Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1979 Feb;29(2):507–516. doi: 10.1128/jvi.29.2.507-516.1979

Nature of Rous Sarcoma Virus-Specific RNA in Transformed and Revertant Field Vole Cells

Richard A Krzyzek 1, Alan F Lau 1, Anthony J Faras 1
PMCID: PMC353183  PMID: 219246

Abstract

Cytoplasmic and polyribosomal RNAs from Rous sarcoma virus-transformed and phenotypically reverted field vole cells were fractionated by rate-zonal sedimentation and hybridized with a 3H-labeled complementary DNA viral probe to determine the size classes of virus-specific RNA present in these cell types. In contrast to Rous sarcoma virus-infected permissive avian cells, only two of three discrete species of virus-specific RNA were detected in the cytoplasm of these vole cells. These included genome-length 35S RNA and a 21S RNA. However, viral 28S RNA, routinely detected in the cytoplasm of productively infected avian cells, could not be found in cytoplasmic RNA from vole cells. In addition, a low-molecular-weight viral RNA sedimenting less than 16S was detected in both infected avian and vole cells. Because of its heterogeneity this latter species is most likely generated from the intracellular degradation of the larger viral RNAs. Both the viral 35S and 21S RNA were also found to be associated with total polyribosomes from these vole cells. Studies were also performed to determine the distribution of both total viral genomic and sarcoma-specific RNA sequences among the size classes of fractionated total polyribosomes. In both vole cell types the majority of cytoplasmic viral RNA sequences were also associated with polyribosomes and were similarly distributed among the size classes of total polyribosomes. Sarcoma-specific sequences were present on both the 35S and 21S RNA species. These data suggest that the expression of the viral transforming gene in revertant field vole cells may be controlled at some stage subsequent to translation of the viral RNA.

Full text

PDF
514

Selected References

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

  1. Bernstein A., MacCormick R., Martin G. S. Transformation-defective mutants of avian sarcoma viruses: the genetic relationship between conditional and nonconditional mutants. Virology. 1976 Mar;70(1):206–209. doi: 10.1016/0042-6822(76)90254-3. [DOI] [PubMed] [Google Scholar]
  2. Bishop J. M., Levinson W. E., Quintrell N., Sullivan D., Fanshier L., Jackson J. The low molecular weight RNAs of Rous sarcoma virus. I. The 4 S RNA. Virology. 1970 Sep;42(1):182–195. doi: 10.1016/0042-6822(70)90251-5. [DOI] [PubMed] [Google Scholar]
  3. Boettiger D. Reversion and induction of Rous sarcoma virus expression in virus-transformed baby hamster kidney cells. Virology. 1974 Dec;62(2):522–529. doi: 10.1016/0042-6822(74)90412-7. [DOI] [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. Deng C. T., Boettiger D., Macpherson I., Varmus H. E. The persistence and expression of virus-specific DNA in revertants of Rous sarcoma virus-transformed BHK-21 cells. Virology. 1974 Dec;62(2):512–521. doi: 10.1016/0042-6822(74)90411-5. [DOI] [PubMed] [Google Scholar]
  6. Deng C. T., Stehelin D., Bishop J. M., Varmus H. E. Characteristics of virus-specific RNA in avian sarcoma virus-transformed BHK-21 cells and revertants. Virology. 1977 Jan;76(1):313–330. doi: 10.1016/0042-6822(77)90305-1. [DOI] [PubMed] [Google Scholar]
  7. Eisenman R., Vogt V. M., Diggelmann H. Synthesis of avian RNA tumor virus structural proteins. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):1067–1075. doi: 10.1101/sqb.1974.039.01.122. [DOI] [PubMed] [Google Scholar]
  8. Faras A. J., Dibble N. A. RNA-directed DNA synthesis by the DNA polymerase of Rous sarcoma virus: structural and functional identification of 4S primer RNA in uninfected cells. Proc Natl Acad Sci U S A. 1975 Mar;72(3):859–863. doi: 10.1073/pnas.72.3.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Faras A. J., Taylor J. M., McDonnell J. P., Levinson W. E., Bishop J. M. Purification and characterization of the deoxyribonucleic acid polymerase associated with Rous sarcoma virus. Biochemistry. 1972 Jun 6;11(12):2334–2342. doi: 10.1021/bi00762a020. [DOI] [PubMed] [Google Scholar]
  10. Gielkens A. L., Salden M. H., Bloemendal H. Virus-specific messenger RNA on free and membrane-bound polyribosomes from cells infected with Rauscher leukemia virus. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1093–1097. doi: 10.1073/pnas.71.4.1093. [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. Kawai S., Hanafusa H. The effects of reciprocal changes in temperature on the transformed state of cells infected with a rous sarcoma virus mutant. Virology. 1971 Nov;46(2):470–479. doi: 10.1016/0042-6822(71)90047-x. [DOI] [PubMed] [Google Scholar]
  13. Kieras R. M., Faras A. J. DNA polymerase of reticuloendotheliosis virus: inability to detect endogenous RNA-directed DNA synthesis. Virology. 1975 Jun;65(2):514–523. doi: 10.1016/0042-6822(75)90056-2. [DOI] [PubMed] [Google Scholar]
  14. Krzyzek R. A., Collett M. S., Lau A. F., Perdue M. L., Leis J. P., Faras A. J. Evidence for splicing of avian sarcoma virus 5'-terminal genomic sequences into viral-specific RNA in infected cells. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1284–1288. doi: 10.1073/pnas.75.3.1284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Krzyzek R. A., Lau A. F., Faras A. J., Spector D. H. Post-transcriptional control of avian oncornavirus transforming gene sequences in mammalian cells. Nature. 1977 Sep 8;269(5624):175–179. doi: 10.1038/269175a0. [DOI] [PubMed] [Google Scholar]
  16. Krzyzek R. A., Lau A. F., Vogt P. K., Faras A. J. Quantitation and localization of Rous sarcoma virus-specific RNA in transformed and revertant field vole cells. J Virol. 1978 Feb;25(2):518–526. doi: 10.1128/jvi.25.2.518-526.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Leong J. A., Garapin A. C., Jackson N., Fanshier L., Levinson W., Bishop J. M. Virus-specific ribonucleic acid in cells producing rous sarcoma virus: detection and characterization. J Virol. 1972 Jun;9(6):891–902. doi: 10.1128/jvi.9.6.891-902.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Martin G. S. Rous sarcoma virus: a function required for the maintenance of the transformed state. Nature. 1970 Sep 5;227(5262):1021–1023. doi: 10.1038/2271021a0. [DOI] [PubMed] [Google Scholar]
  19. McKnight G. S., Schimke R. T. Ovalbumin messenger RNA: evidence that the initial product of transcription is the same size as polysomal ovalbumin messenger. Proc Natl Acad Sci U S A. 1974 Nov;71(11):4327–4331. doi: 10.1073/pnas.71.11.4327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Oppermann H., Bishop J. M., Varmus H. E., Levintow L. A joint produce of the genes gag and pol of avian sarcoma virus: a possible precursor of reverse transcriptase. Cell. 1977 Dec;12(4):993–1005. doi: 10.1016/0092-8674(77)90164-7. [DOI] [PubMed] [Google Scholar]
  21. Paterson B. M., Marciani D. J., Papas T. S. Cell-free synthesis of the precursor polypeptide for avian myeloblastosis virus DNA polymerase. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4951–4954. doi: 10.1073/pnas.74.11.4951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pawson T., Martin G. S., Smith A. E. Cell-free translation of virion RNA from nondefective and transformation-defective Rous sarcoma viruses. J Virol. 1976 Sep;19(3):950–967. doi: 10.1128/jvi.19.3.950-967.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Purchio A. F., Erikson E., Erikson R. L. Translation of 35S and of subgenomic regions of avian sarcoma virus RNA. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4661–4665. doi: 10.1073/pnas.74.10.4661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Reynolds F. H., Jr, Hanson C. A., Aaronson S. A., Stephenson J. R. Type C viral gag gene expression in chicken embryo fibroblasts and avian sarcoma virus-transformed mammalian cells. J Virol. 1977 Jul;23(1):74–79. doi: 10.1128/jvi.23.1.74-79.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schincariol A. L., Joklik W. K. Early synthesis of virus-specific RNA and DNA in cells rapidly transformed with Rous sarcoma virus. Virology. 1973 Dec;56(2):532–548. doi: 10.1016/0042-6822(73)90056-1. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Weiss S. R., Varmus H. E., Bishop J. M. The size and genetic composition of virus-specific RNAs in the cytoplasm of cells producing avian sarcoma-leukosis viruses. Cell. 1977 Dec;12(4):983–992. doi: 10.1016/0092-8674(77)90163-5. [DOI] [PubMed] [Google Scholar]
  28. Wyke J. A., Bell J. G., Beamand J. A. Genetic recombination among temperature-sensitive mutnats of Rous sarcoma virus. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):897–905. doi: 10.1101/sqb.1974.039.01.104. [DOI] [PubMed] [Google Scholar]
  29. de la Maza L. M., Faras A., Varmus H., Vogt P. K., Yunis J. J. Integration of avian sarcoma virus specific DNA in mammalian chromatin. Exp Cell Res. 1975 Jul;93(2):484–486. doi: 10.1016/0014-4827(75)90477-2. [DOI] [PubMed] [Google Scholar]

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

RESOURCES