Skip to main content
SpringerLink
Log in

Genetic variation and phylogenetic analysis of 22 French isolates of equine arteritis virus

  • Published:
Archives of Virology Aims and scope Submit manuscript

Summary

Genetic variation and phylogenetic relationships among 22 French isolates of equine arteritis virus (EAV) obtained over four breeding seasons (2001–2004) were determined by sequencing open reading frames (ORFs) 2a–7. The ORFs 2a–7 of 22 isolates differed from the prototype virulent Bucyrus strain of EAV by between 14 (99.5% identity) and 328 (88.7% identity) nucleotides, and differed from each other by between 0 (100% identity) and 346 (88.1% identity) nucleotides, confirming genetic diversity among EAV strains circulating in France. Phylogenetic analysis based on the partial ORF5 sequences (nucleotides 11296–11813) of 22 French isolates and 216 additional EAV strains available in GenBank clustered the global isolates of EAV into two distinct groups: North American and European. The latter could be further divided into two large subgroups: European subgroup 1 (EU-1) and European subgroup 2 (EU-2). Phylogenetic analysis based on 100 EAV ORF3 sequences yielded similar results. Of the 22 French EAV isolates, the 11 isolates obtained before January 28, 2003 clustered with either the EU-1 (9 isolates) or EU-2 (2 isolates) subgroup. In contrast, by the criteria used in this study, the 11 isolates obtained after January 30, 2003 belong to the North American group, strongly suggesting that these strains were recently introduced into France.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • D Archambault G Laganiere S Carman G St-Laurent (1997) ArticleTitleComparison of nucleic and amino acid sequences and phylogenetic analysis of open reading frames 3 and 4 of various equine arteritis virus isolates Vet Res 28 505–516 Occurrence Handle9428144 Occurrence Handle1:CAS:528:DyaK2sXnvFGhtLw%3D

    PubMed  CAS  Google Scholar 

  • UB Balasuriya PV Rossitto CD DeMaula NJ MacLachlan (1993) ArticleTitleA 29K envelope glycoprotein of equine arteritis virus expresses neutralization determinants recognized by murine monoclonal antibodies J Gen Virol 74 IssueIDPt 11 2525–2529 Occurrence Handle7504076 Occurrence Handle1:CAS:528:DyaK2cXmsVej

    PubMed  CAS  Google Scholar 

  • UB Balasuriya NJ Maclachlan AA De Vries PV Rossitto PJ Rottier (1995) ArticleTitleIdentification of a neutralization site in the major envelope glycoprotein (GL) of equine arteritis virus Virology 207 518–527 Occurrence Handle7533965 Occurrence Handle10.1006/viro.1995.1112 Occurrence Handle1:CAS:528:DyaK2MXktl2qsbk%3D

    Article  PubMed  CAS  Google Scholar 

  • UB Balasuriya PJ Timoney WH McCollum NJ MacLachlan (1995) ArticleTitlePhylogenetic analysis of open reading frame 5 of field isolates of equine arteritis virus and identification of conserved and nonconserved regions in the GL envelope glycoprotein Virology 214 690–697 Occurrence Handle8553578 Occurrence Handle10.1006/viro.1995.0087 Occurrence Handle1:CAS:528:DyaK28Xislylsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • UB Balasuriya JF Patton PV Rossitto PJ Timoney WH McCollum NJ MacLachlan (1997) ArticleTitleNeutralization determinants of laboratory strains and field isolates of equine arteritis virus: identification of four neutralization sites in the amino-terminal ectodomain of the G(L) envelope glycoprotein Virology 232 114–128 Occurrence Handle9185595 Occurrence Handle10.1006/viro.1997.8551 Occurrence Handle1:CAS:528:DyaK2sXjsFaqtL8%3D

    Article  PubMed  CAS  Google Scholar 

  • UB Balasuriya JF Evermann JF Hedges AJ McKeirnan JQ Mitten JC Beyer WH McCollum PJ Timoney NJ MacLachlan (1998) ArticleTitleSerologic and molecular characterization of an abortigenic strain of equine arteritis virus isolated from infective frozen semen and an aborted equine fetus J Am Vet Med Assoc 213 1586–1589 Occurrence Handle9838958 Occurrence Handle1:CAS:528:DyaK1cXnvFOitLY%3D

    PubMed  CAS  Google Scholar 

  • UB Balasuriya JF Hedges SA Nadler WH McCollum PJ Timoney NJ MacLachlan (1999) ArticleTitleGenetic stability of equine arteritis virus during horizontal and vertical transmission in an outbreak of equine viral arteritis J Gen Virol 80 IssueIDPt 8 1949–1958 Occurrence Handle10466790 Occurrence Handle1:CAS:528:DyaK1MXlt1aqtb0%3D

    PubMed  CAS  Google Scholar 

  • UB Balasuriya JC Dobbe HW Heidner VL Smalley A Navarrette EJ Snijder NJ MacLachlan (2004) ArticleTitleCharacterization of the neutralization determinants of equine arteritis virus using recombinant chimeric viruses and site-specific mutagenesis of an infectious cDNA clone Virology 321 235–246 Occurrence Handle15051384 Occurrence Handle10.1016/j.virol.2003.12.015 Occurrence Handle1:CAS:528:DC%2BD2cXis1Wgurg%3D

    Article  PubMed  CAS  Google Scholar 

  • UB Balasuriya JF Hedges VL Smalley A Navarrette WH McCollum PJ Timoney EJ Snijder NJ MacLachlan (2004) ArticleTitleGenetic characterization of equine arteritis virus during persistent infection of stallions J Gen Virol 85 379–390 Occurrence Handle14769895 Occurrence Handle10.1099/vir.0.19545-0 Occurrence Handle1:CAS:528:DC%2BD2cXitVGitL8%3D

    Article  PubMed  CAS  Google Scholar 

  • UB Balasuriya NJ MacLachlan (2004) ArticleTitleThe immune response to equine arteritis virus: potential lessons for other arteriviruses Vet Immunol Immunopathol 102 107–129 Occurrence Handle15507299 Occurrence Handle10.1016/j.vetimm.2004.09.003 Occurrence Handle1:CAS:528:DC%2BD2cXovFajsrc%3D

    Article  PubMed  CAS  Google Scholar 

  • UB Balasuriya EJ Snijder HW Heidner J Zhang JC Zevenhoven-Dobbe JD Boone WH McCollum PJ Timoney NJ Maclachlan (2007) ArticleTitleDevelopment and characterization of an infectious cDNA clone of the virulent Bucyrus strain of equine arteritis virus J Gen Virol 88 918–924 Occurrence Handle17325365 Occurrence Handle10.1099/vir.0.82415-0 Occurrence Handle1:CAS:528:DC%2BD2sXivVyqurg%3D

    Article  PubMed  CAS  Google Scholar 

  • D Cavanagh (1997) ArticleTitleNidovirales: a new order comprising Coronaviridae and Arteriviridae Arch Virol 142 629–633 Occurrence Handle9349308 Occurrence Handle1:CAS:528:DyaK2sXivFGrurY%3D

    PubMed  CAS  Google Scholar 

  • ED Chirnside CM Wearing MM Binns JA Mumford (1994) ArticleTitleComparison of M and N gene sequences distinguishes variation amongst equine arteritis virus isolates J Gen Virol 75 IssueIDPt 6 1491–1497 Occurrence Handle8207415 Occurrence Handle1:CAS:528:DyaK2cXlsFSis7w%3D

    PubMed  CAS  Google Scholar 

  • ED Chirnside AA de Vries JA Mumford PJ Rottier (1995) ArticleTitleEquine arteritis virus-neutralizing antibody in the horse is induced by a determinant on the large envelope glycoprotein GL J Gen Virol 76 IssueIDPt 8 1989–1998 Occurrence Handle7636479 Occurrence Handle1:CAS:528:DyaK2MXnsVCmtrw%3D

    PubMed  CAS  Google Scholar 

  • AA de Vries ED Chirnside MC Horzinek PJ Rottier (1992) ArticleTitleStructural proteins of equine arteritis virus J Virol 66 6294–6303 Occurrence Handle1328669 Occurrence Handle1:CAS:528:DyaK3sXhvV2msA%3D%3D

    PubMed  CAS  Google Scholar 

  • JA den Boon EJ Snijder ED Chirnside AA de Vries MC Horzinek WJ Spaan (1991) ArticleTitleEquine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily J Virol 65 2910–2920 Occurrence Handle1851863 Occurrence Handle1:CAS:528:DyaK38XnslCjtw%3D%3D

    PubMed  CAS  Google Scholar 

  • D Deregt AA de Vries MJ Raamsman LD Elmgren PJ Rottier (1994) ArticleTitleMonoclonal antibodies to equine arteritis virus proteins identify the GL protein as a target for virus neutralization J Gen Virol 75 IssueIDPt 9 2439–2444 Occurrence Handle8077945 Occurrence Handle1:CAS:528:DyaK2cXlslOiu74%3D

    PubMed  CAS  Google Scholar 

  • AL Glaser AA de Vries EJ Dubovi (1995) ArticleTitleComparison of equine arteritis virus isolates using neutralizing monoclonal antibodies and identification of sequence changes in GL associated with neutralization resistance J Gen Virol 76 IssueIDPt 9 2223–2233 Occurrence Handle7561759 Occurrence Handle1:CAS:528:DyaK2MXnvVyqu7g%3D Occurrence Handle10.1099/0022-1317-76-9-2223

    Article  PubMed  CAS  Google Scholar 

  • AJ Guthrie PG Howell JF Hedges AM Bosman UB Balasuriya WH McCollum PJ Timoney NJ MacLachlan (2003) ArticleTitleLateral transmission of equine arteritis virus among Lipizzaner stallions in South Africa Equine Vet J 35 IssueID6 596–600 Occurrence Handle14515961 Occurrence Handle10.2746/042516403775467162 Occurrence Handle1:STN:280:DC%2BD3svos1Kltw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • JF Hedges UB Balasuriya PJ Timoney WH McCollum NJ MacLachlan (1996) ArticleTitleGenetic variation in open reading frame 2 of field isolates and laboratory strains of equine arteritis virus Virus Res 42 41–52 Occurrence Handle8806173 Occurrence Handle10.1016/0168-1702(96)01294-4 Occurrence Handle1:CAS:528:DyaK28XjsV2ntbg%3D

    Article  PubMed  CAS  Google Scholar 

  • JF Hedges UB Balasuriya PJ Timoney WH McCollum NJ MacLachlan (1999) ArticleTitleGenetic divergence with emergence of novel phenotypic variants of equine arteritis virus during persistent infection of stallions J Virol 73 3672–3681 Occurrence Handle10196259 Occurrence Handle1:CAS:528:DyaK1MXis1ens78%3D

    PubMed  CAS  Google Scholar 

  • JF Hedges UB Balasuriya JB Topol DW Lee NJ MacLachlan (2001) ArticleTitleGenetic variation of ORFs 3 and 4 of equine arteritis virus Adv Exp Med Biol 494 69–72 Occurrence Handle11774546 Occurrence Handle1:CAS:528:DC%2BD38XnsVCmsr8%3D

    PubMed  CAS  Google Scholar 

  • A Hornyak T Bakonyi G Tekes L Szeredi M Rusvai (2005) ArticleTitleA novel subgroup among genotypes of equine arteritis virus: genetic comparison of 40 strains J Vet Med B Infect Dis Vet Public Health 52 112–118 Occurrence Handle15876222 Occurrence Handle1:CAS:528:DC%2BD2MXls1aks78%3D

    PubMed  CAS  Google Scholar 

  • LE Larsen T Storgaard E Holm (2001) ArticleTitlePhylogenetic characterisation of the G(L) sequences of equine arteritis virus isolated from semen of asymptomatic stallions and fatal cases of equine viral arteritis in Denmark Vet Microbiol 80 339–346 Occurrence Handle11348770 Occurrence Handle10.1016/S0378-1135(01)00323-6 Occurrence Handle1:CAS:528:DC%2BD3MXjtlCisro%3D

    Article  PubMed  CAS  Google Scholar 

  • N Lepage G St-Laurent S Carman D Archambault (1996) ArticleTitleComparison of nucleic and amino acid sequences and phylogenetic analysis of the Gs protein of various equine arteritis virus isolates Virus Genes 13 87–91 Occurrence Handle8938984 Occurrence Handle10.1007/BF00576983 Occurrence Handle1:CAS:528:DyaK28XntVyktL8%3D

    Article  PubMed  CAS  Google Scholar 

  • K Li T Schuler Z Chen GE Glass JE Childs PG Plagemann (2000) ArticleTitleIsolation of lactate dehydrogenase-elevating viruses from wild house mice and their biological and molecular characterization Virus Res 67 153–162 Occurrence Handle10867194 Occurrence Handle10.1016/S0168-1702(00)00142-8 Occurrence Handle1:CAS:528:DC%2BD3cXktFCntr0%3D

    Article  PubMed  CAS  Google Scholar 

  • McCollum WH, Timoney PJ, Lee JW Jr, Habacker PL, Balasuriya UBR, MacLachlan NJ (1998) Features of an outbreak of equine viral arteritis on a breeding farm associated with abortion and fatal interstitial pneumonia in neonatal foals. In: Proceedings of Eighth International Conference (equine infectious diseases VIII), Dubai. R & W Publications, Newmarket, pp 559–560

  • C Mittelholzer T Stadejek I Johansson C Baule I Ciabatti D Hannant D Paton GL Autorino N Nowotny S Belak (2006) ArticleTitleExtended phylogeny of equine arteritis virus: division into new subgroups J Vet Med B Infect Dis Vet Publ Health 53 55–58 Occurrence Handle1:CAS:528:DC%2BD28Xkslent7g%3D

    CAS  Google Scholar 

  • BD Moore UB Balasuriya JP Nurton WH McCollum PJ Timoney AJ Guthrie NJ MacLachlan (2003) ArticleTitleDifferentiation of strains of equine arteritis virus of differing virulence to horses by growth in equine endothelial cells Am J Vet Res 64 IssueID6 779–784 Occurrence Handle12828265 Occurrence Handle10.2460/ajvr.2003.64.779

    Article  PubMed  Google Scholar 

  • JF Patton UB Balasuriya JF Hedges TM Schweidler PJ Hullinger NJ MacLachlan (1999) ArticleTitlePhylogenetic characterization of a highly attenuated strain of equine arteritis virus from the semen of a persistently infected standardbred stallion Arch Virol 144 IssueID4 817–827 Occurrence Handle10365172 Occurrence Handle10.1007/s007050050547 Occurrence Handle1:CAS:528:DyaK1MXjs12rur8%3D

    Article  PubMed  CAS  Google Scholar 

  • GW Plagemann (1996) Lactate dehydrogenase-elevating virus and related viruses BN Fields DM Knipe PM Howley (Eds) Fields virology EditionNumber3 Lippincott-Raven New York 1105–1120

    Google Scholar 

  • GW Plagemann Z Chen K Li (1996) ArticleTitlePolylactosaminoglycan chain on the ectodomain of the primary envelope glycoprotein of an artervirus determines its neuropathogenicity, sensitivity to antibody neutralization and immunopathogenicity of the neutralization epitope Curr Top Virol 1 27–43

    Google Scholar 

  • EJ Snijder JJ Meulenberg (1998) ArticleTitleThe molecular biology of arteriviruses J Gen Virol 79 IssueIDPt 5 961–979 Occurrence Handle9603311 Occurrence Handle1:CAS:528:DyaK1cXivFOlt74%3D

    PubMed  CAS  Google Scholar 

  • EJ Snijder H van Tol KW Pedersen MJ Raamsman AA de Vries (1999) ArticleTitleIdentification of a novel structural protein of arteriviruses J Virol 73 6335–6345 Occurrence Handle10400725 Occurrence Handle1:CAS:528:DyaK1MXksFKnsbk%3D

    PubMed  CAS  Google Scholar 

  • EJ Snijder JJ Meulenberg (2001) Arteriviruses EditionNumber4 Lippincott Williams & Wilkins Philadelphia, USA

    Google Scholar 

  • G St-Laurent N Lepage S Carman D Archambault (1997) ArticleTitleGenetic and amino acid analysis of the GL protein of Canadian, American and European equine arteritis virus isolates Can J Vet Res 61 72–76 Occurrence Handle9008807 Occurrence Handle1:CAS:528:DyaK2sXpt1egug%3D%3D

    PubMed  CAS  Google Scholar 

  • T Stadejek H Bjorklund CR Bascunana IM Ciabatti MT Scicluna D Amaddeo WH McCollum GL Autorino PJ Timoney DJ Paton B Klingeborn S Belak (1999) ArticleTitleGenetic diversity of equine arteritis virus J Gen Virol 80 IssueIDPt 3 691–699 Occurrence Handle10092009 Occurrence Handle1:CAS:528:DyaK1MXhvVymtLk%3D

    PubMed  CAS  Google Scholar 

  • T Stadejek C Mittelholzer MB Oleksiewicz J Paweska S Belak (2006) ArticleTitleHighly diverse type of equine arteritis virus (EAV) from the semen of a South African donkey: short communication Acta Vet Hung 54 263–270 Occurrence Handle16841763 Occurrence Handle10.1556/AVet.54.2006.2.12 Occurrence Handle1:STN:280:DC%2BD28vhvF2mug%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res 25 4876–4882 Occurrence Handle9396791 Occurrence Handle10.1093/nar/25.24.4876 Occurrence Handle1:CAS:528:DyaK1cXntFyntQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • PJ Timoney WH McCollum (1993) ArticleTitleEquine viral arteritis Vet Clin North Am Equ Pract 9 295–309 Occurrence Handle1:STN:280:ByyA28votVQ%3D

    CAS  Google Scholar 

  • D van Aken J Zevenhoven-Dobbe AE Gorbalenya EJ Snijder (2006) ArticleTitleProteolytic maturation of replicase polyprotein pp1a by the nsp4 main proteinase is essential for equine arteritis virus replication and includes internal cleavage of nsp7 J Gen Virol 87 3473–3482 Occurrence Handle17098961 Occurrence Handle10.1099/vir.0.82269-0 Occurrence Handle1:CAS:528:DC%2BD28XhtlSjtbrI

    Article  PubMed  CAS  Google Scholar 

  • LC van Dinten JA den Boon AL Wassenaar WJ Spaan EJ Snijder (1997) ArticleTitleAn infectious arterivirus cDNA clone: identification of a replicase point mutation that abolishes discontinuous mRNA transcription Proc Natl Acad Sci USA 94 991–996 Occurrence Handle9023370 Occurrence Handle10.1073/pnas.94.3.991 Occurrence Handle1:CAS:528:DyaK2sXhtVyjt74%3D

    Article  PubMed  CAS  Google Scholar 

  • R Wieringa AA de Vries J van der Meulen GJ Godeke JJ Onderwater H van Tol HK Koerten AM Mommaas EJ Snijder PJ Rottier (2004) ArticleTitleStructural protein requirements in equine arteritis virus assembly J Virol 78 13019–13027 Occurrence Handle15542653 Occurrence Handle10.1128/JVI.78.23.13019-13027.2004 Occurrence Handle1:CAS:528:DC%2BD2cXhtVaqtbnJ

    Article  PubMed  CAS  Google Scholar 

  • J Ziebuhr EJ Snijder AE Gorbalenya (2000) ArticleTitleVirus-encoded proteinases and proteolytic processing in the Nidovirales J Gen Virol 81 853–879 Occurrence Handle10725411 Occurrence Handle1:CAS:528:DC%2BD3cXisVektLg%3D

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, USA

    J. Zhang, U. B. R. Balasuriya & P. J. Timoney

  2. Frank Duncombe Departmental Laboratory, Animal Health Department, Caen, France

    F. Miszczak, S. Pronost, C. Fortier & G. Fortier

  3. UMR 1161 AFSSA/INRA/ENVA, Maisons-Alfort, France

    S. Zientara

Authors
  1. J. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Miszczak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Pronost
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Fortier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. U. B. R. Balasuriya
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Zientara
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. G. Fortier
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. P. J. Timoney
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

The first two authors contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, J., Miszczak, F., Pronost, S. et al. Genetic variation and phylogenetic analysis of 22 French isolates of equine arteritis virus. Arch Virol 152, 1977–1994 (2007). https://doi.org/10.1007/s00705-007-1040-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-007-1040-z

Keywords

Search

Navigation