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. 1972 Jun;9(6):891–902. doi: 10.1128/jvi.9.6.891-902.1972

Virus-Specific Ribonucleic Acid in Cells Producing Rous Sarcoma Virus: Detection and Characterization

Jo-Ann Leong 1, Axel-Claude Garapin 1, Nola Jackson 1, Lois Fanshier 1, Warren Levinson 1, J Michael Bishop 1
PMCID: PMC356393  PMID: 4338637

Abstract

Cells producing Rous sarcoma virus contain virus-specific ribonucleic acid (RNA) which can be identified by hybridization to single-stranded deoxyribonucleic acid (DNA) synthesized with RNA-directed DNA polymerase. Hybridization was detected by either fractionation on hydroxyapatite or hydrolysis with single strand-specific nucleases. Similar results were obtained with both procedures. The hybrids formed between enzymatically synthesized DNA and viral RNA have a high order of thermal stability, with only minor evidence of mismatched nucleotide sequences. Virus-specific RNA is present in both nuclei and cytoplasm of infected cells. This RNA is remarkably heterogeneous in size, including molecules which are probably restricted to the nucleus and which sediment in their native state more rapidly than the viral genome. The nature of the RNA found in cytoplasmic fractions varies from preparation to preparation, but heterogeneous RNA (ca. 4-50S), smaller than the viral genome, is always present in substantial amounts.

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Selected References

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

  1. Ando T. A nuclease specific for heat-denatured DNA in isolated from a product of Aspergillus oryzae. Biochim Biophys Acta. 1966 Jan 18;114(1):158–168. doi: 10.1016/0005-2787(66)90263-2. [DOI] [PubMed] [Google Scholar]
  2. BADER J. P. THE ROLE OF DEOXYRIBONUCLEIC ACID IN THE SYNTHESIS OF ROUS SARCOMA VIRUS. Virology. 1964 Apr;22:462–468. doi: 10.1016/0042-6822(64)90067-4. [DOI] [PubMed] [Google Scholar]
  3. Baltimore D. RNA-dependent DNA polymerase in virions of RNA tumour viruses. Nature. 1970 Jun 27;226(5252):1209–1211. doi: 10.1038/2261209a0. [DOI] [PubMed] [Google Scholar]
  4. Birnstiel M. L., Sells B. H., Purdom I. F. Kinetic complexity of RNA molecules. J Mol Biol. 1972 Jan 14;63(1):21–39. doi: 10.1016/0022-2836(72)90519-0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Bishop J. O. The effect of genetic complexity on the time-course of ribonucleic acid-deoxyribonucleic acid hybridization. Biochem J. 1969 Aug;113(5):805–811. doi: 10.1042/bj1130805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Britten R. J., Kohne D. E. Repeated sequences in DNA. Hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms. Science. 1968 Aug 9;161(3841):529–540. doi: 10.1126/science.161.3841.529. [DOI] [PubMed] [Google Scholar]
  8. Burton A., Sinsheimer R. L. The process of infection with bacteriophage phi-X174 VII. Ultracentrifugal analysis of the replicative form. J Mol Biol. 1965 Dec;14(2):327–347. doi: 10.1016/s0022-2836(65)80185-1. [DOI] [PubMed] [Google Scholar]
  9. Duesberg P. H. Physical properties of Rous Sarcoma Virus RNA. Proc Natl Acad Sci U S A. 1968 Aug;60(4):1511–1518. doi: 10.1073/pnas.60.4.1511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Erikson R. L. Studies on the RNA from avian myeloblastosis virus. Virology. 1969 Jan;37(1):124–131. doi: 10.1016/0042-6822(69)90313-4. [DOI] [PubMed] [Google Scholar]
  11. Fanshier L., Garapin A. C., McDonnell J., Faras A., Levinson W., Bishop J. M. Deoxyribonucleic acid polymerase associated with avian tumor viruses: secondary structure of the deoxyribonucleic acid product. J Virol. 1971 Jan;7(1):77–86. doi: 10.1128/jvi.7.1.77-86.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Faras A., Fanshier L., Garapin A. C., Levinson W., Bishop J. M. Deoxyribonucleic acid polymerase of Rous sarcoma virus: studies on the mechanism of double-stranded deoxyribonucleic acid synthesis. J Virol. 1971 May;7(5):539–548. doi: 10.1128/jvi.7.5.539-548.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Garapin A. C., Fanshier L., Leong J. A., Jackson J., Levinson W., Bishop J. M. Deoxyribonucleic acid polymerases of Rous sarcoma virus: kinetics of deoxyribonucleic acid synthesis and specificity of the products. J Virol. 1971 Feb;7(2):227–232. doi: 10.1128/jvi.7.2.227-232.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Garapin A. C., Leong J., Fanshier L., Levinson W. E., Bishop J. M. Identification of virus-specific RNA in cells infected with Rous sarcoma virus. Biochem Biophys Res Commun. 1971 Mar 5;42(5):919–925. doi: 10.1016/0006-291x(71)90518-3. [DOI] [PubMed] [Google Scholar]
  15. Garapin A. C., McDonnell J. P., Levinson W., Quintrell N., Fanshier L., Bishop J. M. Deoxyribonucleic acid polymerase associated with Rous sarcoma virus and avian myeloblastosis virus: properties of the enzyme and its product. J Virol. 1970 Nov;6(5):589–598. doi: 10.1128/jvi.6.5.589-598.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Green M., Rokutanda H., Rokutanda M. Virus specific RNA in cells transformed by RNA tumour viruses. Nat New Biol. 1971 Apr 21;230(16):229–232. doi: 10.1038/newbio230229a0. [DOI] [PubMed] [Google Scholar]
  17. Jaenisch R. Evidence for SV40 specific RNA containing virus and host specific sequences. Nat New Biol. 1972 Jan 12;235(54):46–47. doi: 10.1038/newbio235046a0. [DOI] [PubMed] [Google Scholar]
  18. Kohne D. E. Isolation and characterization of bacterial ribosomal RNA cistrons. Biophys J. 1968 Oct;8(10):1104–1118. doi: 10.1016/S0006-3495(68)86542-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Manly K. F., Smoler D. F., Bromfeld E., Baltimore D. Forms of deoxyribonucleic acid produced by virions of the ribonucleic acid tumor viruses. J Virol. 1971 Jan;7(1):106–111. doi: 10.1128/jvi.7.1.106-111.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Payne L. N., Chubb R. C. Studies on the nature and genetic control of an antigen in normal chick embryos which reacts in the COFAL test. J Gen Virol. 1968 Dec;3(3):379–391. doi: 10.1099/0022-1317-3-3-379. [DOI] [PubMed] [Google Scholar]
  21. Penman S. RNA metabolism in the HeLa cell nucleus. J Mol Biol. 1966 May;17(1):117–130. doi: 10.1016/s0022-2836(66)80098-0. [DOI] [PubMed] [Google Scholar]
  22. Rabin E. Z., Preiss B., Fraser M. J. A nuclease from Neurospora crassa conidia specific for single-stranded nucleic acids. Prep Biochem. 1971;1(4):283–307. doi: 10.1080/00327487108081946. [DOI] [PubMed] [Google Scholar]
  23. Rokutanda M., Rokutanda H., Green M., Fujinaga K., Ray R. K., Gurgo C. Formation of viral RNA-DNA hybrid molecules by the DNA polymerase of sarcoma-leukaemia viruses. Nature. 1970 Sep 5;227(5262):1026–1028. doi: 10.1038/2271026a0. [DOI] [PubMed] [Google Scholar]
  24. Spiegelman S., Burny A., Das M. R., Keydar J., Schlom J., Travnicek M., Watson K. Characterization of the products of DNA-directed DNA polymerases in oncogenic RNA viruses. Nature. 1970 Aug 8;227(5258):563–567. doi: 10.1038/227563a0. [DOI] [PubMed] [Google Scholar]
  25. Sutton W. D. A crude nuclease preparation suitable for use in DNA reassociation experiments. Biochim Biophys Acta. 1971 Jul 29;240(4):522–531. doi: 10.1016/0005-2787(71)90709-x. [DOI] [PubMed] [Google Scholar]
  26. TEMIN H. M. THE EFFECTS OF ACTINOMYCIN D ON GROWTH OF ROUS SARCOMA VIRUS IN VITRO. Virology. 1963 Aug;20:577–582. doi: 10.1016/0042-6822(63)90282-4. [DOI] [PubMed] [Google Scholar]
  27. Temin H. M. Mechanism of cell transformation by RNA tumor viruses. Annu Rev Microbiol. 1971;25:609–648. doi: 10.1146/annurev.mi.25.100171.003141. [DOI] [PubMed] [Google Scholar]
  28. Temin H. M., Mizutani S. RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature. 1970 Jun 27;226(5252):1211–1213. doi: 10.1038/2261211a0. [DOI] [PubMed] [Google Scholar]
  29. Verma I. M., Temple G. F., Fan H., Baltimore D. In vitro synthesis of DNA complementary to rabbit reticulocyte 10S RNA. Nat New Biol. 1972 Feb 9;235(58):163–167. doi: 10.1038/newbio235163a0. [DOI] [PubMed] [Google Scholar]
  30. Vogt P. K., Friis R. R. An avian leukosis virus related to RSV(O): properties and evidence for helper activity. Virology. 1971 Jan;43(1):223–234. doi: 10.1016/0042-6822(71)90240-6. [DOI] [PubMed] [Google Scholar]
  31. Wall R., Darnell J. E. Presence of cell and virus specific sequences in the same molecules of nuclear RNA from virus transformed cells. Nat New Biol. 1971 Jul 21;232(29):73–76. doi: 10.1038/newbio232073a0. [DOI] [PubMed] [Google Scholar]
  32. Zimmerman S. B., Sandeen D. The ribonuclease activity of crystallized pancreatic deoxyribonuclease. Anal Biochem. 1966 Feb;14(2):269–277. doi: 10.1016/0003-2697(66)90137-0. [DOI] [PubMed] [Google Scholar]

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