{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T08:07:46Z","timestamp":1791360466163,"version":"4.3.1"},"reference-count":79,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2021,7,26]],"date-time":"2021-07-26T00:00:00Z","timestamp":1627257600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000780","name":"European Commission","doi-asserted-by":"publisher","award":["PALE-Blu\u201d grant number 727393"],"award-info":[{"award-number":["PALE-Blu\u201d grant number 727393"]}],"id":[{"id":"10.13039\/501100000780","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BBS\/E\/I\/00001877"],"award-info":[{"award-number":["BBS\/E\/I\/00001877"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Bluetongue (BT) is a severe and economically important disease of ruminants that is widely distributed around the world, caused by the bluetongue virus (BTV). More than 28 different BTV serotypes have been identified in serum neutralisation tests (SNT), which, along with geographic variants (topotypes) within each serotype, reflect differences in BTV outer-capsid protein VP2. VP2 is the primary target for neutralising antibodies, although the basis for cross-reactions and serological variations between and within BTV serotypes is poorly understood. Recombinant BTV VP2 proteins (rVP2) were expressed in Nicotiana benthamiana, based on sequence data for isolates of thirteen BTV serotypes (primarily from Europe), including three \u2018novel\u2019 serotypes (BTV-25, -26 and -27) and alternative topotypes of four serotypes. Cross-reactions within and between these viruses were explored using rabbit anti-rVP2 sera and post BTV-infection sheep reference-antisera, in I-ELISA (with rVP2 target antigens) and SNT (with reference strains of BTV-1 to -24, -26 and -27). Strong reactions were generally detected with homologous rVP2 proteins or virus strains\/serotypes. The sheep antisera were largely serotype-specific in SNT, but more cross-reactive by ELISA. Rabbit antisera were more cross-reactive in SNT, and showed widespread, high titre cross-reactions against homologous and heterologous rVP2 proteins in ELISA. Results were analysed and visualised by antigenic cartography, showing closer relationships in some, but not all cases, between VP2 topotypes within the same serotype, and between serotypes belonging to the same \u2018VP2 nucleotype\u2019.<\/jats:p>","DOI":"10.3390\/v13081455","type":"journal-article","created":{"date-parts":[[2021,7,26]],"date-time":"2021-07-26T22:22:46Z","timestamp":1627338166000},"page":"1455","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":25,"title":["Serological Cross-Reactions between Expressed VP2 Proteins from Different Bluetongue Virus Serotypes"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5808-4284","authenticated-orcid":false,"given":"Petra C.","family":"Fay","sequence":"first","affiliation":[{"name":"School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington, Loughborough LE12 5RD, UK"},{"name":"The Pirbright Institute, Surrey, Woking GU24 ONF, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fauziah","family":"Mohd Jaafar","sequence":"additional","affiliation":[{"name":"UMR VIROLOGIE 1161, INRAE, Ecole Nationale V\u00e9t\u00e9rinaire d\u2019Alfort, ANSES, Universit\u00e9 Paris-Est, F-94700 Maisons-Alfort, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4274-7375","authenticated-orcid":false,"given":"Carrie","family":"Batten","sequence":"additional","affiliation":[{"name":"The Pirbright Institute, Surrey, Woking GU24 ONF, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9639-9981","authenticated-orcid":false,"given":"Houssam","family":"Attoui","sequence":"additional","affiliation":[{"name":"UMR VIROLOGIE 1161, INRAE, Ecole Nationale V\u00e9t\u00e9rinaire d\u2019Alfort, ANSES, Universit\u00e9 Paris-Est, F-94700 Maisons-Alfort, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5606-9627","authenticated-orcid":false,"given":"Keith","family":"Saunders","sequence":"additional","affiliation":[{"name":"John Innes Centre, Department of Biochemistry and Metabolism, Norwich Research Park, Norwich NR4 7UH, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0700-906X","authenticated-orcid":false,"given":"George P.","family":"Lomonossoff","sequence":"additional","affiliation":[{"name":"John Innes Centre, Department of Biochemistry and Metabolism, Norwich Research Park, Norwich NR4 7UH, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth","family":"Reid","sequence":"additional","affiliation":[{"name":"School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington, Loughborough LE12 5RD, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel","family":"Horton","sequence":"additional","affiliation":[{"name":"Pathology and Infectious Diseases, School of Veterinary Medicine, University of Surrey, Guildford GU2 7XH, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sushila","family":"Maan","sequence":"additional","affiliation":[{"name":"Department of Animal Biotechnology, Lala Lajpat Rai University of Veterinary & Animal Sciences, Hisar 125004, India"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Haig","sequence":"additional","affiliation":[{"name":"School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington, Loughborough LE12 5RD, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1912-4500","authenticated-orcid":false,"given":"Janet M.","family":"Daly","sequence":"additional","affiliation":[{"name":"School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington, Loughborough LE12 5RD, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter P. C.","family":"Mertens","sequence":"additional","affiliation":[{"name":"School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington, Loughborough LE12 5RD, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,7,26]]},"reference":[{"key":"ref_1","first-page":"426","article-title":"Bluetongue virus replication, molecular and structural biology","volume":"40","author":"Mertens","year":"2004","journal-title":"Vet. Ital."},{"key":"ref_2","unstructured":"Fauquet, M.A.M., Maniloff, J., Desselberger, U., and Ball, L.A. (2004). Orbivirus, Reoviridae. Virus Taxonomy VIIIth Report of the ICTV, Academic Press."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1038\/26694","article-title":"The atomic structure of the bluetongue virus core","volume":"395","author":"Grimes","year":"1998","journal-title":"Nature"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.coviro.2017.05.003","article-title":"Bluetongue virus structure and assembly","volume":"24","author":"Roy","year":"2017","journal-title":"Curr. Opin. Virol."},{"key":"ref_5","first-page":"4957","article-title":"Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016\/429): Bluetongue","volume":"15","author":"More","year":"2017","journal-title":"EFSA J."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"329","DOI":"10.20506\/rst.34.2.2360","article-title":"Bluetongue","volume":"34","author":"Maclachlan","year":"2015","journal-title":"Rev. Sci. Technol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Batten, C., Darpel, K., Henstock, M., Fay, P., Veronesi, E., Gubbins, S., Graves, S., Frost, L., and Oura, C. (2014). Evidence for transmission of bluetongue virus serotype 26 through direct contact. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0096049"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e251","DOI":"10.1111\/tbed.12780","article-title":"Bluetongue virus serotype 27: Experimental infection of goats, sheep and cattle with three BTV-27 variants reveal atypical characteristics and likely direct contact transmission BTV-27 between goats","volume":"65","author":"Breard","year":"2018","journal-title":"Transbound Emerg. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1111\/tbed.13338","article-title":"Characterization of bluetongue virus serotype 28","volume":"67","author":"Bumbarov","year":"2020","journal-title":"Transbound Emerg. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Ries, C., Sharav, T., Tseren-Ochir, E.-O., Beer, M., and Hoffmann, B. (2021). Putative Novel Serotypes \u201833\u2019 and \u201835\u2019 in Clinically Healthy Small Ruminants in Mongolia Expand the Group of Atypical BTV. Viruses, 13.","DOI":"10.3390\/v13010042"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.meegid.2017.03.021","article-title":"Novel putative Bluetongue virus in healthy goats from Sardinia, Italy","volume":"51","author":"Savini","year":"2017","journal-title":"Infect. Genet. Evol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2123","DOI":"10.3201\/eid2012.140924","article-title":"Novel bluetongue virus in goats, Corsica, France, 2014","volume":"20","author":"Zientara","year":"2014","journal-title":"Emerg. Infect. Dis."},{"key":"ref_13","unstructured":"Wright, I. (2014). Serological and Genetic Characterisation of Putative New Serotypes of Blue-Tongue Virus and Epizootic Haemorrhagic Disease Virus Isolated from Alpaca. [Master\u2019s Thesis, North-West University]."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Pullinger, G.D., Guimera Busquets, M., Nomikou, K., Boyce, M., Attoui, H., and Mertens, P.P. (2016). Identification of the Genome Segments of Bluetongue Virus Serotype 26 (Isolate KUW2010\/02) that Restrict Replication in a Culicoides sonorensis Cell Line (KC Cells). PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0149709"},{"key":"ref_15","first-page":"1864","article-title":"Bluetongue virus spread in Europe is a consequence of climatic, landscape and vertebrate host factors as revealed by phylogeographic inference","volume":"284","author":"Jacquot","year":"2017","journal-title":"Proc. Biol. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Kundlacz, C., Caignard, G., Sailleau, C., Viarouge, C., Postic, L., Vitour, D., Zientara, S., and Breard, E. (2019). Bluetongue Virus in France: An Illustration of the European and Mediterranean Context since the 2000s. Viruses, 11.","DOI":"10.3390\/v11070672"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Pascall, D.J., Nomikou, K., Breard, E., Zientara, S., Filipe, A.D.S., Hoffmann, B., Jacquot, M., Singer, J.B., De Clercq, K., and Botner, A. (2020). \u201cFrozen evolution\u201d of an RNA virus suggests accidental release as a potential cause of arbovirus re-emergence. PLoS Biol., 18.","DOI":"10.1371\/journal.pbio.3000673"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Belhouchet, M., Mohd Jaafar, F., Firth, A.E., Grimes, J.M., Mertens, P.P., and Attoui, H. (2011). Detection of a fourth orbivirus non-structural protein. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0025697"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"9832","DOI":"10.1128\/JVI.73.12.9832-9842.1999","article-title":"Expression and functional characterization of bluetongue virus VP2 protein: Role in cell entry","volume":"73","author":"Hassan","year":"1999","journal-title":"J. Virol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Maan, N.S., Maan, S., Belaganahalli, M.N., Ostlund, E.N., Johnson, D.J., Nomikou, K., and Mertens, P.P. (2012). Identification and differentiation of the twenty six bluetongue virus serotypes by RT-PCR amplification of the serotype-specific genome segment 2. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0032601"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/0042-6822(83)90345-8","article-title":"Monoclonal antibody analysis of serotype-restricted and unrestricted bluetongue viral antigenic determinants","volume":"124","author":"Appleton","year":"1983","journal-title":"Virology"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1016\/0042-6822(89)90447-9","article-title":"Analysis of the roles of bluetongue virus outer capsid proteins VP2 and VP5 in determination of virus serotype","volume":"170","author":"Mertens","year":"1989","journal-title":"Virology"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"100026","DOI":"10.1016\/j.jvacx.2019.100026","article-title":"Bluetongue virus outer-capsid protein VP2 expressed in Nicotiana benthamiana raises neutralising antibodies and a protective immune response in IFNAR (\u2212\/\u2212) mice","volume":"2","author":"Fay","year":"2019","journal-title":"Vaccine X"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1099\/vir.0.82456-0","article-title":"Analysis and phylogenetic comparisons of full-length VP2 genes of the 24 bluetongue virus serotypes","volume":"88","author":"Maan","year":"2007","journal-title":"J. Gen. Virol."},{"key":"ref_25","first-page":"59","article-title":"The application of improved techniques to the identification of strains of bluetongue virus","volume":"37","author":"Howell","year":"1970","journal-title":"Onderstepoort J. Vet. Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1128\/jvi.48.3.627-632.1983","article-title":"Molecular basis of bluetongue virus neutralization","volume":"48","author":"Kahlon","year":"1983","journal-title":"J. Virol."},{"key":"ref_27","first-page":"484","article-title":"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","volume":"40","author":"Maan","year":"2004","journal-title":"Vet. Ital."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1016\/j.jviromet.2010.08.002","article-title":"Expression and secretion of Bluetongue virus serotype 8 (BTV-8)VP2 outer capsid protein by mammalian cells","volume":"169","author":"Capocefalo","year":"2010","journal-title":"J. Virol. Methods"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1038\/nrmicro2052","article-title":"Prospects for improved bluetongue vaccines","volume":"7","author":"Roy","year":"2009","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1016\/0042-6822(87)90209-1","article-title":"A comparison of different cloned bluetongue virus genome segments as probes for the detection of virus-specified RNA","volume":"158","author":"Huismans","year":"1987","journal-title":"Virology"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"4059","DOI":"10.1016\/j.vaccine.2014.05.056","article-title":"Immunisation with bacterial expressed VP2 and VP5 of bluetongue virus (BTV) protect alpha\/beta interferon-receptor knock-out (IFNAR(\u2212\/\u2212)) mice from homologous lethal challenge","volume":"32","author":"Belhouchet","year":"2014","journal-title":"Vaccine"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.jviromet.2014.11.012","article-title":"A quantitative real-time reverse transcription PCR (qRT-PCR) assay to detect genome segment 9 of all 26 bluetongue virus serotypes","volume":"213","author":"Maan","year":"2015","journal-title":"J. Virol. Methods"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"vez027","DOI":"10.1093\/ve\/vez027","article-title":"Contrasting selective patterns across the segmented genome of bluetongue virus in a global reassortment hotspot","volume":"5","author":"Jacquot","year":"2019","journal-title":"Virus Evol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/0168-1702(90)90078-P","article-title":"Relationships amongst bluetongue viruses revealed by comparisons of capsid and outer coat protein nucleotide sequences","volume":"17","author":"Gould","year":"1990","journal-title":"Virus Res."},{"key":"ref_35","unstructured":"Dinter, Z., and Morein, B. (1990). Bluetongue virus. Virus Infections of Ruminants, Elsevier Science Publishers."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/S0168-1702(00)00130-1","article-title":"Changes in the outer capsid proteins of bluetongue virus serotype ten that abrogate neutralization by monoclonal antibodies","volume":"67","author":"Bonneau","year":"2000","journal-title":"Virus Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1016\/S0034-5288(18)31885-X","article-title":"Clinical and serological outcome following the simultaneous inoculation of three bluetongue virus types into sheep","volume":"37","author":"Jeggo","year":"1984","journal-title":"Res. Vet. Sci."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Ma, G., Eschbaumer, M., Said, A., Hoffmann, B., Beer, M., and Osterrieder, N. (2012). An equine herpesvirus type 1 (EHV-1) expressing VP2 and VP5 of serotype 8 bluetongue virus (BTV-8) induces protection in a murine infection model. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0034425"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1186\/s12985-014-0205-0","article-title":"Plant-based vaccines against viruses","volume":"11","author":"Rybicki","year":"2014","journal-title":"Virol. J."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1016\/j.virol.2008.04.028","article-title":"Sequence analysis of bluetongue virus serotype 8 from the Netherlands 2006 and comparison to other European strains","volume":"377","author":"Maan","year":"2008","journal-title":"Virology"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Maan, S., Maan, N.S., van Rijn, P.A., van Gennip, R.G., Sanders, A., Wright, I.M., Batten, C., Hoffmann, B., Eschbaumer, M., and Oura, C.A. (2010). Full genome characterisation of bluetongue virus serotype 6 from the Netherlands 2008 and comparison to other field and vaccine strains. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0010323"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"886","DOI":"10.3201\/eid1705.101742","article-title":"Novel bluetongue virus serotype from Kuwait","volume":"17","author":"Maan","year":"2011","journal-title":"Emerg. Infect. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1007\/s11103-013-0036-1","article-title":"The pEAQ vector series: The easy and quick way to produce recombinant proteins in plants","volume":"83","author":"Peyret","year":"2013","journal-title":"Plant Mol. Biol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1111\/pbi.12076","article-title":"A method for rapid production of heteromultimeric protein complexes in plants: Assembly of protective bluetongue virus-like particles","volume":"11","author":"Thuenemann","year":"2013","journal-title":"Plant Biotechnol. J."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1007\/BF01863914","article-title":"Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Naunyn-Schmiedebergs","volume":"162","year":"1931","journal-title":"Archiv. Exp. Pathol. Pharmakol."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Nomikou, K., Hughes, J., Wash, R., Kellam, P., Breard, E., Zientara, S., Palmarini, M., Biek, R., and Mertens, P. (2015). Widespread Reassortment Shapes the Evolution and Epidemiology of Bluetongue Virus following European Invasion. PLoS Pathog., 11.","DOI":"10.1371\/journal.ppat.1005056"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"13122","DOI":"10.1128\/JVI.02393-12","article-title":"Full genome sequence of bluetongue virus serotype 4 from China","volume":"86","author":"Yang","year":"2012","journal-title":"J. Virol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"8333","DOI":"10.1128\/JVI.01101-12","article-title":"Complete genome sequence of bluetongue virus serotype 9: Implications for serotyping","volume":"86","author":"Rao","year":"2012","journal-title":"J. Virol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1111\/tbed.12178","article-title":"Full-Genome Sequencing of Four Bluetongue Virus Serotype 11 Viruses","volume":"62","author":"Vandenbussche","year":"2015","journal-title":"Transbound Emerg. Dis."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"e00016-15","DOI":"10.1128\/genomeA.00016-15","article-title":"Complete coding genome sequence of putative novel bluetongue virus serotype 27","volume":"3","author":"Jenckel","year":"2015","journal-title":"Genome Announc."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"2073","DOI":"10.1099\/jgv.0.000557","article-title":"Bluetongue virus serotype 27: Detection and characterization of two novel variants in Corsica, France","volume":"97","author":"Schulz","year":"2016","journal-title":"J. Gen. Virol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1126\/science.1097211","article-title":"Mapping the antigenic and genetic evolution of influenza virus","volume":"305","author":"Smith","year":"2004","journal-title":"Science"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Maan, S., Maan, N.S., Nomikou, K., Veronesi, E., Bachanek-Bankowska, K., Belaganahalli, M.N., Attoui, H., and Mertens, P.P. (2011). Complete genome characterisation of a novel 26th bluetongue virus serotype from Kuwait. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0026147"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/0378-1135(89)90089-8","article-title":"Cross-neutralization of genetic reassortants of bluetongue virus serotypes 20 and 21","volume":"19","author":"Cowley","year":"1989","journal-title":"Vet. Microbiol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1099\/0022-1317-71-6-1325","article-title":"Conformation of the VP2 protein of bluetongue virus (BTV) determines the involvement in virus neutralization of highly conserved epitopes within the BTV serogroup","volume":"71","author":"White","year":"1990","journal-title":"J. Gen. Virol."},{"key":"ref_56","first-page":"51","article-title":"Identification of the serotype-specific and group-specific antigens of bluetongue virus","volume":"48","author":"Huismans","year":"1981","journal-title":"Onderstepoort J. Vet. Res."},{"key":"ref_57","first-page":"59","article-title":"A comparison of an australian bluetongue virus isolate (CSIRO 19) with other bluetongue virus serotypes by cross-hybridization and cross-immune precipitation","volume":"48","author":"Huismans","year":"1981","journal-title":"Onderstepoort J. Vet. Res."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/0378-1135(81)90039-0","article-title":"A serological comparison of the australian isolate of bluetongue virus type 20 (CSIRO 19) with bluetongue group viruses","volume":"6","author":"Sellers","year":"1981","journal-title":"Vet. Microbiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1947","DOI":"10.1099\/0022-1317-73-8-1947","article-title":"Neutralizing epitopes of the serotypes of bluetongue virus present in the United States","volume":"73","author":"Rossitto","year":"1992","journal-title":"J. Gen. Virol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/0378-1135(92)90123-B","article-title":"Variation amongst the neutralizing epitopes of bluetongue viruses isolated in the United States in 1979\u20131981","volume":"31","author":"MacLachlan","year":"1992","journal-title":"Vet. Microbiol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"2502","DOI":"10.1128\/jvi.62.7.2502-2504.1988","article-title":"Identification of a neutralizing epitope shared by bluetongue virus serotypes 2 and 13","volume":"62","author":"Ristow","year":"1988","journal-title":"J. Virol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1016\/0042-6822(87)90050-X","article-title":"Identification and characterization of conserved and variable regions in the neutralization VP2 gene of bluetongue virus","volume":"160","author":"Ghiasi","year":"1987","journal-title":"Virology"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/0147-9571(94)90041-8","article-title":"The orbivirus genus. Diversity, structure, replication and phylogenetic relationships","volume":"17","author":"Gould","year":"1994","journal-title":"Comp. Immunol. Microbiol. Infect. Dis."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1016\/0042-6822(83)90346-X","article-title":"Heterogeneity of neutralization-related epitopes within a bluetongue virus serotype","volume":"124","author":"Letchworth","year":"1983","journal-title":"Virology"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/S0165-2427(97)00084-6","article-title":"Antibody responses and protective immunity to recombinant vaccinia virus-expressed bluetongue virus antigens","volume":"59","author":"Lobato","year":"1997","journal-title":"Vet. Immunol. Immunopathol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1051\/vetres:2008023","article-title":"Bluetongue virus: Virology, pathogenesis and immunity","volume":"39","author":"Mertens","year":"2008","journal-title":"Vet. Res."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"11841","DOI":"10.1128\/JVI.01153-10","article-title":"Quantifying antigenic relationships among the lyssaviruses","volume":"84","author":"Horton","year":"2010","journal-title":"J. Virol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1099\/vir.0.057521-0","article-title":"Antigenic variation of foot-and-mouth disease virus serotype A","volume":"95","author":"Ludi","year":"2014","journal-title":"J. Gen. Virol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1089\/vim.1989.2.195","article-title":"In vitro neutralization of antigenic variants of bluetongue virus is related to in vivo protection","volume":"2","author":"Sundin","year":"1989","journal-title":"Viral Immunol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1038\/nsmb.3134","article-title":"Atomic model of a nonenveloped virus reveals pH sensors for a coordinated process of cell entry","volume":"23","author":"Zhang","year":"2016","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"2185","DOI":"10.3390\/v7052185","article-title":"Genetic characterization of the tick-borne orbiviruses","volume":"7","author":"Belaganahalli","year":"2015","journal-title":"Viruses"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/S0034-5288(18)32261-6","article-title":"Clinical and serological response of sheep to serial challenge with different bluetongue virus types","volume":"34","author":"Jeggo","year":"1983","journal-title":"Res. Vet. Sci."},{"key":"ref_73","first-page":"616","article-title":"The use of vaccination in the control of bluetongue in southern Africa","volume":"40","author":"Dungu","year":"2004","journal-title":"Vet. Ital."},{"key":"ref_74","first-page":"631","article-title":"Virological and serological response of sheep following field vaccination with bivalent modified-live vaccine against bluetongue virus serotypes 2 and 9","volume":"40","author":"Savini","year":"2004","journal-title":"Vet. Ital."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"2374","DOI":"10.3390\/v3122374","article-title":"The human antibody response to dengue virus infection","volume":"3","author":"Wahala","year":"2011","journal-title":"Viruses"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"12479","DOI":"10.1073\/pnas.1106568108","article-title":"Ligation of Fc gamma receptor IIB inhibits antibody-dependent enhancement of dengue virus infection","volume":"108","author":"Chan","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_77","first-page":"119","article-title":"Serological differentiation of five bluetongue virus serotypes in indirect ELISA","volume":"59","year":"1992","journal-title":"Onderstepoort J. Vet. Res."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1128\/iai.39.1.208-212.1983","article-title":"Passive protection of mice and sheep against bluetongue virus by a neutralizing monoclonal antibody","volume":"39","author":"Letchworth","year":"1983","journal-title":"Infect. Immun."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1705","DOI":"10.1128\/jcm.25.9.1705-1710.1987","article-title":"Comparison of competitive and indirect enzyme-linked immunosorbent assays for detection of bluetongue virus antibodies in serum and whole blood","volume":"25","author":"Afshar","year":"1987","journal-title":"J. Clin. Microbiol."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/8\/1455\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:35:15Z","timestamp":1760164515000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/8\/1455"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,7,26]]},"references-count":79,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2021,8]]}},"alternative-id":["v13081455"],"URL":"https:\/\/doi.org\/10.3390\/v13081455","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,7,26]]}}}