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. 1991 Sep;65(9):4741–4748. doi: 10.1128/jvi.65.9.4741-4748.1991

Host-derived 5' ends and overlapping complementary 3' ends of the two mRNAs transcribed from the ambisense S segment of Uukuniemi virus.

J F Simons 1, R F Pettersson 1
PMCID: PMC248931  PMID: 1831239

Abstract

Two mRNAs, coding for the N and NSS proteins, are transcribed from the small (S) Uukuniemi virus RNA segment by an ambisense strategy (J. F. Simons, U. Hellman, and R. F. Pettersson, J. Virol. 64:247-255, 1990). In this report, we describe the analysis of the 5' and 3' ends of the two mRNAs. Primer extension as well as cloning and sequencing of individual mRNAs showed that the 5' ends of both mRNAs contained nonviral sequences ranging from 7 to 25 residues in length (mean, 12 residues), indicating a cap-snatching mechanism similar to the one originally described for priming of influenza virus mRNA synthesis. In 35% of the cases, the first virion-specified nucleotide (an A residue) was substituted with a G residue. Between the translation termination codons of N and NSS, there is a 74-residue-long noncoding intergenic region (Simons et al., J. Virol. 64:247-255, 1990). Nuclease protection assays using both RNA and DNA hybridization probes showed that the 3' ends of the N and NSS mRNAs overlap each other by about 100 nucleotides. The 3' end of the NSS mRNA extends into the coding sequence of the N mRNA, whereas the N mRNA is terminated just prior to the stop codon of NSS. To our knowledge, this is the first example of overlapping complementary mRNAs in viruses with an ambisense coding strategy. No obvious transcription termination sequence was identified. However, because of a short palindromic sequence in the intergenic region, the 3' ends of both mRNAs (and consequently also the template RNAs) can be folded into an A/U-rich hairpin structure. It remains to be determined whether this structure plays any role in transcription termination.

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Selected References

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  1. Auperin D. D., Romanowski V., Galinski M., Bishop D. H. Sequencing studies of pichinde arenavirus S RNA indicate a novel coding strategy, an ambisense viral S RNA. J Virol. 1984 Dec;52(3):897–904. doi: 10.1128/jvi.52.3.897-904.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Auperin D. D., Sasso D. R., McCormick J. B. Nucleotide sequence of the glycoprotein gene and intergenic region of the Lassa virus S genome RNA. Virology. 1986 Oct 15;154(1):155–167. doi: 10.1016/0042-6822(86)90438-1. [DOI] [PubMed] [Google Scholar]
  3. Bishop D. H., Gay M. E., Matsuoko Y. Nonviral heterogeneous sequences are present at the 5' ends of one species of snowshoe hare bunyavirus S complementary RNA. Nucleic Acids Res. 1983 Sep 24;11(18):6409–6418. doi: 10.1093/nar/11.18.6409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bouloy M., Pardigon N., Vialat P., Gerbaud S., Girard M. Characterization of the 5' and 3' ends of viral messenger RNAs isolated from BHK21 cells infected with Germiston virus (Bunyavirus). Virology. 1990 Mar;175(1):50–58. doi: 10.1016/0042-6822(90)90185-t. [DOI] [PubMed] [Google Scholar]
  5. Bucher P., Trifonov E. N. Compilation and analysis of eukaryotic POL II promoter sequences. Nucleic Acids Res. 1986 Dec 22;14(24):10009–10026. doi: 10.1093/nar/14.24.10009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Collett M. S. Messenger RNA of the M segment RNA of Rift Valley fever virus. Virology. 1986 May;151(1):151–156. doi: 10.1016/0042-6822(86)90114-5. [DOI] [PubMed] [Google Scholar]
  7. Elliott R. M. Molecular biology of the Bunyaviridae. J Gen Virol. 1990 Mar;71(Pt 3):501–522. doi: 10.1099/0022-1317-71-3-501. [DOI] [PubMed] [Google Scholar]
  8. Fazakerley J. K., Gonzalez-Scarano F., Strickler J., Dietzschold B., Karush F., Nathanson N. Organization of the middle RNA segment of snowshoe hare Bunyavirus. Virology. 1988 Dec;167(2):422–432. [PubMed] [Google Scholar]
  9. Fuller F., Bhown A. S., Bishop D. H. Bunyavirus nucleoprotein, N, and a non-structural protein, NSS, are coded by overlapping reading frames in the S RNA. J Gen Virol. 1983 Aug;64(Pt 8):1705–1714. doi: 10.1099/0022-1317-64-8-1705. [DOI] [PubMed] [Google Scholar]
  10. Garcin D., Kolakofsky D. A novel mechanism for the initiation of Tacaribe arenavirus genome replication. J Virol. 1990 Dec;64(12):6196–6203. doi: 10.1128/jvi.64.12.6196-6203.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Giorgi C., Accardi L., Nicoletti L., Gro M. C., Takehara K., Hilditch C., Morikawa S., Bishop D. H. Sequences and coding strategies of the S RNAs of Toscana and Rift Valley fever viruses compared to those of Punta Toro, Sicilian Sandfly fever, and Uukuniemi viruses. Virology. 1991 Feb;180(2):738–753. doi: 10.1016/0042-6822(91)90087-r. [DOI] [PubMed] [Google Scholar]
  12. Hacker D., Rochat S., Kolakofsky D. Anti-mRNAs in La Crosse bunyavirus-infected cells. J Virol. 1990 Oct;64(10):5051–5057. doi: 10.1128/jvi.64.10.5051-5057.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ihara T., Akashi H., Bishop D. H. Novel coding strategy (ambisense genomic RNA) revealed by sequence analyses of Punta Toro Phlebovirus S RNA. Virology. 1984 Jul 30;136(2):293–306. doi: 10.1016/0042-6822(84)90166-1. [DOI] [PubMed] [Google Scholar]
  14. Ihara T., Smith J., Dalrymple J. M., Bishop D. H. Complete sequences of the glycoproteins and M RNA of Punta Toro phlebovirus compared to those of Rift Valley fever virus. Virology. 1985 Jul 15;144(1):246–259. doi: 10.1016/0042-6822(85)90321-6. [DOI] [PubMed] [Google Scholar]
  15. Krug R. M. Priming of influenza viral RNA transcription by capped heterologous RNAs. Curr Top Microbiol Immunol. 1981;93:125–149. doi: 10.1007/978-3-642-68123-3_6. [DOI] [PubMed] [Google Scholar]
  16. Marriott A. C., Ward V. K., Nuttall P. A. The S RNA segment of Sandfly Fever Sicilian virus: evidence for an ambisense genome. Virology. 1989 Apr;169(2):341–345. doi: 10.1016/0042-6822(89)90159-1. [DOI] [PubMed] [Google Scholar]
  17. Patterson J. L., Holloway B., Kolakofsky D. La Crosse virions contain a primer-stimulated RNA polymerase and a methylated cap-dependent endonuclease. J Virol. 1984 Oct;52(1):215–222. doi: 10.1128/jvi.52.1.215-222.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Patterson J. L., Kolakofsky D. Characterization of La Crosse virus small-genome transcripts. J Virol. 1984 Mar;49(3):680–685. doi: 10.1128/jvi.49.3.680-685.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pettersson R., Käriäinen L. The ribonucleic acids of Uukuniemi virus, a noncubical tick-borne arbovirus. Virology. 1973 Dec;56(2):608–619. doi: 10.1016/0042-6822(73)90062-7. [DOI] [PubMed] [Google Scholar]
  20. Raju R., Raju L., Hacker D., Garcin D., Compans R., Kolakofsky D. Nontemplated bases at the 5' ends of Tacaribe virus mRNAs. Virology. 1990 Jan;174(1):53–59. doi: 10.1016/0042-6822(90)90053-t. [DOI] [PubMed] [Google Scholar]
  21. Rönnholm R., Pettersson R. F. Complete nucleotide sequence of the M RNA segment of Uukuniemi virus encoding the membrane glycoproteins G1 and G2. Virology. 1987 Sep;160(1):191–202. doi: 10.1016/0042-6822(87)90060-2. [DOI] [PubMed] [Google Scholar]
  22. Schmaljohn C. S., Jennings G. B., Hay J., Dalrymple J. M. Coding strategy of the S genome segment of Hantaan virus. Virology. 1986 Dec;155(2):633–643. doi: 10.1016/0042-6822(86)90223-0. [DOI] [PubMed] [Google Scholar]
  23. Simons J. F., Hellman U., Pettersson R. F. Uukuniemi virus S RNA segment: ambisense coding strategy, packaging of complementary strands into virions, and homology to members of the genus Phlebovirus. J Virol. 1990 Jan;64(1):247–255. doi: 10.1128/jvi.64.1.247-255.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ulmanen I., Seppälä P., Pettersson R. F. In vitro translation of Uukuniemi virus-specific RNAs: identification of a nonstructural protein and a precursor to the membrane glycoproteins. J Virol. 1981 Jan;37(1):72–79. doi: 10.1128/jvi.37.1.72-79.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ward V. K., Marriott A. C., el-Ghorr A. A., Nuttall P. A. Coding strategy of the S RNA segment of Dugbe virus (Nairovirus; Bunyaviridae). Virology. 1990 Apr;175(2):518–524. doi: 10.1016/0042-6822(90)90436-u. [DOI] [PubMed] [Google Scholar]

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