1887

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.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000005
2015-03-01
2020-01-23
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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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;. [CrossRef]
    [Google Scholar]
  17. Elliott R. M.. ( 2014;). Orthobunyaviruses: recent genetic and structural insights. . Nat Rev Microbiol 12:, 673–685. [CrossRef][PubMed]
    [Google Scholar]
  18. Elliott R. M., Brennan B.. ( 2014;). Emerging phleboviruses. . Curr Opin Virol 5:, 50–57. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000005
Loading
/content/journal/jgv/10.1099/jgv.0.000005
Loading

Data & Media loading...

Most cited articles

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