FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Viruses / African Horse Sickness: A Review of Current Understanding an...
Viruses2019; 11(9); doi: 10.3390/v11090844

African Horse Sickness: A Review of Current Understanding and Vaccine Development.

Abstract: African horse sickness is a devastating disease that causes great suffering and many fatalities amongst horses in sub-Saharan Africa. It is caused by nine different serotypes of the orbivirus African horse sickness virus (AHSV) and it is spread by Culicoid midges. The disease has significant economic consequences for the equine industry both in southern Africa and increasingly further afield as the geographic distribution of the midge vector broadens with global warming and climate change. Live attenuated vaccines (LAV) have been used with relative success for many decades but carry the risk of reversion to virulence and/or genetic re-assortment between outbreak and vaccine strains. Furthermore, the vaccines lack DIVA capacity, the ability to distinguish between vaccine-induced immunity and that induced by natural infection. These concerns have motivated interest in the development of new, more favourable recombinant vaccines that utilize viral vectors or are based on reverse genetics or virus-like particle technologies. This review summarizes the current understanding of AHSV structure and the viral replication cycle and also evaluates existing and potential vaccine strategies that may be applied to prevent or control the disease.
Get Full Text
Publication Date: 2019-09-11 PubMed ID: 31514299PubMed Central: PMC6783979DOI: 10.3390/v11090844Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't
  • Review

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

African horse sickness is an ongoing concern in the horse industry, especially in sub-Saharan Africa, due to its devastating effects and underlying causes. The focus of this research is to provide a summary of the current knowledge about African horse sickness virus (AHSV) and the efforts being put in to develop vaccines to combat the disease.

Understanding African Horse Sickness

  • The research delves into understanding African horse sickness, a severe disease that has been causing significant damage to horses, mainly in sub-Saharan Africa. African horse sickness is a viral infection, caused by nine different serotypes of the orbivirus African horse sickness virus (AHSV).
  • Key factors contributing to the spread of this disease include the Culicoid midges, which are known to spread the disease, and certain climatic changes, particularly global warming, which have led to an expansion in the geographic reach of the midge vectors.
  • The disease not only has a harmful impact on the health of horses, leading to many fatalities, but it also results in major economic ramifications for the equine industry through both its presence in southern Africa and its potential to spread further afield.

Current and Potential Vaccine Strategies

  • This review also delves into the vaccines that have been used to tackle this disease. Historically, Live attenuated vaccines (LAV) have been utilized with a level of success; however, these carry the risk of the virus reverting to virulence or genetic re-assortment between outbreak and vaccine strains.
  • The fact that current vaccines lack DIVA (Differentiating Infected from Vaccinated Animals) capacity, meaning it is impossible to distinguish between animals’ immunity due to vaccination and as a result of natural infection, adds another level of complexity to controlling the disease, and is an area of concern.
  • This necessitated the exploration and development of new vaccine strategies. The paper discusses potential recombinant vaccines that could serve as possible alternatives. Such vaccines would use viral vectors or be based on reverse genetics or virus-like particle technologies, which may prove more efficient in controlling or preventing the disease.

Wrapping Up

  • The paper serves as a comprehensive summary of the understanding of the African horse sickness virus, its effect on horses, specific differences between the nine serotypes of the orbivirus, how the disease is spread, as well as potential new strategies and improvements that could be made to vaccines to control and prevent the spread of the disease.
  • The examination of such aspects signifies the importance of this study, given the health and economic ramifications the disease has on the equine industry, and the potential scope for improvement in its mitigation strategies.

Cite This Article

APA
Dennis SJ, Meyers AE, Hitzeroth II, Rybicki EP. (2019). African Horse Sickness: A Review of Current Understanding and Vaccine Development. Viruses, 11(9). https://doi.org/10.3390/v11090844

Publication

Viruses
ISSN: 1999-4915
NlmUniqueID: 101509722
Country: Switzerland
Language: English
Volume: 11
Issue: 9

Researcher Affiliations

Dennis, Susan J
  • Biopharming Research Unit, Department of Molecular and Cell Biology, University of Cape Town, Rondebosch 7701, Cape Town, South Africa. sue.dennis@uct.ac.za.
Meyers, Ann E
  • Biopharming Research Unit, Department of Molecular and Cell Biology, University of Cape Town, Rondebosch 7701, Cape Town, South Africa. ann.meyers@uct.ac.za.
Hitzeroth, Inga I
  • Biopharming Research Unit, Department of Molecular and Cell Biology, University of Cape Town, Rondebosch 7701, Cape Town, South Africa. inga.hitzeroth@uct.ac.za.
Rybicki, Edward P
  • Biopharming Research Unit, Department of Molecular and Cell Biology, University of Cape Town, Rondebosch 7701, Cape Town, South Africa. ed.rybicki@uct.ac.za.
  • Institute of Infectious Disease and Molecular Medicine, Faculty of Health Sciences, University of Cape Town, Observatory 7925, Cape Town, South Africa. ed.rybicki@uct.ac.za.

MeSH Terms

  • Africa, Southern
  • African Horse Sickness / prevention & control
  • African Horse Sickness Virus / genetics
  • African Horse Sickness Virus / immunology
  • Animals
  • Antibodies, Neutralizing / immunology
  • Antibodies, Viral / immunology
  • Ceratopogonidae / virology
  • Horses
  • Reverse Genetics
  • Vaccines, Attenuated / immunology
  • Vaccines, Synthetic
  • Viral Vaccines / immunology

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 161 references
  1. Mellor P.S., Hamblin C.. African horse sickness. Vet. Res. 2004;35:445–466.
    doi: 10.1051/vetres:2004021pubmed: 15236676google scholar: lookup
  2. Henning M.W. Animal Diseases of South Africa. 3rd ed. Central News Agency Ltd.; Pretoria, Africa: 1956. African Horse Sickness, Perdesiekte, Pestis Equorum; pp. 785–808.
  3. Coetzer J.A.W., Guthrie A.J.. African horse sickness. 2004. pp. 1231–1246.
  4. Vandenbergh S.. The story of a disease: African horsesickness and its direct influence on the necessary development of veterinary science in South Africa c. 1890s–1920s. Historia 2010;55:243–262.
  5. Lubroth J.. African Horsesickness and the epizootic in Spain, 1987. Equine Pract. 1988;10:26–33.
  6. Mirchamsy H., Hazrati A.. A review on etiology and pathogeny of African horse sickness. Arch. Razi Inst. 1973;25:23–46.
  7. Mellor P.. African horse sickness: Transmission and epidemiology. Vet. Res. 1993;24:199–212.
    pubmed: 8102076
  8. Howell P.G.. The 1960 epizootic of African Horsesickness in the Middle East and SW Asia. J. S. Afr. Vet. Assoc. 1960;31:329–334.
  9. De Vos C.J., Hoek C.A., Nodelijk G.. Risk of introducing African horse sickness virus into the Netherlands by international equine movements. Prev. Vet. Med. 2012;106:108–122.
    doi: 10.1016/j.prevetmed.2012.01.019pubmed: 22341773google scholar: lookup
  10. Herholz C., Fussel A.E., Timoney P., Schwermer H., Bruckner L., Leadon D.. Equine travellers to the Olympic Games in Hong Kong 2008: A review of worldwide challenges to equine health, with particular reference to vector-borne diseases. Equine Vet. J. 2008;40:87–95.
    doi: 10.2746/042516408X253136pubmed: 18083666google scholar: lookup
  11. Hopley R., Toth B.. Focus on: African horse sickness. Vet. Rec. 2013;173:13–14.
    doi: 10.1136/vr.f4250pubmed: 23832906google scholar: lookup
  12. M’Fadyean J.. African horse-sickness. J. Comp. Pathol. Ther. 1900;13:1–20.
    doi: 10.1016/S0368-1742(00)80001-6google scholar: lookup
  13. Howell P.G.. The isolation and identification of further antigenic types of African horsesickness virus. Onderstepoort J. Vet. Res. 1962;29:139–149.
  14. McIntosh B.M.. Immunological types of horsesickness virus and their significance in immunization. Onderstepoort J. Vet. Res. 1958;27:465–536.
  15. Calisher C.H., Mertens P.P.. Taxonomy of African horse sickness viruses. 1998.
    pubmed: 9785490
  16. Du Toit R.M.. The transmission of bluetongue and horse sickness by Culicoides. Onderstepoort J. Vet. Sci. Anim. Ind. 1944;19:7–16.
  17. Mellor P.S., Boorman J., Jennings M.. The multiplication of African horse-sickness virus in two species ofCulicoides (Diptera, Ceratopogonidae). Arch. Virol. 1975;47:351–356.
    doi: 10.1007/BF01347976pubmed: 1169931google scholar: lookup
  18. Boorman J., Mellor P.S., Penn M., Jennings M.. The growth of African horse-sickness virus in embryonated hen eggs and the transmission of virus byCulicoides variipennis Coquillett (Diptera, Ceratopogonidae). Arch. Virol. 1975;47:343–349.
    doi: 10.1007/BF01347975pubmed: 1169930google scholar: lookup
  19. Carpenter S., Mellor P.S., Fall A.G., Garros C., Venter G.J.. African Horse Sickness Virus: History, Transmission, and Current Status. Annu. Rev. Entomol. 2017;62:343–358.
    doi: 10.1146/annurev-ento-031616-035010pubmed: 28141961google scholar: lookup
  20. Roy P.. Genetically engineered structure-based vaccine for bluetongue disease. Vet. Ital. 2004;40:594–600.
    pubmed: 20422594
  21. Barnard B.J.H.. Epidemiology of African horse sickness and the role of the zebra in South Africa. 1998. pp. 13–19.
    pubmed: 9785491
  22. Theiler A.. The susceptibility of the dog to african horse-sickness. J. Comp. Pathol. Ther. 1910;23:315–325.
    doi: 10.1016/S0368-1742(10)80058-Xgoogle scholar: lookup
  23. McIntosh B.M.. Horsesickness antibodies in the sera of dogs in enzootic areas. J. S. Afr. Vet. Assoc. 1955;26:269–272.
  24. Oellermann R., Els H., Erasmus B.. Characterization of African horsesiekness virus. Arch. Fur Die Gesamte Virusforsch. 1970;29:163–174.
    doi: 10.1007/BF01249302pubmed: 4193496google scholar: lookup
  25. Coetzer J.A.W., Erasmus B.J.. African Horse Sickness. 1994. pp. 460–475.
  26. Grubman M.J., Lewis S.A.. Identification and characterization of the structural and nonstructural proteins of African horsesickness virus and determination of the genome coding assignments. Virology 1992;186:444–451.
    doi: 10.1016/0042-6822(92)90009-Epubmed: 1531096google scholar: lookup
  27. Bremer C.W.. A gel electrophoretic study of the protein and nucleic acid components of African horsesickness virus. Onderstepoort J. Vet. Res. 1976;43:193–199.
    pubmed: 1023091
  28. Bremer C.W., Huismans H., Van Dijk A.A.. Characterization and cloning of the African horsesickness virus genome. J. Gen. Virol. 1990;71:793–799.
    doi: 10.1099/0022-1317-71-4-793pubmed: 2324709google scholar: lookup
  29. Roy P., Mertens P.P., Casal I.. African horse sickness virus structure. Comp. Immunol. Microbiol. Infect. Dis. 1994;17:243–273.
    doi: 10.1016/0147-9571(94)90046-9pubmed: 8001348google scholar: lookup
  30. Zhang X., Patel A., Celma C.C., Yu X., Roy P., Zhou Z.H.. Atomic model of a nonenveloped virus reveals pH sensors for a coordinated process of cell entry. Nat. Struct. Mol. Biol. 2016;23:74–80.
    doi: 10.1038/nsmb.3134pmc: PMC5669276pubmed: 26641711google scholar: lookup
  31. Grimes J.M., Burroughs J.N., Gouet P., Diprose J.M., Malby R., Zientara S., Mertens P.P.C., Stuart D.I.. The atomic structure of the bluetongue virus core. Nature 1998;395:470–478.
    doi: 10.1038/26694pubmed: 9774103google scholar: lookup
  32. Zhang X., Boyce M., Bhattacharya B., Zhang X., Schein S., Roy P., Zhou Z.H.. Bluetongue virus coat protein VP2 contains sialic acid-binding domains, and VP5 resembles enveloped virus fusion proteins. Proc. Natl. Acad. Sci. USA 2010;107:6292–6297.
    doi: 10.1073/pnas.0913403107pmc: PMC2852009pubmed: 20332209google scholar: lookup
  33. Nason E.L., Rothagel R., Mukherjee S.K., Kar A.K., Forzan M., Prasad B.V., Roy P.. Interactions between the inner and outer capsids of bluetongue virus. J. Virol. 2004;78:8059–8067.
    doi: 10.1128/JVI.78.15.8059-8067.2004pmc: PMC446137pubmed: 15254177google scholar: lookup
  34. Roy P.. Bluetongue virus structure and assembly. Curr. Opin. Virol. 2017;24:115–123.
    doi: 10.1016/j.coviro.2017.05.003pubmed: 28609677google scholar: lookup
  35. Iwata H., Yamagaw M., Roy P.. Evolutionary relationships among the gnat-transmitted orbiviruses that cause African horse sickness, bluetongue, and epizootic hemorrhagic disease as evidenced by their capsid protein sequences. Virology 1992;191:251–261.
    doi: 10.1016/0042-6822(92)90187-Tpubmed: 1329319google scholar: lookup
  36. Caspar D.L.D., Klug A.. Physical principles in the construction of regular viruses. Cold Spring Harb. Symp. Quant. Biol. 1962;27:1–24.
    doi: 10.1101/SQB.1962.027.001.005pubmed: 14019094google scholar: lookup
  37. Stuart D.I., Gouet P., Grimes J., Malby R., Diprose J., Zientara S., Burroughs J.N., Mertens P.P.. Structural studies of orbivirus particles. Arch. Virol. Suppl. 1998;14:235–250.
    pubmed: 9785510
  38. Manole V., Laurinmaki P., Van Wyngaardt W., Potgieter C.A., Wright I.M., Venter G.J., van Dijk A.A., Sewell B.T., Butcher S.J.. Structural insight into African horsesickness virus infection. J. Virol. 2012;86:7858–7866.
    doi: 10.1128/JVI.00517-12pmc: PMC3421665pubmed: 22593166google scholar: lookup
  39. Gouet P., Diprose J.M., Grimes J.M., Malby R., Burroughs J.N., Zientara S., Stuart D.I., Mertens P.P.. The highly ordered double-stranded RNA genome of bluetongue virus revealed by crystallography. Cell 1999;97:481–490.
    doi: 10.1016/S0092-8674(00)80758-8pubmed: 10338212google scholar: lookup
  40. Stuart D., Grimes J.. Structural Studies on Orbivirus Proteins and Particles. 2006. pp. 221–244.
    pubmed: 16909901
  41. Chuma T., Le Blois H., Sanchez-Vizcaino J.M., Diaz-Laviada M., Roy P.. Expression of the major core antigen VP7 of African horsesickness virus by a recombinant baculovirus and its use as a group-specific diagnostic reagent. J. Gen. Virol. 1992;73:925–931.
    doi: 10.1099/0022-1317-73-4-925pubmed: 1378881google scholar: lookup
  42. Grimes J., Basak A.K., Roy P., Stuart D.. The crystal structure of bluetongue virus VP7. Nature 1995;373:167.
    doi: 10.1038/373167a0pubmed: 7816101google scholar: lookup
  43. Basak A.K., Gouet P., Grimes J., Roy P., Stuart D.. Crystal structure of the top domain of African horse sickness virus VP7: Comparisons with bluetongue virus VP7. J. Virol. 1996;70:3797–3806.
    pmc: PMC190256pubmed: 8648715
  44. Grimes J.M., Jakana J., Ghosh M., Basak A.K., Roy P., Chiu W., Stuart D.I., Prasad B.V.V.. An atomic model of the outer layer of the bluetongue virus core derived from X-ray crystallography and electron cryomicroscopy. Structure 1997;5:885–893.
    doi: 10.1016/S0969-2126(97)00243-8pubmed: 9261080google scholar: lookup
  45. Roy P., Noad R.. Bluetongue Virus Assembly and Morphogenesis. 2006. pp. 87–116.
    pubmed: 16909898
  46. Limn C.-K., Staeuber N., Monastyrskaya K., Gouet P., Roy P.. Functional dissection of the major structural protein of bluetongue virus: Identification of key residues within VP7 essential for capsid assembly. J. Virol. 2000;74:8658–8669.
    doi: 10.1128/JVI.74.18.8658-8669.2000pmc: PMC116377pubmed: 10954567google scholar: lookup
  47. Roy P., Hirasawa T., Fernandez M., Blinov V.M., Rodrique S.-V.J.M.. The complete sequence of the group-specific antigen, VP7, of African horsesickness disease virus serotype 4 reveals a close relationship to bluetongue virus. J. Gen. Virol. 1991;72:1237–1241.
    doi: 10.1099/0022-1317-72-6-1237pubmed: 1646273google scholar: lookup
  48. Burroughs J.N., O’Hara R.S., Smale C.J., Hamblin C., Walton A., Armstrong R., Mertens P.P.. Purification and properties of virus particles, infectious subviral particles, cores and VP7 crystals of African horsesickness virus serotype 9. J. Gen. Virol. 1994;75:1849–1857.
    doi: 10.1099/0022-1317-75-8-1849pubmed: 8046387google scholar: lookup
  49. Burrage T.G., Trevejo R., Stone-Marschat M., Laegreid W.W.. Neutralizing epitopes of African horsesickness virus serotype 4 are located on VP2. Virology 1993;196:799–803.
    doi: 10.1006/viro.1993.1537pubmed: 7690505google scholar: lookup
  50. Hewat E.A., Booth T.F., Roy P.. Structure of bluetongue virus particles by cryoelectron microscopy. J. Struct. Biol. 1992;109:61–69.
    doi: 10.1016/1047-8477(92)90068-Lpubmed: 1337461google scholar: lookup
  51. Boyce M., Celma C.P., Roy P.. Bluetongue virus non-structural protein 1 is a positive regulator of viral protein synthesis. Virol. J. 2012;9:178.
    doi: 10.1186/1743-422X-9-178pmc: PMC3479040pubmed: 22931514google scholar: lookup
  52. Van Staden V., Theron J., Greyling B., Huismans H., Nel L.. A comparison of the nucleotide sequences of cognate NS2 genes of three different orbiviruses. Virology 1991;185:500–504.
    doi: 10.1016/0042-6822(91)90808-Opubmed: 1656603google scholar: lookup
  53. Patel A., Roy P.. The molecular biology of Bluetongue virus replication. Virus Res. 2014;182:5–20.
    doi: 10.1016/j.virusres.2013.12.017pmc: PMC7162684pubmed: 24370866google scholar: lookup
  54. Quan M., Van Vuuren M., Howell P.G., Groenewald D., Guthrie A.J.. Molecular epidemiology of the African horse sickness virus S10 gene. J. Gen. Virol. 2008;89:1159–1168.
    doi: 10.1099/vir.0.83502-0pubmed: 18420793google scholar: lookup
  55. Celma C.C.P., Roy P.. Interaction of calpactin light chain (S100A10/p11) and a viral NS protein is essential for intracellular trafficking of non-enveloped Bluetongue virus. J. Virol. 2011;85:4783–4791.
    doi: 10.1128/JVI.02352-10pmc: PMC3126219pubmed: 21411520google scholar: lookup
  56. Zwart L., Potgieter C.A., Clift S.J., van Staden V.. Characterising Non-Structural Protein NS4 of African Horse Sickness Virus. PLoS ONE 2015;10:e0124281.
    doi: 10.1371/journal.pone.0124281pmc: PMC4411093pubmed: 25915516google scholar: lookup
  57. Ratinier M., Caporale M., Golder M., Franzoni G., Allan K., Nunes S.F., Armezzani A., Bayoumy A., Rixon F., Shaw A.. Identification and characterization of a novel non-structural protein of bluetongue virus. PLoS Pathog. 2011;7:e1002477.
    doi: 10.1371/journal.ppat.1002477pmc: PMC3248566pubmed: 22241985google scholar: lookup
  58. Hassan S.H., Wirblich C., Forzan M., Roy P.. Expression and functional characterization of bluetongue virus VP5 protein: Role in cellular permeabilization. J. Virol. 2001;75:8356–8367.
    doi: 10.1128/JVI.75.18.8356-8367.2001pmc: PMC115081pubmed: 11507181google scholar: lookup
  59. Mecham J.O., McHolland L.E.. Measurement of bluetongue virus binding to a mammalian cell surface receptor by an in situ immune fluorescent staining technique. J. Virol. Methods 2010;165:112–115.
    doi: 10.1016/j.jviromet.2009.12.011pubmed: 20026123google scholar: lookup
  60. Stevens L.M., Moffat K., Cooke L., Nomikou K., Mertens P.P.C., Jackson T., Darpel K.E.. A low-passage insect-cell isolate of bluetongue virus uses a macropinocytosis-like entry pathway to infect natural target cells derived from the bovine host. J. Gen. Virol. 2019;100:568–582.
    doi: 10.1099/jgv.0.001240pubmed: 30843784google scholar: lookup
  61. Eaton B.T., Crameri G.S.. The Site of Bluetongue Virus Attachment to Glycophorins from a Number of Animal Erythrocytes. J. Gen. Virol. 1989;70:3347–3353.
    doi: 10.1099/0022-1317-70-12-3347pubmed: 2558161google scholar: lookup
  62. Hassan S.S., Roy P.. Expression and Functional Characterization of Bluetongue Virus VP2 Protein: Role in Cell Entry. J. Virol. 1999;73:9832.
    pmc: PMC113032pubmed: 10559295
  63. Marchi P.R., Rawlings P., Burroughs J.N., Wellby M., Mertens P.P.C., Mellor P.S., Wade-Evans A.M.. Proteolytic cleavage of VP2, an outer capsid protein of African horse sickness virus, by species-specific serum proteases enhances infectivity in Culicoides. J. Gen. Virol. 1995;76:2607–2611.
    doi: 10.1099/0022-1317-76-10-2607pubmed: 7595366google scholar: lookup
  64. Forzan M., Marsh M., Roy P.. Bluetongue virus entry into cells. J. Virol. 2007;81:4819–4827.
    doi: 10.1128/JVI.02284-06pmc: PMC1900141pubmed: 17267479google scholar: lookup
  65. Forzan M., Wirblich C., Roy P.. A capsid protein of nonenveloped Bluetongue virus exhibits membrane fusion activity. Proc. Natl. Acad. Sci. USA 2004;101:2100–2105.
    doi: 10.1073/pnas.0306448101pmc: PMC357058pubmed: 14762165google scholar: lookup
  66. Boyce M., Wehrfritz J., Noad R., Roy P.. Purified recombinant bluetongue virus VP1 exhibits RNA replicase activity. J. Virol. 2004;78:3994–4002.
    doi: 10.1128/JVI.78.8.3994-4002.2004pmc: PMC374272pubmed: 15047815google scholar: lookup
  67. Ramadevi N., Burroughs N.J., Mertens P.P.C., Jones I.M., Roy P.. Capping and methylation of mRNA by purified recombinant VP4 protein of bluetongue virus. Proc. Natl. Acad. Sci. USA 1998;95:13537–13542.
    doi: 10.1073/pnas.95.23.13537pmc: PMC24854pubmed: 9811835google scholar: lookup
  68. Kar A.K., Bhattacharya B., Roy P.. Bluetongue virus RNA binding protein NS2 is a modulator of viral replication and assembly. BMC Mol. Biol. 2007;8:4.
    doi: 10.1186/1471-2199-8-4pmc: PMC1794256pubmed: 17241458google scholar: lookup
  69. Modrof J., Lymperopoulos K., Roy P.. Phosphorylation of bluetongue virus nonstructural protein 2 is essential for formation of viral inclusion bodies. J. Virol. 2005;79:10023–10031.
    doi: 10.1128/JVI.79.15.10023-10031.2005pmc: PMC1181561pubmed: 16014962google scholar: lookup
  70. Mohl B.-P., Roy P.. Cellular casein kinase 2 and protein phosphatase 2A modulate replication site assembly of bluetongue virus. J. Biol. Chem. 2016;291:14566–14574.
    doi: 10.1074/jbc.M116.714766pmc: PMC4938178pubmed: 27226558google scholar: lookup
  71. Beaton A.R., Rodriguez J., Reddy Y.K., Roy P.. The membrane trafficking protein calpactin forms a complex with bluetongue virus protein NS3 and mediates virus release. Proc. Natl. Acad. Sci. USA 2002;99:13154–13159.
    doi: 10.1073/pnas.192432299pmc: PMC130602pubmed: 12235365google scholar: lookup
  72. Celma C.C.P., Roy P.. A viral nonstructural protein regulates bluetongue virus trafficking and release. J. Virol. 2009;83:6806–6816.
    doi: 10.1128/JVI.00263-09pmc: PMC2698550pubmed: 19369335google scholar: lookup
  73. Venter E., Van der Merwe C.F., Buys A.V., Huismans H., Van Staden V.. Comparative ultrastructural characterization of African horse sickness virus-infected mammalian and insect cells reveals a novel potential virus release mechanism from insect cells. J. Gen. Virol. 2014;95:642–651.
    doi: 10.1099/vir.0.060400-0pubmed: 24347494google scholar: lookup
  74. Mertens P.P.C., Burroughs J.N., Walton A., Wellby M.P., Fu H., O’Hara R.S., Brookes S.M., Mellor P.S.. Enhanced infectivity of modified bluetongue virus particles for two insect cell lines and for TwoCulicoidesVector species. Virology 1996;217:582–593.
    doi: 10.1006/viro.1996.0153pubmed: 8610450google scholar: lookup
  75. Ruoslahti E.. Rgd and Other Recognition Sequences for Integrins. Annu. Rev. Cell Dev. Biol. 1996;12:697–715.
    doi: 10.1146/annurev.cellbio.12.1.697pubmed: 8970741google scholar: lookup
  76. Burrage T.G., Laegreid W.W.. African horsesickness: Pathogenesis and immunity. Comp. Immunol. Microbiol. Infect. Dis. 1994;17:275–285.
    doi: 10.1016/0147-9571(94)90047-7pubmed: 8001349google scholar: lookup
  77. Wohlsein P., Pohlenz J.F., Davidson F.L., Salt J.S., Hamblin C.. Immunohistochemical demonstration of African horse sickness viral antigen in formalin-fixed equine tissues. Vet. Pathol. 1997;34:568–574.
    doi: 10.1177/030098589703400604pubmed: 9396137google scholar: lookup
  78. Erasmus B.. A new Approach to Polyvalent Immunization Against African Horsesickness. 1978. pp. 401–403.
  79. Erasmus B.J.. The Pathogenesis of African Horsesickness. 1974. pp. 1–11.
  80. Alexander R.A.. Studies on the neurotropic virus of horsesickness III: The intracerebral protection test and its application to the study of immunity. Onderstepoort J. Vet. Sci. Anim. Ind. 1935;4:349–377.
  81. Bentley L., Fehrsen J., Jordaan F., Huismans H., Du Plessis D.H.. Identification of antigenic regions on VP2 of African horsesickness virus serotype 3 by using phage-displayed epitope libraries. J. Gen. Virol. 2000;81:993–1000.
    doi: 10.1099/0022-1317-81-4-993pubmed: 10725425google scholar: lookup
  82. Mathebula E.M., Faber F.E., van Wyngaardt W., van Schalkwyk A., Pretorius A., Fehrsen J.. B-cell epitopes of African horse sickness virus serotype 4 recognised by immune horse sera. Onderstepoort J. Vet. Res. 2017;84:1–12.
    doi: 10.4102/ojvr.v84i1.1313pmc: PMC6238682pubmed: 28281773google scholar: lookup
  83. Martinez-Torrecuadrada J.L., Langeveld J.P., Meloen R.H., Casal J.I.. Definition of neutralizing sites on African horse sickness virus serotype 4 VP2 at the level of peptides. J. Gen. Virol. 2001;82:2415–2424.
    doi: 10.1099/0022-1317-82-10-2415pubmed: 11562535google scholar: lookup
  84. Venter M., Napier G., Huismans H.. Cloning, sequencing and expression of the gene that encodes the major neutralisation-specific antigen of African horsesickness virus serotype 9. J. Virol. Methods 2000;86:41–53.
    doi: 10.1016/S0166-0934(99)00176-7pubmed: 10713375google scholar: lookup
  85. De la Poza F., Marin-Lopez A., Castillo-Olivares J., Calvo-Pinilla E., Ortego J.. Identification of CD8 T cell epitopes in VP2 and NS1 proteins of African horse sickness virus in IFNAR(-/-) mice. Virus Res. 2015;210:149–153.
    doi: 10.1016/j.virusres.2015.08.005pubmed: 26272673google scholar: lookup
  86. El Garch H., Crafford J.E., Amouyal P., Durand P.Y., Edlund Toulemonde C., Lemaitre L., Cozette V., Guthrie A., Minke J.M.. An African horse sickness virus serotype 4 recombinant canarypox virus vaccine elicits specific cell-mediated immune responses in horses. Vet. Immunol. Immunopathol. 2012;149:76–85.
    doi: 10.1016/j.vetimm.2012.06.009pubmed: 22763149google scholar: lookup
  87. Pretorius A., Van Kleef M., Van Wyngaardt W., Heath J.. Virus-specific CD8+ T-cells detected in PBMC from horses vaccinated against African horse sickness virus. Vet. Immunol. Immunopathol. 2012;146:81–86.
    doi: 10.1016/j.vetimm.2012.01.016pubmed: 22365333google scholar: lookup
  88. Weyer C.T., Grewar J.D., Burger P., Rossouw E., Lourens C., Joone C., le Grange M., Coetzee P., Venter E., Martin D.P.. African Horse Sickness Caused by Genome Reassortment and Reversion to Virulence of Live, Attenuated Vaccine Viruses, South Africa, 2004–2014. Emerg. Infect. Dis. 2016;22:2087–2096.
    doi: 10.3201/eid2212.160718pmc: PMC5189153pubmed: 27442883google scholar: lookup
  89. Weyer C.T.. African Horse Sickness Outbreak Investigation and Disease Surveillance Using Molecular Techniques. 2017.
  90. Sailleau C., Hamblin C., Paweska J., Zientara S.. 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. 2000;81:831–837.
    doi: 10.1099/0022-1317-81-3-831pubmed: 10675421google scholar: lookup
  91. Maree S., Paweska J.T.. Preparation of recombinant African horse sickness virus VP7 antigen via a simple method and validation of a VP7-based indirect ELISA for the detection of group-specific IgG antibodies in horse sera. J. Virol. Methods 2005;125:55–65.
    doi: 10.1016/j.jviromet.2004.12.002pubmed: 15737417google scholar: lookup
  92. Weyer C.T., Joone C., Lourens C.W., Monyai M.S., Koekemoer O., Grewar J.D., van Schalkwyk A., Majiwa P.O., MacLachlan N.J., Guthrie A.J.. Development of three triplex real-time reverse transcription PCR assays for the qualitative molecular typing of the nine serotypes of African horse sickness virus. J. Virol. Methods 2015;223:69–74.
    doi: 10.1016/j.jviromet.2015.07.015pubmed: 26232526google scholar: lookup
  93. Agüero M., Gomez-Tejedor C., Cubillo Á.M., Rubio C., Romero E., Jiménez-Clavero M.A.. Real-time fluorogenic reverse transcription polymerase chain reaction assay for detection of African horse sickness virus. J. Vet. Diagn. Investig. 2008;20:325–328.
    doi: 10.1177/104063870802000310pubmed: 18460619google scholar: lookup
  94. Guthrie A.J., MacLachlan N.J., Joone C., Lourens C.W., Weyer C.T., Quan M., Monyai M.S., Gardner I.A.. Diagnostic accuracy of a duplex real-time reverse transcription quantitative PCR assay for detection of African horse sickness virus. J. Virol. Methods 2013;189:30–35.
    doi: 10.1016/j.jviromet.2012.12.014pubmed: 23291102google scholar: lookup
  95. Quan M., Lourens C.W., MacLachlan N.J., Gardner I.A., Guthrie A.J.. Development and optimisation of a duplex real-time reverse transcription quantitative PCR assay targeting the VP7 and NS2 genes of African horse sickness virus. J. Virol. Methods 2010;167:45–52.
    doi: 10.1016/j.jviromet.2010.03.009pubmed: 20304015google scholar: lookup
  96. Rodriguez-Sanchez B., Fernandez-Pinero J., Sailleau C., Zientara S., Belak S., Arias M., Sanchez-Vizcaino J.M.. Novel gel-based and real-time PCR assays for the improved detection of African horse sickness virus. J. Virol. Methods 2008;151:87–94.
    doi: 10.1016/j.jviromet.2008.03.029pubmed: 18501973google scholar: lookup
  97. OIE. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. 2018.
  98. Koekemoer J.J.O.. Serotype-specific detection of African horsesickness virus by real-time PCR and the influence of genetic variations. J. Virol. Methods 2008;154:104–110.
    doi: 10.1016/j.jviromet.2008.08.010pubmed: 18793672google scholar: lookup
  99. Bachanek-Bankowska K., Maan S., Castillo-Olivares J., Manning N.M., Maan N.S., Potgieter A.C., Di Nardo A., Sutton G., Batten C., Mertens P.P.. Real time RT-PCR assays for detection and typing of African horse sickness virus. PLoS ONE 2014;9:e93758.
    doi: 10.1371/journal.pone.0093758pmc: PMC3983086pubmed: 24721971google scholar: lookup
  100. Meiswinkel R., Baylis M., Labuschagne K.. Stabling and the protection of horses from Culicoides bolitinos (Diptera: Ceratopogonidae), a recently identified vector of African horse sickness. Bull. Entomol. Res. 2000;90:509–515.
    doi: 10.1017/S0007485300000626pubmed: 11107252google scholar: lookup
  101. Alexander R.A.. The immunization of horses and mules against Horse Sickness by means of the neurotropic virus of mice and guinea-pigs. Onderstepoort J. Vet. Sci Anim Ind. 1934;2:375–391.
  102. Erasmus B.J.. Cultivation of horsesickness virus in tissue culture. Nature 1963;200:716.
    doi: 10.1038/200716a0pubmed: 14109987google scholar: lookup
  103. Von Teichman B.F., Smit T.K.. Evaluation of the pathogenicity of African Horsesickness (AHS) isolates in vaccinated animals. Vaccine 2008;26:5014–5021.
    doi: 10.1016/j.vaccine.2008.07.037pubmed: 18682269google scholar: lookup
  104. Von Teichman B.F., Dungu B., Smit T.K.. In vivo cross-protection to African horse sickness Serotypes 5 and 9 after vaccination with Serotypes 8 and 6. Vaccine 2010;28:6505–6517.
    doi: 10.1016/j.vaccine.2010.06.105pubmed: 20638456google scholar: lookup
  105. Molini U., Marucchella G., Maseke A., Ronchi G.F., Di Ventura M., Salini R., Scacchia M., Pini A.. Immunization of horses with a polyvalent live-attenuated African horse sickness vaccine: Serological response and disease occurrence under field conditions. Trials Vaccinol. 2015;4:24–28.
    doi: 10.1016/j.trivac.2015.03.001google scholar: lookup
  106. Weyer C.T., Grewar J.D., Burger P., Joone C., Lourens C., MacLachlan N.J., Guthrie A.J.. Dynamics of African horse sickness virus nucleic acid and antibody in horses following immunization with a commercial polyvalent live attenuated vaccine. Vaccine 2017;35:2504–2510.
    doi: 10.1016/j.vaccine.2017.03.005pubmed: 28341113google scholar: lookup
  107. Mirchamsy H., Taslimi H.. Inactivated African horse sickness virus cell culture vaccine. Immunology 1968;14:81.
    pmc: PMC1409248pubmed: 5635756
  108. Weyer C.T., Quan M., Joone C., Lourens C.W., MacLachlan N.J., Guthrie A.J.. African horse sickness in naturally infected, immunised horses. Equine Vet. J. 2013;45:117–119.
    doi: 10.1111/j.2042-3306.2012.00590.xpubmed: 22612775google scholar: lookup
  109. Lelli R., Molini U., Ronchi G.F., Rossi E., Franchi P., Ulisse S., Armillotta G., Capista S., Khaiseb S., Di Ventura M.. Inactivated and adjuvanted vaccine for the control of the African horse sickness virus serotype 9 infection: Evaluation of efficacy in horses and guinea-pig model. Vet. Ital. 2013;49:89–98.
    pubmed: 23564590
  110. Erasmus B.J.. Preliminary observations on the value of the guinea-pig in determining the innocuity and antigenicity of neurotropic attenuated horsesickness strains. Onderstepoort J. Vet. Res. 1963;30:11–22.
  111. Romito M., Du Plessis D.H., Viljoen G.J.. Immune responses in a horse inoculated with the VP2 gene of African horsesickness virus. Onderstepoort J. Vet. Res. 1999;66:139–144.
    pubmed: 10486832
  112. Roy P., Bishop D.H., Howard S., Aitchison H., Erasmus B.. Recombinant baculovirus-synthesized African horsesickness virus (AHSV) outer-capsid protein VP2 provides protection against virulent AHSV challenge. J. Gen. Virol. 1996;77:2053–2057.
    doi: 10.1099/0022-1317-77-9-2053pubmed: 8811002google scholar: lookup
  113. Martinez-Torrecuadrada J.L., Diaz-Laviada M., Roy P., Sanchez C., Vela C., Sanchez-Vizcaino J.M., Casal J.I.. Full protection against African horsesickness (AHS) in horses induced by baculovirus-derived AHS virus serotype 4 VP2, VP5 and VP7. J. Gen. Virol. 1996;77:1211–1221.
    doi: 10.1099/0022-1317-77-6-1211pubmed: 8683209google scholar: lookup
  114. Kanai Y., van Rijn P.A., Maris-Veldhuis M., Kaname Y., Athmaram T.N., Roy P.. Immunogenicity of recombinant VP2 proteins of all nine serotypes of African horse sickness virus. Vaccine 2014;32:4932–4937.
    doi: 10.1016/j.vaccine.2014.07.031pmc: PMC4148702pubmed: 25045805google scholar: lookup
  115. Du Plessis M., Cloete M., Aitchison H., Van Dijk A.A.. Protein aggregation complicates the development of baculovirus-expressed African horsesickness virus serotype 5 VP2 subunit vaccines. Onderstepoort J. Vet. Res. 1998;65:321–329.
    pubmed: 10192846
  116. Scanlen M., Paweska J.T., Verschoor J.A., van Dijk A.A.. The protective efficacy of a recombinant VP2-based African horsesickness subunit vaccine candidate is determined by adjuvant. Vaccine 2002;20:1079–1088.
    doi: 10.1016/S0264-410X(01)00445-5pubmed: 11803068google scholar: lookup
  117. Guthrie A.J., Quan M., Lourens C.W., Audonnet J.C., Minke J.M., Yao J., He L., Nordgren R., Gardner I.A., Maclachlan N.J.. Protective immunization of horses with a recombinant canarypox virus vectored vaccine co-expressing genes encoding the outer capsid proteins of African horse sickness virus. Vaccine 2009;27:4434–4438.
    doi: 10.1016/j.vaccine.2009.05.044pubmed: 19490959google scholar: lookup
  118. Calvo-Pinilla E., Casanova I., Bachanek-Bankowska K., Chiam R., Maan S., Nieto J.M., Ortego J., Mertens P.P.C., Castillo-Olivares J.. A modified vaccinia Ankara virus (MVA) vaccine expressing African horse sickness virus (AHSV) VP2 protects against AHSV challenge in an IFNAR -/- mouse model. PLoS ONE 2011;6:e16503.
    pmc: PMC3027694pubmed: 21298069
  119. Manning N.M., Bachanek-Bankowska K., Mertens P.P.C., Castillo-Olivares J.. Vaccination with recombinant Modified Vaccinia Ankara (MVA) viruses expressing single African horse sickness virus VP2 antigens induced cross-reactive virus neutralising antibodies (VNAb) in horses when administered in combination. Vaccine 2017;35:6024–6029.
    doi: 10.1016/j.vaccine.2017.04.005pubmed: 28438410google scholar: lookup
  120. Alberca B., Bachanek-Bankowska K., Cabana M., Calvo-Pinilla E., Viaplana E., Frost L., Gubbins S., Urniza A., Mertens P., Castillo-Olivares J.. Vaccination of horses with a recombinant modified vaccinia Ankara virus (MVA) expressing African horse sickness (AHS) virus major capsid protein VP2 provides complete clinical protection against challenge. Vaccine 2014;32:3670–3674.
    doi: 10.1016/j.vaccine.2014.04.036pmc: PMC4061461pubmed: 24837765google scholar: lookup
  121. Chiam R., Sharp E., Maan S., Rao S., Mertens P., Blacklaws B., Davis-Poynter N., Wood J., Castillo-Olivares J.. Induction of antibody responses to African horse sickness virus (AHSV) in ponies after vaccination with recombinant modified vaccinia Ankara (MVA). PLoS ONE 2009;4:e5997.
    doi: 10.1371/journal.pone.0005997pmc: PMC2694985pubmed: 19543394google scholar: lookup
  122. Calvo-Pinilla E., Gubbins S., Mertens P., Ortego J., Castillo-Olivares J.. The immunogenicity of recombinant vaccines based on modified Vaccinia Ankara (MVA) viruses expressing African horse sickness virus VP2 antigens depends on the levels of expressed VP2 protein delivered to the host. Antivir. Res. 2018;154:132–139.
    doi: 10.1016/j.antiviral.2018.04.015pmc: PMC5966619pubmed: 29678552google scholar: lookup
  123. Calvo-Pinilla E., de la Poza F., Gubbins S., Mertens P.P., Ortego J., Castillo-Olivares J.. Vaccination of mice with a modified Vaccinia Ankara (MVA) virus expressing the African horse sickness virus (AHSV) capsid protein VP2 induces virus neutralising antibodies that confer protection against AHSV upon passive immunisation. Virus Res. 2014;180:23–30.
    doi: 10.1016/j.virusres.2013.12.002pubmed: 24333835google scholar: lookup
  124. Gilbert S.C.. Clinical development of Modified Vaccinia virus Ankara vaccines. Vaccine 2013;31:4241–4246.
    doi: 10.1016/j.vaccine.2013.03.020pubmed: 23523410google scholar: lookup
  125. Cottingham M.G., Carroll M.W.. Recombinant MVA vaccines: Dispelling the myths. Vaccine 2013;31:4247–4251.
    doi: 10.1016/j.vaccine.2013.03.021pubmed: 23523407google scholar: lookup
  126. Calvo-Pinilla E., de la Poza F., Gubbins S., Mertens P.P., Ortego J., Castillo-Olivares J.. Antiserum from mice vaccinated with modified vaccinia Ankara virus expressing African horse sickness virus (AHSV) VP2 provides protection when it is administered 48h before, or 48h after challenge. Antivir. Res. 2015;116:27–33.
    doi: 10.1016/j.antiviral.2015.01.009pmc: PMC7125940pubmed: 25643968google scholar: lookup
  127. Lulla V., Lulla A., Wernike K., Aebischer A., Beer M., Roy P.. Assembly of Replication-Incompetent African Horse Sickness Virus Particles: Rational Design of Vaccines for All Serotypes. J. Virol. 2016;90:7405–7414.
    doi: 10.1128/JVI.00548-16pmc: PMC4984648pubmed: 27279609google scholar: lookup
  128. Vermaak E., Paterson D.J., Conradie A., Theron J.. Directed genetic modification of African horse sickness virus by reverse genetics. S. Afr. J. Sci. 2015;111:1–8.
    doi: 10.17159/sajs.2015/20140331google scholar: lookup
  129. Van de Water S.G., van Gennip R.G., Potgieter C.A., Wright I.M., van Rijn P.A.. VP2 Exchange and NS3/NS3a Deletion in African Horse Sickness Virus (AHSV) in Development of Disabled Infectious Single Animal Vaccine Candidates for AHSV. J. Virol. 2015;89:8764–8772.
    doi: 10.1128/JVI.01052-15pmc: PMC4524073pubmed: 26063433google scholar: lookup
  130. Kaname Y., Celma C.C., Kanai Y., Roy P.. Recovery of African horse sickness virus from synthetic RNA. J. Gen. Virol. 2013;94:2259–2265.
    doi: 10.1099/vir.0.055905-0pubmed: 23860489google scholar: lookup
  131. Lulla V., Losada A., Lecollinet S., Kerviel A., Lilin T., Sailleau C., Beck C., Zientara S., Roy P.. Protective efficacy of multivalent replication-abortive vaccine strains in horses against African horse sickness virus challenge. Vaccine 2017;35:4262–4269.
    doi: 10.1016/j.vaccine.2017.06.023pmc: PMC5518735pubmed: 28625521google scholar: lookup
  132. Van Rijn P.A., Maris-Veldhuis M.A., Potgieter C.A., van Gennip R.G.P.. African horse sickness virus (AHSV) with a deletion of 77 amino acids in NS3/NS3a protein is not virulent and a safe promising AHS Disabled Infectious Single Animal (DISA) vaccine platform. Vaccine 2018;36:1925–1933.
    doi: 10.1016/j.vaccine.2018.03.003pubmed: 29525278google scholar: lookup
  133. Boyce M., Celma C.C.P., Roy P.. Development of reverse genetics systems for bluetongue virus: Recovery of infectious virus from synthetic RNA transcripts. J. Virol. 2008;82:8339–8348.
    doi: 10.1128/JVI.00808-08pmc: PMC2519640pubmed: 18562540google scholar: lookup
  134. Van Rijn P.A., van de Water S.G., Feenstra F., van Gennip R.G.. Requirements and comparative analysis of reverse genetics for bluetongue virus (BTV) and African horse sickness virus (AHSV). Virol. J. 2016;13:119.
    doi: 10.1186/s12985-016-0574-7pmc: PMC4930614pubmed: 27368544google scholar: lookup
  135. Feenstra F., Pap J.S., van Rijn P.A.. Application of bluetongue Disabled Infectious Single Animal (DISA) vaccine for different serotypes by VP2 exchange or incorporation of chimeric VP2. Vaccine 2015;33:812–818.
    doi: 10.1016/j.vaccine.2014.12.003pubmed: 25510389google scholar: lookup
  136. Conradie A.M., Stassen L., Huismans H., Potgieter C.A., Theron J.. Establishment of different plasmid only-based reverse genetics systems for the recovery of African horse sickness virus. Virology 2016;499:144–155.
    doi: 10.1016/j.virol.2016.07.010pmc: PMC7172382pubmed: 27657835google scholar: lookup
  137. Matsuo E., Celma C.C., Roy P.. A reverse genetics system of African horse sickness virus reveals existence of primary replication. FEBS Lett. 2010;584:3386–3391.
    doi: 10.1016/j.febslet.2010.06.030pubmed: 20600010google scholar: lookup
  138. Celma C.C., Stewart M., Wernike K., Eschbaumer M., Gonzalez-Molleda L., Breard E., Schulz C., Hoffmann B., Haegeman A., De Clercq K.. Replication-deficient particles: New insights into the next generation of bluetongue virus vaccines. J. Virol. 2016;91:e01892-16.
    doi: 10.1128/JVI.01892-16pmc: PMC5165199pubmed: 27795442google scholar: lookup
  139. Noad R., Roy P.. Virus-like particles as immunogens. Trends Microbiol. 2003;11:438–444.
    doi: 10.1016/S0966-842X(03)00208-7pubmed: 13678860google scholar: lookup
  140. Bachmann M.F., Rohrer U.H., Kundig T.M., Burki K., Hengartner H., Zinkernagel R.M.. The influence of antigen organization on B cell responsiveness. Science 1993;262:1448.
    doi: 10.1126/science.8248784pubmed: 8248784google scholar: lookup
  141. Lechner F., Jegerlehner A., Tissot A.C., Maurer P., Sebbel P., Renner W.A., Jennings G.T., Bachmann M.F.. Virus-Like Particles as a Modular System for Novel Vaccines. Intervirology 2002;45:212–217.
    doi: 10.1159/000067912pubmed: 12566703google scholar: lookup
  142. Lua L.H.L., Connors N.K., Sainsbury F., Chuan Y.P., Wibowo N., Middelberg A.P.J.. Bioengineering virus-like particles as vaccines. Biotechnol. Bioeng. 2014;111:425–440.
    doi: 10.1002/bit.25159pubmed: 24347238google scholar: lookup
  143. Grgacic E.V., Anderson D.A.. Virus-like particles: Passport to immune recognition. Methods 2006;40:60–65.
    doi: 10.1016/j.ymeth.2006.07.018pmc: PMC7128828pubmed: 16997714google scholar: lookup
  144. Pattenden L.K., Middelberg A.P.J., Niebert M., Lipin D.I.. Towards the preparative and large-scale precision manufacture of virus-like particles. Trends Biotechnol. 2005;23:523–529.
    doi: 10.1016/j.tibtech.2005.07.011pubmed: 16084615google scholar: lookup
  145. Roy P., French T., Erasmus B.. Protective efficacy of virus-like particles for bluetongue disease. Vaccine 1992;10:28–32.
    doi: 10.1016/0264-410X(92)90415-Gpubmed: 1311487google scholar: lookup
  146. Roy P., Bishop D.H.L., LeBlois H., Erasmus B.J.. Long-lasting protection of sheep against bluetongue challenge after vaccination with virus-like particles: Evidence for homologous and partial heterologous protection. Vaccine 1994;12:805–811.
    doi: 10.1016/0264-410X(94)90289-5pubmed: 7975859google scholar: lookup
  147. Stewart M., Bhatia Y., Athmaran T.N., Noad R., Gastaldi C., Dubois E., Russo P., Thiéry R., Sailleau C., Bréard E.. Validation of a novel approach for the rapid production of immunogenic virus-like particles for bluetongue virus. Vaccine 2010;28:3047–3054.
    doi: 10.1016/j.vaccine.2009.10.072pubmed: 19887134google scholar: lookup
  148. Lomonossoff G.P., D’Aoust M.-A.. Plant-produced biopharmaceuticals: A case of technical developments driving clinical deployment. Science 2016;353:1237–1240.
    doi: 10.1126/science.aaf6638pubmed: 27634524google scholar: lookup
  149. Rybicki E.P.. Plant-made vaccines for humans and animals. Plant. Biotechnol. J. 2010;8:620–637.
    doi: 10.1111/j.1467-7652.2010.00507.xpmc: PMC7167690pubmed: 20233333google scholar: lookup
  150. Fischer R., Schillberg S., Buyel J.F., Twyman R.M.. Commercial aspects of pharmaceutical protein production in plants. Curr. Pharm. Des. 2013;19:5471–5477.
    doi: 10.2174/1381612811319310002pubmed: 23394566google scholar: lookup
  151. Ma J.K.C., Drake P.M.W., Christou P.. Genetic modification: The production of recombinant pharmaceutical proteins in plants. Nat. Rev. Genet. 2003;4:794.
    doi: 10.1038/nrg1177pubmed: 14526375google scholar: lookup
  152. Rybicki E.. History and Promise of Plant-Made Vaccines for Animals. 2018. pp. 1–22.
  153. Rybicki E.P.. Plant-based vaccines against viruses. Virol. J. 2014;11:205.
    doi: 10.1186/s12985-014-0205-0pmc: PMC4264547pubmed: 25465382google scholar: lookup
  154. Thuenemann E.C., Meyers A.E., Verwey J., Rybicki E.P., Lomonossoff G.P.. A method for rapid production of heteromultimeric protein complexes in plants: Assembly of protective bluetongue virus-like particles. Plant Biotechnol. J. 2013;11:839–846.
    doi: 10.1111/pbi.12076pubmed: 23647743google scholar: lookup
  155. Van Zyl A.R., Meyers A.E., Rybicki E.P.. Transient Bluetongue virus serotype 8 capsid protein expression in Nicotiana benthamiana. Biotechnol. Rep. 2016;9:15–24.
    doi: 10.1016/j.btre.2015.12.001pmc: PMC5360979pubmed: 28352588google scholar: lookup
  156. Maree S., Durbach S., Huismans H.. Intracellular production of African horsesickness virus core-like particles by expression of the two major core proteins, VP3 and VP7, in insect cells. J. Gen. Virol. 1998;79:333–337.
    doi: 10.1099/0022-1317-79-2-333pubmed: 9472617google scholar: lookup
  157. Maree S., Maree F.F., Putterill J.F., de Beer T.A., Huismans H., Theron J.. Synthesis of empty african horse sickness virus particles. Virus Res. 2016;213:184–194.
    doi: 10.1016/j.virusres.2015.12.006pubmed: 26686484google scholar: lookup
  158. Dennis S.J., Meyers A.E., Guthrie A.J., Hitzeroth I.I., Rybicki E.P.. Immunogenicity of plant-produced African horse sickness virus-like particles: Implications for a novel vaccine. Plant Biotechnol. J. 2018;16:442–450.
    doi: 10.1111/pbi.12783pmc: PMC5787833pubmed: 28650085google scholar: lookup
  159. Dennis S.J., O’Kennedy M.M., Rutkowska D., Tsekoa T., Lourens C.W., Hitzeroth I.I., Meyers A.E., Rybicki E.P.. Safety and immunogenicity of plant-produced African horse sickness virus-like particles in horses. Vet. Res. 2018;49:105.
    doi: 10.1186/s13567-018-0600-4pmc: PMC6389048pubmed: 30309390google scholar: lookup
  160. MacLachlan N.J., Balasuriya U.B., Davis N.L., Collier M., Johnston R.E., Ferraro G.L., Guthrie A.J.. Experiences with new generation vaccines against equine viral arteritis, West Nile disease and African horse sickness. Vaccine 2007;25:5577–5582.
    doi: 10.1016/j.vaccine.2006.12.058pubmed: 17267078google scholar: lookup
  161. House J.A.. Recommendations for African horse sickness vaccines for use in nonendemic areas. Rev. D’élevage Et De Médecine Vétérinaire Des. Pays Trop. 1993;46:77–81.
    pubmed: 8134660
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.