Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1985 Sep;55(3):617–622. doi: 10.1128/jvi.55.3.617-622.1985

Susceptibility to erbB-induced erythroblastosis is a dominant trait of 151 chickens.

H L Robinson, B D Miles, D E Catalano, W E Briles, L B Crittenden
PMCID: PMC255023  PMID: 2991584

Abstract

Rous-associated virus-1 (RAV-1)-induced erythroblastosis results from proviral insertions into or viral transductions of the c-erbB region of the epidermal growth factor gene. Most chickens develop low incidences (less than 5%) of RAV-1-induced erythroblastosis. However, an inbred line of chickens (151) suffers high incidences (approximately 80%) of RAV-1-induced erythroblastosis. Analysis of 151, K28, and (K28 X 151) X K28 chickens for susceptibility to RAV-1-induced erythroblastosis revealed that susceptibility to RAV-1-induced erythroblastosis is a dominant trait of line 151 chickens. Analysis of 151 X K28 and K28 chicks for susceptibility to the induction of erythroblastosis by two new c-erbB-transducing viruses (avian erythroblastosis virus strains AEV-5005 and AEV-5009) revealed that susceptibility to transformation by new c-erbB-transducing viruses is also a dominant trait of 151 chickens. We think it is likely that both of these dominant traits are encoded by the same gene or genes. Our hypothesis is that this gene (or genes) potentiates the ability of the transmembrane and cytoplasmic domains of the epidermal growth factor receptor to transform cells.

Full text

PDF
621

Selected References

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

  1. Astrin S. M., Robinson H. L. Gs, an allele of chickens for endogenous avian leukosis viral antigens, segregates with ev 3, a genetic locus that contains structural genes for virus. J Virol. 1979 Aug;31(2):420–425. doi: 10.1128/jvi.31.2.420-425.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bacon L. D., Crittenden L. B., Witter R. L., Fadly A., Motta J. B5 and B15 associated with progressive Marek's disease, Rous sarcoma, and avian leukosis virus-induced tumors in inbred 15I4 chickens. Poult Sci. 1983 Apr;62(4):573–578. doi: 10.3382/ps.0620573. [DOI] [PubMed] [Google Scholar]
  3. Bacon L. D., Witter R. L., Crittenden L. B., Fadly A., Motta J. B-haplotype influence on Marek's disease, Rous sarcoma, and lymphoid leukosis virus-induced tumors in chickens. Poult Sci. 1981 Jun;60(6):1132–1139. doi: 10.3382/ps.0601132. [DOI] [PubMed] [Google Scholar]
  4. Briles W. E., Bumstead N., Ewert D. L., Gilmour D. G., Gogusev J., Hála K., Koch C., Longenecker B. M., Nordskog A. W., Pink J. R. Nomenclature for chicken major histocompatibility (B) complex. Immunogenetics. 1982;15(5):441–447. doi: 10.1007/BF00345903. [DOI] [PubMed] [Google Scholar]
  5. Coffin J. M., Varmus H. E., Bishop J. M., Essex M., Hardy W. D., Jr, Martin G. S., Rosenberg N. E., Scolnick E. M., Weinberg R. A., Vogt P. K. Proposal for naming host cell-derived inserts in retrovirus genomes. J Virol. 1981 Dec;40(3):953–957. doi: 10.1128/jvi.40.3.953-957.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Downward J., Yarden Y., Mayes E., Scrace G., Totty N., Stockwell P., Ullrich A., Schlessinger J., Waterfield M. D. Close similarity of epidermal growth factor receptor and v-erb-B oncogene protein sequences. Nature. 1984 Feb 9;307(5951):521–527. doi: 10.1038/307521a0. [DOI] [PubMed] [Google Scholar]
  7. Frykberg L., Palmieri S., Beug H., Graf T., Hayman M. J., Vennström B. Transforming capacities of avian erythroblastosis virus mutants deleted in the erbA or erbB oncogenes. Cell. 1983 Jan;32(1):227–238. doi: 10.1016/0092-8674(83)90513-5. [DOI] [PubMed] [Google Scholar]
  8. Fung Y. K., Fadly A. M., Crittenden L. B., Kung H. J. On the mechanism of retrovirus-induced avian lymphoid leukosis: deletion and integration of the proviruses. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3418–3422. doi: 10.1073/pnas.78.6.3418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Graf T., Fink D., Beug H., Royer-Pokora B. Oncornavirus-induced sarcoma formation obscured by rapid development of lethal leukemia. Cancer Res. 1977 Jan;37(1):59–63. [PubMed] [Google Scholar]
  11. Graf T., Royer-Pokora B., Schubert G. E., Beug H. Evidence for the multiple oncogenic potential of cloned leukemia virus: in vitro and in vitro studies with avian erythroblastosis virus. Virology. 1976 Jun;71(2):423–433. doi: 10.1016/0042-6822(76)90370-6. [DOI] [PubMed] [Google Scholar]
  12. Greenberg M. E., Ziff E. B. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature. 1984 Oct 4;311(5985):433–438. doi: 10.1038/311433a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Hihara H., Yamamoto H., Shimohira H., Arai K., Shimizu T. Avian erythroblastosis virus isolated from chick erythroblastosis induced by lymphatic leukemia virus subgroup A. J Natl Cancer Inst. 1983 May;70(5):891–897. [PubMed] [Google Scholar]
  15. Kelly K., Cochran B. H., Stiles C. D., Leder P. Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor. Cell. 1983 Dec;35(3 Pt 2):603–610. doi: 10.1016/0092-8674(83)90092-2. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Miles B. D., Robinson H. L. High-frequency transduction of c-erbB in avian leukosis virus-induced erythroblastosis. J Virol. 1985 May;54(2):295–303. doi: 10.1128/jvi.54.2.295-303.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nishida T., Sakamoto S., Yamamoto T., Hayman M., Kawai S., Toyoshima K. Comparison of genome structures among three different strains of avian erythroblastosis virus. Gan. 1984 Apr;75(4):325–333. [PubMed] [Google Scholar]
  20. 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]
  21. RUBIN H., VOGT P. K. An avian leukosis virus associated with stocks of Rous sarcoma virus. Virology. 1962 May;17:184–194. doi: 10.1016/0042-6822(62)90096-x. [DOI] [PubMed] [Google Scholar]
  22. Raines M. A., Lewis W. G., Crittenden L. B., Kung H. J. c-erbB activation in avian leukosis virus-induced erythroblastosis: clustered integration sites and the arrangement of provirus in the c-erbB alleles. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2287–2291. doi: 10.1073/pnas.82.8.2287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Robinson H. L. Intracellular restriction on the growth of induced subgroup E avian type C viruses in chicken cells. J Virol. 1976 Jun;18(3):856–866. doi: 10.1128/jvi.18.3.856-866.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Robinson H. L., Lamoreux W. F. Expression of endogenous ALV antigens and susceptibility to subgroup E ALV in three strains of chickens (endogenous avian C-type virus). Virology. 1976 Jan;69(1):50–62. doi: 10.1016/0042-6822(76)90193-8. [DOI] [PubMed] [Google Scholar]
  25. Robinson H. L., Pearson M. N., DeSimone D. W., Tsichlis P. N., Coffin J. M. Subgroup-E avian-leukosis-virus-associated disease in chickens. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 2):1133–1141. doi: 10.1101/sqb.1980.044.01.122. [DOI] [PubMed] [Google Scholar]
  26. Robinson H. L. Retroviruses and cancer. Rev Infect Dis. 1982 Sep-Oct;4(5):1015–1025. doi: 10.1093/clinids/4.5.1015. [DOI] [PubMed] [Google Scholar]
  27. Sealy L., Privalsky M. L., Moscovici G., Moscovici C., Bishop J. M. Site-specific mutagenesis of avian erythroblastosis virus: erb-B is required for oncogenicity. Virology. 1983 Oct 15;130(1):155–178. doi: 10.1016/0042-6822(83)90125-3. [DOI] [PubMed] [Google Scholar]
  28. Sergeant A., Saule S., Leprince D., Begue A., Rommens C., Stehelin D. Molecular cloning and characterization of the chicken DNA locus related to the oncogene erbB of avian erythroblastosis virus. EMBO J. 1982;1(2):237–242. doi: 10.1002/j.1460-2075.1982.tb01153.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tracy S. E., Woda B. A., Robinson H. L. Induction of angiosarcoma by a c-erbB transducing virus. J Virol. 1985 May;54(2):304–310. doi: 10.1128/jvi.54.2.304-310.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ullrich A., Coussens L., Hayflick J. S., Dull T. J., Gray A., Tam A. W., Lee J., Yarden Y., Libermann T. A., Schlessinger J. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. 1984 May 31-Jun 6Nature. 309(5967):418–425. doi: 10.1038/309418a0. [DOI] [PubMed] [Google Scholar]
  31. Vennström B., Bishop J. M. Isolation and characterization of chicken DNA homologous to the two putative oncogenes of avian erythroblastosis virus. Cell. 1982 Jan;28(1):135–143. doi: 10.1016/0092-8674(82)90383-x. [DOI] [PubMed] [Google Scholar]
  32. Yamamoto T., Hihara H., Nishida T., Kawai S., Toyoshima K. A new avian erythroblastosis virus, AEV-H, carries erbB gene responsible for the induction of both erythroblastosis and sarcomas. Cell. 1983 Aug;34(1):225–232. doi: 10.1016/0092-8674(83)90153-8. [DOI] [PubMed] [Google Scholar]

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

RESOURCES