1887

Journal of General Virology header logo

Volume 96, Issue 3

Establishment of a minigenome system for Oropouche virus reveals the S genome segment to be significantly longer than reported previously Free

Abstract

Oropouche virus (OROV) is a medically important orthobunyavirus, which causes frequent outbreaks of a febrile illness in the northern parts of Brazil. However, despite being the cause of an estimated half a million human infections since its first isolation in Trinidad in 1955, details of the molecular biology of this tripartite, negative-sense RNA virus remain limited. We have determined the complete nucleotide sequence of the Brazilian prototype strain of OROV, BeAn 19991, and found a number of differences compared with sequences in the database. Most notable were that the S segment contained an additional 204 nt at the 3′ end and that there was a critical nucleotide mismatch at position 9 within the base-paired terminal panhandle structure of each genome segment. In addition, we obtained the complete sequence of the Trinidadian prototype strain TRVL-9760 that showed similar characteristics to the BeAn 19991 strain. By using a T7 RNA polymerase-driven minigenome system, we demonstrated that cDNA clones of the BeAn 19991 L and S segments expressed functional proteins, and also that the newly determined terminal untranslated sequences acted as functional promoters in the minigenome assay. By co-transfecting a cDNA to the viral glycoproteins, virus-like particles were generated that packaged a minigenome and were capable of infecting naive cells.

  • Received:
  • Accepted:
  • Published Online:
© 2015 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000005
2015-03-01
2023-03-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/3/513.html?itemId=/content/journal/jgv/10.1099/jgv.0.000005&mimeType=html&fmt=ahah

References

  1. Afonso A., Abrahantes J. C., Conraths F., Veldhuis A., Elbers A., Roberts H., Van der Stede Y., Méroc E., Gache K., Richardson J. 2014; The Schmallenberg virus epidemic in Europe – 2011–2013. Prev Vet Med 116:391–403 [View Article][PubMed]
     [Google Scholar]
  2. Anderson C. R., Spence L., Downs W. G., Aitken T. H. 1961; Oropouche virus: a new human disease agent from Trinidad, West Indies. Am J Trop Med Hyg 10:574–578[PubMed]
     [Google Scholar]
  3. Aquino V. H., Figueiredo L. T. 2004; Linear amplification followed by single primer polymerase chain reaction to amplify unknown DNA fragments: complete nucleotide sequence of Oropouche virus M RNA segment. J Virol Methods 115:51–57 [View Article][PubMed]
     [Google Scholar]
  4. Aquino V. H., Moreli M. L., Moraes Figueiredo L. T. 2003; Analysis of oropouche virus L protein amino acid sequence showed the presence of an additional conserved region that could harbour an important role for the polymerase activity. Arch Virol 148:19–28 [View Article][PubMed]
     [Google Scholar]
  5. Barr J. N., Wertz G. W. 2004; Bunyamwera bunyavirus RNA synthesis requires cooperation of 3′- and 5′-terminal sequences. J Virol 78:1129–1138 [View Article][PubMed]
     [Google Scholar]
  6. 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 [View Article][PubMed]
     [Google Scholar]
  7. 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 [View Article][PubMed]
     [Google Scholar]
  8. 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 [View Article][PubMed]
     [Google Scholar]
  9. 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[PubMed]
     [Google Scholar]
  10. Dilcher M., Alves M. J., Finkeisen D., Hufert F., Weidmann M. 2012a; Genetic characterization of Bhanja virus and Palma virus, two tick-borne phleboviruses. Virus Genes 45:311–315 [View Article][PubMed]
     [Google Scholar]
  11. Dilcher M., Hasib L., Lechner M., Wieseke N., Middendorf M., Marz M., Koch A., Spiegel M., Dobler G.other authors 2012b; Genetic characterization of Tribeč virus and Kemerovo virus, two tick-transmitted human-pathogenic Orbiviruses. Virology 423:68–76 [View Article][PubMed]
     [Google Scholar]
  12. Dunn E. F., Pritlove D. C., Elliott R. M. 1994; The S RNA genome segments of Batai, Cache Valley, Guaroa, Kairi, Lumbo, Main Drain and Northway bunyaviruses: sequence determination and analysis. J Gen Virol 75:597–608 [View Article][PubMed]
     [Google Scholar]
  13. 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 [View Article][PubMed]
     [Google Scholar]
  14. 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 [View Article][PubMed]
     [Google Scholar]
  15. 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 [View Article][PubMed]
     [Google Scholar]
  16. Elliott R. M. 2012; Bunyavirus reverse genetics and applications to studying interactions with host cells. In Reverse Genetics of RNA Viruses: Applications and Perspectives pp. 200–223 Edited by Bridgen A. Chichester: Wiley; [View Article]
     [Google Scholar]
  17. Elliott R. M. 2014; Orthobunyaviruses: recent genetic and structural insights. Nat Rev Microbiol 12:673–685 [View Article][PubMed]
     [Google Scholar]
  18. Elliott R. M., Brennan B. 2014; Emerging phleboviruses. Curr Opin Virol 5:50–57 [View Article][PubMed]
     [Google Scholar]
  19. Elliott R. M., Schmaljohn C. S., Collett M. S. 1991; Bunyaviridae genome structure and gene expression. Curr Top Microbiol Immunol 169:91–141[PubMed]
     [Google Scholar]
  20. Elliott R. M., Blakqori G., van Knippenberg I. C., Koudriakova E., Li P., McLees A., Shi X., Szemiel A. M. 2013; Establishment of a reverse genetics system for Schmallenberg virus, a newly emerged orthobunyavirus in Europe. J Gen Virol 94:851–859 [View Article][PubMed]
     [Google Scholar]
  21. Johnson K. N., Zeddam J. L., Ball L. A. 2000; Characterization and construction of functional cDNA clones of Pariacoto virus, the first Alphanodavirus isolated outside Australasia. J Virol 74:5123–5132 [View Article][PubMed]
     [Google Scholar]
  22. Kohl A., Bridgen A., Dunn E., Barr J. N., Elliott R. M. 2003; Effects of a point mutation in the 3′ end of the S genome segment of naturally occurring and engineered Bunyamwera viruses. J Gen Virol 84:789–793 [View Article][PubMed]
     [Google Scholar]
  23. Kohl A., Dunn E. F., Lowen A. C., Elliott R. M. 2004; 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 [View Article][PubMed]
     [Google Scholar]
  24. Ladner J. T., Beitzel B., Chain P. S., Davenport M. G., Donaldson E. F., Frieman M., Kugelman J. R., Kuhn J. H., O’Rear J.other authors 2014a; Standards for sequencing viral genomes in the era of high-throughput sequencing. MBio 5:e01360–e14 [View Article][PubMed]
     [Google Scholar]
  25. Ladner J. T., Savji N., Lofts L., Travassos da Rosa A., Wiley M. R., Gestole M. C., Rosen G. E., Guzman H., Vasconcelos P. F.other authors 2014b; Genomic and phylogenetic characterization of viruses included in the Manzanilla and Oropouche species complexes of the genus Orthobunyavirus, family Bunyaviridae. J Gen Virol 95:1055–1066 [View Article][PubMed]
     [Google Scholar]
  26. Lambert A. J., Lanciotti R. S. 2008; Molecular characterization of medically important viruses of the genus Orthobunyavirus. J Gen Virol 89:2580–2585 [View Article][PubMed]
     [Google Scholar]
  27. Matsuno K., Weisend C., Travassos da Rosa A. P., Anzick S. L., Dahlstrom E., Porcella S. F., Dorward D. W., Yu X. J., Tesh R. B., Ebihara H. 2013; Characterization of the Bhanja serogroup viruses (Bunyaviridae): a novel species of the genus Phlebovirus and its relationship with other emerging tick-borne phleboviruses. J Virol 87:3719–3728 [View Article][PubMed]
     [Google Scholar]
  28. Moss B., Elroy-Stein O., Mizukami T., Alexander W. A., Fuerst T. R. 1990; New mammalian expression vectors. Nature 348:91–92 [View Article][PubMed]
     [Google Scholar]
  29. Ogawa Y., Sugiura K., Kato K., Tohya Y., Akashi H. 2007; Rescue of Akabane virus (family Bunyaviridae) entirely from cloned cDNAs by using RNA polymerase I. J Gen Virol 88:3385–3390 [View Article][PubMed]
     [Google Scholar]
  30. Pinheiro F. P., Pinheiro M., Bensabath G., Causey O. R., Shope R. E. 1962; Oropouche virus epidemic in Bélem. Rev Serv Esp Saude Pub 12:15–23 (in Portugese)
    [Google Scholar]
  31. Pinheiro F. P., Hoch A. L., Gomes M. L., Roberts D. R. 1981a; Oropouche virus. IV. Laboratory transmission by Culicoides paraensis. Am J Trop Med Hyg 30:172–176[PubMed]
     [Google Scholar]
  32. Pinheiro F. P., Travassos da Rosa A. P., Travassos da Rosa J. F., Ishak R., Freitas R. B., Gomes M. L., LeDuc J. W., Oliva O. F. 1981b; Oropouche virus. I. A review of clinical, epidemiological, and ecological findings. Am J Trop Med Hyg 30:149–160[PubMed]
     [Google Scholar]
  33. Pinheiro F. P., Travassos da Rosa A. P., Gomes M. L., LeDuc J. W., Hoch A. L. 1982; Transmission of Oropouche virus from man to hamster by the midge Culicoides paraensis. Science 215:1251–1253 [View Article][PubMed]
     [Google Scholar]
  34. Plyusnin A., Elliott R. M.editors 2011 Bunyaviridae. Molecular and Cellular Biology Norfolk: Caister Academic Press;
     [Google Scholar]
  35. Saeed M. F., Wang H., Nunes M., Vasconcelos P. F., Weaver S. C., Shope R. E., Watts D. M., Tesh R. B., Barrett A. D. 2000; Nucleotide sequences and phylogeny of the nucleocapsid gene of Oropouche virus. J Gen Virol 81:743–748[PubMed]
     [Google Scholar]
  36. Shi X., Kohl A., Li P., Elliott R. M. 2007; Role of the cytoplasmic tail domains of Bunyamwera orthobunyavirus glycoproteins Gn and Gc in virus assembly and morphogenesis. J Virol 81:10151–10160 [View Article][PubMed]
     [Google Scholar]
  37. Varela M., Schnettler E., Caporale M., Murgia C., Barry G., McFarlane M., McGregor E., Piras I. M., Shaw A.other authors 2013; Schmallenberg virus pathogenesis, tropism and interaction with the innate immune system of the host. PLoS Pathog 9:e1003133 [View Article][PubMed]
     [Google Scholar]
  38. Vasconcelos H. B., Nunes M. R., Casseb L. M., Carvalho V. L., Pinto da Silva E. V., Silva M., Casseb S. M., Vasconcelos P. F. 2011; Molecular epidemiology of Oropouche virus, Brazil. Emerg Infect Dis 17:800–806 [View Article][PubMed]
     [Google Scholar]
  39. Wang H., Beasley D. W., Li L., Holbrook M. R., Barrett A. D. 2001; Nucleotide sequence and deduced amino acid sequence of the medium RNA segment of Oropouche, a Simbu serogroup virus: comparison with the middle RNA of Bunyamwera and California serogroup viruses. Virus Res 73:153–162 [View Article][PubMed]
     [Google Scholar]
  40. 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 [View Article][PubMed]
     [Google Scholar]
  41. Weber F., Bridgen A., Fazakerley J. K., Streitenfeld H., Kessler N., Randall R. E., Elliott R. M. 2002; Bunyamwera bunyavirus nonstructural protein NSs counteracts the induction of alpha/beta interferon. J Virol 76:7949–7955 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000005
Loading
Establishment of a minigenome system for Oropouche virus reveals the S genome segment to be significantly longer than reported previously
J. Gen. Virol. 96, 513 (2015); https://doi.org/10.1099/jgv.0.000005
/content/journal/jgv/10.1099/jgv.0.000005
/content/journal/jgv/10.1099/jgv.0.000005
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error