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. 1979 Aug;31(2):557–567. doi: 10.1128/jvi.31.2.557-567.1979

Virus production by Abelson murine leukemia virus-transformed lymphoid cells.

A Shields, N Rosenberg, D Baltimore
PMCID: PMC353478  PMID: 90175

Abstract

Cell lines obtained by in vitro transformation of bone marrow with Abelson murine leukemia virus (A-MuLV) can be divided into three classes: producers, releasing reverse transcriptase-containing particles and infectious virus; nonproducers, releasing no viral particles; and defective producers, the most common phenotype, releasing particulate reverse transcriptase in the absence of infectious virus. When such cell lines were analyzed 1 to 2 weeks after their isolation, however, all produced infectious virus. Because these cell lines were carried in culture, many ceased to release infectious virus but produced defective virions. One defective producer, SWR4, has been extensively studied. The particles it produces have the same density as that of virions of Moloney murine leukemia virus (M-MuLV). The particles contain no 35 to 70S RNA, as determined by analysis of [3H]uridine-labeled particles, and exhibit no endogenous reverse transcriptase activity. Although the reverse transcriptase enzyme is of normal size, the major structural protein of the defective virions has a molecular weight of 28,000 (p28), in contrast to the p30 of M-MuLV, and no viral glycoprotein was evident. The defective particles do not appear to arise either from the helper virus or from Abelson virus. An alteration of the protein of the helper virus is an unlikely source of p28 because particles produced by lymphoid cells transformed with another strain of M-MuLV as helper (M-MuLV-TB) contained p28 with an unaltered cleavage pattern, although M-MuLV-TB p30 differs from M-MuLV p30. The A-MuLV genome lacks the capacity to code for the reverse transcriptase virions. Clones of fibroblasts infected with A-MuLV only occasionally produce defective particles. The defective particles therefore probably arose from an endogenous virus that is preferentially expressed in the class of lymphoid cells transformed by A-MuLV. This interpretation implies that the majority of A-MuLV-transformed lymphoid cells completely lose expression of the helper virus genome.

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Selected References

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

  1. Aaronson S. A., Stephenson J. R. Widespread natural occurrence of high titers of neutralizing antibodies to a specific class of endogenous mouse type-C virus. Proc Natl Acad Sci U S A. 1974 May;71(5):1957–1961. doi: 10.1073/pnas.71.5.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Besmer P., Smotkin D., Haseltine W., Fan H., Wilson A. T., Paskind M., Weinberg R., Baltimore D. Mechanism of induction of RNA tumor viruses by halogenated pyrimidines. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):1103–1107. doi: 10.1101/sqb.1974.039.01.125. [DOI] [PubMed] [Google Scholar]
  4. Cleveland D. W., Fischer S. G., Kirschner M. W., Laemmli U. K. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977 Feb 10;252(3):1102–1106. [PubMed] [Google Scholar]
  5. Eisenman R. N., Vogt V. M. The biosynthesis of oncovirus proteins. Biochim Biophys Acta. 1978 Apr 6;473(3-4):187–239. doi: 10.1016/0304-419x(78)90014-8. [DOI] [PubMed] [Google Scholar]
  6. Fan H., Paskind M. Measurement of the sequence complexity of cloned Moloney murine leukemia virus 60 to 70S RNA: evidence for a haploid genome. J Virol. 1974 Sep;14(3):421–429. doi: 10.1128/jvi.14.3.421-429.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Freedman H. A., Lilly F. Properties of cell lines derived from tumors induced by Friend virus in BALB/c and BALB/c-H-2b mice. J Exp Med. 1975 Jul 1;142(1):212–223. doi: 10.1084/jem.142.1.212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. GREENWOOD F. C., HUNTER W. M., GLOVER J. S. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY. Biochem J. 1963 Oct;89:114–123. doi: 10.1042/bj0890114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Kessler S. W. Rapid isolation of antigens from cells with a staphylococcal protein A-antibody adsorbent: parameters of the interaction of antibody-antigen complexes with protein A. J Immunol. 1975 Dec;115(6):1617–1624. [PubMed] [Google Scholar]
  11. Levin J. G., Grimley P. M., Ramseur J. M., Berezesky I. K. Deficiency of 60 to 70S RNA in murine leukemia virus particles assembled in cells treated with actinomycin D. J Virol. 1974 Jul;14(1):152–161. doi: 10.1128/jvi.14.1.152-161.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Moroni C., Schumann G. Lipopolysaccharide induces C-type virus in short term cultures of BALB/c spleen cells. Nature. 1975 Mar 6;254(5495):60–61. doi: 10.1038/254060a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Philipson L., Andersson P., Olshevsky U., Weinberg R., Baltimore D., Gesteland R. Translation of MuLV and MSV RNAs in nuclease-treated reticulocyte extracts: enhancement of the gag-pol polypeptide with yeast suppressor tRNA. Cell. 1978 Jan;13(1):189–199. doi: 10.1016/0092-8674(78)90149-6. [DOI] [PubMed] [Google Scholar]
  15. Phillips D. R., Morrison M. Exposed protein on the intact human erythrocyte. Biochemistry. 1971 May 11;10(10):1766–1771. doi: 10.1021/bi00786a006. [DOI] [PubMed] [Google Scholar]
  16. Pratt D. M., Strominger J., Parkman R., Kaplan D., Schwaber J., Rosenberg N., Scher C. D. Abelson virus-transformed lymphocytes: null cells that modulate H-2. Cell. 1977 Nov;12(3):683–690. doi: 10.1016/0092-8674(77)90268-9. [DOI] [PubMed] [Google Scholar]
  17. Premkumar E., Potter M., Singer P. A., Sklar M. D. Synthesis, surface deposition, and secretion of immunoglobulins by Abelson virus-transformed lymphosarcoma cell lines. Cell. 1975 Oct;6(2):149–159. doi: 10.1016/0092-8674(75)90005-7. [DOI] [PubMed] [Google Scholar]
  18. Reynolds F. H., Jr, Sacks T. L., Deobagkar D. N., Stephenson J. R. Cells nonproductively transformed by Abelson murine leukemia virus express a high molecular weight polyprotein containing structural and nonstructural components. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3974–3978. doi: 10.1073/pnas.75.8.3974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rosenberg N., Baltimore D. A quantitative assay for transformation of bone marrow cells by Abelson murine leukemia virus. J Exp Med. 1976 Jun 1;143(6):1453–1463. doi: 10.1084/jem.143.6.1453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rosenberg N., Baltimore D. The effect of helper virus on Abelson virus-induced transformation of lymphoid cells. J Exp Med. 1978 Apr 1;147(4):1126–1141. doi: 10.1084/jem.147.4.1126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rowe W. P., Pugh W. E., Hartley J. W. Plaque assay techniques for murine leukemia viruses. Virology. 1970 Dec;42(4):1136–1139. doi: 10.1016/0042-6822(70)90362-4. [DOI] [PubMed] [Google Scholar]
  22. Scher C. D. Effect of pseudotype on Abelson virus and Kirsten sarcoma virus-induced leukemia. J Exp Med. 1978 Apr 1;147(4):1044–1053. doi: 10.1084/jem.147.4.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Scher C. D., Siegler R. Direct transformation of 3T3 cells by Abelson murine leukaemia virus. Nature. 1975 Feb 27;253(5494):729–731. doi: 10.1038/253729a0. [DOI] [PubMed] [Google Scholar]
  24. Shields A., Witte W. N., Rothenberg E., Baltimore D. High frequency of aberrant expression of Moloney murine leukemia virus in clonal infections. Cell. 1978 Jul;14(3):601–609. doi: 10.1016/0092-8674(78)90245-3. [DOI] [PubMed] [Google Scholar]
  25. Siden E. J., Baltimore D., Clark D., Rosenberg N. E. Immunoglobulin synthesis by lymphoid cells transformed in vitro by Abelson murine leukemia virus. Cell. 1979 Feb;16(2):389–396. doi: 10.1016/0092-8674(79)90014-x. [DOI] [PubMed] [Google Scholar]
  26. Sklar M. D., Shevach E. M., Green I., Potter M. Transplantation and preliminary characterisation of lymphocyte surface markers of Abelson virus-induced lymphomas. Nature. 1975 Feb 13;253(5492):550–552. doi: 10.1038/253550a0. [DOI] [PubMed] [Google Scholar]
  27. Staber F. G., Schläfli E., Moroni C. Expression of endogenous C-type viral antigen on normal mouse haemopoietic stem cells. Nature. 1978 Oct 19;275(5681):669–671. doi: 10.1038/275669a0. [DOI] [PubMed] [Google Scholar]
  28. Steffen D., Weinberg R. A. The integrated genome of murine leukemia virus. Cell. 1978 Nov;15(3):1003–1010. doi: 10.1016/0092-8674(78)90284-2. [DOI] [PubMed] [Google Scholar]
  29. Stephenson J. R., Aaronson S. A. Induction of an endogenous B-tropic type C RNA virus from SWR/J mouse embryo cells in tissue culture. Virology. 1976 Apr;70(2):352–359. doi: 10.1016/0042-6822(76)90277-4. [DOI] [PubMed] [Google Scholar]
  30. Weimann B. J. Induction of immunoglobulin synthesis in Abelson murine leukemia virus-transformed mouse lymphoma cells in culture. Cold Spring Harb Symp Quant Biol. 1977;41(Pt 1):163–164. doi: 10.1101/sqb.1977.041.01.021. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Witte O. N., Rosenberg N., Paskind M., Shields A., Baltimore D. Identification of an Abelson murine leukemia virus-encoded protein present in transformed fibroblast and lymphoid cells. Proc Natl Acad Sci U S A. 1978 May;75(5):2488–2492. doi: 10.1073/pnas.75.5.2488. [DOI] [PMC free article] [PubMed] [Google Scholar]

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