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. 1989 May;63(5):1989–1994. doi: 10.1128/jvi.63.5.1989-1994.1989

Multiple steps are required for the induction of tumors by Abelson murine leukemia virus.

P L Green 1, D A Kaehler 1, L M Bennett 1, R Risser 1
PMCID: PMC250613  PMID: 2539498

Abstract

Helper virus-free Abelson murine leukemia virus (A-MuLV) was used to induce monoclonal pre-B-cell tumors in mice. The clonality, patterns of immunoglobulin heavy-chain gene rearrangement, tumorigenicity, and v-abl oncogene expression in individual preleukemic and leukemic colonies were compared. Our results indicate that A-MuLV preleukemic cells with low or undetectable tumorigenic potential give rise to leukemic cells with high tumorigenic potential by a process of subclone selection. The levels of v-abl oncogene product in preleukemic and leukemic cell populations were not significantly different. These results suggest that an additional event(s) unrelated to the level of the v-abl protein product is required for A-MuLV-transformed cells to become fully malignant.

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Selected References

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  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. Alt F., Rosenberg N., Lewis S., Thomas E., Baltimore D. Organization and reorganization of immunoglobulin genes in A-MULV-transformed cells: rearrangement of heavy but not light chain genes. Cell. 1981 Dec;27(2 Pt 1):381–390. doi: 10.1016/0092-8674(81)90421-9. [DOI] [PubMed] [Google Scholar]
  3. Baumbach W. R., Keath E. J., Cole M. D. A mouse c-myc retrovirus transforms established fibroblast lines in vitro and induces monocyte-macrophage tumors in vivo. J Virol. 1986 Aug;59(2):276–283. doi: 10.1128/jvi.59.2.276-283.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Engelman A., Rosenberg N. Isolation of temperature-sensitive Abelson virus mutants by site-directed mutagenesis. Proc Natl Acad Sci U S A. 1987 Nov;84(22):8021–8025. doi: 10.1073/pnas.84.22.8021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Green P. L., Kaehler D. A., McKearn J., Risser R. Substitution of the LTR of Abelson murine leukemia virus does not alter the cell type of virally induced tumors. Oncogene. 1988 Jun;2(6):585–592. [PubMed] [Google Scholar]
  6. Green P. L., Kaehler D. A., Risser R. Cell transformation and tumor induction by Abelson murine leukemia virus in the absence of helper virus. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5932–5936. doi: 10.1073/pnas.84.16.5932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Green P. L., Kaehler D. A., Risser R. Clonal dominance and progression in Abelson murine leukemia virus lymphomagenesis. J Virol. 1987 Jul;61(7):2192–2197. doi: 10.1128/jvi.61.7.2192-2197.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Horowitz J. M., Risser R. A locus that enhances the induction of endogenous ecotropic murine leukemia viruses is distinct from genome-length ecotropic proviruses. J Virol. 1982 Dec;44(3):950–957. doi: 10.1128/jvi.44.3.950-957.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kipreos E. T., Lee G. J., Wang J. Y. Isolation of temperature-sensitive tyrosine kinase mutants of v-abl oncogene by screening with antibodies for phosphotyrosine. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1345–1349. doi: 10.1073/pnas.84.5.1345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  11. Land H., Parada L. F., Weinberg R. A. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature. 1983 Aug 18;304(5927):596–602. doi: 10.1038/304596a0. [DOI] [PubMed] [Google Scholar]
  12. Newell N., Richards J. E., Tucker P. W., Blattner F. R. J genes for heavy chain immunoglobulins of mouse. Science. 1980 Sep 5;209(4461):1128–1132. doi: 10.1126/science.6250219. [DOI] [PubMed] [Google Scholar]
  13. Ohno S., Migita S., Wiener F., Babonits M., Klein G., Mushinski J. F., Potter M. Chromosomal translocations activating myc sequences and transduction of v-abl are critical events in the rapid induction of plasmacytomas by pristane and abelson virus. J Exp Med. 1984 Jun 1;159(6):1762–1777. doi: 10.1084/jem.159.6.1762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Poirier Y., Kozak C., Jolicoeur P. Identification of a common helper provirus integration site in Abelson murine leukemia virus-induced lymphoma DNA. J Virol. 1988 Nov;62(11):3985–3992. doi: 10.1128/jvi.62.11.3985-3992.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. 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]
  18. Ruley H. E. Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature. 1983 Aug 18;304(5927):602–606. doi: 10.1038/304602a0. [DOI] [PubMed] [Google Scholar]
  19. Savard P., DesGroseillers L., Rassart E., Poirier Y., Jolicoeur P. Important role of the long terminal repeat of the helper Moloney murine leukemia virus in Abelson virus-induced lymphoma. J Virol. 1987 Oct;61(10):3266–3275. doi: 10.1128/jvi.61.10.3266-3275.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. 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]
  23. Sinn E., Muller W., Pattengale P., Tepler I., Wallace R., Leder P. Coexpression of MMTV/v-Ha-ras and MMTV/c-myc genes in transgenic mice: synergistic action of oncogenes in vivo. Cell. 1987 May 22;49(4):465–475. doi: 10.1016/0092-8674(87)90449-1. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Whitlock C. A., Robertson D., Witte O. N. Murine B cell lymphopoiesis in long term culture. J Immunol Methods. 1984 Mar 16;67(2):353–369. doi: 10.1016/0022-1759(84)90475-7. [DOI] [PubMed] [Google Scholar]
  28. Whitlock C. A., Witte O. N. Abelson virus-infected cells can exhibit restricted in vitro growth and low oncogenic potential. J Virol. 1981 Nov;40(2):577–584. doi: 10.1128/jvi.40.2.577-584.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Whitlock C. A., Ziegler S. F., Witte O. N. Progression of the transformed phenotype in clonal lines of Abelson virus-infected lymphocytes. Mol Cell Biol. 1983 Apr;3(4):596–604. doi: 10.1128/mcb.3.4.596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]

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