Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1988 Nov;85(22):8506–8510. doi: 10.1073/pnas.85.22.8506

In vitro-derived leukemic erythroid cell lines induced by a raf- and myc-containing retrovirus differentiate in response to erythropoietin.

S P Klinken 1, N A Nicola 1, G R Johnson 1
PMCID: PMC282487  PMID: 2847163

Abstract

In vitro infection of murine fetal liver cells with a retrovirus containing v-raf and v-myc oncogenes has produced continuous lines of immature erythroid cells that are leukemogenic. These cells synthesized a factor that stimulated their growth in vitro before autonomous variants emerged. Approximately 1000 high-affinity erythropoietin receptors could be detected per cell, and the hormone induced terminal differentiation in these cells. The lines were generated at an extremely low frequency (approximately 1 in 10(7) cells), suggesting that the combination of raf and myc is insufficient to develop erythroid cell lines and that additional events are necessary for transformation.

Full text

PDF
8506

Images in this article

Selected References

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

  1. Adams J. M., Harris A. W., Pinkert C. A., Corcoran L. M., Alexander W. S., Cory S., Palmiter R. D., Brinster R. L. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature. 1985 Dec 12;318(6046):533–538. doi: 10.1038/318533a0. [DOI] [PubMed] [Google Scholar]
  2. Anderson S. M., Scolnick E. M. Construction and isolation of a transforming murine retrovirus containing the src gene of Rous sarcoma virus. J Virol. 1983 May;46(2):594–605. doi: 10.1128/jvi.46.2.594-605.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Austyn J. M., Gordon S. F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol. 1981 Oct;11(10):805–815. doi: 10.1002/eji.1830111013. [DOI] [PubMed] [Google Scholar]
  4. Bowtell D. D. Rapid isolation of eukaryotic DNA. Anal Biochem. 1987 May 1;162(2):463–465. doi: 10.1016/0003-2697(87)90421-0. [DOI] [PubMed] [Google Scholar]
  5. Calvo J. C., Radicella J. P., Charreau E. H. Measurement of specific radioactivities in labelled hormones by self-displacement analysis. Biochem J. 1983 May 15;212(2):259–264. doi: 10.1042/bj2120259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Contreras M. A., Bale W. F., Spar I. L. Iodine monochloride (IC1) iodination techniques. Methods Enzymol. 1983;92:277–292. [PubMed] [Google Scholar]
  7. Cooper M. C., Levy J., Cantor L. N., Marks P. A., Rifkind R. A. The effect of erythropoietin on colonial growth of erythroid precursor cells in vitro. Proc Natl Acad Sci U S A. 1974 May;71(5):1677–1680. doi: 10.1073/pnas.71.5.1677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Coppola J. A., Cole M. D. Constitutive c-myc oncogene expression blocks mouse erythroleukaemia cell differentiation but not commitment. Nature. 1986 Apr 24;320(6064):760–763. doi: 10.1038/320760a0. [DOI] [PubMed] [Google Scholar]
  9. Dmitrovsky E., Kuehl W. M., Hollis G. F., Kirsch I. R., Bender T. P., Segal S. Expression of a transfected human c-myc oncogene inhibits differentiation of a mouse erythroleukaemia cell line. Nature. 1986 Aug 21;322(6081):748–750. doi: 10.1038/322748a0. [DOI] [PubMed] [Google Scholar]
  10. Gonda T. J., Sheiness D. K., Bishop J. M. Transcripts from the cellular homologs of retroviral oncogenes: distribution among chicken tissues. Mol Cell Biol. 1982 Jun;2(6):617–624. doi: 10.1128/mcb.2.6.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hankins W. D., Kost T. A., Koury M. J., Krantz S. B. Erythroid bursts produced by Friend leukaemia virus in vitro. Nature. 1978 Nov 30;276(5687):506–508. doi: 10.1038/276506a0. [DOI] [PubMed] [Google Scholar]
  12. Hofer E., Darnell J. E., Jr The primary transcription unit of the mouse beta-major globin gene. Cell. 1981 Feb;23(2):585–593. doi: 10.1016/0092-8674(81)90154-9. [DOI] [PubMed] [Google Scholar]
  13. Holmes K. L., Langdon W. Y., Fredrickson T. N., Coffman R. L., Hoffman P. M., Hartley J. W., Morse H. C., 3rd Analysis of neoplasms induced by Cas-Br-M MuLV tumor extracts. J Immunol. 1986 Jul 15;137(2):679–688. [PubMed] [Google Scholar]
  14. Johnson G. R., Metcalf D. Pure and mixed erythroid colony formation in vitro stimulated by spleen conditioned medium with no detectable erythropoietin. Proc Natl Acad Sci U S A. 1977 Sep;74(9):3879–3882. doi: 10.1073/pnas.74.9.3879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lachman H. M., Cheng G. H., Skoultchi A. I. Transfection of mouse erythroleukemia cells with myc sequences changes the rate of induced commitment to differentiate. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6480–6484. doi: 10.1073/pnas.83.17.6480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Leder P., Battey J., Lenoir G., Moulding C., Murphy W., Potter H., Stewart T., Taub R. Translocations among antibody genes in human cancer. Science. 1983 Nov 18;222(4625):765–771. doi: 10.1126/science.6356357. [DOI] [PubMed] [Google Scholar]
  17. Li C. L., Johnson G. R. Stimulation of multipotential, erythroid and other murine haematopoietic progenitor cells by adherent cell lines in the absence of detectable multi-CSF (IL-3). Nature. 1985 Aug 15;316(6029):633–636. doi: 10.1038/316633a0. [DOI] [PubMed] [Google Scholar]
  18. Mager D. L., Mak T. W., Bernstein A. Quantitative colony method for tumorigenic cells transformed by two distinct strains of Friend leukemia virus. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1703–1707. doi: 10.1073/pnas.78.3.1703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mann R., Mulligan R. C., Baltimore D. Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus. Cell. 1983 May;33(1):153–159. doi: 10.1016/0092-8674(83)90344-6. [DOI] [PubMed] [Google Scholar]
  20. Marks P. A., Rifkind R. A. Erythroleukemic differentiation. Annu Rev Biochem. 1978;47:419–448. doi: 10.1146/annurev.bi.47.070178.002223. [DOI] [PubMed] [Google Scholar]
  21. Mayeux P., Billat C., Jacquot R. Murine erythroleukaemia cells (Friend cells) possess high-affinity binding sites for erythropoietin. FEBS Lett. 1987 Jan 26;211(2):229–233. doi: 10.1016/0014-5793(87)81442-4. [DOI] [PubMed] [Google Scholar]
  22. Mihara A., Fujiwara K., Sato S., Okabe T., Fujiyoshi N. N-terminal amino acid sequence of leukemia derived growth factor (LGF) from human erythroleukemia cell culture. In Vitro Cell Dev Biol. 1987 Apr;23(4):317–322. doi: 10.1007/BF02623717. [DOI] [PubMed] [Google Scholar]
  23. Myers A. C., Kovach J. S., Vuk-Pavlović S. Binding, internalization, and intracellular processing of protein ligands. Derivation of rate constants by computer modeling. J Biol Chem. 1987 May 15;262(14):6494–6499. [PubMed] [Google Scholar]
  24. Nicola N. A., Metcalf D. Binding of iodinated multipotential colony-stimulating factor (interleukin-3) to murine bone marrow cells. J Cell Physiol. 1986 Aug;128(2):180–188. doi: 10.1002/jcp.1041280207. [DOI] [PubMed] [Google Scholar]
  25. Nordan R. P., Pumphrey J. G., Rudikoff S. Purification and NH2-terminal sequence of a plasmacytoma growth factor derived from the murine macrophage cell line P388D1. J Immunol. 1987 Aug 1;139(3):813–817. [PubMed] [Google Scholar]
  26. Okabe T., Fujisawa M., Mihara A., Sato S., Fujiyoshi N., Takaku F. Growth factor(s) produced by a human leukemic cell line growing in a protein-free chemically defined medium. Cancer Res. 1986 Mar;46(3):1043–1046. [PubMed] [Google Scholar]
  27. Piechaczyk M., Blanchard J. M., Marty L., Dani C., Panabieres F., El Sabouty S., Fort P., Jeanteur P. Post-transcriptional regulation of glyceraldehyde-3-phosphate-dehydrogenase gene expression in rat tissues. Nucleic Acids Res. 1984 Sep 25;12(18):6951–6963. doi: 10.1093/nar/12.18.6951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rapp U. R., Cleveland J. L., Fredrickson T. N., Holmes K. L., Morse H. C., 3rd, Jansen H. W., Patschinsky T., Bister K. Rapid induction of hemopoietic neoplasms in newborn mice by a raf(mil)/myc recombinant murine retrovirus. J Virol. 1985 Jul;55(1):23–33. doi: 10.1128/jvi.55.1.23-33.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rapp U. R., Goldsborough M. D., Mark G. E., Bonner T. I., Groffen J., Reynolds F. H., Jr, Stephenson J. R. Structure and biological activity of v-raf, a unique oncogene transduced by a retrovirus. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4218–4222. doi: 10.1073/pnas.80.14.4218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sasaki R., Yanagawa S., Hitomi K., Chiba H. Characterization of erythropoietin receptor of murine erythroid cells. Eur J Biochem. 1987 Oct 1;168(1):43–48. doi: 10.1111/j.1432-1033.1987.tb13384.x. [DOI] [PubMed] [Google Scholar]
  31. Sawyer S. T., Krantz S. B., Goldwasser E. Binding and receptor-mediated endocytosis of erythropoietin in Friend virus-infected erythroid cells. J Biol Chem. 1987 Apr 25;262(12):5554–5562. [PubMed] [Google Scholar]
  32. Scher C. D., Scolnick E. M., Siegler R. Induction of erythroid leukaemia by Harvey and Kirsten sarcoma viruses. Nature. 1975 Jul 17;256(5514):225–226. doi: 10.1038/256225a0. [DOI] [PubMed] [Google Scholar]
  33. Shibuya T., Mak T. W. Isolation and induction of erythroleukemic cell lines with properties of erythroid progenitor burst-forming cell (BFU-E) and erythroid precursor cell (CFU-E). Proc Natl Acad Sci U S A. 1983 Jun;80(12):3721–3725. doi: 10.1073/pnas.80.12.3721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Srinivasan A., Reddy E. P., Aaronson S. A. Abelson murine leukemia virus: molecular cloning of infectious integrated proviral DNA. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2077–2081. doi: 10.1073/pnas.78.4.2077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Stanton L. W., Watt R., Marcu K. B. Translocation, breakage and truncated transcripts of c-myc oncogene in murine plasmacytomas. Nature. 1983 Jun 2;303(5916):401–406. doi: 10.1038/303401a0. [DOI] [PubMed] [Google Scholar]
  36. Tambourin P. E., Wendling F., Jasmin C., Smadja-Joffe F. The physiopathology of Friend leukemia. Leuk Res. 1979;3(3):117–129. doi: 10.1016/0145-2126(79)90009-2. [DOI] [PubMed] [Google Scholar]
  37. Tambourin P., Casadevall N., Choppin J., Lacombe C., Heard J. M., Fichelson S., Wendling F., Varet B. Production of erythropoietin-like activity by a murine erythroleukemia cell line. Proc Natl Acad Sci U S A. 1983 Oct;80(20):6269–6273. doi: 10.1073/pnas.80.20.6269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Todokoro K., Kanazawa S., Amanuma H., Ikawa Y. Specific binding of erythropoietin to its receptor on responsive mouse erythroleukemia cells. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4126–4130. doi: 10.1073/pnas.84.12.4126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Waneck G. L., Keyes L., Rosenberg N. Abelson virus drives the differentiation of Harvey virus-infected erythroid cells. Cell. 1986 Jan 31;44(2):337–344. doi: 10.1016/0092-8674(86)90768-3. [DOI] [PubMed] [Google Scholar]
  40. Wendling F., Moreau-Gachelin F., Tambourin P. Emergence of tumorigenic cells during the course of Friend virus leukemias. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3614–3618. doi: 10.1073/pnas.78.6.3614. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES