1887

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Volume 87, Issue 1

Genetic elements regulating packaging of the Bunyamwera orthobunyavirus genome Free

Abstract

The genome of (BUN; family , genus ) comprises three segments of negative-sense, single-stranded RNA. The RNA segments are encapsidated by the viral nucleocapsid (N) protein and form panhandle-like structures through interaction of complementary sequences at their 5′ and 3′ termini. Transcription and replication of a BUN genome analogue (minireplicon), comprising the viral non-coding sequences flanking a reporter gene, requires just the viral RNA polymerase (L protein) and N protein. Here, sequences of Bunyamwera serogroup M segment RNAs were compared and conserved elements within nt 20–33 of the 3′ and 5′ non-coding regions that can affect packaging of minireplicons into virions were identified. RNA-folding models suggest that a conserved sequence within nt 20–33 of the 5′ end of the genome segments maintains conserved structural features necessary for efficient transcription. Competitive packaging experiments using M, L and S segment-derived minireplicons that encode different reporter genes showed variable packaging efficiencies of the three segments. Packaging of a particular segment appeared to be independent of the presence of other segments and, for the S segment, packaging efficiency was unaffected by the inclusion of viral coding sequences in the minireplicon.

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2006-01-01
2024-04-20
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References

  1. 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]
  2. 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]
  3. 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]
  4. Blakqori G., Kochs G., Haller O., Weber F. 2003; Functional L polymerase of La Crosse virus allows in vivo reconstitution of recombinant nucleocapsids. J Gen Virol 84:1207–1214 [CrossRef]
     [Google Scholar]
  5. Bowen M. D., Trappier S. G., Sanchez A. J. & 7 other authors 2001; A reassortant bunyavirus isolated from acute hemorrhagic fever cases in Kenya and Somalia. Virology 291:185–190 [CrossRef]
     [Google Scholar]
  6. 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]
  7. Buchholz U. J., Finke S., Conzelmann K.-K. 1999; Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73:251–259
     [Google Scholar]
  8. Dunn E. F., Pritlove D. C., Jin H., Elliott R. M. 1995; Transcription of a recombinant bunyavirus RNA template by transiently expressed bunyavirus proteins. Virology 211:133–143 [CrossRef]
     [Google Scholar]
  9. Elliott R. M. 1996; The bunyaviridae: concluding remarks and future prospects. In The Bunyaviridae pp  295–332 Edited by Elliott R. M. New York: Plenum;
     [Google Scholar]
  10. Elliott R. M. 1997; Emerging viruses: the Bunyaviridae . Mol Med 3:572–577
     [Google Scholar]
  11. Flick R., Pettersson R. F. 2001; Reverse genetics system for Uukuniemi virus ( Bunyaviridae ): RNA polymerase I-catalyzed expression of chimeric viral RNAs. J Virol 75:1643–1655 [CrossRef]
     [Google Scholar]
  12. Flick R., Elgh F., Pettersson R. F. 2002; Mutational analysis of the Uukuniemi virus ( Bunyaviridae family) promoter reveals two elements of functional importance. J Virol 76:10849–10860 [CrossRef]
     [Google Scholar]
  13. Flick K., Hooper J. W., Schmaljohn C. S., Pettersson R. F., Feldmann H., Flick R. 2003a; Rescue of hantaan virus minigenomes. Virology 306:219–224 [CrossRef]
     [Google Scholar]
  14. Flick R., Flick K., Feldmann H., Elgh F. 2003b; Reverse genetics for Crimean-Congo hemorrhagic fever virus. J Virol 77:5997–6006 [CrossRef]
     [Google Scholar]
  15. Flick K., Katz A., Överby A., Feldmann H., Pettersson R. F., Flick R. 2004; Functional analysis of the noncoding regions of the Uukuniemi virus ( Bunyaviridae ) RNA segments. J Virol 78:11726–11738 [CrossRef]
     [Google Scholar]
  16. Fujii Y., Goto H., Watanabe T., Yoshida T., Kawaoka Y. 2003; Selective incorporation of influenza virus RNA segments into virions. Proc Natl Acad Sci U S A 100:2002–2007 [CrossRef]
     [Google Scholar]
  17. Fujii K., Fujii Y., Noda T., Muramoto Y., Watanabe T., Takada A., Goto H., Horimoto T., Kawaoka Y. 2005; Importance of both the coding and the segment-specific noncoding regions of the influenza A virus NS segment for its efficient incorporation into virions. J Virol 79:3766–3774 [CrossRef]
     [Google Scholar]
  18. Gerrard S. R., Li L., Barrett A. D., Nichol S. T. 2004; Ngari virus is a Bunyamwera virus reassortant that can be associated with large outbreaks of hemorrhagic fever in Africa. J Virol 78:8922–8926 [CrossRef]
     [Google Scholar]
  19. Kohl A., Clayton R. F., Weber F., Bridgen A., Randall R. E., Elliott R. M. 2003; Bunyamwera virus nonstructural protein NSs counteracts interferon regulatory factor 3-mediated induction of early cell death. J Virol 77:7999–8008 [CrossRef]
     [Google Scholar]
  20. Kohl A., Dunn E. F., Lowen A. C., Elliott R. M. 2004a; Complementarity, sequence and structural elements within the 3′ and 5′ non-coding regions of the Bunyamwera orthobunyavirus S segment determine promoter strength. J Gen Virol 85:3269–3278 [CrossRef]
     [Google Scholar]
  21. Kohl A., Hart T. J., Noonan C., Royall E., Roberts L. O., Elliott R. M. 2004b; A Bunyamwera virus minireplicon system in mosquito cells. J Virol 78:5679–5685 [CrossRef]
     [Google Scholar]
  22. Lopez N., Muller R., Prehaud C., Bouloy M. 1995; The L protein of Rift Valley fever virus can rescue viral ribonucleoproteins and transcribe synthetic genome-like RNA molecules. J Virol 69:3972–3979
     [Google Scholar]
  23. Lowen A. C., Boyd A., Fazakerley J. K., Elliott R. M. 2005; Attenuation of bunyavirus replication by rearrangement of viral coding and noncoding sequences. J Virol 79:6940–6946 [CrossRef]
     [Google Scholar]
  24. Osborne J. C., Elliott R. M. 2000; RNA binding properties of Bunyamwera virus nucleocapsid protein and selective binding to an element in the 5′ terminus of the negative-sense S segment. J Virol 74:9946–9952 [CrossRef]
     [Google Scholar]
  25. Schmaljohn C. S., Hooper J. W. 2001; Bunyaviridae : the viruses and their replication. In Fields Virology , 4th edn. pp  1581–1602 Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams & Wilkins;
     [Google Scholar]
  26. Shi X., Elliott R. M. 2002; Golgi localization of Hantaan virus glycoproteins requires coexpression of G1 and G2. Virology 300:31–38 [CrossRef]
     [Google Scholar]
  27. Shi X., Lappin D. F., Elliott R. M. 2004; Mapping the Golgi targeting and retention signal of Bunyamwera virus glycoproteins. J Virol 78:10793–10802 [CrossRef]
     [Google Scholar]
  28. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997; The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882 [CrossRef]
     [Google Scholar]
  29. Watanabe T., Watanabe S., Noda T., Fujii Y., Kawaoka Y. 2003; Exploitation of nucleic acid packaging signals to generate a novel influenza virus-based vector stably expressing two foreign genes. J Virol 77:10575–10583 [CrossRef]
     [Google Scholar]
  30. Watret G. E., Pringle C. R., Elliott R. M. 1985; Synthesis of bunyavirus-specific proteins in a continuous cell line (XTC-2) derived from Xenopus laevis . J Gen Virol 66:473–482 [CrossRef]
     [Google Scholar]
  31. Weber F., Dunn E. F., Bridgen A., Elliott R. M. 2001; The Bunyamwera virus nonstructural protein NSs inhibits viral RNA synthesis in a minireplicon system. Virology 281:67–74 [CrossRef]
     [Google Scholar]
  32. Zuker M., Jaeger J. A., Turner D. H. 1991; A comparison of optimal and suboptimal RNA secondary structures predicted by free energy minimization with structures determined by phylogenetic comparison. Nucleic Acids Res 19:2707–2714 [CrossRef]
     [Google Scholar]
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Genetic elements regulating packaging of the Bunyamwera orthobunyavirus genome
J. Gen. Virol. 87, 177 (2006); https://doi.org/10.1099/vir.0.81227-0
/content/journal/jgv/10.1099/vir.0.81227-0
/content/journal/jgv/10.1099/vir.0.81227-0
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