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. 1979 Aug;31(2):398–407. doi: 10.1128/jvi.31.2.398-407.1979

RNA-directed DNA synthesis in Moloney murine leukemia virus: interaction between the primer tRNA and the genome RNA.

G Peters, J E Dahlberg
PMCID: PMC353462  PMID: 480476

Abstract

Initiation of RNA-directed DNA synthesis in virions of Moloney murine leukemia virus requires a cellular tRNAPro as primer. The site(s) on the Moloney murine leukemia virus genome RNA at which functional primer molecules are bound and at which purified tRNAPro hybridizes has been located near (within 20%) the 5' end of the genome. A relatively stable duplex (temperature at which 50% dissociation has occurred, 76 degrees C) is formed between the amino acid acceptor stem of the tRNAPro and a complementary sequence in the Moloney murine leukemia virus 35S RNA. The interaction involves 19 base pairs, extending from the penultimate nucleotide at the 3' end of the tRNAPro but apparently not including the 3'-terminal adenosine residue. In most respects, the interaction between primer and template in Moloney murine leukemia virus parallels the situation in the avian leukosis-sarcoma viruses.

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Selected References

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

  1. 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]
  2. Coffin J. M., Hageman T. C., Maxam A. M., Haseltine W. A. Structure of the genome of Moloney murine leukemia virus: a terminally redundant sequence. Cell. 1978 Apr;13(4):761–773. doi: 10.1016/0092-8674(78)90226-x. [DOI] [PubMed] [Google Scholar]
  3. Coffin J. M., Haseltine W. A. Nucleotide sequence of Rous sarcoma virus RNA at the initiation site of DNA synthesis: The 102nd nucleotide is U. J Mol Biol. 1977 Dec 15;117(3):805–814. doi: 10.1016/0022-2836(77)90071-7. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. Dahlberg A. E., Dingman C. W., Peacock A. C. Electrophoretic characterization of bacterial polyribosomes in agarose-acrylamide composite gels. J Mol Biol. 1969 Apr 14;41(1):139–147. doi: 10.1016/0022-2836(69)90131-4. [DOI] [PubMed] [Google Scholar]
  7. Dahlberg J. E., Kintner C., Lund E. Specific binding of tRNAMet to 23S rRNA of Escherichia coli. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1071–1075. doi: 10.1073/pnas.75.3.1071. [DOI] [PMC free article] [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., Nichols J. L. Characterization of poly(riboadenylic acid) segments in L-cell messenger ribonucleic acid. Biochemistry. 1973 Sep 25;12(20):3951–3956. doi: 10.1021/bi00744a026. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Fan H., Baltimore D. RNA metabolism of murine leukemia virus: detection of virus-specific RNA sequences in infected and uninfected cells and identification of virus-specific messenger RNA. J Mol Biol. 1973 Oct 15;80(1):93–117. doi: 10.1016/0022-2836(73)90235-0. [DOI] [PubMed] [Google Scholar]
  13. Fan H., Paskind M. Measurement of the sequence complexity of cloned Moloney murine leukemia virus 60 to 70S RNA: evidence for a haploid genome. J Virol. 1974 Sep;14(3):421–429. doi: 10.1128/jvi.14.3.421-429.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  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. Flügel R. M., Rapp U., Wells R. D. RNA-DNA covalent bonds between the RNA primers and the DNA products formed by RNA tumor virus DNA polymerase. J Virol. 1973 Dec;12(6):1491–1502. doi: 10.1128/jvi.12.6.1491-1502.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  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. 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]
  20. Haseltine W. A., Panet A., Smoler D., Baltimore D., Peters G., Harada F., Dahlberg J. E. Interaction of tryptophan tRNA and avian myeloblastosis virus reverse transcriptase: further characterization of the binding reaction. Biochemistry. 1977 Aug 9;16(16):3625–3632. doi: 10.1021/bi00635a019. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Peacock A. C., Dingman C. W. Molecular weight estimation and separation of ribonucleic acid by electrophoresis in agarose-acrylamide composite gels. Biochemistry. 1968 Feb;7(2):668–674. doi: 10.1021/bi00842a023. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. 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]
  27. Staskus K. A., Collett M. S., Faras A. J. Initiation of DNA synthesis by the avian oncornavirus RNA-directed DNA polymerase: structural and functional localization of the major species of primer RNA on the oncornavirus genome. Virology. 1976 May;71(1):162–168. doi: 10.1016/0042-6822(76)90102-1. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Taylor J. M., Illmensee R. Site on the RNA of an avian sarcoma virus at which primer is bound. J Virol. 1975 Sep;16(3):553–558. doi: 10.1128/jvi.16.3.553-558.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. Waters L. C. Transfer RNAs associated with the 70S RNA of AKR murine leukemia virus. Biochem Biophys Res Commun. 1975 Aug 4;65(3):1130–1136. doi: 10.1016/s0006-291x(75)80503-1. [DOI] [PubMed] [Google Scholar]

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