Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1980 Nov;77(11):6536–6540. doi: 10.1073/pnas.77.11.6536

Homology exists among the transforming sequences of avian and feline sarcoma viruses.

M Shibuya, T Hanafusa, H Hanafusa, J R Stephenson
PMCID: PMC350320  PMID: 6256742

Abstract

Fujinami sarcoma virus (FSV) of chickens does not contain nucleotide sequences related to the src gene of Rous sarcoma virus, but it carries unique sequences of at least 3000 bases, which are likely to code for the transforming protein of this virus. Using radioactive DNA complementary to FSV-unique sequences, we investigated the relatedness of FSV to other sarcoma-leukemia retroviruses in vertebrates. Under conditions of moderate stringency, no cross-hybridization was detected between FSV cDNA and RNAs of Rous sarcoma virus, Y73 avian sarcoma virus, several representative avian acute leukemia viruses, or Abelson murine leukemia virus. This cDNA, however, did hybridize with RNA of PRCII sarcoma virus of chickens to the extent of 56%. In addition, FSV cDNA was found to hybridize with RNAs of Gardner-Arnstein and Snyder-Theilen strains of feline sarcoma virus to the extent of 27% and 19%, respectively, but not with RNA of McDonough feline sarcoma virus. Studies on thermal denaturation of hybrids showed that the melting temperatures of the heteroduplexes of the FSV cDNA with RNAs of PRCII and Gardner-Arnstein feline sarcoma virus were 7 degrees C and 12 degrees C lower, respectively, compared with the melting temperature of the homologous hybrid of FSV, and suggested less than 10% mismatching in both heteroduplexes. These results indicate that nucleotide sequences closely related to at least a part of FSV-unique sequences are present in the genomes of other sarcoma viruses obtained in chickens and in cats.

Full text

PDF
6538

Selected References

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

  1. Barbacid M., Lauver A. V., Devare S. G. Biochemical and immunological characterization of polyproteins coded for by the McDonough, Gardner-Arnstein, and Snyder-Theilen strains of feline sarcoma virus. J Virol. 1980 Jan;33(1):196–207. doi: 10.1128/jvi.33.1.196-207.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. CARR J. G., CAMPBELL J. G. Three new virus-induced fowl sarcomata. Br J Cancer. 1958 Dec;12(4):631–635. doi: 10.1038/bjc.1958.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Collett M. S., Erikson E., Purchio A. F., Brugge J. S., Erikson R. L. A normal cell protein similar in structure and function to the avian sarcoma virus transforming gene product. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3159–3163. doi: 10.1073/pnas.76.7.3159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Collett M. S., Erikson R. L. Protein kinase activity associated with the avian sarcoma virus src gene product. Proc Natl Acad Sci U S A. 1978 Apr;75(4):2021–2024. doi: 10.1073/pnas.75.4.2021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Frankel A. E., Fischinger P. J. Rate of divergence of cellular sequences homologous to segments of Moloney sarcoma virus. J Virol. 1977 Jan;21(1):153–160. doi: 10.1128/jvi.21.1.153-160.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Frankel A. E., Gilbert J. H., Porzig K. J., Scolnick E. M., Aaronson S. A. Nature and distribution of feline sarcoma virus nucleotide sequences. J Virol. 1979 Jun;30(3):821–827. doi: 10.1128/jvi.30.3.821-827.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gardner M. B., Rongey R. W., Arnstein P., Estes J. D., Sarma P., Huebner R. J., Rickard C. G. Experimental transmission of feline fibrosarcoma to cats and dogs. Nature. 1970 May 30;226(5248):807–809. doi: 10.1038/226807a0. [DOI] [PubMed] [Google Scholar]
  8. Hanafusa H., Halpern C. C., Buchhagen D. L., Kawai S. Recovery of avian sarcoma virus from tumors induced by transformation-defective mutants. J Exp Med. 1977 Dec 1;146(6):1735–1747. doi: 10.1084/jem.146.6.1735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hanafusa T., Wang L. H., Anderson S. M., Karess R. E., Hayward W. S., Hanafusa H. Characterization of the transforming gene of Fujinami sarcoma virus. Proc Natl Acad Sci U S A. 1980 May;77(5):3009–3013. doi: 10.1073/pnas.77.5.3009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hayward W. S., Hanafusa H. Recombination between endogenous and exogenous RNA tumor virus genes as analyzed by nucleic acid hybridization. J Virol. 1975 Jun;15(6):1367–1377. doi: 10.1128/jvi.15.6.1367-1377.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hayward W. S. Size and genetic content of viral RNAs in avian oncovirus-infected cells. J Virol. 1977 Oct;24(1):47–63. doi: 10.1128/jvi.24.1.47-63.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Itohara S., Hirata K., Inoue M., Hatsuoka M., Sato A. Isolation of a sarcoma virus from a spontaneous chicken tumor. Gan. 1978 Dec;69(6):825–830. [PubMed] [Google Scholar]
  13. Karess R. E., Hayward W. S., Hanafusa H. Cellular information in the genome of recovered avian sarcoma virus directs the synthesis of transforming protein. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3154–3158. doi: 10.1073/pnas.76.7.3154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kawai S., Yoshida M., Segawa K., Sugiyama H., Ishizaki R., Toyoshima K. Characterization of Y73, an avian sarcoma virus: a unique transforming gene and its product, a phosphopolyprotein with protein kinase activity. Proc Natl Acad Sci U S A. 1980 Oct;77(10):6199–6203. doi: 10.1073/pnas.77.10.6199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Khan A. S., Deobagkar D. N., Stephenson J. R. Isolation and characterization of a feline sarcoma virus-coded precursor polyprotein. Competition immunoassay for nonstructural components. J Biol Chem. 1978 Dec 25;253(24):8894–8901. [PubMed] [Google Scholar]
  16. Lee W. H., Bister K., Pawson A., Robins T., Moscovici C., Duesberg P. H. Fujinami sarcoma virus: an avian RNA tumor virus with a unique transforming gene. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2018–2022. doi: 10.1073/pnas.77.4.2018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. McDonough S. K., Larsen S., Brodey R. S., Stock N. D., Hardy W. D., Jr A transmissible feline fibrosarcoma of viral origin. Cancer Res. 1971 Jul;31(7):953–956. [PubMed] [Google Scholar]
  18. Oppermann H., Levinson A. D., Varmus H. E., Levintow L., Bishop J. M. Uninfected vertebrate cells contain a protein that is closely related to the product of the avian sarcoma virus transforming gene (src). Proc Natl Acad Sci U S A. 1979 Apr;76(4):1804–1808. doi: 10.1073/pnas.76.4.1804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Purchio A. F., Erikson E., Brugge J. S., Erikson R. L. Identification of a polypeptide encoded by the avian sarcoma virus src gene. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1567–1571. doi: 10.1073/pnas.75.3.1567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Reynolds F. H., Jr, Sacks T. L., Deobagkar D. N., Stephenson J. R. Cells nonproductively transformed by Abelson murine leukemia virus express a high molecular weight polyprotein containing structural and nonstructural components. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3974–3978. doi: 10.1073/pnas.75.8.3974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Roussel M., Saule S., Lagrou C., Rommens C., Beug H., Graf T., Stehelin D. Three new types of viral oncogene of cellular origin specific for haematopoietic cell transformation. Nature. 1979 Oct 11;281(5731):452–455. doi: 10.1038/281452a0. [DOI] [PubMed] [Google Scholar]
  22. Sarma P. S., Sharar A. L., McDonough S. The SM strain of feline sarcoma virus. Biologic and antigenic characterization of virus. Proc Soc Exp Biol Med. 1972 Sep;140(4):1365–1368. doi: 10.3181/00379727-140-36675. [DOI] [PubMed] [Google Scholar]
  23. Sherr C. J., Fedele L. A., Oskarsson M., Maizel J., Vande Woude G. Molecular cloning of Snyder-Theilen feline leukemia and sarcoma viruses: comparative studies of feline sarcoma virus with its natural helper virus and with Moloney murine sarcoma virus. J Virol. 1980 Apr;34(1):200–212. doi: 10.1128/jvi.34.1.200-212.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Shih T. Y., Williams D. R., Weeks M. O., Maryak J. M., Vass W. C., Scolnick E. M. Comparison of the genomic organization of Kirsten and Harvey sarcoma viruses. J Virol. 1978 Jul;27(1):45–55. doi: 10.1128/jvi.27.1.45-55.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Shih T. Y., Williams D. R., Weeks M. O., Maryak J. M., Vass W. C., Scolnick E. M. Comparison of the genomic organization of Kirsten and Harvey sarcoma viruses. J Virol. 1978 Jul;27(1):45–55. doi: 10.1128/jvi.27.1.45-55.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Snyder S. P., Theilen G. H. Transmissible feline fibrosarcoma. Nature. 1969 Mar 15;221(5185):1074–1075. doi: 10.1038/2211074a0. [DOI] [PubMed] [Google Scholar]
  27. Spector D. H., Varmus H. E., Bishop J. M. Nucleotide sequences related to the transforming gene of avian sarcoma virus are present in DNA of uninfected vertebrates. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4102–4106. doi: 10.1073/pnas.75.9.4102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Stehelin D., Guntaka R. V., Varmus H. E., Bishop J. M. Purification of DNA complementary to nucleotide sequences required for neoplastic transformation of fibroblasts by avian sarcoma viruses. J Mol Biol. 1976 Mar 5;101(3):349–365. doi: 10.1016/0022-2836(76)90152-2. [DOI] [PubMed] [Google Scholar]
  29. Stehelin D., Varmus H. E., Bishop J. M., Vogt P. K. DNA related to the transforming gene(s) of avian sarcoma viruses is present in normal avian DNA. Nature. 1976 Mar 11;260(5547):170–173. doi: 10.1038/260170a0. [DOI] [PubMed] [Google Scholar]
  30. Taylor J. M., Illmensee R., Summers J. Efficeint transcription of RNA into DNA by avian sarcoma virus polymerase. Biochim Biophys Acta. 1976 Sep 6;442(3):324–330. doi: 10.1016/0005-2787(76)90307-5. [DOI] [PubMed] [Google Scholar]
  31. Ullman J. S., McCarthy B. J. The relationship between mismatched base pairs and the thermal stability of DNA duplexes. II. Effects of deamination of cytosine. Biochim Biophys Acta. 1973 Feb 4;294(1):416–424. doi: 10.1016/0005-2787(73)90096-8. [DOI] [PubMed] [Google Scholar]
  32. Van de Ven W. J., Khan A. S., Reynolds F. H., Jr, Mason K. T., Stephenson J. R. Translational products encoded by newly acquired sequences of independently derived feline sarcoma virus isolates are structurally related. J Virol. 1980 Mar;33(3):1034–1045. doi: 10.1128/jvi.33.3.1034-1045.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Van de Ven W. J., Reynolds F. H., Jr, Stephenson J. R. The nonstructural components of polyproteins encoded by replication-defective mammalian transforming retroviruses are phosphorylated and have associated protein kinase activity. Virology. 1980 Feb;101(1):185–197. doi: 10.1016/0042-6822(80)90495-x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES