1887

Abstract

During the compulsory vaccination programme against bluetongue virus serotype 1 (BTV-1) in Corsica (France) in 2014, a BTV strain belonging to a previously uncharacterized serotype (BTV-27) was isolated from asymptomatic goats. The present study describes the detection and molecular characterization of two additional distinct BTV-27 variants found in goats in Corsica in 2014 and 2015. The full coding genome of these two novel BTV-27 variants show high homology (90–93 % nucleotide/93–95 % amino acid) with the originally described BTV-27 isolate from Corsican goats in 2014. These three variants constitute the novel serotype BTV-27 (‘BTV-27/FRA2014/v01 to v03’). Phylogenetic analyses with the 26 other established BTV serotypes revealed the closest relationship to BTV-25 (SWI2008/01) (80 % nucleotide/86 % amino acid) and to BTV-26 (KUW2010/02) (73–74 % nucleotide/80–81 % amino acid). However, highest sequence homologies between individual segments of BTV-27/FRA2014/v01–v03 with BTV-25 and BTV-26 vary. All three variants share the same segment 2 nucleotype with BTV-25. Neutralization assays of anti-BTV27/FRA2014/v01–v03 sera with a reassortant virus containing the outer capsid proteins of BTV-25 (BTV1) further confirmed that BTV-27 represents a distinct BTV serotype. Relationships between the variants and with BTV-25 and BTV-26, hypotheses about their origin, reassortment events and evolution are discussed.

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2016-09-01
2019-10-23
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References

  1. Backx A., Heutink C. G., van Rooij E. M., van Rijn P. A..( 2007;). Clinical signs of bluetongue virus serotype 8 infection in sheep and goats. . Vet Rec 161: 591–592. [CrossRef] [PubMed]
    [Google Scholar]
  2. Batten C., Darpel K., Henstock M., Fay P., Veronesi E., Gubbins S., Graves S., Frost L., Oura C..( 2014;). Evidence for transmission of bluetongue virus serotype 26 through direct contact. . PLoS One 9: e96049. [CrossRef] [PubMed]
    [Google Scholar]
  3. Boyle D. B., Bulach D. M., Amos-Ritchie R., Adams M. M., Walker P. J., Weir R..( 2012;). Genomic sequences of Australian bluetongue virus prototype serotypes reveal global relationships and possible routes of entry into Australia. . J Virol 86: 6724–6731. [CrossRef] [PubMed]
    [Google Scholar]
  4. Boyle D. B., Amos-Ritchie R., Broz I., Walker P. J., Melville L., Flanagan D., Davis S., Hunt N., Weir R..( 2014;). Evolution of bluetongue virus serotype 1 in northern Australia over 30 years. . J Virol 88: 13981–13989. [CrossRef] [PubMed]
    [Google Scholar]
  5. Bréard E., Sailleau C., Quenault H., Lucas P., Viarouge C., Touzain F., Fablet A., Vitour D., Attoui H. et al.( 2016;). Complete genome sequence of bluetongue virus serotype 8, which reemerged in France in August 2015. . Genome Announc 4: e00163-16. [CrossRef] [PubMed]
    [Google Scholar]
  6. Caporale M., Di Gialleonorado L., Janowicz A., Wilkie G., Shaw A., Savini G., Van Rijn P. A., Mertens P., Di Ventura M., Palmarini M..( 2014;). Virus and host factors affecting the clinical outcome of bluetongue virus infection. . J Virol 88: 10399–10411. [CrossRef] [PubMed]
    [Google Scholar]
  7. Celma C. C., Bhattacharya B., Eschbaumer M., Wernike K., Beer M., Roy P..( 2014;). Pathogenicity study in sheep using reverse-genetics-based reassortant bluetongue viruses. . Vet Microbiol 174: 139–147. [CrossRef] [PubMed]
    [Google Scholar]
  8. Chaignat V., Worwa G., Scherrer N., Hilbe M., Ehrensperger F., Batten C., Cortyen M., Hofmann M., Thuer B..( 2009;). Toggenburg Orbivirus, a new bluetongue virus: initial detection, first observations in field and experimental infection of goats and sheep. . Vet Microbiol 138: 11–19. [CrossRef] [PubMed]
    [Google Scholar]
  9. Dal Pozzo F., De Clercq K., Guyot H., Vandemeulebroucke E., Sarradin P., Vandenbussche F., Thiry E., Saegerman C..( 2009a;). Experimental reproduction of bluetongue virus serotype 8 clinical disease in calves. . Vet Microbiol 136: 352–358. [CrossRef] [PubMed]
    [Google Scholar]
  10. Dal Pozzo F., Saegerman C., Thiry E..( 2009b;). Bovine infection with bluetongue virus with special emphasis on European serotype 8. . Vet J 182: 142–151. [CrossRef]
    [Google Scholar]
  11. Eschbaumer M., Hoffmann B., Moss A., Savini G., Leone A., König P., Zemke J., Conraths F., Beer M..( 2010;). Emergence of bluetongue virus serotype 6 in Europe – German field data and experimental infection of cattle. . Vet Microbiol 143: 189–195. [CrossRef] [PubMed]
    [Google Scholar]
  12. Hofmann M. A., Renzullo S., Mader M., Chaignat V., Worwa G., Thuer B..( 2008;). Genetic characterization of toggenburg orbivirus, a new bluetongue virus. . Emerg Infect Dis 14: 1855–1861.[Crossref]
    [Google Scholar]
  13. Jacquet S., Garros C., Lombaert E., Walton C., Restrepo J., Allene X., Baldet T., Cetre-Sossah C., Chaskopoulou A. et al.( 2015;). Colonisation of the Mediterranean Basin by the vector-biting midge species Culicoides imicola: an old story. . Mol Ecol 24: 5707–5725. [CrossRef] [PubMed]
    [Google Scholar]
  14. Janowicz A., Caporale M., Shaw A., Gulletta S., Di Gialleonardo L., Ratinier M., Palmarini M..( 2015;). Multiple genome segments determine virulence of bluetongue virus serotype 8. . J Virol 89: 5238–5249. [CrossRef] [PubMed]
    [Google Scholar]
  15. Jenckel M., Bréard E., Schulz C., Sailleau C., Viarouge C., Hoffmann B., Höper D., Beer M., Zientara S..( 2015;). Complete coding genome sequence of putative novel bluetongue virus serotype 27. . Genome Announc 3: e0001600015. [CrossRef] [PubMed]
    [Google Scholar]
  16. Katoh K., Misawa K., Kuma K., Miyata T..( 2002;). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. . Nucleic Acids Res 30: 3059–3066. [CrossRef] [PubMed]
    [Google Scholar]
  17. Maan S., Maan N. S., Samuel A. R., O'Hara R., Meyer A. J., Rao S., Mertens P. P..( 2004;). Completion of the sequence analysis and comparisons of genome segment 2 (encoding outer capsid protein VP2) from representative isolates of the 24 bluetongue virus serotypes. . Vet Ital 40: 484–488.[PubMed]
    [Google Scholar]
  18. Maan S., Maan N. S., van Rijn P. A., van Gennip R. G., Sanders A., Wright I. M., Batten C., Hoffmann B., Eschbaumer M. et al.( 2010;). Full genome characterisation of bluetongue virus serotype 6 from the Netherlands 2008 and comparison to other field and vaccine strains. . PLoS One 5: e10323. [CrossRef] [PubMed]
    [Google Scholar]
  19. Maan S., Maan N. S., Nomikou K., Batten C., Antony F., Belaganahalli M. N., Samy A. M., Abdel Reda A., Al-Rashid S. A. et al.( 2011a;). Novel bluetongue virus serotype from Kuwait. . Emerg Infect Dis 17: 886–889. [CrossRef]
    [Google Scholar]
  20. Maan S., Maan N. S., Nomikou K., Veronesi E., Bachanek-Bankowska K., Belaganahalli M. N., Attoui H., Mertens P. P. C..( 2011b;). Complete genome characterisation of a novel 26th bluetongue virus serotype from Kuwait. . PLoS ONE 6: e26147. [CrossRef]
    [Google Scholar]
  21. Maan S., Maan N. S., Belaganahalli M. N., Kumar A., Batra K., Rao P. P., Hemadri D., Reddy Y. N., Putty K. et al.( 2015a;). Genome sequence of bluetongue virus type 2 from India: evidence for reassortment between outer capsid protein genes. . Genome Announc 3: e0004500015. [CrossRef] [PubMed]
    [Google Scholar]
  22. Maan S., Maan N. S., Belaganahalli M. N., Rao P. P., Singh K. P., Hemadri D., Putty K., Kumar A., Batra K. et al.( 2015b;). Full-genome sequencing as a basis for molecular epidemiology studies of bluetongue virus in India. . PLoS One 10: e0131257. [CrossRef]
    [Google Scholar]
  23. Maclachlan N. J., Drew C. P., Darpel K. E., Worwa G..( 2009;). The pathology and pathogenesis of bluetongue. . J Comp Pathol 141: 1–16. [CrossRef] [PubMed]
    [Google Scholar]
  24. Mintiens K., Méroc E., Mellor P. S., Staubach C., Gerbier G., Elbers A. R., Hendrickx G., De Clercq K..( 2008;). Possible routes of introduction of bluetongue virus serotype 8 into the epicentre of the 2006 epidemic in north-western Europe. . Prev Vet Med 87: 131–144. [CrossRef] [PubMed]
    [Google Scholar]
  25. Nguyen L. T., Schmidt H. A., von Haeseler A., Minh B. Q..( 2015;). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. . Mol Biol Evol 32: 268–274. [CrossRef] [PubMed]
    [Google Scholar]
  26. Nomikou K., Hughes J., Wash R., Kellam P., Breard E., Zientara S., Palmarini M., Biek R., Mertens P..( 2015;). Widespread reassortment shapes the evolution and epidemiology of bluetongue virus following European invasion. . PLoS Pathog 11: e1005056. [CrossRef] [PubMed]
    [Google Scholar]
  27. Nunes S. F., Hamers C., Ratinier M., Shaw A., Brunet S., Hudelet P., Palmarini M..( 2014;). A synthetic biology approach for a vaccine platform against known and newly emerging serotypes of bluetongue virus. . J Virol 88: 12222–12232. [CrossRef] [PubMed]
    [Google Scholar]
  28. Pages N., Bréard E., Urien C., Talavera S., Viarouge C., Lorca-Oro C., Jouneau L., Charley B., Zientara S. et al.( 2014;). Culicoides midge bites modulate the host response and impact on bluetongue virus infection in sheep. . PLoS One 9: e83683. [CrossRef] [PubMed]
    [Google Scholar]
  29. Purse B. V., Brown H. E., Harrup L., Mertens P. P., Rogers D. J..( 2008;). Invasion of bluetongue and other orbivirus infections into Europe: the role of biological and climatic processes. . Rev Sci Tech 27: 427–442.[PubMed] [Crossref]
    [Google Scholar]
  30. Ratinier M., Caporale M., Golder M., Franzoni G., Allan K., Nunes S. F., Armezzani A., Bayoumy A., Rixon F. et al.( 2011;). Identification and characterisation of a novel non-structural protein of bluetongue virus. . PLoS Pathog 7: e1002477. [CrossRef] [PubMed]
    [Google Scholar]
  31. Ratinier M., Shaw A. E., Barry G., Gu Q., Di Gialleonardo L., Janowicz A., Varela M., Randall R. E., Caporale M., Palmarini M..( 2016;). Bluetongue virus ns4 protein is an interferon antagonist and a determinant of virus virulence. . J Virol 90: 5427–5439. [CrossRef] [PubMed]
    [Google Scholar]
  32. Saegerman C., Berkvens D., Mellor P. S..( 2008;). Bluetongue epidemiology in the European Union. . Emerg Infect Dis 14: 539–544. [CrossRef] [PubMed]
    [Google Scholar]
  33. Sailleau C., Hamblin C., Paweska J. T., Zientara S..( 2000;). Identification and differentiation of the nine African horse sickness virus serotypes by RT-PCR amplification of the serotype-specific genome segment 2. . J Gen Virol 81: 831–837. [CrossRef] [PubMed]
    [Google Scholar]
  34. Schulz C., Eschbaumer M., Ziller M., Wäckerlin R., Beer M., Gauly M., Grevelding C. G., Hoffmann B., Bauer C..( 2012;). Cross-sectional study of bluetongue virus serotype 8 infection in South American camelids in Germany (2008/2009). . Vet Microbiol 160: 35–42. [CrossRef] [PubMed]
    [Google Scholar]
  35. Schwartz-Cornil I., Mertens P. P., Contreras V., Hemati B., Pascale F., Bréard E., Mellor P. S., MacLachlan N. J., Zientara S..( 2008;). Bluetongue virus: virology, pathogenesis and immunity. . Vet Res 39: 46. [CrossRef] [PubMed]
    [Google Scholar]
  36. Shaw A. E., Ratinier M., Nunes S. F., Nomikou K., Caporale M., Golder M., Allan K., Hamers C., Hudelet P. et al.( 2013;). Reassortment between two serologically unrelated bluetongue virus strains is flexible and can involve any genome segment. . J Virol 87: 543–557. [CrossRef] [PubMed]
    [Google Scholar]
  37. Singh K. P., Maan S., Samuel A. R., Rao S., Meyer A. J., Mertens P. P..( 2004;). Phylogenetic analysis of bluetongue virus genome segment 6 (encoding VP5) from different serotypes. . Vet Ital 40: 479–483.[PubMed]
    [Google Scholar]
  38. Wilson A., Mellor P..( 2008;). Bluetongue in Europe: vectors, epidemiology and climate change. . Parasitol Res 103: 69–77. [CrossRef]
    [Google Scholar]
  39. Wilson A. J., Mellor P. S..( 2009;). Bluetongue in Europe: past, present and future. . Philos Trans R Soc Lond B Biol Sci 364: 2669–2681. [CrossRef]
    [Google Scholar]
  40. Wright, I. M..( 2014;). Serological and genetic characterisation of putative new serotypes of bluetongue virus and epizootic haemorrhagic disease virus isolated from an alpaca. MSc Thesis, p.102: North-West University, Potchefstroom, South Africa.
    [Google Scholar]
  41. Zientara S., Sailleau C., Viarouge C., Höper D., Beer M., Jenckel M., Hoffmann B., Romey A., Bakkali-Kassimi L. et al.( 2014;). Novel bluetongue virus in goats, Corsica, France, 2014. . Emerg Infect Dis 20: 2123–2132. [CrossRef] [PubMed]
    [Google Scholar]
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