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.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000557
2016-09-01
2020-09-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/9/2073.html?itemId=/content/journal/jgv/10.1099/jgv.0.000557&mimeType=html&fmt=ahah

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 Rec161:591–592 [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 One9: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 Virol86:6724–6731 [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 Virol88:13981–13989 [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 Announc4: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 Virol88:10399–10411 [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 Microbiol174:139–147 [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 Microbiol138:11–19 [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 Microbiol136:352–358 [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 J182:142–151 [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 Microbiol143:189–195 [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 Dis14:1855–1861[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 Ecol24:5707–5725 [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 Virol89:5238–5249 [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 Announc3: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 Res30:3059–3066 [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 Ital40:484–488[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 One5: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 Dis17:886–889 [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 ONE6: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 Announc3: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 One10: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 Pathol141:1–16 [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 Med87:131–144 [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 Evol32:268–274 [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 Pathog11: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 Virol88:12222–12232 [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 One9: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 Tech27:427–442[PubMed]
    [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 Pathog7: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 Virol90:5427–5439 [CrossRef][PubMed]
    [Google Scholar]
  32. Saegerman C., Berkvens D., Mellor P. S.. 2008; Bluetongue epidemiology in the European Union. Emerg Infect Dis14:539–544 [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 Virol81:831–837 [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 Microbiol160:35–42 [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 Res39:46 [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 Virol87:543–557 [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 Ital40:479–483[PubMed]
    [Google Scholar]
  38. Wilson A., Mellor P.. 2008; Bluetongue in Europe: vectors, epidemiology and climate change. Parasitol Res103:69–77 [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 Sci364:2669–2681 [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 Dis20:2123–2132 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000557
Loading
/content/journal/jgv/10.1099/jgv.0.000557
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

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