Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1983 Jan;3(1):56–63. doi: 10.1128/mcb.3.1.56

Some lymphoid cell lines transformed by Abelson murine leukemia virus lack a major 36,000-dalton tyrosine protein kinase substrate.

B M Sefton, T Hunter, J A Cooper
PMCID: PMC368502  PMID: 6298608

Abstract

Fibroblasts transformed by Abelson murine leukemia virus differ from normal fibroblasts in that they contain several cellular proteins, including one of 29 and one of 36 kilodaltons, which are phosphorylated at tyrosine residues. Since it has been shown before that these proteins also become phosphorylated at tyrosine after transformation of fibroblasts by a number of other retroviruses, their phosphorylation may play an important role in the transformation of these cells. In contrast, the 36-kilodalton phosphoprotein was not detectable in three of the four lines of Abelson virus-transformed B lymphoma cell lines studied here. These three cell lines, RAW307.1.1, 18-48, and 18-81, and a B lymphoma induced by mineral oil, WEHI 279, were all found to lack both the phosphorylated and unphosphorylated forms of the 36-kilodalton protein. It thus appears that expression of this major cell protein is not essential for the survival of B lymphoma cells in culture and that the phosphorylation of the 36-kilodalton protein at tyrosine is not essential for transformation of pre-B lymphocytes by Abelson virus.

Full text

PDF
59

Images in this article

Selected References

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

  1. Abelson H. T., Rabstein L. S. Lymphosarcoma: virus-induced thymic-independent disease in mice. Cancer Res. 1970 Aug;30(8):2213–2222. [PubMed] [Google Scholar]
  2. Burnette W. N. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981 Apr;112(2):195–203. doi: 10.1016/0003-2697(81)90281-5. [DOI] [PubMed] [Google Scholar]
  3. Cheng Y. S., Chen L. B. Detection of phosphotyrosine-containing 34,000-dalton protein in the framework of cells transformed with Rous sarcoma virus. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2388–2392. doi: 10.1073/pnas.78.4.2388. [DOI] [PMC free article] [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. Cooper J. A., Hunter T. Changes in protein phosphorylation in Rous sarcoma virus-transformed chicken embryo cells. Mol Cell Biol. 1981 Feb;1(2):165–178. doi: 10.1128/mcb.1.2.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cooper J. A., Hunter T. Discrete primary locations of a tyrosine-protein kinase and of three proteins that contain phosphotyrosine in virally transformed chick fibroblasts. J Cell Biol. 1982 Aug;94(2):287–296. doi: 10.1083/jcb.94.2.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cooper J. A., Hunter T. Four different classes of retroviruses induce phosphorylation of tyrosines present in similar cellular proteins. Mol Cell Biol. 1981 May;1(5):394–407. doi: 10.1128/mcb.1.5.394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Erikson E., Cook R., Miller G. J., Erikson R. L. The same normal cell protein is phosphorylated after transformation by avian sarcoma viruses with unrelated transforming genes. Mol Cell Biol. 1981 Jan;1(1):43–50. doi: 10.1128/mcb.1.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Erikson E., Erikson R. L. Identification of a cellular protein substrate phosphorylated by the avian sarcoma virus-transforming gene product. Cell. 1980 Oct;21(3):829–836. doi: 10.1016/0092-8674(80)90446-8. [DOI] [PubMed] [Google Scholar]
  10. Erikson E., Shealy D. J., Erikson R. L. Evidence that viral transforming gene products and epidermal growth factor stimulate phosphorylation of the same cellular protein with similar specificity. J Biol Chem. 1981 Nov 25;256(22):11381–11384. [PubMed] [Google Scholar]
  11. Garrels J. I. Two dimensional gel electrophoresis and computer analysis of proteins synthesized by clonal cell lines. J Biol Chem. 1979 Aug 25;254(16):7961–7977. [PubMed] [Google Scholar]
  12. Goff S. P., Gilboa E., Witte O. N., Baltimore D. Structure of the Abelson murine leukemia virus genome and the homologous cellular gene: studies with cloned viral DNA. Cell. 1980 Dec;22(3):777–785. doi: 10.1016/0092-8674(80)90554-1. [DOI] [PubMed] [Google Scholar]
  13. Hunter T., Cooper J. A. Epidermal growth factor induces rapid tyrosine phosphorylation of proteins in A431 human tumor cells. Cell. 1981 Jun;24(3):741–752. doi: 10.1016/0092-8674(81)90100-8. [DOI] [PubMed] [Google Scholar]
  14. Hyman R., Stallings V. Complementation patterns of Thy-1 variants and evidence that antigen loss variants "pre-exist" in the parental population. J Natl Cancer Inst. 1974 Feb;52(2):429–436. doi: 10.1093/jnci/52.2.429. [DOI] [PubMed] [Google Scholar]
  15. Kobayashi N., Kaji A. Phosphoprotein associated with activation of the src gene product in myogenic cells. Biochem Biophys Res Commun. 1980 Mar 13;93(1):278–284. doi: 10.1016/s0006-291x(80)80277-4. [DOI] [PubMed] [Google Scholar]
  16. Martinez R., Nakamura K. D., Weber M. J. Identification of phosphotyrosine-containing proteins in untransformed and Rous sarcoma virus-transformed chicken embryo fibroblasts. Mol Cell Biol. 1982 Jun;2(6):653–665. doi: 10.1128/mcb.2.6.653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. North J. R., Raschke W. C. Differentiation antigens on normal and Abelson virus transformed lymphocytes. J Immunol. 1979 Jun;122(6):2571–2576. [PubMed] [Google Scholar]
  18. Pawson T., Guyden J., Kung T. H., Radke K., Gilmore T., Martin G. S. A strain of Fujinami sarcoma virus which is temperature-sensitive in protein phosphorylation and cellular transformation. Cell. 1980 Dec;22(3):767–775. doi: 10.1016/0092-8674(80)90553-x. [DOI] [PubMed] [Google Scholar]
  19. Radke K., Gilmore T., Martin G. S. Transformation by Rous sarcoma virus: a cellular substrate for transformation-specific protein phosphorylation contains phosphotyrosine. Cell. 1980 Oct;21(3):821–828. doi: 10.1016/0092-8674(80)90445-6. [DOI] [PubMed] [Google Scholar]
  20. Radke K., Martin G. S. Transformation by Rous sarcoma virus: effects of src gene expression on the synthesis and phosphorylation of cellular polypeptides. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5212–5216. doi: 10.1073/pnas.76.10.5212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Raschke W. C., Baird S., Ralph P., Nakoinz I. Functional macrophage cell lines transformed by Abelson leukemia virus. Cell. 1978 Sep;15(1):261–267. doi: 10.1016/0092-8674(78)90101-0. [DOI] [PubMed] [Google Scholar]
  22. Raschke W. C. Transformation by Abelson murine leukemia virus: properties of the transformed cells. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 2):1187–1194. doi: 10.1101/sqb.1980.044.01.128. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Reynolds F. H., Jr, Van de Ven W. J., Stephenson J. R. Abelson murine leukemia virus transformation-defective mutants with impaired P120-associated protein kinase activity. J Virol. 1980 Nov;36(2):374–386. doi: 10.1128/jvi.36.2.374-386.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rosenberg N. E., Clark D. R., Witte O. N. Abelson murine leukemia virus mutants deficient in kinase activity and lymphoid cell transformation. J Virol. 1980 Dec;36(3):766–774. doi: 10.1128/jvi.36.3.766-774.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Rübsamen H., Saltenberger K., Friis R. R., Eigenbrodt E. Cytosolic malic dehydrogenase activity is associated with a putative substrate for the transforming gene product of Rous sarcoma virus. Proc Natl Acad Sci U S A. 1982 Jan;79(2):228–232. doi: 10.1073/pnas.79.2.228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Sefton B. M., Beemon K., Hunter T. Comparison of the expression of the src gene of Rous sarcoma virus in vitro and in vivo. J Virol. 1978 Dec;28(3):957–971. doi: 10.1128/jvi.28.3.957-971.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sefton B. M., Hunter T., Ball E. H., Singer S. J. Vinculin: a cytoskeletal target of the transforming protein of Rous sarcoma virus. Cell. 1981 Apr;24(1):165–174. doi: 10.1016/0092-8674(81)90512-2. [DOI] [PubMed] [Google Scholar]
  31. Sefton B. M., Hunter T., Beemon K., Eckhart W. Evidence that the phosphorylation of tyrosine is essential for cellular transformation by Rous sarcoma virus. Cell. 1980 Jul;20(3):807–816. doi: 10.1016/0092-8674(80)90327-x. [DOI] [PubMed] [Google Scholar]
  32. Sefton B. M., Hunter T., Raschke W. C. Evidence that the Abelson virus protein functions in vivo as a protein kinase that phosphorylates tyrosine. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1552–1556. doi: 10.1073/pnas.78.3.1552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Shields A., Goff S., Paskind M., Otto G., Baltimore D. Structure of the Abelson murine leukemia virus genome. Cell. 1979 Dec;18(4):955–962. doi: 10.1016/0092-8674(79)90208-3. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Waneck G. L., Rosenberg N. Abelson leukemia virus induces lymphoid and erythroid colonies in infected fetal cell cultures. Cell. 1981 Oct;26(1 Pt 1):79–89. doi: 10.1016/0092-8674(81)90035-0. [DOI] [PubMed] [Google Scholar]
  37. Warner N. L. Neoplasms of immunoglobulin-producing cells in mice. Recent Results Cancer Res. 1978;64:316–324. doi: 10.1007/978-3-642-81246-0_37. [DOI] [PubMed] [Google Scholar]
  38. Witte O. N., Dasgupta A., Baltimore D. Abelson murine leukaemia virus protein is phosphorylated in vitro to form phosphotyrosine. Nature. 1980 Feb 28;283(5750):826–831. doi: 10.1038/283826a0. [DOI] [PubMed] [Google Scholar]
  39. Witte O. N., Goff S., Rosenberg N., Baltimore D. A transformation-defective mutant of Abelson murine leukemia virus lacks protein kinase activity. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4993–4997. doi: 10.1073/pnas.77.8.4993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. 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]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES