Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1980 Jul;35(1):31–40. doi: 10.1128/jvi.35.1.31-40.1980

tRNA's and priming of RNA-directed DNA synthesis in mouse mammary tumor virus.

G Peters, C Glover
PMCID: PMC288780  PMID: 6157839

Abstract

The low-molecular-weight RNAs of mouse mammary tumor virus (MuMTV) were examined by two-dimensional acrylamide gel electrophoresis. Unlike other retroviruses, MuMTV was found to contain only two major fractions of tRNA. These have been fully characterized and shown to correspond to the published sequences for tRNA1+2Lys and tRNA3Lys. By determining which of these tRNA's was most tightly associated with the MuMTV genome and which of them acquired label from [alpha-32P]deoxynucleoside triphosphates in limited DNA synthesis reactions, we identified tRNA3Lys as the primer for MuMTV reverse transcription in vitro. tRNA3Lys does not share any unusual sequence feature with the other previously characterized retrovirus primers, tRNATrp and tRNAPro.

Full text

PDF
31

Images in this article

33Image
on p.33
34Image
on p.34
35Image
on p.35
37Image
on p.37

Selected References

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

  1. Aaronson S. A., Stephenson J. R. Endogenous type-C RNA viruses of mammalian cells. Biochim Biophys Acta. 1976 Dec 23;458(4):323–354. doi: 10.1016/0304-419x(76)90006-8. [DOI] [PubMed] [Google Scholar]
  2. BERNHARD W. Electron microscopy of tumor cells and tumor viruses; a review. Cancer Res. 1958 Jun;18(5):491–509. [PubMed] [Google Scholar]
  3. Bentvelzen P. Host-virus interactions in murine mammary carcinogenesis. Biochim Biophys Acta. 1974 Dec 31;355(3-4):236–259. doi: 10.1016/0304-419x(74)90012-2. [DOI] [PubMed] [Google Scholar]
  4. Canaani E., Duesberg P. Role of subunits of 60 to 70S avian tumor virus ribonucleic acid in its template activity for the viral deoxyribonucleic acid polymerase. J Virol. 1972 Jul;10(1):23–31. doi: 10.1128/jvi.10.1.23-31.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cohen J. C., Varmus H. E. Endogenous mammary tumour virus DNA varies among wild mice and segregates during inbreeding. Nature. 1979 Mar 29;278(5703):418–423. doi: 10.1038/278418a0. [DOI] [PubMed] [Google Scholar]
  6. Cordell B., Stavnezer E., Friedrich R., Bishop J. M., Goodman H. M. Nucleotide sequence that binds primer for DNA synthesis to the avian sarcoma virus genome. J Virol. 1976 Aug;19(2):548–558. doi: 10.1128/jvi.19.2.548-558.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cordell B., Swanstrom R., Goodman H. M., Bishop J. M. tRNATrp as primer for RNA-directed DNA polymerase: structural determinants of function. J Biol Chem. 1979 Mar 25;254(6):1866–1874. [PubMed] [Google Scholar]
  8. 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]
  9. Eiden J. J., Bolognesi D. P., Langlois A. J., Nichols J. L. The initial nucleotide sequence of DNA transcribed from avian myeloblastosis virus 70 S RNA by RNA-dependent DNA polymerase. Virology. 1975 May;65(1):163–172. doi: 10.1016/0042-6822(75)90016-1. [DOI] [PubMed] [Google Scholar]
  10. Eiden J. J., Quade K., Nichols J. L. Interaction of tryptophan transfer RNA with Rous sarcoma virus 35S RNA. Nature. 1976 Jan 22;259(5540):245–247. doi: 10.1038/259245a0. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. 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]
  14. 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]
  15. Harada F., Peters G. G., Dahlberg J. E. The primer tRNA for Moloney murine leukemia virus DNA synthesis. Nucleotide sequence and aminoacylation of tRNAPro. J Biol Chem. 1979 Nov 10;254(21):10979–10985. [PubMed] [Google Scholar]
  16. 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]
  17. Haseltine W. A., Kleid D. G. A method for classification of 5' termini of retroviruses. Nature. 1978 Jun 1;273(5661):358–364. doi: 10.1038/273358a0. [DOI] [PubMed] [Google Scholar]
  18. Haseltine W. A., Kleid D. G., Panet A., Rothenberg E., Baltimore D. Ordered transcription of RNA tumor virus genomes. J Mol Biol. 1976 Sep 5;106(1):109–131. doi: 10.1016/0022-2836(76)90303-x. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Kleiman L., Woodward-Jack J., Cedergren R. J., Dion R. Alterations in lysine transfer RNA during erythroid differentiation of the Friend cell. Nucleic Acids Res. 1978 Mar;5(3):851–859. doi: 10.1093/nar/5.3.851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lovinger G. G., Schochetman G. 5'-terminal nucleotide sequences of the Rauscher leukemia virus and gibbon ape leukemia virus genomes exhibit a high degree of correspondence. J Virol. 1979 Dec;32(3):803–811. doi: 10.1128/jvi.32.3.803-811.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ortwerth B. J., Liu L. P. Correlation between a specific isoaccepting lysyl transfer ribonucleic acid and cell division in mammalian tissues. Biochemistry. 1973 Sep 25;12(20):3978–3984. doi: 10.1021/bi00744a030. [DOI] [PubMed] [Google Scholar]
  23. Peters G. G., Glover C. Low-molecular-weight RNAs and initiation of RNA-directed DNA synthesis in avian reticuloendotheliosis virus. J Virol. 1980 Feb;33(2):708–716. doi: 10.1128/jvi.33.2.708-716.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Peters G., Dahlberg J. E. RNA-directed DNA synthesis in Moloney murine leukemia virus: interaction between the primer tRNA and the genome RNA. J Virol. 1979 Aug;31(2):398–407. doi: 10.1128/jvi.31.2.398-407.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Raba M., Limburg K., Burghagen M., Katze J. R., Simsek M., Heckman J. E., Rajbhandary U. L., Gross H. J. Nucleotide sequence of three isoaccepting lysine tRNAs from rabbit liver and SV40-transformed mouse fibroblasts. Eur J Biochem. 1979 Jun;97(1):305–318. doi: 10.1111/j.1432-1033.1979.tb13115.x. [DOI] [PubMed] [Google Scholar]
  27. Ringold G., Lasfargues E. Y., Bishop J. M., Varmus H. E. Production of mouse mammary tumor virus by cultured cells in the absence and presence of hormones: assay by molecular hybridization. Virology. 1975 May;65(1):135–147. doi: 10.1016/0042-6822(75)90014-8. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Sanger F., Brownlee G. G., Barrell B. G. A two-dimensional fractionation procedure for radioactive nucleotides. J Mol Biol. 1965 Sep;13(2):373–398. doi: 10.1016/s0022-2836(65)80104-8. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Taylor J. M. An analysis of the role of tRNA species as primers for the transcription into DNA of RNA tumor virus genomes. Biochim Biophys Acta. 1977 Mar 21;473(1):57–71. doi: 10.1016/0304-419x(77)90007-5. [DOI] [PubMed] [Google Scholar]
  32. Taylor J. M., Cordell-Stewart B., Rohde W., Goodman H. M., Bishop J. M. Reassociation of 4 S and 5 S RNA's with the genome of avian sarcoma virus. Virology. 1975 May;65(1):248–259. doi: 10.1016/0042-6822(75)90025-2. [DOI] [PubMed] [Google Scholar]
  33. Taylor J. M., Garfin D. E., Levinson W. E., Bishop J. M., Goodman H. M. Tumor virus ribonucleic acid directed deoxyribonucleic acid synthesis: nucleotide sequence at the 5' terminus of nascent deoxyribonucleic acid. Biochemistry. 1974 Jul 16;13(15):3159–3163. doi: 10.1021/bi00712a024. [DOI] [PubMed] [Google Scholar]
  34. Temin H. M., Baltimore D. RNA-directed DNA synthesis and RNA tumor viruses. Adv Virus Res. 1972;17:129–186. doi: 10.1016/s0065-3527(08)60749-6. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Verma I. M., Meuth N. L., Baltimore D. Covalent linkage between ribonucleic Acid primer and deoxyribonucleic Acid product of the avian myeloblastosis virus deoxyribonucleic Acid polymerase. J Virol. 1972 Oct;10(4):622–627. doi: 10.1128/jvi.10.4.622-627.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Waters L. C. Lysine tRNA is the predominant tRNA in murine mammary tumor virus. Biochem Biophys Res Commun. 1978 Apr 14;81(3):822–827. doi: 10.1016/0006-291x(78)91425-0. [DOI] [PubMed] [Google Scholar]
  38. Waters L. C., Mullin B. C. Transfer RNA into RNA tumor viruses. Prog Nucleic Acid Res Mol Biol. 1977;20:131–160. doi: 10.1016/s0079-6603(08)60471-7. [DOI] [PubMed] [Google Scholar]
  39. Závada J., Dickson C., Weiss R. Pseudotypes of vesicular stomatitis virus with envelope antigens provided by murine mammary tumor virus. Virology. 1977 Oct 1;82(1):221–231. doi: 10.1016/0042-6822(77)90045-9. [DOI] [PubMed] [Google Scholar]

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

RESOURCES