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. 1978 Oct;75(10):4754–4758. doi: 10.1073/pnas.75.10.4754

Polyoma virus giant RNAs contain tandem repeats of the nucleotide sequence of the entire viral genome.

N H Acheson
PMCID: PMC336198  PMID: 216998

Abstract

The bulk of late virus-specific RNA synthesized in polyoma virus-infected mouse cells is larger than a single strand of poloma DNA. The arrangement of viral nucleotide sequences in these giant polyoma RNAs was studied by electron microscopy of hybrids between purified high molecular weight viral RNA and the HindII-1 fragment of polyoma DNA, which contains 91% of the viral genome. Hybrid molecules containing a short single-stranded gap (corresponding to the 9% of viral sequences not present in HindII-1), flanked by double-stranded regions, were photographed and measured. The majority of hybrid molecules contained no single-stranded loops or branches, showing that all viral sequences are transcribed contiguously and that no nonviral sequences are present in the RNA. Hybrid molecules, containing RNA up to 3.5 times the genome length, had a repeating structure of single-stranded gaps 8% of genome length interspersed with double-stranded regions 89% of genome length, showing that giant polyoma RNAs contain tandem repeats of the nucleotide sequence of the entire viral DNA. A small proportion of hybrid molecules contained single-stranded branches or deletion loops in characteristic positions, indicating that RNA "splicing" may occur on high molecular weight nuclear polyoma RNA.

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Selected References

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  1. Acheson N. H., Buetti E., Scherrer K., Weil R. Transcription of the polyoma virus genome: synthesis and cleavage of giant late polyoma-specific RNA. Proc Natl Acad Sci U S A. 1971 Sep;68(9):2231–2235. doi: 10.1073/pnas.68.9.2231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Acheson N. H. Transcription during productive infection with polyoma virus and Simian virus 40. Cell. 1976 May;8(1):1–12. doi: 10.1016/0092-8674(76)90179-3. [DOI] [PubMed] [Google Scholar]
  3. Aloni Y., Dhar R., Laub O., Horowitz M., Khoury G. Novel mechanism for RNA maturation: the leader sequences of simian virus 40 mRNA are not transcribed adjacent to the coding sequences. Proc Natl Acad Sci U S A. 1977 Sep;74(9):3686–3690. doi: 10.1073/pnas.74.9.3686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beard P., Acheson N. H., Maxwell I. H. Strand-specific transcription of polyoma virus DNA-early in productive infection and in transformed cells. J Virol. 1975 Jan;17(1):20–26. doi: 10.1128/jvi.17.1.20-26.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Birg F., Favaloro J., Kamen R. Analysis of polyoma virus nuclear RNA by mini-blot hybridization. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3138–3142. doi: 10.1073/pnas.74.8.3138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Buetti E. Characterization of late polyoma mRNA. J Virol. 1974 Aug;14(2):249–260. doi: 10.1128/jvi.14.2.249-260.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Casey J., Davidson N. Rates of formation and thermal stabilities of RNA:DNA and DNA:DNA duplexes at high concentrations of formamide. Nucleic Acids Res. 1977;4(5):1539–1552. doi: 10.1093/nar/4.5.1539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Condit R. C., Cowie A., Kamen R., Birg F. Polyoma virus transcription in vitro. J Mol Biol. 1977 Sep 15;115(2):215–235. doi: 10.1016/0022-2836(77)90098-5. [DOI] [PubMed] [Google Scholar]
  9. Cuzin F., Vogt M., Dieckmann M., Berg P. Induction of virus multiplication in 3T3 cells transformed by a thermosensitive mutant of polyoma virus. II. Formation of oligometric polyoma DNA molecules. J Mol Biol. 1970 Feb 14;47(3):317–333. doi: 10.1016/0022-2836(70)90305-0. [DOI] [PubMed] [Google Scholar]
  10. Flavell A. J., Kamen R. Strand-specific transcription of polyoma virus DNA late during productive infection. J Mol Biol. 1977 Sep 15;115(2):237–242. doi: 10.1016/0022-2836(77)90099-7. [DOI] [PubMed] [Google Scholar]
  11. Folk W. R., Fishel B. R., Anderson D. M. Sites in the polyoma genome cleaved by restriction endonuclease HindII. Virology. 1975 Mar;64(1):277–280. doi: 10.1016/0042-6822(75)90100-2. [DOI] [PubMed] [Google Scholar]
  12. Fraser R. S., Loening U. E. Binding of radioactive homopolynucleotides to RNA. A simple method for the detection, during gel electrophoresis or sedimentation, of messenger RNAs which contain poly(A) sequences. Eur J Biochem. 1973 Apr 2;34(1):153–158. doi: 10.1111/j.1432-1033.1973.tb02741.x. [DOI] [PubMed] [Google Scholar]
  13. Gariglio P., Mousset S. Isolation and partial characterization of a nuclear RNA polymerase - SV40 DNA complex. FEBS Lett. 1975 Aug 1;56(1):149–155. doi: 10.1016/0014-5793(75)80130-x. [DOI] [PubMed] [Google Scholar]
  14. Green M. H., Brooks T. L. Isolation of two forms of SV40 nucleoprotein containing RNA polymerase from infected monkey cells. Virology. 1976 Jul 1;72(1):110–120. doi: 10.1016/0042-6822(76)90316-0. [DOI] [PubMed] [Google Scholar]
  15. Griffin B. E. Fine structure of polyoma virus DNA. J Mol Biol. 1977 Dec 5;117(2):447–471. doi: 10.1016/0022-2836(77)90137-1. [DOI] [PubMed] [Google Scholar]
  16. Hsu M. T., Ford J. Sequence arrangement of the 5' ends of simian virus 40 16S and 19S mRNAs. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4982–4985. doi: 10.1073/pnas.74.11.4982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jaenisch R., Levine A. DNA replication in SV40-infected cells. V. Circular and catenated oligomers of SV40 DNA. Virology. 1971 Jun;44(3):480–493. doi: 10.1016/0042-6822(71)90361-8. [DOI] [PubMed] [Google Scholar]
  18. KIRBY K. S. ISOLATION AND CHARACTERIZATION OF RIBOSOMAL RIBONUCLEIC ACID. Biochem J. 1965 Jul;96:266–269. doi: 10.1042/bj0960266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kamen R., Lindstrom D. M., Shure H., Old R. W. Virus-specific RNA in cells productively infected or transformed by polyoma virus. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 1):187–198. doi: 10.1101/sqb.1974.039.01.025. [DOI] [PubMed] [Google Scholar]
  20. Kamen R., Shure H. Topography of polyoma virus messenger RNA molecules. Cell. 1976 Mar;7(3):361–371. doi: 10.1016/0092-8674(76)90165-3. [DOI] [PubMed] [Google Scholar]
  21. Lavi S., Groner Y. 5'-Terminal sequences and coding region of late simian virus 40 mRNAs are derived from noncontiguous segments of the viral genome. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5323–5327. doi: 10.1073/pnas.74.12.5323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lev Z., Manor H. Amount and distribution of virus-specific sequences in giant RNA molecules isolated from polyoma-infected mouse kidney cells. J Virol. 1977 Mar;21(3):831–842. doi: 10.1128/jvi.21.3.831-842.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McConaughy B. L., Laird C. D., McCarthy B. J. Nucleic acid reassociation in formamide. Biochemistry. 1969 Aug;8(8):3289–3295. doi: 10.1021/bi00836a024. [DOI] [PubMed] [Google Scholar]
  24. Rosenthal L. J., Salomon C., Weil R. Isolation and characterization of poly(A)-containing intranuclear polyoma-specific "giant" RNA'S. Nucleic Acids Res. 1976 May;3(5):1167–1183. doi: 10.1093/nar/3.5.1167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Strauss J. H., Jr, Kelly R. B., Sinsheimer R. L. Denaturation of RNA with dimethyl sulfoxide. Biopolymers. 1968 Jun;6(6):793–807. doi: 10.1002/bip.1968.360060604. [DOI] [PubMed] [Google Scholar]
  26. Türler H., Salomon C., Allet B., Weil R. Mapping of the three species of polyoma mRNA. Proc Natl Acad Sci U S A. 1976 May;73(5):1480–1484. doi: 10.1073/pnas.73.5.1480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Weinberg R. A., Warnaar S. O., Winocour E. Isolation and characterization of simian virus 40 ribonucleic acid. J Virol. 1972 Aug;10(2):193–201. doi: 10.1128/jvi.10.2.193-201.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wellauer P. K., Dawid I. B. The structural organization of ribosomal DNA in Drosophila melanogaster. Cell. 1977 Feb;10(2):193–212. doi: 10.1016/0092-8674(77)90214-8. [DOI] [PubMed] [Google Scholar]

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