Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1989 May;63(5):2335–2339. doi: 10.1128/jvi.63.5.2335-2339.1989

Avian erythroblastosis virus transforms a novel mast cell-basophil precursor target in the Japanese quail.

M G Moscovici 1, M L Siegel 1, C Moscovici 1
PMCID: PMC250652  PMID: 2539521

Abstract

Hematopoietic cells of the Japanese quail were transformed by avian erythroblastosis virus in vivo and in vitro. In both circumstances, the infected hematopoietic tissues exhibited a dual oncogenic response of erythroid and mast cell-basophil elements. The erythroid transformants escaped the avian erythroblastosis virus block in differentiation and progressed to hemoglobinization. Resulting basophilic cells were morphologically, biochemically, and ultrastructurally identical to mast cell-basophils observed in other species. None of the virally transformed cells actively produced reverse transcriptase activity. Nonproducer cell lines synthesized viral RNA and both v-erbA and v-erbB proteins. These results indicate that the Japanese quail has a viral target cell different from that of the chicken. The implications of a single bipotential transformation target yielding both erythroid and mast cell-basophil colonies is discussed.

Full text

PDF
2335

Images in this article

2336Image
on p.2336
2337Image
on p.2337
2338Image
on p.2338

Selected References

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

  1. Boucher P., Koning A., Privalsky M. L. The avian erythroblastosis virus erbA oncogene encodes a DNA-binding protein exhibiting distinct nuclear and cytoplasmic subcellular localizations. J Virol. 1988 Feb;62(2):534–544. doi: 10.1128/jvi.62.2.534-544.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Debuire B., Henry C., Bernissa M., Biserte G., Claverie J. M., Saule S., Martin P., Stehelin D. Sequencing the erbA gene of avian erythroblastosis virus reveals a new type of oncogene. Science. 1984 Jun 29;224(4656):1456–1459. doi: 10.1126/science.6328658. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Gandrillon O., Jurdic P., Benchaibi M., Xiao J. H., Ghysdael J., Samarut J. Expression of the v-erbA oncogene in chicken embryo fibroblasts stimulates their proliferation in vitro and enhances tumor growth in vivo. Cell. 1987 Jun 5;49(5):687–697. doi: 10.1016/0092-8674(87)90545-9. [DOI] [PubMed] [Google Scholar]
  6. Gazzolo L., Samarut J., Bouabdelli M., Blanchet J. P. Early precursors in the erythroid lineage are the specific target cells of avian erythroblastosis virus in vitro. Cell. 1980 Dec;22(3):683–691. doi: 10.1016/0092-8674(80)90544-9. [DOI] [PubMed] [Google Scholar]
  7. Gilmore T., DeClue J. E., Martin G. S. Protein phosphorylation at tyrosine is induced by the v-erbB gene product in vivo and in vitro. Cell. 1985 Mar;40(3):609–618. doi: 10.1016/0092-8674(85)90209-0. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Graf T., Beug H. Role of the v-erbA and v-erbB oncogenes of avian erythroblastosis virus in erythroid cell transformation. Cell. 1983 Aug;34(1):7–9. doi: 10.1016/0092-8674(83)90130-7. [DOI] [PubMed] [Google Scholar]
  10. Green S., Walter P., Kumar V., Krust A., Bornert J. M., Argos P., Chambon P. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature. 1986 Mar 13;320(6058):134–139. doi: 10.1038/320134a0. [DOI] [PubMed] [Google Scholar]
  11. Hayman M. J., Beug H. Identification of a form of the avian erythroblastosis virus erb-B gene product at the cell surface. 1984 May 31-Jun 6Nature. 309(5967):460–462. doi: 10.1038/309460a0. [DOI] [PubMed] [Google Scholar]
  12. Hayman M. J., Ramsay G. M., Savin K., Kitchener G., Graf T., Beug H. Identification and characterization of the avian erythroblastosis virus erbB gene product as a membrane glycoprotein. Cell. 1983 Feb;32(2):579–588. doi: 10.1016/0092-8674(83)90477-4. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Kahn P., Frykberg L., Brady C., Stanley I., Beug H., Vennström B., Graf T. v-erbA cooperates with sarcoma oncogenes in leukemic cell transformation. Cell. 1986 May 9;45(3):349–356. doi: 10.1016/0092-8674(86)90320-x. [DOI] [PubMed] [Google Scholar]
  15. Kris R. M., Lax I., Gullick W., Waterfield M. D., Ullrich A., Fridkin M., Schlessinger J. Antibodies against a synthetic peptide as a probe for the kinase activity of the avian EGF receptor and v-erbB protein. Cell. 1985 Mar;40(3):619–625. doi: 10.1016/0092-8674(85)90210-7. [DOI] [PubMed] [Google Scholar]
  16. Krust A., Green S., Argos P., Kumar V., Walter P., Bornert J. M., Chambon P. The chicken oestrogen receptor sequence: homology with v-erbA and the human oestrogen and glucocorticoid receptors. EMBO J. 1986 May;5(5):891–897. doi: 10.1002/j.1460-2075.1986.tb04300.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lagunoff D. Contributions of electron microscopy to the study of mast cells. J Invest Dermatol. 1972 May;58(5):296–311. doi: 10.1111/1523-1747.ep12540314. [DOI] [PubMed] [Google Scholar]
  18. Morikawa S., Yoshikawa Y., Mizutani M., Taniguchi H., Morita M., Yamanouchi K. Oncogenecity of an avian erythroblastosis virus in mutant strains of Japanese quails. Jpn J Med Sci Biol. 1984 Jun;37(3):105–116. doi: 10.7883/yoken1952.37.105. [DOI] [PubMed] [Google Scholar]
  19. Moscovici C., Samarut J., Gazzolo L., Moscovici M. G. Myeloid and erythroid neoplastic responses to avian defective leukemia viruses in chickens and in quail. Virology. 1981 Sep;113(2):765–768. doi: 10.1016/0042-6822(81)90205-1. [DOI] [PubMed] [Google Scholar]
  20. Pierce J. H., Di Fiore P. P., Aaronson S. A., Potter M., Pumphrey J., Scott A., Ihle J. N. Neoplastic transformation of mast cells by Abelson-MuLV: abrogation of IL-3 dependence by a nonautocrine mechanism. Cell. 1985 Jul;41(3):685–693. doi: 10.1016/s0092-8674(85)80049-0. [DOI] [PubMed] [Google Scholar]
  21. Privalsky M. L., Bishop J. M. Subcellular localization of the v-erb-B protein, the product of a transforming gene of avian erythroblastosis virus. Virology. 1984 Jun;135(2):356–368. doi: 10.1016/0042-6822(84)90192-2. [DOI] [PubMed] [Google Scholar]
  22. Privalsky M. L., Ralston R., Bishop J. M. The membrane glycoprotein encoded by the retroviral oncogene v-erb-B is structurally related to tyrosine-specific protein kinases. Proc Natl Acad Sci U S A. 1984 Feb;81(3):704–707. doi: 10.1073/pnas.81.3.704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Privalsky M. L., Sealy L., Bishop J. M., McGrath J. P., Levinson A. D. The product of the avian erythroblastosis virus erbB locus is a glycoprotein. Cell. 1983 Apr;32(4):1257–1267. doi: 10.1016/0092-8674(83)90307-0. [DOI] [PubMed] [Google Scholar]
  24. Raines M. A., Maihle N. J., Moscovici C., Moscovici M. G., Kung H. J. Molecular characterization of three erbB transducing viruses generated during avian leukosis virus-induced erythroleukemia: extensive internal deletion near the kinase domain activates the fibrosarcoma- and hemangioma-inducing potentials of erbB. J Virol. 1988 Jul;62(7):2444–2452. doi: 10.1128/jvi.62.7.2444-2452.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Samarut J., Gazzolo L. Target cells infected by avian erythroblastosis virus differentiate and become transformed. Cell. 1982 Apr;28(4):921–929. doi: 10.1016/0092-8674(82)90071-x. [DOI] [PubMed] [Google Scholar]
  26. Saule S., Roussel M., Lagrou C., Stehelin D. Characterization of the oncogene (erb) of avian erythroblastosis virus and its cellular progenitor. J Virol. 1981 May;38(2):409–419. doi: 10.1128/jvi.38.2.409-419.1981. [DOI] [PMC free article] [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. Siegel M. L., Horwitz R., Morris T. D., Di Venere R. M., Siden E. J. Isolation and characterization of Abelson murine leukemia virus-transformed mast cell lines from midgestation embryonic placenta. Eur J Immunol. 1985 Nov;15(11):1136–1141. doi: 10.1002/eji.1830151113. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. 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]
  32. 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]
  33. Weinberger C., Hollenberg S. M., Rosenfeld M. G., Evans R. M. Domain structure of human glucocorticoid receptor and its relationship to the v-erb-A oncogene product. Nature. 1985 Dec 19;318(6047):670–672. doi: 10.1038/318670a0. [DOI] [PubMed] [Google Scholar]
  34. Wight P. A. The mast cells of Gallus domesticus. I. Distribution and ultrastructure. Acta Anat (Basel) 1970;75(1):100–113. doi: 10.1159/000143444. [DOI] [PubMed] [Google Scholar]
  35. 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