Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1989 Dec;63(12):5092–5100. doi: 10.1128/jvi.63.12.5092-5100.1989

FH3, a v-myc avian retrovirus with limited transforming ability.

C Chen 1, B J Biegalke 1, R N Eisenman 1, M L Linial 1
PMCID: PMC251171  PMID: 2555545

Abstract

We have isolated a new acute avian transforming virus which contains the oncogene myc. This virus, designated FH3, was isolated after injection of a 10-day-old chick embryo with avian leukosis virus. While FH3 shares many properties with other v-myc-containing avian retroviruses, it also has several unique properties. The primary target for transformation in vitro is chicken macrophages; infection of chicken fibroblasts does not lead to complete morphological transformation. FH3 also exhibits a limited host range, in that Japanese quail macrophages and fibroblasts are infected but are not completely transformed. FH3 induces in vivo a limited tumor type if injected into 10-day-old chick embryos; only a cranial myelocytoma, which does not appear to be metastatic, can be detected. The v-myc gene of FH3 is expressed predominantly as a P145 Gag-Myc protein which is encoded by a ca. 8-kilobase genomic RNA. This FH3-encoded polyprotein is localized in the nucleus of all infected cells, whether or not they are transformed.

Full text

PDF
5092

Images in this article

5095Image
on p.5095
5095Image
on p.5095
5096Image
on p.5096
5096Image
on p.5096
5098Image
on p.5098
5098Image
on p.5098
5099Image
on p.5099

Selected References

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

  1. Alexander R. W., Moscovici C., Vogt P. K. Avian oncovirus Mill Hill No. 2: pathogenicity in chickens. J Natl Cancer Inst. 1979 Feb;62(2):359–366. [PubMed] [Google Scholar]
  2. Alitalo K., Bishop J. M., Smith D. H., Chen E. Y., Colby W. W., Levinson A. D. Nucleotide sequence to the v-myc oncogene of avian retrovirus MC29. Proc Natl Acad Sci U S A. 1983 Jan;80(1):100–104. doi: 10.1073/pnas.80.1.100. [DOI] [PMC free article] [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. Biegalke B. J., Heaney M. L., Bouton A., Parsons J. T., Linial M. MC29 deletion mutants which fail to transform chicken macrophages are competent for transformation of quail macrophages. J Virol. 1987 Jul;61(7):2138–2142. doi: 10.1128/jvi.61.7.2138-2142.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Biegalke B., Linial M. Retention or loss of v-mil sequences after propagation of MH2 virus in vivo or in vitro. J Virol. 1987 Jun;61(6):1949–1956. doi: 10.1128/jvi.61.6.1949-1956.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bister K., Löliger H. C., Duesberg P. H. Oligoribonucleotide map and protein of CMII: detection of conserved and nonconserved genetic elements in avian acute leukemia viruses CMII, MC29, and MH2. J Virol. 1979 Oct;32(1):208–219. doi: 10.1128/jvi.32.1.208-219.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bister K., Ramsay G. M., Hayman M. J. Deletions within the transformation-specific RNA sequences of acute leukemia virus MC29 give rise to partially transformation-defective mutants. J Virol. 1982 Mar;41(3):754–766. doi: 10.1128/jvi.41.3.754-766.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Coll J., Righi M., Taisne C., Dissous C., Gegonne A., Stehelin D. Molecular cloning of the avian acute transforming retrovirus MH2 reveals a novel cell-derived sequence (v-mil) in addition to the myc oncogene. EMBO J. 1983;2(12):2189–2194. doi: 10.1002/j.1460-2075.1983.tb01722.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dugaiczyk A., Haron J. A., Stone E. M., Dennison O. E., Rothblum K. N., Schwartz R. J. Cloning and sequencing of a deoxyribonucleic acid copy of glyceraldehyde-3-phosphate dehydrogenase messenger ribonucleic acid isolated from chicken muscle. Biochemistry. 1983 Mar 29;22(7):1605–1613. doi: 10.1021/bi00276a013. [DOI] [PubMed] [Google Scholar]
  10. Eisenman R. N., Mason W. S., Linial M. Synthesis and processing of polymerase proteins of wild-type and mutant avian retroviruses. J Virol. 1980 Oct;36(1):62–78. doi: 10.1128/jvi.36.1.62-78.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Enrietto P. J. A small deletion in the carboxy terminus of the viral myc gene renders the virus MC29 partially transformation defective in avian fibroblasts. Virology. 1989 Feb;168(2):256–266. doi: 10.1016/0042-6822(89)90265-1. [DOI] [PubMed] [Google Scholar]
  12. Enrietto P. J., Hayman M. J. Restriction enzyme analysis of partially transformation-defective mutants of acute leukemia virus MC29. J Virol. 1982 Nov;44(2):711–715. doi: 10.1128/jvi.44.2.711-715.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Hann S. R., Abrams H. D., Rohrschneider L. R., Eisenman R. N. Proteins encoded by v-myc and c-myc oncogenes: identification and localization in acute leukemia virus transformants and bursal lymphoma cell lines. Cell. 1983 Oct;34(3):789–798. doi: 10.1016/0092-8674(83)90535-4. [DOI] [PubMed] [Google Scholar]
  15. Hann S. R., Eisenman R. N. Proteins encoded by the human c-myc oncogene: differential expression in neoplastic cells. Mol Cell Biol. 1984 Nov;4(11):2486–2497. doi: 10.1128/mcb.4.11.2486. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hayflick J., Seeburg P. H., Ohlsson R., Pfeifer-Ohlsson S., Watson D., Papas T., Duesberg P. H. Nucleotide sequence of two overlapping myc-related genes in avian carcinoma virus OK10 and their relation to the myc genes of other viruses and the cell. Proc Natl Acad Sci U S A. 1985 May;82(9):2718–2722. doi: 10.1073/pnas.82.9.2718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hayman M. J., Kitchener G., Graf T. Cells transformed by avian myelocytomatosis virus strain CMII contain a 90K gag-related protein. Virology. 1979 Oct 15;98(1):191–199. doi: 10.1016/0042-6822(79)90537-3. [DOI] [PubMed] [Google Scholar]
  18. Hayward W. S., Neel B. G., Astrin S. M. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature. 1981 Apr 9;290(5806):475–480. doi: 10.1038/290475a0. [DOI] [PubMed] [Google Scholar]
  19. Heaney M. L., Pierce J., Parsons J. T. Site-directed mutagenesis of the gag-myc gene of avian myelocytomatosis virus 29: biological activity and intracellular localization of structurally altered proteins. J Virol. 1986 Oct;60(1):167–176. doi: 10.1128/jvi.60.1.167-176.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hihara H., Shimizu T., Yamamoto H. Establishment of tumor cell lines cultured from chickens with avian lymphoid leukosis. Natl Inst Anim Health Q (Tokyo) 1974 Winter;14(4):163–173. [PubMed] [Google Scholar]
  21. Jansen H. W., Rückert B., Lurz R., Bister K. Two unrelated cell-derived sequences in the genome of avian leukemia and carcinoma inducing retrovirus MH2. EMBO J. 1983;2(11):1969–1975. doi: 10.1002/j.1460-2075.1983.tb01686.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kan N. C., Flordellis C. S., Garon C. F., Duesberg P. H., Papas T. S. Avian carcinoma virus MH2 contains a transformation-specific sequence, mht, and shares the myc sequence with MC29, CMII, and OK10 viruses. Proc Natl Acad Sci U S A. 1983 Nov;80(21):6566–6570. doi: 10.1073/pnas.80.21.6566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Linial M., Groudine M. Transcription of three c-myc exons is enhanced in chicken bursal lymphoma cell lines. Proc Natl Acad Sci U S A. 1985 Jan;82(1):53–57. doi: 10.1073/pnas.82.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Linial M. Two retroviruses with similar transforming genes exhibit differences in transforming potential. Virology. 1982 Jun;119(2):382–391. doi: 10.1016/0042-6822(82)90097-6. [DOI] [PubMed] [Google Scholar]
  25. Lüscher B., Eisenman R. N. c-myc and c-myb protein degradation: effect of metabolic inhibitors and heat shock. Mol Cell Biol. 1988 Jun;8(6):2504–2512. doi: 10.1128/mcb.8.6.2504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mladenov Z., Heine U., Beard D., Beard J. W. Strain MC29 avian leukosis virus. Myelocytoma, endothelioma, and renal growths: pathomorphological and ultrastructural aspects. J Natl Cancer Inst. 1967 Mar;38(3):251–285. [PubMed] [Google Scholar]
  27. Oker-Blom N., Hortling L., Kallio A., Nurmiaho E. L., Westermarck H. OK 10 virus, an avian retrovirus resembling the acute leukaemia viruses. J Gen Virol. 1978 Sep;40(3):623–633. doi: 10.1099/0022-1317-40-3-623. [DOI] [PubMed] [Google Scholar]
  28. Palmieri S. Isolation of an MH2 retrovirus mutant temperature sensitive for macrophage but not fibroblast transformation. J Virol. 1986 Apr;58(1):134–141. doi: 10.1128/jvi.58.1.134-141.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Patschinsky T., Jansen H. W., Blöcker H., Frank R., Bister K. Structure and transforming function of transduced mutant alleles of the chicken c-myc gene. J Virol. 1986 Aug;59(2):341–353. doi: 10.1128/jvi.59.2.341-353.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Payne G. S., Bishop J. M., Varmus H. E. Multiple arrangements of viral DNA and an activated host oncogene in bursal lymphomas. Nature. 1982 Jan 21;295(5846):209–214. doi: 10.1038/295209a0. [DOI] [PubMed] [Google Scholar]
  31. Pfaff S. L., Duesberg P. H. Two autonomous myc oncogenes in avian carcinoma virus OK10. J Virol. 1988 Oct;62(10):3703–3709. doi: 10.1128/jvi.62.10.3703-3709.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ramsay G., Graf T., Hayman M. J. Mutants of avian myelocytomatosis virus with smaller gag gene-related proteins have an altered transforming ability. Nature. 1980 Nov 13;288(5787):170–172. doi: 10.1038/288170a0. [DOI] [PubMed] [Google Scholar]
  33. Ramsay G., Hayman M. J. Analysis of cells transformed by defective leukemia virus OK10: production of noninfectious particles and synthesis of Pr76gag and an additional 200,000-dalton protein. Virology. 1980 Oct 15;106(1):71–81. doi: 10.1016/0042-6822(80)90222-6. [DOI] [PubMed] [Google Scholar]
  34. Reddy E. P., Reynolds R. K., Watson D. K., Schultz R. A., Lautenberger J., Papas T. S. Nucleotide sequence analysis of the proviral genome of avian myelocytomatosis virus (MC29). Proc Natl Acad Sci U S A. 1983 May;80(9):2500–2504. doi: 10.1073/pnas.80.9.2500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Royer-Pokora B., Beug H., Claviez M., Winkhardt H. J., Friis R. R., Graf T. Transformation parameters in chicken fibroblasts transformed by AEV and MC29 avian leukemia viruses. Cell. 1978 Apr;13(4):751–760. doi: 10.1016/0092-8674(78)90225-8. [DOI] [PubMed] [Google Scholar]
  36. Schwartz D. E., Tizard R., Gilbert W. Nucleotide sequence of Rous sarcoma virus. Cell. 1983 Mar;32(3):853–869. doi: 10.1016/0092-8674(83)90071-5. [DOI] [PubMed] [Google Scholar]
  37. Shaw J., Hayman M. J., Enrietto P. J. Analysis of a deleted MC29 provirus: gag sequences are not required for fibroblast transformation. J Virol. 1985 Dec;56(3):943–950. doi: 10.1128/jvi.56.3.943-950.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Walther N., Jansen H. W., Trachmann C., Bister K. Nucleotide sequence of the CMII v-myc allele. Virology. 1986 Oct 15;154(1):219–223. doi: 10.1016/0042-6822(86)90444-7. [DOI] [PubMed] [Google Scholar]
  39. Walther N., Lurz R., Patschinsky T., Jansen H. W., Bister K. Molecular cloning of proviral DNA and structural analysis of the transduced myc oncogene of avian oncovirus CMII. J Virol. 1985 May;54(2):576–585. doi: 10.1128/jvi.54.2.576-585.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Watson D. K., Reddy E. P., Duesberg P. H., Papas T. S. Nucleotide sequence analysis of the chicken c-myc gene reveals homologous and unique coding regions by comparison with the transforming gene of avian myelocytomatosis virus MC29, delta gag-myc. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2146–2150. doi: 10.1073/pnas.80.8.2146. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES