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. 1979 Mar;29(3):863–871. doi: 10.1128/jvi.29.3.863-871.1979

Comparison of the small RNAs of polymerase-deficient and polymerase-positive Rous sarcoma virus and another species of avian retrovirus.

R C Sawyer, H Hanafusa
PMCID: PMC353245  PMID: 87521

Abstract

The small RNAs contained in virions of avian leukosis and sarcoma viruses are a virus-specific subset of the total small RNA population of the host cell. The reverse transcriptase protein must be present in the budding virion for this selection to take place. Virions of the alpha form of the Bryan strain of Rous sarcoma virus, which lack detectable reverse transcriptase, incorporated an unselected population of small RNAs identical to total chicken cell small RNA. Virions of reticuloendotheliosis virus, which contain a reverse transcriptase unrelated to that of the avian leukosis and sarcoma viruses, contained a distinctly different population of small RNAs although both the avian leukosis and sarcoma and the reticuloendotheliosis viruses were grown in chicken cells. Because the primer for avian leukosis and sarcoma virus RNA-dependent DNA synthesis is a host cell tRNA, the differences in reverse transcriptase small RNA selection may help explain the failure of different species of retrovirus to complement for the reverse transcriptase.

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Selected References

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

  1. 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]
  2. Bishop J. M., Levinson W. E., Sullivan D., Fanshier L., Quintrell N., Jackson J. The low molecular weight RNAs of Rous sarcoma virus. II. The 7 S RNA. Virology. 1970 Dec;42(4):927–937. doi: 10.1016/0042-6822(70)90341-7. [DOI] [PubMed] [Google Scholar]
  3. Bonar R. A., Sverak L., Bolognesi D. P., Langlois A. J., Beard D., Beard J. W. Ribonucleic acid components of BAI strain A (myeloblastosis) avian tumor virus. Cancer Res. 1967 Jun;27(6):1138–1157. [PubMed] [Google Scholar]
  4. Canaani E., Helm K. V., Duesberg P. Evidence for 30-40S RNA as precursor of the 60-70S RNA of Rous sarcoma virus. Proc Natl Acad Sci U S A. 1973 Feb;70(2):401–405. doi: 10.1073/pnas.70.2.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cheung K. S., Smith R. E., Stone M. P., Joklik W. K. Comparison of immature (rapid harvest) and mature Rous sarcoma virus particles. Virology. 1972 Dec;50(3):851–864. doi: 10.1016/0042-6822(72)90439-4. [DOI] [PubMed] [Google Scholar]
  6. Dahlberg J. E., Sawyer R. C., Taylor J. M., Faras A. J., Levinson W. E., Goodman H. M., Bishop J. M. Transcription of DNA from the 70S RNA of Rous sarcoma virus. I. Identification of a specific 4S RNA which serves as primer. J Virol. 1974 May;13(5):1126–1133. doi: 10.1128/jvi.13.5.1126-1133.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davis N. L., Rueckert R. R. Properties of a ribonucleoprotein particle isolated from Nonidet P-40-treated Rous sarcoma virus. J Virol. 1972 Nov;10(5):1010–1020. doi: 10.1128/jvi.10.5.1010-1020.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Erikson E., Erikson R. L. Association of 4S ribonucleic acid with oncornavirus ribonucleic acids. J Virol. 1971 Aug;8(2):254–256. doi: 10.1128/jvi.8.2.254-256.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Erikson E., Erikson R. L., Henry B., Pace N. R. Comparison of oligonucleotides produced by RNase T1 digestion of 7 S RNA from avian and murine oncornaviruses and from uninfected cells. Virology. 1973 May;53(1):40–46. doi: 10.1016/0042-6822(73)90463-7. [DOI] [PubMed] [Google Scholar]
  11. Erikson E., Erikson R. L. Isolation of amino acid acceptor RNA from purified avian myeloblastosis virus. J Mol Biol. 1970 Sep 14;52(2):387–390. doi: 10.1016/0022-2836(70)90038-0. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Faras A. J., Dahlberg J. E., Sawyer R. C., Harada F., Taylor J. M., Levinson W. E., Bishop J. M., Goodman H. M. Transcription of DNA from the 70S RNA of Rous sarcoma virus. II. Structure of a 4S RNA primer. J Virol. 1974 May;13(5):1134–1142. doi: 10.1128/jvi.13.5.1134-1142.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Faras A. J., Garapin A. C., Levinson W. E., Bishop J. M., Goodman H. M. Characterization of the low-molecular-weight RNAs associated with the 70S RNA of Rous sarcoma virus. J Virol. 1973 Aug;12(2):334–342. doi: 10.1128/jvi.12.2.334-342.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Faras A. J., Taylor J. M., Levinson W. E., Goodman H. M., Bishop J. M. RNA-directed DNA polymerase of Rous sarcoma virus: initiation of synthesis with 70 S viral RNA as template. J Mol Biol. 1973 Sep 5;79(1):163–183. doi: 10.1016/0022-2836(73)90277-5. [DOI] [PubMed] [Google Scholar]
  16. Halpern M. S., Wade E., Rucker E., Baxter-Gabbard K. L., Levine A. S., Friis R. R. A study of the relationship of reticuloendotheliosis virus to the avian leukosis-sarcoma complex of viruses. Virology. 1973 Jun;53(2):287–299. doi: 10.1016/0042-6822(73)90206-7. [DOI] [PubMed] [Google Scholar]
  17. Hanafusa H., Hanafusa T. Further studies on RSV production form transformed cells. Virology. 1968 Apr;34(4):630–636. doi: 10.1016/0042-6822(68)90084-6. [DOI] [PubMed] [Google Scholar]
  18. Hanafusa H., Hanafusa T. Noninfectious RSV deficient in DNA polymerase. Virology. 1971 Jan;43(1):313–316. doi: 10.1016/0042-6822(71)90251-0. [DOI] [PubMed] [Google Scholar]
  19. Hanafusa T., Hanafusa H., Miyamoto T., Fleissner E. Existence and expression of tumor virus genes in chick embryo cells. Virology. 1972 Feb;47(2):475–482. doi: 10.1016/0042-6822(72)90283-8. [DOI] [PubMed] [Google Scholar]
  20. Hanafusa T., Miyamoto T., Hanafusa H. A type of chick embryo cell that fails to support formation of infectious RSV. Virology. 1970 Jan;40(1):55–64. doi: 10.1016/0042-6822(70)90378-8. [DOI] [PubMed] [Google Scholar]
  21. Harada F., Sawyer R. C., Dahlberg J. E. A primer ribonucleic acid for initiation of in vitro Rous sarcarcoma virus deoxyribonucleic acid synthesis. J Biol Chem. 1975 May 10;250(9):3487–3497. [PubMed] [Google Scholar]
  22. Haseltine W. A., Maxam A. M., Gilbert W. Rous sarcoma virus genome is terminally redundant: the 5' sequence. Proc Natl Acad Sci U S A. 1977 Mar;74(3):989–993. doi: 10.1073/pnas.74.3.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ikemura T., Dahlberg J. E. Small ribonucleic acids of Escherichia coli. I. Characterization by polyacrylamide gel electrophoresis and fingerprint analysis. J Biol Chem. 1973 Jul 25;248(14):5024–5032. [PubMed] [Google Scholar]
  24. Kang C. Y., Temin H. M. Lack of sequence homology among RNAs of avian leukosis-sarcoma viruses, reticuloendotheliosis viruses, and chicken endogenous RNA-directed DNA polymerase activity. J Virol. 1973 Dec;12(6):1314–1324. doi: 10.1128/jvi.12.6.1314-1324.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kawai S., Hanafusa H. Plaque assay for some strains of avian leukosis virus. Virology. 1972 Apr;48(1):126–135. doi: 10.1016/0042-6822(72)90120-1. [DOI] [PubMed] [Google Scholar]
  26. Maldonado R. L., Bose H. R. Relationship of reticuloendotheliosis virus to the avian tumor viruses: nucleic acid and polypeptide composition. J Virol. 1973 May;11(5):741–747. doi: 10.1128/jvi.11.5.741-747.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mizutani A., Temin H. M. Purification and properties of spleen necrosis virus DNA polymerase. J Virol. 1975 Oct;16(4):797–806. doi: 10.1128/jvi.16.4.797-806.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mizutani S., Temin H. M. Lack of serological relationship among DNA polymerases of avian leukosis-sarcoma viruses, reticuloendotheliosis viruses, and chicken cells. J Virol. 1973 Sep;12(3):440–448. doi: 10.1128/jvi.12.3.440-448.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Obara T., Bolognesi D. P., Bauer H. Ribosomal RNA in avian leukosis virus particles. Int J Cancer. 1971 May 15;7(3):535–546. doi: 10.1002/ijc.2910070320. [DOI] [PubMed] [Google Scholar]
  30. Panet A., Berliner H. Binding of tRNA to reverse transcriptase of RNA tumor viruses. J Virol. 1978 May;26(2):214–220. doi: 10.1128/jvi.26.2.214-220.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Panet A., Haseltine W. A., Baltimore D., Peters G., Harada F., Dahlberg J. E. Specific binding of tryptophan transfer RNA to avian myeloblastosis virus RNA-dependent DNA polymerase (reverse transcriptase). Proc Natl Acad Sci U S A. 1975 Jul;72(7):2535–2539. doi: 10.1073/pnas.72.7.2535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Peters G., Harada F., Dahlberg J. E., Panet A., Haseltine W. A., Baltimore D. Low-molecular-weight RNAs of Moloney murine leukemia virus: identification of the primer for RNA-directed DNA synthesis. J Virol. 1977 Mar;21(3):1031–1041. doi: 10.1128/jvi.21.3.1031-1041.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Randerath K., Rosenthal L. J., Zamecnik P. C. Base composition differences between avian myeloblastosis virus transfer RNA and transfer RNA isolated from host cells. Proc Natl Acad Sci U S A. 1971 Dec;68(12):3233–3237. doi: 10.1073/pnas.68.12.3233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Robinson W. S., Pitkanen A., Rubin H. The nucleic acid of the Bryan strain of Rous sarcoma virus: purification of the virus and isolation of the nucleic acid. Proc Natl Acad Sci U S A. 1965 Jul;54(1):137–144. doi: 10.1073/pnas.54.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rosenthal L. J., Zamecnik P. C. Amino-acid acceptor activity of the "70S-associated" 4S RNA from avian myeloblastosis virus. Proc Natl Acad Sci U S A. 1973 Apr;70(4):1184–1185. doi: 10.1073/pnas.70.4.1184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sawyer R. C., Dahlberg J. E. Small RNAs of Rous sarcoma virus: characterization by two-dimensional polyacrylamide gel electrophoresis and fingerprint analysis. J Virol. 1973 Dec;12(6):1226–1237. doi: 10.1128/jvi.12.6.1226-1237.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sawyer R. C., Hanafusa H. Formation of reticuloendotheliosis virus pseudotypes of Rous sarcoma virus. J Virol. 1977 Jun;22(3):634–639. doi: 10.1128/jvi.22.3.634-639.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sawyer R. C., Harada F., Dahlberg J. E. Virion-associated RNA primer for Rous sarcoma virus DNA synthesis: isolation from uninfected cells. J Virol. 1974 Jun;13(6):1302–1311. doi: 10.1128/jvi.13.6.1302-1311.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Trávnícek M. RNA with amino acid-acceptor activity isolated from an oncogenic virus. Biochim Biophys Acta. 1968 Oct 29;166(3):757–759. [PubMed] [Google Scholar]
  40. Trávnícek M. Some properties of amino acid-acceptor RNA isolated from avian tumour virus BAI strain A (avian myeloblastosis). Biochim Biophys Acta. 1969 Jun 17;182(2):427–439. [PubMed] [Google Scholar]
  41. Vogt P. K., Spencer J. L., Okazaki W., Witter R. L., Crittenden L. B. Phenotypic mixing between reticuloendotheliosis virus and avian sarcoma viruses. Virology. 1977 Jul 1;80(1):127–135. doi: 10.1016/0042-6822(77)90385-3. [DOI] [PubMed] [Google Scholar]
  42. Wang S., Kothari R. M., Taylor M., Hung P. Transfer RNA activities of Rous sarcoma and Rous associated viruses. Nat New Biol. 1973 Apr 4;242(118):133–135. doi: 10.1038/newbio242133a0. [DOI] [PubMed] [Google Scholar]

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