factors that control oncornavirus formation were analyzed in Friend leukemia cells that undergo hematopoiesis when treated with dimethyl sulfoxide. Suspension cultures of Ostertag FSD-1 cell line were found to enter a G or resting state at the end of their proliferative phase and to simultaneously cease producing helper and dependent components of Friend virus. Whereas the decline in virus production is at least 100-fold, rates of cellular RNA and protein synthesis are only slightly lower in resting than in growing cells. Both resting and growing cells contain similarly large concentrations of the viral proteins P(30) and P(12). Dimethyl sulfoxide induces hemoglobin synthesis in growing cells, but its effects on virus production appear to be indirect results of its action to inhibit cell growth and thus to delay entry of cells into the G resting state. Furthermore, variant cell lines were obtained with differing abilities to synthesize virus or hemoglobin. Some lines no longer produce infectious virus, although they all harbor murine leukemia virus genes which are expressed to varying extents. The major internal protein of these oncornaviruses, P(30), is synthesized in large amounts by all of the cell lines. These results suggest that Friend virus production is not coinduced with erythroid differentiation, as had been proposed, but rather is controlled by a cellular growth cycle.

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Selected References

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

  1. AXELRAD A. A., STEEVES R. A. ASSAY FOR FRIEND LEUKEMIA VIRUS: RAPID QUANTITATIVE METHOD BASED ON ENUMERATION OF MACROSCOPIC SPLEEN FOCI IN MICE. Virology. 1964 Nov;24:513–518. doi: 10.1016/0042-6822(64)90199-0. [DOI] [PubMed] [Google Scholar]
  2. Adams L. R., Kamentsky L. A. Fluorometric characterization of six classes of human leukocytes. Acta Cytol. 1974 Sep-Oct;18(5):389–391. [PubMed] [Google Scholar]
  3. BADER J. P. THE REQUIREMENT FOR DNA SYNTHESIS IN THE GROWTH OF ROUS SARCOMA AND ROUS-ASSOCIATED VIRUSES. Virology. 1965 Jun;26:253–261. doi: 10.1016/0042-6822(65)90272-2. [DOI] [PubMed] [Google Scholar]
  4. Baltimore D. Tumor viruses: 1974. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):1187–1200. doi: 10.1101/sqb.1974.039.01.137. [DOI] [PubMed] [Google Scholar]
  5. Bassin R. H., Tuttle N., Fischinger P. J. Rapid cell culture assay technic for murine leukaemia viruses. Nature. 1971 Feb 19;229(5286):564–566. doi: 10.1038/229564b0. [DOI] [PubMed] [Google Scholar]
  6. Birnboim H. C. Optimal conditions for counting of precipitated 3H-RNA on glass-fiber filters. Anal Biochem. 1970 Sep;37(1):178–182. doi: 10.1016/0003-2697(70)90275-7. [DOI] [PubMed] [Google Scholar]
  7. Dube S. K., Pragnell I. B., Kluge N., Gaedicke G., Steinheider G., Ostertag W. Induction of endogenous and of spleen focus-forming viruses during dimethylsulfoxide-induced differentiation of mouse erythroleukemia cells transformed by spleen focus-forming virus. Proc Natl Acad Sci U S A. 1975 May;72(5):1863–1867. doi: 10.1073/pnas.72.5.1863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fischinger P. F., Tuttle-Fuller N., Hüper G., Bolognesi D. P. Mitosis is required for production of murine leukemia virus and structural proteins during de novo infection. J Virol. 1975 Aug;16(2):267–274. doi: 10.1128/jvi.16.2.267-274.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Friend C., Scher W., Holland J. G., Sato T. Hemoglobin synthesis in murine virus-induced leukemic cells in vitro: stimulation of erythroid differentiation by dimethyl sulfoxide. Proc Natl Acad Sci U S A. 1971 Feb;68(2):378–382. doi: 10.1073/pnas.68.2.378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gallagher R. E., Gallo R. C. Type C RNA tumor virus isolated from cultured human acute myelogenous leukemia cells. Science. 1975 Jan 31;187(4174):350–353. doi: 10.1126/science.46123. [DOI] [PubMed] [Google Scholar]
  11. Greenberger J. S., Aaronson S. A. Cycloheximide induction of xenotropic type C virus from synchronized mouse cells: metabolic requirements for virus activation. J Virol. 1975 Jan;15(1):64–70. doi: 10.1128/jvi.15.1.64-70.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hobom-Schnegg B., Robinson H. L., Robinson W. S. Replication of Rous sarcoma virus in synchronized cells. J Gen Virol. 1970;7(2):85–93. doi: 10.1099/0022-1317-7-2-85. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Ikawa Y., Furusawa M., Sugano H. Erythrocyte membrane-specific antigens in Friend virus-induced leukemia cells. Bibl Haematol. 1973;39:955–967. doi: 10.1159/000427928. [DOI] [PubMed] [Google Scholar]
  15. Kabat D., Sherton C. C., Evans L. H., Bigley R., Koler R. D. Synthesis of erythrocyte-specific proteins in cultured friend leukemia cells. Cell. 1975 Jul;5(3):331–338. doi: 10.1016/0092-8674(75)90109-9. [DOI] [PubMed] [Google Scholar]
  16. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  17. Leder A., Leder P. Butyric acid, a potent inducer of erythroid differentiation in cultured erythroleukemic cells. Cell. 1975 Jul;5(3):319–322. doi: 10.1016/0092-8674(75)90107-5. [DOI] [PubMed] [Google Scholar]
  18. Leder A., Orkin S., Leder P. Differentiation of erythroleukemic cells in the presence of inhibitors of DNA synthesis. Science. 1975 Nov 28;190(4217):893–894. doi: 10.1126/science.1059262. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Lerner R. A., Hodge L. D. Gene expression in synchronized lymphocytes: studies on the control of synthesis of immunoglobulin polypeptides. J Cell Physiol. 1971 Apr;77(2):265–276. doi: 10.1002/jcp.1040770215. [DOI] [PubMed] [Google Scholar]
  21. McClintock P. R., Papaconstantinou J. Regulation of hemoglobin synthesis in a murine erythroblastic leukemic cell: the requirement for replication to induce hemoglobin synthesis. Proc Natl Acad Sci U S A. 1974 Nov;71(11):4551–4555. doi: 10.1073/pnas.71.11.4551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Oroszlan S., Foreman C., Kelloff G., Gilden R. V. The group-specific antigen and other structural proteins of hamster and mouse C-type viruses. Virology. 1971 Mar;43(3):665–674. doi: 10.1016/0042-6822(71)90290-x. [DOI] [PubMed] [Google Scholar]
  23. Ostertag W., Melderis H., Steinheider G., Kluge N., Dube S. Synthesis of mouse haemoglobin and globin mRNA in leukaemic cell cultures. Nat New Biol. 1972 Oct 25;239(95):231–234. doi: 10.1038/newbio239231a0. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. ROWE W. P., BRODSKY I. A graded-response assay for the Friend leukemia virus. J Natl Cancer Inst. 1959 Dec;23:1239–1248. [PubMed] [Google Scholar]
  27. Ross J., Ikawa Y., Leder P. Globin messenger-RNA induction during erythroid differentiation of cultured leukemia cells. Proc Natl Acad Sci U S A. 1972 Dec;69(12):3620–3623. doi: 10.1073/pnas.69.12.3620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sato T., Friend C., De Harven E. Ultrastructural changes in Friend erythroleukemia cells treated with dimethyl sulfoxide. Cancer Res. 1971 Oct;31(10):1402–1417. [PubMed] [Google Scholar]
  29. Sherton C. C., Kabat D. Changes in RNA and protein metabolism preceding onset of hemoglobin synthesis in cultured Friend leukemia cells. Dev Biol. 1976 Jan;48(1):118–131. doi: 10.1016/0012-1606(76)90051-8. [DOI] [PubMed] [Google Scholar]
  30. Stephenson J. R., Wilsnack R. E., Aaronson S. A. Radioimmunoassay for avian C-type virus group-specific antigen: detection in normal and virus-transformed cells. J Virol. 1973 Jun;11(6):893–899. doi: 10.1128/jvi.11.6.893-899.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Stewart M. L., Summers D. F., Soeiro R., Fields B. N., Maizel J. V., Jr Purification of oncornaviruses by agglutination with concanacalin A (murine leukemia virus-phytohemagglutinin-friend virus). Proc Natl Acad Sci U S A. 1973 May;70(5):1308–1312. doi: 10.1073/pnas.70.5.1308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Stewart S. E., Kasnic G., Jr, Draycott C., Ben T. Activation of viruses in human tumors by 5-iododeoxyuridine and dimethyl sulfoxide. Science. 1972 Jan 14;175(4018):198–199. doi: 10.1126/science.175.4018.198. [DOI] [PubMed] [Google Scholar]
  33. Sugano H., Furusawa M., Kawaguchi T., Ikawa Y. Enhancement of erythrocytic maturation of Friend virus-induced leukemia cells in vivo. Bibl Haematol. 1973;39:943–954. doi: 10.1159/000427927. [DOI] [PubMed] [Google Scholar]
  34. Swetly P., Ostertag W. Friend virus release and induction of haemoglobin synthesis in erythroleukaemic cells respond differently to interferon. Nature. 1974 Oct 18;251(5476):642–644. doi: 10.1038/251642a0. [DOI] [PubMed] [Google Scholar]
  35. Tanaka M., Levy J., Terada M., Breslow R., Rifkind R. A., Marks P. A. Induction of erythroid differentiation in murine virus infected eythroleukemia cells by highly polar compounds. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1003–1006. doi: 10.1073/pnas.72.3.1003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Teich N., Lowy D. R., Hartley J. W., Rowe W. P. Studies of the mechanism of induction of infectious murine leukemia virus from AKR mouse embryo cell lines by 5-iododeoxyuridine and 5-bromodeoxyuridine. Virology. 1973 Jan;51(1):163–173. doi: 10.1016/0042-6822(73)90376-0. [DOI] [PubMed] [Google Scholar]
  37. Watson J., Ralph P., Sarkar S., Cohn M. Leukemia viruses associated with mouse myeloma cells. Proc Natl Acad Sci U S A. 1970 Jun;66(2):344–351. doi: 10.1073/pnas.66.2.344. [DOI] [PMC free article] [PubMed] [Google Scholar]

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