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. 1986 Jan;57(1):371–375. doi: 10.1128/jvi.57.1.371-375.1986

Oncogene expression in reticuloendotheliosis virus-transformed lymphoid cell lines and avian tissues.

N K Herzog, W J Bargmann, H R Bose Jr
PMCID: PMC252739  PMID: 2867231

Abstract

The genome of reticuloendotheliosis virus (REV-T) contains a unique oncogene, designated v-rel, which is inserted into the env region. Employing a cloned rel DNA probe, a single 2.9- to 3.0-kilobase v-rel mRNA was identified in poly(A)+ RNA from REV-T-transformed lymphoid cell lines. A 4.0-kilobase rel-specific transcript corresponding to the cellular homolog of the v-rel oncogene was identified in MSB-1 cells, a herpesvirus-transformed lymphoid cell line. Cytodot hybridization was used to quantitate the levels of rel, c-rel, c-myc, c-myb, c-abl, c-fms, c-Ha-ras, c-Ki-ras, c-src, c-yes, c-mos, and c-sis mRNA in REV-T-transformed cells. The levels of rel transcription in REV-T-transformed cells were elevated only two to eightfold over levels found in the transformed immature avian lymphoid cell line MSB-1. The relatively modest levels of rel transcription in REV-T-transformed cells and the significant differences between the lengths of the v-rel and c-rel mRNA suggest that REV-T transformation is the result of the production of an altered rel protein. The c-rel proto-oncogene is expressed in all avian hematopoietic tissues but is not expressed at significant levels in brain and muscle. The transcription of other proto-oncogenes is not enhanced in REV-T-transformed lymphoid cell lines.

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Selected References

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

  1. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beug H., Müller H., Grieser S., Doederlein G., Graf T. Hematopoietic cells transformed in vitro by REVT avian reticuloendotheliosis virus express characteristics of very immature lymphoid cells. Virology. 1981 Dec;115(2):295–309. doi: 10.1016/0042-6822(81)90112-4. [DOI] [PubMed] [Google Scholar]
  3. Beug H., von Kirchbach A., Döderlein G., Conscience J. F., Graf T. Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell. 1979 Oct;18(2):375–390. doi: 10.1016/0092-8674(79)90057-6. [DOI] [PubMed] [Google Scholar]
  4. Breitman M. L., Lai M. M., Vogt P. K. The genomic RNA of avian reticuloendotheliosis virus REV. Virology. 1980 Jan 30;100(2):450–461. doi: 10.1016/0042-6822(80)90535-8. [DOI] [PubMed] [Google Scholar]
  5. Chen I. S., Mak T. W., O'Rear J. J., Temin H. M. Characterization of reticuloendotheliosis virus strain T DNA and isolation of a novel variant of reticuloendotheliosis virus strain T by molecular cloning. J Virol. 1981 Dec;40(3):800–811. doi: 10.1128/jvi.40.3.800-811.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chen I. S., Wilhelmsen K. C., Temin H. M. Structure and expression of c-rel, the cellular homolog to the oncogene of reticuloendotheliosis virus strain T. J Virol. 1983 Jan;45(1):104–113. doi: 10.1128/jvi.45.1.104-113.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cohen R. S., Wong T. C., Lai M. M. Characterization of transformation- and replication-specific sequences of reticuloendotheliosis virus. Virology. 1981 Sep;113(2):672–685. doi: 10.1016/0042-6822(81)90196-3. [DOI] [PubMed] [Google Scholar]
  8. Coll J., Saule S., Martin P., Raes M. B., Lagrou C., Graf T., Beug H., Simon I. E., Stehelin D. The cellular oncogenes c-myc, c-myb and c-erb are transcribed in defined types of avian hematopoietic cells. Exp Cell Res. 1983 Nov;149(1):151–162. doi: 10.1016/0014-4827(83)90388-9. [DOI] [PubMed] [Google Scholar]
  9. Franklin R. B., Kang C. Y., Min-Min Wan K., Bose H. R., Jr Transformation of chick embryo fibroblasts by reticuloendotheliosis virus. Virology. 1977 Dec;83(2):313–321. doi: 10.1016/0042-6822(77)90176-3. [DOI] [PubMed] [Google Scholar]
  10. Franklin R. B., Maldonado R. L., Bose H. R. Isolation and characterization of reticuloendotheliosis virus transformed bone marrow cells. Intervirology. 1974;3(5-6):342–352. doi: 10.1159/000149771. [DOI] [PubMed] [Google Scholar]
  11. Gonda M. A., Rice N. R., Gilden R. V. Avian reticuloendotheliosis virus: characterization of the high-molecular-weight viral RNA in transforming and helper virus populations. J Virol. 1980 Jun;34(3):743–751. doi: 10.1128/jvi.34.3.743-751.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gonda T. J., Metcalf D. Expression of myb, myc and fos proto-oncogenes during the differentiation of a murine myeloid leukaemia. Nature. 1984 Jul 19;310(5974):249–251. doi: 10.1038/310249a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Graf T., Beug H. Avian leukemia viruses: interaction with their target cells in vivo and in vitro. Biochim Biophys Acta. 1978 Nov 17;516(3):269–299. doi: 10.1016/0304-419x(78)90011-2. [DOI] [PubMed] [Google Scholar]
  15. Hoelzer J. D., Franklin R. B., Bose H. R., Jr Transformation by reticuloendotheliosis virus: development of a focus assay and isolation of a nontransforming virus. Virology. 1979 Feb;93(1):20–30. doi: 10.1016/0042-6822(79)90272-1. [DOI] [PubMed] [Google Scholar]
  16. Janković B. D., Knezević Z., Isaković K., Mitrović K., Marković B. M., Rajcević M. Bursa lymphocytes and IgM-containing cells in chicken embryos bursectomized at 52-64 hours of incubation. Eur J Immunol. 1975 Sep;5(9):656–659. doi: 10.1002/eji.1830050915. [DOI] [PubMed] [Google Scholar]
  17. Land H., Parada L. F., Weinberg R. A. Cellular oncogenes and multistep carcinogenesis. Science. 1983 Nov 18;222(4625):771–778. doi: 10.1126/science.6356358. [DOI] [PubMed] [Google Scholar]
  18. Lehrach H., Diamond D., Wozney J. M., Boedtker H. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry. 1977 Oct 18;16(21):4743–4751. doi: 10.1021/bi00640a033. [DOI] [PubMed] [Google Scholar]
  19. Lewis R. B., McClure J., Rup B., Niesel D. W., Garry R. F., Hoelzer J. D., Nazerian K., Bose H. R., Jr Avian reticuloendotheliosis virus: identification of the hematopoietic target cell for transformation. Cell. 1981 Aug;25(2):421–431. doi: 10.1016/0092-8674(81)90060-x. [DOI] [PubMed] [Google Scholar]
  20. MASTER R. W. POSSIBLE SYNTHESIS OF POLYRIBONUCLEOTIDES OF KNOWN BASE-TRIPLET SEQUENCES. Nature. 1965 Apr 3;206:93–93. doi: 10.1038/206093b0. [DOI] [PubMed] [Google Scholar]
  21. Rice N. R., Hiebsch R. R., Gonda M. A., Bose H. R., Jr, Gilden R. V. Genome of reticuloendotheliosis virus: characterization by use of cloned proviral DNA. J Virol. 1982 Apr;42(1):237–252. doi: 10.1128/jvi.42.1.237-252.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  23. Rup B. J., Spence J. L., Hoelzer J. D., Lewis R. B., Carpenter C. R., Rubin A. S., Bose H. R., Jr Immunosuppression induced by avian reticuloendotheliosis virus: mechanism of induction of the suppressor cell. J Immunol. 1979 Sep;123(3):1362–1370. [PubMed] [Google Scholar]
  24. Sheiness D., Gardinier M. Expression of a proto-oncogene (proto-myb) in hemopoietic tissues of mice. Mol Cell Biol. 1984 Jul;4(7):1206–1212. doi: 10.1128/mcb.4.7.1206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Shibuya T., Chen I., Howatson A., Mak T. W. Morphological, immunological, and biochemical analyses of chicken spleen cells transformed in vitro by reticuloendotheliosis virus strain T. Cancer Res. 1982 Jul;42(7):2722–2728. [PubMed] [Google Scholar]
  26. Simek S., Rice N. R. Analysis of the nucleic acid components in reticuloendotheliosis virus. J Virol. 1980 Jan;33(1):320–329. doi: 10.1128/jvi.33.1.320-329.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stephens R. M., Rice N. R., Hiebsch R. R., Bose H. R., Jr, Gilden R. V. Nucleotide sequence of v-rel: the oncogene of reticuloendotheliosis virus. Proc Natl Acad Sci U S A. 1983 Oct;80(20):6229–6233. doi: 10.1073/pnas.80.20.6229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Strohman R. C., Moss P. S., Micou-Eastwood J., Spector D., Przybyla A., Paterson B. Messenger RNA for myosin polypeptides: isolation from single myogenic cell cultures. Cell. 1977 Feb;10(2):265–273. doi: 10.1016/0092-8674(77)90220-3. [DOI] [PubMed] [Google Scholar]
  29. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. White B. A., Bancroft F. C. Cytoplasmic dot hybridization. Simple analysis of relative mRNA levels in multiple small cell or tissue samples. J Biol Chem. 1982 Aug 10;257(15):8569–8572. [PubMed] [Google Scholar]
  31. Wilhelmsen K. C., Eggleton K., Temin H. M. Nucleic acid sequences of the oncogene v-rel in reticuloendotheliosis virus strain T and its cellular homolog, the proto-oncogene c-rel. J Virol. 1984 Oct;52(1):172–182. doi: 10.1128/jvi.52.1.172-182.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wilhelmsen K. C., Temin H. M. Structure and dimorphism of c-rel (turkey), the cellular homolog to the oncogene of reticuloendotheliosis virus strain T. J Virol. 1984 Feb;49(2):521–529. doi: 10.1128/jvi.49.2.521-529.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wong T. C., Lai M. M. Avian reticuloendotheliosis virus contains a new class of oncogene of turkey origin. Virology. 1981 May;111(1):289–293. doi: 10.1016/0042-6822(81)90674-7. [DOI] [PubMed] [Google Scholar]

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