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. 1980 Jul;35(1):52–64. doi: 10.1128/jvi.35.1.52-64.1980

Evidence for the common origin of viral and cellular sequences involved in sarcomagenic transformation.

L H Wang, P Snyder, T Hanafusa, H Hanafusa
PMCID: PMC288782  PMID: 6251277

Abstract

The src genes of six different strains of avian sarcoma virus (ASV) were compared with those of a series of newly isolated sarcoma viruses, termed "recovery avian sarcoma viruses" (rASV's). The rASV's were isolated recently from chicken and quail tumors induced by transformation-defective (td) deletion mutants of Schmidt-Ruppin Rous sarcoma virus. The RNase T1-resistant oligonucleotide maps were constructed for the RNA genomes of different strains of ASV and td mutants. The src-specific sequences, characterized by RNase T1-resistant oligonucleotides ranging from 9 to 19 nucleotides long, were defined as those mapping between approximately 600 and 2,800 nucleotides from the 3' polyadenylate end of individual sarcoma viral RNAs, and missing in the corresponding td viral RNAs. Our results revealed that 12 src-specific oligonucleotides were highly conserved among several strains of ASV, including the rASV's, whereas certain strains of ASV were found to contain one to three characteristic src-specific oligonucleotides. We previously presented evidence supporting the idea that most of the src-specific sequences present in rASV RNAs are derived from cellular genetic information. Our present data indicate that the src genes of rASV's are closely related to other known ASVs. We conclude that the src genes of different strains of ASV and the cellular sarc sequences are of common origin, although some divergence has occurred among different viral src genes and related cellular sequences.

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Selected References

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

  1. Altaner C., Temin H. M. Carcinogenesis by RNA sarcoma viruses. XII. A quantitative study of infection of rat cells in vitro by avian sarcoma viruses. Virology. 1970 Jan;40(1):118–134. doi: 10.1016/0042-6822(70)90384-3. [DOI] [PubMed] [Google Scholar]
  2. Beemon K., Hunter T., Sefton B. M. Polymorphism of avian sarcoma virus src proteins. J Virol. 1979 Apr;30(1):190–200. doi: 10.1128/jvi.30.1.190-200.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brugge J. S., Collett M. S., Siddiqui A., Marczynska B., Deinhardt F., Erikson R. L. Detection of the viral sarcoma gene product in cells infected with various strains of avian sarcoma virus and of a related protein in uninfected chicken cells. J Virol. 1979 Mar;29(3):1196–1203. doi: 10.1128/jvi.29.3.1196-1203.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brugge J. S., Erikson R. L. Identification of a transformation-specific antigen induced by an avian sarcoma virus. Nature. 1977 Sep 22;269(5626):346–348. doi: 10.1038/269346a0. [DOI] [PubMed] [Google Scholar]
  5. Coffin J. M., Billeter M. A. A physical map of the Rous sarcoma virus genome. J Mol Biol. 1976 Jan 25;100(3):293–318. doi: 10.1016/s0022-2836(76)80065-4. [DOI] [PubMed] [Google Scholar]
  6. Collett M. S., Brugge J. S., Erikson R. L. Characterization of a normal avian cell protein related to the avian sarcoma virus transforming gene product. Cell. 1978 Dec;15(4):1363–1369. doi: 10.1016/0092-8674(78)90061-2. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. Duesberg P. H., Kawai S., Wang L. H., Vogt P. K., Murphy H. M., Hanafusa H. RNA of replication-defective strains of Rous sarcoma virus. Proc Natl Acad Sci U S A. 1975 Apr;72(4):1569–1573. doi: 10.1073/pnas.72.4.1569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Erikson E., Collett M. S., Erikson R. L. In vitro synthesis of a functional avian sarcoma virus transforming-gene product. Nature. 1978 Aug 31;274(5674):919–921. doi: 10.1038/274919a0. [DOI] [PubMed] [Google Scholar]
  11. Estis L. F., Temin H. M. Suppression of multiplication of avian sarcoma virus by rapid spread of transformation-defective virus of the same subgroup. J Virol. 1979 Aug;31(2):389–397. doi: 10.1128/jvi.31.2.389-397.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Frankel A. E., Fischinger P. J. Nucleotide sequences in mouse DNA and RNA specific for Moloney sarcoma virus. Proc Natl Acad Sci U S A. 1976 Oct;73(10):3705–3709. doi: 10.1073/pnas.73.10.3705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. HANAFUSA H., HANAFUSA T., RUBIN H. The defectiveness of Rous sarcoma virus. Proc Natl Acad Sci U S A. 1963 Apr;49:572–580. doi: 10.1073/pnas.49.4.572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Halpern C. C., Hayward W. S., Hanafusa H. Characterization of some isolates of newly recovered avian sarcoma virus. J Virol. 1979 Jan;29(1):91–101. doi: 10.1128/jvi.29.1.91-101.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Hayward W. S., Hanafusa H. Independent regulation of endogenous and exogenous avian RNA tumor virus genes. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2259–2263. doi: 10.1073/pnas.73.7.2259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Huebner R. J., Todaro G. J. Oncogenes of RNA tumor viruses as determinants of cancer. Proc Natl Acad Sci U S A. 1969 Nov;64(3):1087–1094. doi: 10.1073/pnas.64.3.1087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Joho R. H., Billeter M. A., Weissmann C. Mapping of biological functions on RNA of avian tumor viruses: location of regions required for transformation and determination of host range. Proc Natl Acad Sci U S A. 1975 Dec;72(12):4772–4776. doi: 10.1073/pnas.72.12.4772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Junghans R. P., Hu S., Knight C. A., Davidson N. Heteroduplex analysis of avian RNA tumor viruses. Proc Natl Acad Sci U S A. 1977 Feb;74(2):477–481. doi: 10.1073/pnas.74.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Kawai S., Duesberg P. H., Hanafusa H. Transformation-defective mutants of Rous sarcoma virus with src gene deletions of varying length. J Virol. 1977 Dec;24(3):910–914. doi: 10.1128/jvi.24.3.910-914.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kawai S., Hanafusa H. Genetic recombination with avian tumor virus. Virology. 1972 Jul;49(1):37–44. doi: 10.1016/s0042-6822(72)80005-9. [DOI] [PubMed] [Google Scholar]
  24. Lai M. M., Duesberg P. H., Horst J., Vogt P. K. Avian tumor virus RNA: a comparison of three sarcoma viruses and their transformation-defective derivatives by oligonucleotide fingerprinting and DNA-RNA hybridization. Proc Natl Acad Sci U S A. 1973 Aug;70(8):2266–2270. doi: 10.1073/pnas.70.8.2266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lai M. M., Hu S. S., Vogt P. K. Occurrence of partial deletion and substitution of the src gene in the RNA genome of avian sarcoma virus. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4781–4785. doi: 10.1073/pnas.74.11.4781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Levinson A. D., Oppermann H., Levintow L., Varmus H. E., Bishop J. M. Evidence that the transforming gene of avian sarcoma virus encodes a protein kinase associated with a phosphoprotein. Cell. 1978 Oct;15(2):561–572. doi: 10.1016/0092-8674(78)90024-7. [DOI] [PubMed] [Google Scholar]
  27. Murphy H. M. A new replication-defective variant of the Bryan high-titer strain Rous sarcoma virus. Virology. 1977 Apr;77(2):705–721. doi: 10.1016/0042-6822(77)90493-7. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. PRINCE A. M. Quantitative studies on Rous sarcoma virus. V. An analysis of the mechanism of virulence of the Bryan "high titer" strain of RSV. Virology. 1960 Jun;11:371–399. doi: 10.1016/0042-6822(60)90082-9. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Robins T., Duesberg P. Specific RNA sequences of Rous sarcoma virus (RSV) recovered from tumors induced by transformation-defective RSV deletion mutants. Virology. 1979 Mar;93(2):427–434. doi: 10.1016/0042-6822(79)90246-0. [DOI] [PubMed] [Google Scholar]
  32. Rohrschneider L. R., Eisenman R. N., Leitch C. R. Identification of a Rous sarcoma virus transformation-related protein in normal avian and mammalian cells. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4479–4483. doi: 10.1073/pnas.76.9.4479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rübsamen H., Friis R. R., Bauer H. Src Gene product from different strains of avian sarcoma virus: Kinetics and possible mechanism of heat inactivation of protein kinase activity from cells infected by transformation-defective, temperature-sensitive mutant and wild-type virus. Proc Natl Acad Sci U S A. 1979 Feb;76(2):967–971. doi: 10.1073/pnas.76.2.967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Scheele C. M., Hanafusa H. Electrophoretic analysis of the RNA of avian tumor viruses. Virology. 1972 Dec;50(3):753–764. doi: 10.1016/0042-6822(72)90429-1. [DOI] [PubMed] [Google Scholar]
  35. Scolnick E. M., Rands E., Williams D., Parks W. P. Studies on the nucleic acid sequences of Kirsten sarcoma virus: a model for formation of a mammalian RNA-containing sarcoma virus. J Virol. 1973 Sep;12(3):458–463. doi: 10.1128/jvi.12.3.458-463.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sefton B. M., Hunter T., Beemon K. Product of in vitro translation of the Rous sarcoma virus src gene has protein kinase activity. J Virol. 1979 Apr;30(1):311–318. doi: 10.1128/jvi.30.1.311-318.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Spector D. H., Smith K., Padgett T., McCombe P., Roulland-Dussoix D., Moscovici C., Varmus H. E., Bishop J. M. Uninfected avian cells contain RNA related to the transforming gene of avian sarcoma viruses. Cell. 1978 Feb;13(2):371–379. doi: 10.1016/0092-8674(78)90205-2. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Tal J., Fujita D. J., Kawai S., Varmus H. E., Bishop J. M. Purification of DNA complementary to the env gene of avian sarcoma virus and analysis of relationships among the env genes of avian leukosis-sarcoma viruses. J Virol. 1977 Feb;21(2):497–505. doi: 10.1128/jvi.21.2.497-505.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Temin H. M. The RNA tumor viruses--background and foreground. Proc Natl Acad Sci U S A. 1972 Apr;69(4):1016–1020. doi: 10.1073/pnas.69.4.1016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Todaro G. J., Huebner R. J. N.A.S. symposium: new evidence as the basis for increased efforts in cancer research. Proc Natl Acad Sci U S A. 1972 Apr;69(4):1009–1015. doi: 10.1073/pnas.69.4.1009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Vigne R., Breitman M. L., Moscovici C., Vogt P. K. Restitution of fibroblast-transforming ability in src deletion mutants of avian sarcoma virus during animal passage. Virology. 1979 Mar;93(2):413–426. doi: 10.1016/0042-6822(79)90245-9. [DOI] [PubMed] [Google Scholar]
  43. Wang L. H., Duesberg P. H., Kawai S., Hanafusa H. Location of envelope-specific and sarcoma-specific oligonucleotides on RNA of Schmidt-Ruppin Rous sarcoma virus. Proc Natl Acad Sci U S A. 1976 Feb;73(2):447–451. doi: 10.1073/pnas.73.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wang L. H., Duesberg P. H., Robins T., Yokota H., Vogt P. K. The terminal oligonucleotides of avian tumor virus RNAs are genetically linked. Virology. 1977 Oct 15;82(2):472–492. doi: 10.1016/0042-6822(77)90020-4. [DOI] [PubMed] [Google Scholar]
  45. Wang L. H., Duesberg P., Beemon K., Vogt P. K. Mapping RNase T1-resistant oligonucleotides of avian tumor virus RNAs: sarcoma-specific oligonucleotides are near the poly(A) end and oligonucleotides common to sarcoma and transformation-defective viruses are at the poly(A) end. J Virol. 1975 Oct;16(4):1051–1070. doi: 10.1128/jvi.16.4.1051-1070.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wang L. H., Duesberg P., Mellon P., Vogt P. K. Distribution of envelope-specific and sarcoma-specific nucleotide sequences from different parents in the RNAs of avian tumor virus recombinants. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1073–1077. doi: 10.1073/pnas.73.4.1073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wang L. H., Duesberg P. Properties and location of poly(A) in Rous sarcoma virus RNA. J Virol. 1974 Dec;14(6):1515–1529. doi: 10.1128/jvi.14.6.1515-1529.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wang L. H., Halpern C. C., Nadel M., Hanafusa H. Recombination between viral and cellular sequences generates transforming sarcoma virus. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5812–5816. doi: 10.1073/pnas.75.12.5812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wang L. H., Moscovici C., Karess R. E., Hanafusa H. Analysis of the src gene of sarcoma viruses generated by recombination between transformation-defective mutants and quail cellular sequences. J Virol. 1979 Nov;32(2):546–556. doi: 10.1128/jvi.32.2.546-556.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Wang L. H., Snyder P., Hanafusa T., Moscovici C., Hanafusa H. Comparative analysis of cellular and viral sequences related to sarcomagenic cell transformation. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 2):755–764. doi: 10.1101/sqb.1980.044.01.081. [DOI] [PubMed] [Google Scholar]
  51. Wang L. H. The gene order of avian RNA tumor viruses derived from biochemical analyses of deletion mutants and viral recombinants. Annu Rev Microbiol. 1978;32:561–592. doi: 10.1146/annurev.mi.32.100178.003021. [DOI] [PubMed] [Google Scholar]
  52. Wang L., Galehouse D., Mellon P., Duesberg P., Mason W. S., Vogt P. K. Mapping oligonucleotides of Rous sarcoma virus RNA that segregate with polymerase and group-specific antigen markers in recombinants. Proc Natl Acad Sci U S A. 1976 Nov;73(11):3952–3956. doi: 10.1073/pnas.73.11.3952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Wang S. Y., Hayward W. S., Hanafusa H. Genetic variation in the RNA transcripts of endogenous virus genes in uninfected chicken cells. J Virol. 1977 Oct;24(1):64–73. doi: 10.1128/jvi.24.1.64-73.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]

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