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. 1986 Sep;59(3):564–573. doi: 10.1128/jvi.59.3.564-573.1986

A precise map of splice junctions in the mRNAs of minute virus of mice, an autonomous parvovirus.

C V Jongeneel, R Sahli, G K McMaster, B Hirt
PMCID: PMC253209  PMID: 2942705

Abstract

We have determined the exact splicing patterns of the mRNAs of the minute virus of mice by a combination of cDNA sequencing and S1 nuclease protection analysis. There are four virus-specific mRNA species, each coding for one of the four polypeptides identified by in vitro translation. The R1 mRNA comprises sequences from nucleotide approximately 200 to 2281 and from 2378 to approximately 4800 and codes for the NS1 protein. The R2 mRNA is derived from nucleotides approximately 200 to 515, 1991 to 2281, and 2378 to approximately 4800 and codes for the NS2 protein. Between nucleotides 1991 and 2281, the coding sequence for NS2 overlaps that of NS1, but in a different reading frame. R3 covers nucleotides approximately 2007 to 2281 and 2378 to approximately 4800 and codes for VP2. The fourth species, R3', differs from R3 by using an alternative splice donor and acceptor in the region around 47 map units (nucleotide 2400); it extends from nucleotide approximately 2007 to 2317 and from 2400 to approximately 4800 and almost certainly codes for VP1. The R2 transcript is unusual in that the intron that was removed from it (nucleotides 516 to 1990) starts with GC rather than the canonical GU. With the exception of the splice acceptor at position 2378, which is found only in rodent parvoviruses, the splice junctions are highly conserved among autonomous parvoviruses. These results show that minute virus of mice, like other small DNA viruses, uses multiple strategies to compress the coding information for several viral proteins into a short (5,104 nucleotide) genome.

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Selected References

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

  1. Astell C. R., Gardiner E. M., Tattersall P. DNA sequence of the lymphotropic variant of minute virus of mice, MVM(i), and comparison with the DNA sequence of the fibrotropic prototype strain. J Virol. 1986 Feb;57(2):656–669. doi: 10.1128/jvi.57.2.656-669.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Astell C. R., Thomson M., Merchlinsky M., Ward D. C. The complete DNA sequence of minute virus of mice, an autonomous parvovirus. Nucleic Acids Res. 1983 Feb 25;11(4):999–1018. doi: 10.1093/nar/11.4.999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barnes W. M., Bevan M., Son P. H. Kilo-sequencing: creation of an ordered nest of asymmetric deletions across a large target sequence carried on phage M13. Methods Enzymol. 1983;101:98–122. doi: 10.1016/0076-6879(83)01008-3. [DOI] [PubMed] [Google Scholar]
  4. Ben-Asher E., Aloni Y. Transcription of minute virus of mice, an autonomous parvovirus, may be regulated by attenuation. J Virol. 1984 Oct;52(1):266–276. doi: 10.1128/jvi.52.1.266-276.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  6. Burke J. F. High-sensitivity S1 mapping with single-stranded [32P]DNA probes synthesized from bacteriophage M13mp templates. Gene. 1984 Oct;30(1-3):63–68. doi: 10.1016/0378-1119(84)90105-7. [DOI] [PubMed] [Google Scholar]
  7. Carlson J., Rushlow K., Maxwell I., Maxwell F., Winston S., Hahn W. Cloning and sequence of DNA encoding structural proteins of the autonomous parvovirus feline panleukopenia virus. J Virol. 1985 Sep;55(3):574–582. doi: 10.1128/jvi.55.3.574-582.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cotmore S. F., Sturzenbecker L. J., Tattersall P. The autonomous parvovirus MVM encodes two nonstructural proteins in addition to its capsid polypeptides. Virology. 1983 Sep;129(2):333–343. doi: 10.1016/0042-6822(83)90172-1. [DOI] [PubMed] [Google Scholar]
  9. Cotmore S. F., Tattersall P. Organization of nonstructural genes of the autonomous parvovirus minute virus of mice. J Virol. 1986 Jun;58(3):724–732. doi: 10.1128/jvi.58.3.724-732.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Erbil C., Niessing J. The primary structure of the duck alpha D-globin gene: an unusual 5' splice junction sequence. EMBO J. 1983;2(8):1339–1343. doi: 10.1002/j.1460-2075.1983.tb01589.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fischer H. D., Dodgson J. B., Hughes S., Engel J. D. An unusual 5' splice sequence is efficiently utilized in vivo. Proc Natl Acad Sci U S A. 1984 May;81(9):2733–2737. doi: 10.1073/pnas.81.9.2733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Green M. R., Lebovitz R. M., Roeder R. G. Expression of the autonomous parvovirus H1 genome: evidence for a single transcriptional unit and multiple spliced polyadenylated transcripts. Cell. 1979 Aug;17(4):967–977. doi: 10.1016/0092-8674(79)90336-2. [DOI] [PubMed] [Google Scholar]
  13. McMaster G. K., Beard P., Engers H. D., Hirt B. Characterization of an immunosuppressive parvovirus related to the minute virus of mice. J Virol. 1981 Apr;38(1):317–326. doi: 10.1128/jvi.38.1.317-326.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nielsen P. J., McMaster G. K., Trachsel H. Cloning of eukaryotic protein synthesis initiation factor genes: isolation and characterization of cDNA clones encoding factor eIF-4A. Nucleic Acids Res. 1985 Oct 11;13(19):6867–6880. doi: 10.1093/nar/13.19.6867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Paradiso P. R. Identification of multiple forms of the noncapsid parvovirus protein NCVP1 in H-1 parvovirus-infected cells. J Virol. 1984 Oct;52(1):82–87. doi: 10.1128/jvi.52.1.82-87.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Paradiso P. R., Williams K. R., Costantino R. L. Mapping of the amino terminus of the H-1 parvovirus major capsid protein. J Virol. 1984 Oct;52(1):77–81. doi: 10.1128/jvi.52.1.77-81.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Pintel D., Dadachanji D., Astell C. R., Ward D. C. The genome of minute virus of mice, an autonomous parvovirus, encodes two overlapping transcription units. Nucleic Acids Res. 1983 Feb 25;11(4):1019–1038. doi: 10.1093/nar/11.4.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pintel D., Merchlinsky M. J., Ward D. C. Expression of minute virus of mice structural proteins in murine cell lines transformed by bovine papillomavirus-minute virus of mice plasmid chimera. J Virol. 1984 Nov;52(2):320–327. doi: 10.1128/jvi.52.2.320-327.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pustell J., Kafatos F. C. A convenient and adaptable package of computer programs for DNA and protein sequence management, analysis and homology determination. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):643–655. doi: 10.1093/nar/12.1part2.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rhode S. L., 3rd Nucleotide sequence of the coat protein gene of canine parvovirus. J Virol. 1985 May;54(2):630–633. doi: 10.1128/jvi.54.2.630-633.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rhode S. L., 3rd, Paradiso P. R. Parvovirus genome: nucleotide sequence of H-1 and mapping of its genes by hybrid-arrested translation. J Virol. 1983 Jan;45(1):173–184. doi: 10.1128/jvi.45.1.173-184.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rhode S. L., 3rd trans-Activation of parvovirus P38 promoter by the 76K noncapsid protein. J Virol. 1985 Sep;55(3):886–889. doi: 10.1128/jvi.55.3.886-889.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ruskin B., Krainer A. R., Maniatis T., Green M. R. Excision of an intact intron as a novel lariat structure during pre-mRNA splicing in vitro. Cell. 1984 Aug;38(1):317–331. doi: 10.1016/0092-8674(84)90553-1. [DOI] [PubMed] [Google Scholar]
  24. Sahli R., McMaster G. K., Hirt B. DNA sequence comparison between two tissue-specific variants of the autonomous parvovirus, minute virus of mice. Nucleic Acids Res. 1985 May 24;13(10):3617–3633. doi: 10.1093/nar/13.10.3617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Siegl G., Bates R. C., Berns K. I., Carter B. J., Kelly D. C., Kurstak E., Tattersall P. Characteristics and taxonomy of Parvoviridae. Intervirology. 1985;23(2):61–73. doi: 10.1159/000149587. [DOI] [PubMed] [Google Scholar]
  27. Staden R. Computer methods to locate signals in nucleic acid sequences. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):505–519. doi: 10.1093/nar/12.1part2.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tattersall P., Bratton J. Reciprocal productive and restrictive virus-cell interactions of immunosuppressive and prototype strains of minute virus of mice. J Virol. 1983 Jun;46(3):944–955. doi: 10.1128/jvi.46.3.944-955.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tattersall P., Shatkin A. J., Ward D. C. Sequence homology between the structural polypeptides of minute virus of mice. J Mol Biol. 1977 Apr 25;111(4):375–394. doi: 10.1016/s0022-2836(77)80060-0. [DOI] [PubMed] [Google Scholar]

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