Transformation of quail embryo fibroblasts by a retrovirus carrying a normal human c-myc gene (original) (raw)

Abstract

We have constructed avian retroviruses expressing the human c-myc oncogene. These viruses morphologically transformed primary quail embryo fibroblasts upon transfection and infection. Transformed cells produced viruses harboring a spliced c-myc gene and contained high levels of p64-67c-myc protein. One of these infectious viruses, vSX-AHM, was molecularly cloned and the nucleotide sequence of the spliced c-myc insert determined. No mutation was found within the c-myc coding sequence of this transforming clone when compared to the normal genomic progenitor. Thus, we concluded that no mutation within the human c-myc gene is required to induce primary avian embryo fibroblast transformation.

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  1. 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]
  2. Battey J., Moulding C., Taub R., Murphy W., Stewart T., Potter H., Lenoir G., Leder P. The human c-myc oncogene: structural consequences of translocation into the IgH locus in Burkitt lymphoma. Cell. 1983 Oct;34(3):779–787. doi: 10.1016/0092-8674(83)90534-2. [DOI] [PubMed] [Google Scholar]
  3. Capon D. J., Seeburg P. H., McGrath J. P., Hayflick J. S., Edman U., Levinson A. D., Goeddel D. V. Activation of Ki-ras2 gene in human colon and lung carcinomas by two different point mutations. Nature. 1983 Aug 11;304(5926):507–513. doi: 10.1038/304507a0. [DOI] [PubMed] [Google Scholar]
  4. Cohen J. B., Unger T., Rechavi G., Canaani E., Givol D. Rearrangement of the oncogene c-mos in mouse myeloma NSI and hybridomas. Nature. 1983 Dec 22;306(5945):797–799. doi: 10.1038/306797a0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Corcoran L. M., Cory S., Adams J. M. Transposition of the immunoglobulin heavy chain enhancer to the myc oncogene in a murine plasmacytoma. Cell. 1985 Jan;40(1):71–79. doi: 10.1016/0092-8674(85)90310-1. [DOI] [PubMed] [Google Scholar]
  7. Fung Y. K., Lewis W. G., Crittenden L. B., Kung H. J. Activation of the cellular oncogene c-erbB by LTR insertion: molecular basis for induction of erythroblastosis by avian leukosis virus. Cell. 1983 Jun;33(2):357–368. doi: 10.1016/0092-8674(83)90417-8. [DOI] [PubMed] [Google Scholar]
  8. Gambke C., Hall A., Moroni C. Activation of an N-ras gene in acute myeloblastic leukemia through somatic mutation in the first exon. Proc Natl Acad Sci U S A. 1985 Feb;82(3):879–882. doi: 10.1073/pnas.82.3.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gazin C., Dupont de Dinechin S., Hampe A., Masson J. M., Martin P., Stehelin D., Galibert F. Nucleotide sequence of the human c-myc locus: provocative open reading frame within the first exon. EMBO J. 1984 Feb;3(2):383–387. doi: 10.1002/j.1460-2075.1984.tb01816.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Graf T., Stéhelin D. Avian leukemia viruses. Oncogenes and genome structure. Biochim Biophys Acta. 1982 Jun 28;651(4):245–271. doi: 10.1016/0304-419x(82)90014-2. [DOI] [PubMed] [Google Scholar]
  11. Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Hayashi K. A cloning vehicle suitable for strand separation. Gene. 1980 Oct;11(1-2):109–115. doi: 10.1016/0378-1119(80)90091-8. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Hérissé J., Courtois G., Galibert F. Nucleotide sequence of the EcoRI D fragment of adenovirus 2 genome. Nucleic Acids Res. 1980 May 24;8(10):2173–2192. doi: 10.1093/nar/8.10.2173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kan N. C., Flordellis C. S., Mark G. E., Duesberg P. H., Papas T. S. A common onc gene sequence transduced by avian carcinoma virus MH2 and by murine sarcoma virus 3611. Science. 1984 Feb 24;223(4638):813–816. doi: 10.1126/science.6320371. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Lee W. M., Schwab M., Westaway D., Varmus H. E. Augmented expression of normal c-myc is sufficient for cotransformation of rat embryo cells with a mutant ras gene. Mol Cell Biol. 1985 Dec;5(12):3345–3356. doi: 10.1128/mcb.5.12.3345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Martin P., Henry C., Ferre F., Bechade C., Begue A., Calothy C., Debuire B., Stehelin D., Saule S. Characterization of a myc-containing retrovirus generated by propagation of an MH2 viral subgenomic RNA. J Virol. 1986 Mar;57(3):1191–1194. doi: 10.1128/jvi.57.3.1191-1194.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  22. Mougneau E., Lemieux L., Rassoulzadegan M., Cuzin F. Biological activities of v-myc and rearranged c-myc oncogenes in rat fibroblast cells in culture. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5758–5762. doi: 10.1073/pnas.81.18.5758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Murray M. J., Cunningham J. M., Parada L. F., Dautry F., Lebowitz P., Weinberg R. A. The HL-60 transforming sequence: a ras oncogene coexisting with altered myc genes in hematopoietic tumors. Cell. 1983 Jul;33(3):749–757. doi: 10.1016/0092-8674(83)90017-x. [DOI] [PubMed] [Google Scholar]
  24. Neiman P., Wolf C., Enrietto P. J., Cooper G. M. A retroviral myc gene induces preneoplastic transformation of lymphocytes in a bursal transplantation assay. Proc Natl Acad Sci U S A. 1985 Jan;82(1):222–226. doi: 10.1073/pnas.82.1.222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Papas T. S., Lautenberger J. A. Sequence curiosity in v-myc oncogene. Nature. 1985 Nov 21;318(6043):237–237. doi: 10.1038/318237a0. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Rabbitts T. H., Forster A., Hamlyn P., Baer R. Effect of somatic mutation within translocated c-myc genes in Burkitt's lymphoma. Nature. 1984 Jun 14;309(5969):592–597. doi: 10.1038/309592a0. [DOI] [PubMed] [Google Scholar]
  28. Rabbitts T. H., Hamlyn P. H., Baer R. Altered nucleotide sequences of a translocated c-myc gene in Burkitt lymphoma. Nature. 1983 Dec 22;306(5945):760–765. doi: 10.1038/306760a0. [DOI] [PubMed] [Google Scholar]
  29. Santos E., Tronick S. R., Aaronson S. A., Pulciani S., Barbacid M. T24 human bladder carcinoma oncogene is an activated form of the normal human homologue of BALB- and Harvey-MSV transforming genes. Nature. 1982 Jul 22;298(5872):343–347. doi: 10.1038/298343a0. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Showe L. C., Ballantine M., Nishikura K., Erikson J., Kaji H., Croce C. M. Cloning and sequencing of a c-myc oncogene in a Burkitt's lymphoma cell line that is translocated to a germ line alpha switch region. Mol Cell Biol. 1985 Mar;5(3):501–509. doi: 10.1128/mcb.5.3.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Swift R. A., Shaller E., Witter R. L., Kung H. J. Insertional activation of c-myc by reticuloendotheliosis virus in chicken B lymphoma: nonrandom distribution and orientation of the proviruses. J Virol. 1985 Jun;54(3):869–872. doi: 10.1128/jvi.54.3.869-872.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vennström B., Fanshier L., Moscovici C., Bishop J. M. Molecular cloning of the avian erythroblastosis virus genome and recovery of oncogenic virus by transfection of chicken cells. J Virol. 1980 Nov;36(2):575–585. doi: 10.1128/jvi.36.2.575-585.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Vennström B., Kahn P., Adkins B., Enrietto P., Hayman M. J., Graf T., Luciw P. Transformation of mammalian fibroblasts and macrophages in vitro by a murine retrovirus encoding an avian v-myc oncogene. EMBO J. 1984 Dec 20;3(13):3223–3229. doi: 10.1002/j.1460-2075.1984.tb02282.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Vennström B., Moscovici C., Goodman H. M., Bishop J. M. Molecular cloning of the avian myelocytomatosis virus genome and recovery of infectious virus by transfection of chicken cells. J Virol. 1981 Aug;39(2):625–631. doi: 10.1128/jvi.39.2.625-631.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Westaway D., Payne G., Varmus H. E. Proviral deletions and oncogene base-substitutions in insertionally mutagenized c-myc alleles may contribute to the progression of avian bursal tumors. Proc Natl Acad Sci U S A. 1984 Feb;81(3):843–847. doi: 10.1073/pnas.81.3.843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wiman K. G., Clarkson B., Hayday A. C., Saito H., Tonegawa S., Hayward W. S. Activation of a translocated c-myc gene: role of structural alterations in the upstream region. Proc Natl Acad Sci U S A. 1984 Nov;81(21):6798–6802. doi: 10.1073/pnas.81.21.6798. [DOI] [PMC free article] [PubMed] [Google Scholar]