Identification of the Bunyamwera bunyavirus transcription termination signal Free

Abstract

(BUNV) is the prototype of the family , which comprises segmented RNA viruses. Each of the BUNV negative-strand segments, small (S), medium (M) and large (L), serves as template for two distinct RNA-synthesis activities: (i) replication to generate antigenomes that are in turn replicated to yield further genomes; and (ii) transcription to generate a single species of mRNA. BUNV mRNAs are truncated at their 3′ ends relative to the genome template, presumably because the BUNV transcriptase terminates transcription before reaching the 5′ terminus of the genomic template. Here, identification of the transcription termination signal responsible for 3′-end truncation of BUNV S-segment mRNA was carried out. It was shown that efficient transcription termination was signalled by a 33 nt sequence within the 5′ non-translated region (NTR) of the S segment. A 6 nt region (3′-GUCGAC-5′) within this sequence was found to play a major role in termination signalling, with other nucleotides possessing individually minor, but collectively significant, signalling ability. By abrogating the signalling ability of these 33 nt, we identified a second, functionally independent termination signal located 32 nt downstream. This downstream signal was 9 nt in length and contained a pentanucleotide sequence, 3′-UGUCG-5′, that overlapped the 6 nt major signalling component of the upstream signal. The pentanucleotide sequence was also found within the 5′ NTR of the BUNV L segment and in several other members of the genus , suggesting that the mechanism responsible for BUNV transcription termination may be common to other orthobunyaviruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81355-0
2006-01-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/1/189.html?itemId=/content/journal/jgv/10.1099/vir.0.81355-0&mimeType=html&fmt=ahah

References

  1. Barr J. N., Wertz G. W. 2001; Polymerase slippage at vesicular stomatitis virus gene junctions to generate poly(A) is regulated by the upstream 3′-AUAC-5′ tetranucleotide: implications for the mechanism of transcription termination. J Virol 75:6901–6913 [CrossRef]
    [Google Scholar]
  2. Barr J. N., Wertz G. W. 2004; Bunyamwera bunyavirus RNA synthesis requires cooperation of 3′- and 5′-terminal sequences. J Virol 78:1129–1138 [CrossRef]
    [Google Scholar]
  3. Barr J. N., Wertz G. W. 2005; Role of the conserved nucleotide mismatch within 3′- and 5′-terminal regions of Bunyamwera virus in signaling transcription. J Virol 79:3586–3594 [CrossRef]
    [Google Scholar]
  4. Barr J. N., Whelan S. P. J., Wertz G. W. 1997; cis -Acting signals involved in termination of vesicular stomatitis virus mRNA synthesis include the conserved AUAC and the U7 signal for polyadenylation. J Virol 71:8718–8725
    [Google Scholar]
  5. Barr J. N., Elliott R. M., Dunn E. F., Wertz G. W. 2003; Segment-specific terminal sequences of Bunyamwera bunyavirus regulate genome replication. Virology 311:326–338 [CrossRef]
    [Google Scholar]
  6. Barr J. N., Rodgers J. W., Wertz G. W. 2005; The Bunyamwera virus mRNA transcription signal resides within both the 3′ and the 5′ terminal regions and allows ambisense transcription from a model RNA segment. J Virol 79:12602–12607 [CrossRef]
    [Google Scholar]
  7. Bouloy M., Plotch S. J., Krug R. M. 1978; Globin mRNAs are primers for the transcription of influenza viral RNA in vitro . Proc Natl Acad Sci U S A 75:4886–4890 [CrossRef]
    [Google Scholar]
  8. Bouloy M., Pardigon N., Vialat P., Gerbaud S., Girard M. 1990; Characterization of the 5′ and 3′ ends of viral messenger RNAs isolated from BHK21 cells infected with Germiston virus (Bunyavirus). Virology 175:50–58 [CrossRef]
    [Google Scholar]
  9. Bridgen A., Elliott R. M. 1996; Rescue of a segmented negative-strand RNA virus entirely from cloned complementary DNAs. Proc Natl Acad Sci U S A 93:15400–15404 [CrossRef]
    [Google Scholar]
  10. Cunningham C., Szilágyi J. F. 1987; Viral RNAs synthesized in cells infected with Germiston bunyavirus. Virology 157:431–439 [CrossRef]
    [Google Scholar]
  11. Elliott R. M. 1985; Identification of nonstructural proteins encoded by viruses of the Bunyamwera serogroup (family Bunyaviridae ). Virology 143:119–126 [CrossRef]
    [Google Scholar]
  12. Elliott R. M. 1989a; Nucleotide sequence analysis of the large (L) genomic RNA segment of Bunyamwera virus, the prototype of the family Bunyaviridae . Virology 173:426–436 [CrossRef]
    [Google Scholar]
  13. Elliott R. M. 1989b; Nucleotide sequence analysis of the small (S) RNA segment of Bunyamwera virus, the prototype of the family Bunyaviridae. J Gen Virol 70:1281–1285 [CrossRef]
    [Google Scholar]
  14. Eshita Y., Ericson B., Romanowski V., Bishop D. H. L. 1985; Analyses of the mRNA transcription processes of snowshoe hare bunyavirus S and M RNA species. J Virol 55:681–689
    [Google Scholar]
  15. Fuerst T. R., Niles E. G., Studier F. W., Moss B. 1986; Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc Natl Acad Sci U S A 83:8122–8126 [CrossRef]
    [Google Scholar]
  16. Fuller F., Bishop D. H. L. 1982; Identification of virus-coded nonstructural polypeptides in bunyavirus-infected cells. J Virol 41:643–648
    [Google Scholar]
  17. Fuller F., Bhown A. S., Bishop D. H. L. 1983; Bunyavirus nucleoprotein, N, and a non-structural protein, NSS, are coded by overlapping reading frames in the S RNA. J Gen Virol 64:1705–1714 [CrossRef]
    [Google Scholar]
  18. Gentsch J. R., Bishop D. H. L. 1979; M viral RNA segment of bunyaviruses codes for two glycoproteins, G1 and G2. J Virol 30:767–770
    [Google Scholar]
  19. Hutchinson K. L., Peters C. J., Nichol S. T. 1996; Sin Nombre virus mRNA synthesis. Virology 224:139–149 [CrossRef]
    [Google Scholar]
  20. Hwang L. N., Englund N., Pattnaik A. K. 1998; Polyadenylation of vesicular stomatitis virus mRNA dictates efficient transcription termination at the intercistronic gene junctions. J Virol 72:1805–1813
    [Google Scholar]
  21. Jin H., Elliott R. M. 1993; Characterization of Bunyamwera virus S RNA that is transcribed and replicated by the L protein expressed from recombinant vaccinia virus. J Virol 67:1396–1404
    [Google Scholar]
  22. Krug R. M., Broni B. A., Bouloy M. 1979; Are the 5′ ends of influenza viral mRNAs synthesized in vivo donated by host mRNAs?. Cell 18:329–334 [CrossRef]
    [Google Scholar]
  23. Li X., Palese P. 1994; Characterization of the polyadenylation signal of influenza virus RNA. J Virol 68:1245–1249
    [Google Scholar]
  24. Patterson J. L., Kolakofsky D. 1984; Characterization of La Crosse virus small-genome transcripts. J Virol 49:680–685
    [Google Scholar]
  25. Plotch S. J., Bouloy M., Ulmanen I., Krug R. M. 1981; A unique cap(m7GpppXm)-dependent influenza virion endonuclease cleaves capped RNAs to generate the primers that initiate viral RNA transcription. Cell 23:847–858 [CrossRef]
    [Google Scholar]
  26. Poon L. L. M., Pritlove D. C., Fodor E., Brownlee G. G. 1999; Direct evidence that the poly(A) tail of influenza A virus mRNA is synthesized by reiterative copying of a U track in the virion RNA template. J Virol 73:3473–3476
    [Google Scholar]
  27. Whelan S. P., Barr J. N., Wertz G. W. 2004; Transcription and replication of nonsegmented negative-strand RNA viruses. Curr Top Microbiol Immunol 283:61–119
    [Google Scholar]
  28. Zuker M. 2003; Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81355-0
Loading
/content/journal/jgv/10.1099/vir.0.81355-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed