Analyze Diet
Virology2014; 462-463; 388-403; doi: 10.1016/j.virol.2014.04.029

Experiences with infectious cDNA clones of equine arteritis virus: lessons learned and insights gained.

Abstract: The advent of recombinant DNA technology, development of infectious cDNA clones of RNA viruses, and reverse genetic technologies have revolutionized how viruses are studied. Genetic manipulation of full-length cDNA clones has become an especially important and widely used tool to study the biology, pathogenesis, and virulence determinants of both positive and negative stranded RNA viruses. The first full-length infectious cDNA clone of equine arteritis virus (EAV) was developed in 1996 and was also the first full-length infectious cDNA clone constructed from a member of the order Nidovirales. This clone was extensively used to characterize the molecular biology of EAV and other Nidoviruses. The objective of this review is to summarize the characterization of the virulence (or attenuation) phenotype of the recombinant viruses derived from several infectious cDNA clones of EAV in horses, as well as their application for characterization of the molecular basis of viral neutralization, persistence, and cellular tropism.
Publication Date: 2014-06-07 PubMed ID: 24913633PubMed Central: PMC7172799DOI: 10.1016/j.virol.2014.04.029Google 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.
  • Journal Article
  • Research Support
  • U.S. Gov't
  • Non-P.H.S.
  • 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.

This research article presents a comprehensive review of the various studies conducted on equine arteritis virus (EAV) using infectious cDNA clone technology. The study includes the applications of this technology in checking viral neutralization, persistence, and cellular tropism, along with examining the virulence of recombinant viruses derived from EAV clones.

Understanding Infectious cDNA Clones of RNA Viruses

  • The article focuses on the utilization of recombinant DNA technology, infectious cDNA clones (clones containing the entire genetic material of a virus) of RNA viruses, and reverse genetic technologies. These advanced methodologies have significantly transformed the way viruses are investigated.
  • Genetic manipulation of full-length cDNA clones has emerged as a crucially important tool in studying the biology, pathogenesis, and factors determining the virulence of both positive and negative stranded RNA viruses.

The First Infectious cDNA Clone of Equine Arteritis Virus (EAV)

  • The first full-length infectious cDNA clone of equine arteritis virus (EAV) was developed in 1996. This clone was unique as it was the first full-length infectious cDNA clone developed from a member of the order Nidovirales.
  • This clone was widely used to explore the molecular biology of EAV and other Nidoviruses. Understanding the virus at a molecular level aids in crafting efficient treatment strategies.

Characterizing Virulence and Attenuation Phenotypes of EAV

  • The review summarizes the characterization of the virulence (or attenuation) phenotype of the recombinant viruses derived from several infectious cDNA clones of EAV in horses.
  • These findings are essential to understand how the virus behaves and how its virulence changes when it infects a host organism. This knowledge could be crucial in predicting the severity of outbreaks and in developing effective vaccinations or treatments.

Molecular Basis of Viral Neutralization, Persistence, and Cellular Tropism

  • Besides the study of virulence, the infectious cDNA clones of EAV were also used to explore the molecular basis of viral neutralization, persistence, and cellular tropism.
  • Viral neutralization is the mechanism by which a virus is rendered non-infectious. Persistence refers to the ability of a virus to remain in a host for long periods, while cellular tropism concerns the preference of a virus to infect specific cell types.
  • The understanding of these aspects is critical for research into virus-host interactions, as well as for designing appropriate therapeutic interventions.

Cite This Article

APA
Balasuriya UB, Zhang J, Go YY, MacLachlan NJ. (2014). Experiences with infectious cDNA clones of equine arteritis virus: lessons learned and insights gained. Virology, 462-463, 388-403. https://doi.org/10.1016/j.virol.2014.04.029

Publication

ISSN: 1096-0341
NlmUniqueID: 0110674
Country: United States
Language: English
Volume: 462-463
Pages: 388-403

Researcher Affiliations

Balasuriya, Udeni B R
  • 108 Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY 40546, USA. Electronic address: ubalasuriya@uky.edu.
Zhang, Jianqiang
  • Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USA.
Go, Yun Young
  • Virus Research and Testing Group, Division of Drug Discovery Research, Korea Research Institute of Chemical Technology, Daejeon 305-343, South Korea.
MacLachlan, N James
  • Department of Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California, Davis, CA 95616, USA.

MeSH Terms

  • Animals
  • Cloning, Molecular
  • DNA, Complementary / genetics
  • Equartevirus / genetics
  • Equartevirus / pathogenicity
  • Equartevirus / physiology
  • Horses
  • Reverse Genetics
  • Virulence

References

This article includes 113 references
  1. Alexander H.E., Koch G., Mountain I.M., Sprunt K., Van Damme O.. Infectivity of ribonucleic acid of poliovirus on HeLa cell mono-layers.. Virology 1958;5:172–173.
    pubmed: 13519758
  2. Alexander H.E., Koch G., Mountain I.M., Van Damme O.. Infectivity of ribonucleic acid from poliovirus in human cell monolayers.. J. Exp. Med. 1958;108:493–506.
    pmc: PMC2136898pubmed: 13575680
  3. Balasuriya U.B., Dobbe J.C., Heidner H.W., Smalley V.L., Navarrette A., Snijder E.J., MacLachlan N.J.. Characterization of the neutralization determinants of equine arteritis virus using recombinant chimeric viruses and site-specific mutagenesis of an infectious cDNA clone.. Virology 2004;321:235–246.
    pubmed: 15051384
  4. Balasuriya U.B., Evermann J.F., Hedges J.F., McKeirnan A.J., Mitten J.Q., Beyer J.C., McCollum W.H., Timoney P.J., MacLachlan N.J.. Serologic 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. 1998;213(1586–1589):1570.
    pubmed: 9838958
  5. Balasuriya U.B., Go Y.Y., Maclachlan N.J.. Equine arteritis virus.. Vet. Microbiol. 2013;167:93–122.
    pmc: PMC7126873pubmed: 23891306
  6. Balasuriya U.B., Hedges J.F., Nadler S.A., McCollum W.H., Timoney P.J., MacLachlan N.J.. Genetic stability of equine arteritis virus during horizontal and vertical transmission in an outbreak of equine viral arteritis.. J. Gen. Virol. 1999;80(Pt 8):1949–1958.
    pubmed: 10466790
  7. Balasuriya U.B., Hedges J.F., Smalley V.L., Navarrette A., McCollum W.H., Timoney P.J., Snijder E.J., MacLachlan N.J.. Genetic characterization of equine arteritis virus during persistent infection of stallions.. J. Gen. Virol. 2004;85:379–390.
    pubmed: 14769895
  8. Balasuriya U.B., Heidner H.W., Davis N.L., Wagner H.M., Hullinger P.J., Hedges J.F., Williams J.C., Johnston R.E., David Wilson W., Liu I.K., James MacLachlan N.. Alphavirus replicon particles expressing the two major envelope proteins of equine arteritis virus induce high level protection against challenge with virulent virus in vaccinated horses.. Vaccine 2002;20:1609–1617.
    pubmed: 11858869
  9. Balasuriya U.B., MacLachlan N.J.. The immune response to equine arteritis virus: potential lessons for other arteriviruses.. Vet. Immunol. Immunopathol. 2004;102:107–129.
    pubmed: 15507299
  10. Balasuriya U.B., MaclLchlan N.J., De Vries A.A., Rossitto P.V., Rottier P.J.. Identification of a neutralization site in the major envelope glycoprotein (GL) of equine arteritis virus.. Virology 1995;207:518–527.
    pubmed: 7533965
  11. Balasuriya U.B., Patton J.F., Rossitto P.V., Timoney P.J., McCollum W.H., MacLachlan N.J.. Neutralization 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 1997;232:114–128.
    pubmed: 9185595
  12. Balasuriya U.B., Snijder E.J.. Arterivirus.. Animal Viruses: Molecular Biology 2008;pp. 97–148.
  13. Balasuriya U.B., Snijder E.J., Heidner H.W., Zhang J., Zevenhoven-Dobbe J.C., Boone J.D., McCollum W.H., Timoney P.J., MacLachlan N.J.. Development and characterization of an infectious cDNA clone of the virulent Bucyrus strain of equine arteritis virus.. J. Gen. Virol. 2007;88:918–924.
    pubmed: 17325365
  14. Balasuriya U.B., Snijder E.J., van Dinten L.C., Heidner H.W., Wilson W.D., Hedges J.F., Hullinger P.J., MacLachlan N.J.. Equine arteritis virus derived from an infectious cDNA clone is attenuated and genetically stable in infected stallions.. Virology 1999;260:201–208.
    pubmed: 10405372
  15. Balasuriya U.B.R., Snijder E.J., MacLachlan N.J.. Phenotypic characterization of equine arteritis virus with an infectious cDNA clone.. 2000.
  16. Boyer J.C., Haenni A.L.. Infectious transcripts and cDNA clones of RNA viruses.. Virology 1994;198:415–426.
    pubmed: 8291226
  17. Castillo-Olivares J., Wieringa R., Bakonyi T.. Generation of a candidate live marker vaccine for equine arteritis virus by deletion of the major virus neutralization domain.. J. Virol. 2003;77:8470–8480.
    pmc: PMC165223pubmed: 12857916
  18. Chen Z., Li K., Plagemann P.G.. Neuropathogenicity and sensitivity to antibody neutralization of lactate dehydrogenase-elevating virus are determined by polylactosaminoglycan chains on the primary envelope glycoprotein.. Virology 2000;266:88–98.
    pubmed: 10612663
  19. Chirnside E.D., Francis P.M., de Vries A.A.. Development and evaluation of an ELISA using recombinant fusion protein to detect the presence of host antibody to equine arteritis virus.. J. Virol. Methods. 1995;54:1–13.
    pmc: PMC7119792pubmed: 7559853
  20. Deregt D., de Vries A.A., Raamsman M.J.. Monoclonal antibodies to equine arteritis virus proteins identify the GL protein as a target for virus neutralization.. J. Gen. Virol. 1994;75(Pt 9):2439–2444.
    pubmed: 8077945
  21. Dobbe J.C., van der Meer Y., Spaan W.J.. Construction of chimeric arteriviruses reveals that the ectodomain of the major glycoprotein is not the main determinant of equine arteritis virus tropism in cell culture.. Virology 2001;288:283–294.
    pubmed: 11601900
  22. Das P.B., Vu H.L., Dinh P.X., Cooney J.L., Kwon B., Osorio F.A., Pattnaik A.K.. Glycosylation of minor envelope glycoproteins of porcine reproductive and respiratory syndrome virus in infectious virus recovery, receptor interaction, and immune response.. Virology 2011;410:385–394.
    pubmed: 21195444
  23. de Vries A.A., Glaser A.L., Raamsman M.J., de Haan C.A., Sarnataro S., Godeke G.J., Rottier P.J.. Genetic manipulation of equine arteritis virus using full-length cDNA clones: separation of overlapping genes and expression of a foreign epitope.. Virology 2000;270:84–97.
    pubmed: 10772982
  24. de Vries A.A., Glaser A.L., Raamsman M.J., Rottier P.J.. Recombinant equine arteritis virus as an expression vector.. Virology 2001;284:259–276.
    pubmed: 11384225
  25. Del Piero F.. Equine viral arteritis.. Vet. Pathol. 2000;37:287–296.
    pubmed: 10896389
  26. den Boon J.A., Faaberg K.S., Meulenberg J.J., Wassenaar A.L., Plagemann P.G., Gorbalenya A.E., Snijder E.J.. Processing and evolution of the N-terminal region of the arterivirus replicase ORF1a protein: identification of two papainlike cysteine proteases.. J. Virol. 1995;69:4500–4505.
    pmc: PMC189193pubmed: 7769711
  27. den Boon J.A., Snijder E.J., Chirnside E.D., de Vries A.A., Horzinek M.C., Spaan W.J.. Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily.. J. Virol. 1991;65:2910–2920.
    pmc: PMC240924pubmed: 1851863
  28. den Boon J.A., Snijder E.J., Locker J.K., Horzinek M.C., Rottier P.J.. Another triple-spanning envelope protein among intracellularly budding RNA viruses: the torovirus E protein.. Virology 1991;182:655–663.
    pmc: PMC7130535pubmed: 2024492
  29. Doll E.R., Bryans J.T., McCollum W.H., Crowe M.E.. Isolation of a filterable agent causing arteritis of horses and abortion by mares; its differentiation from the equine abortion (influenza) virus.. Cornell Vet. 1957;47:3–41.
    pubmed: 13397177
  30. Doll E.R., Bryans J.T., Wilson J.C., McCollum W.H.. Immunization against equine viral arteritis using modified live virus propagated in cell cultures of rabbit kidney.. Cornell Vet. 1968;48:497–524.
    pubmed: 4971878
  31. Doll E.R., Knappenberger R.E., Bryans J.T.. An outbreak of abortion caused by the equine arteritis virus.. Cornell Vet. 1957;47:69–75.
    pubmed: 13397180
  32. Dunowska M., Biggs P.J., Zheng T., Perrott M.R.. Identification of a novel nidovirus associated with a neurological disease of the Australian brushtail possum (Trichosurus vulpecula). Vet. Microbiol. 2012;156:418–424.
    pmc: PMC7117198pubmed: 22153843
  33. Firth A.E., Zevenhoven-Dobbe J.C., Wills N.M., Go Y.Y., Balasuriya U.B., Atkins J.F., Snijder E.J., Posthuma C.C.. Discovery of a small arterivirus gene that overlaps the GP5 coding sequence and is important for virus production.. J. Gen. Virol. 2011;92:1097–1106.
    pmc: PMC3139419pubmed: 21307223
  34. Fukunaga Y., McCollum W.H.. Complement-fixation reactions in equine viral arteritis.. Am. J. Vet. Res. 1977;38:2043–2046.
    pubmed: 202179
  35. Glaser A.L., deVries A.A., Dubovi E.J.. Comparison of equine arteritis virus isolates using neutralizing monoclonal antibodies and identification of sequence changes in GL associated with neutralization resistance.. J. Gen. Virol. 1995;76(Pt 9):2223–2233.
    pubmed: 7561759
  36. Glaser A., de Vries A.A.F., Raamsman M.J.B., Horzinek M.C., Rottier P.J.M.. An infectious cDNA clone of equine arteritis virus: a tool for future fundamental studies and vaccine development.. Proceeding of the Eigth Equine Infectious Disease 1999;pp. 166–176.
  37. Go Y.Y., Bailey E., Cook F.R.. Genome-wide association study among four horse breeds identifies a common haplotype associated with in vitro CD3+ T cell susceptibility/resistance to equine arteritis virus infection.. J. Virol. 2011;85:13174–13184.
    pmc: PMC3233183pubmed: 21994447
  38. Go Y.Y., Bailey E., Timoney P.J., Shuck K.M., Balasuriya U.B.. Evidence that in vitro susceptibility of CD3+ T lymphocytes to equine arteritis virus infection reflects genetic predisposition of naturally infected stallions to become carriers of the virus.. J Virol. 2012;86(22):12407–12410.
    pmc: PMC3486460pubmed: 22933293
  39. Go Y.Y., Cook R.F., Fulgencio J.Q., Campos J.R., Henney P., Timoney P.J., Horohov D.W., Balasuriya U.B.. Assessment of correlation between in vitro CD3+ T cell susceptibility to EAV infection and clinical outcome following experimental infection.. Vet. Microbiol. 2012;157:220–225.
    pubmed: 22177968
  40. Go Y.Y., Zhang J., Timoney P.J., Cook R.F., Horohov D.W., Balasuriya U.B.. Complex interactions between the major and minor envelope proteins of equine arteritis virus determine its tropism for equine CD3+ T lymphocytes and CD14+ monocytes.. J. Virol. 2010;84:4898–4911.
    pmc: PMC2863813pubmed: 20219931
  41. Gorbalenya A.E., Enjuanes L., Ziebuhr J., Snijder E.J.. Nidovirales: evolving the largest RNA virus genome.. Virus Res. 2006;117:17–37.
    pmc: PMC7114179pubmed: 16503362
  42. Harry T.O., McCollum W.H.. Stability of viability and immunizing potency of lyophilized, modified equine arteritis live-virus vaccine.. Am. J. Vet. Res. 1981;42:1501–1505.
    pubmed: 6275755
  43. Hedges J.F., Balasuriya U.B., Timoney P.J., McCollum W.H., MacLachlan N.J.. Genetic divergence with emergence of novel phenotypic variants of equine arteritis virus during persistent infection of stallions.. J. Virol. 1999;73:3672–3681.
    pmc: PMC104142pubmed: 10196259
  44. Hedges J.F., Demaula C.D., Moore B.D., McLaughlin B.E., Simon S.I., MacLachlan N.J.. Characterization of equine E-selectin.. Immunology 2001;103:498–504.
    pmc: PMC1783268pubmed: 11529941
  45. Hyllseth B.. A plaque assay of equine arteritis virus in BHK-21 cells.. Arch. Ges. Virusforsch. 1969;28:26–33.
    pubmed: 4988871
  46. Jones T.C., Doll E.R., Bryans J.T.. The lesions of equine viral arteritis.. Cornell Vet. 1957;47:52–68.
    pubmed: 13397179
  47. Konishi S., Akashi H., Sentsui H., Ogata M.. Studies on equine viral arteritis. I. Characterization of the virus and trial survey on antibody with Vero cell cultures.. Nihon Juigaku Zasshi. 1975;37:259–267.
    pubmed: 172689
  48. Kroese M.V., Zevenhoven-Dobbe J.C., Bos-de Ruijter J.N., Peeters B.P., Meulenberg J.J., Cornelissen L.A., Snijder E.J.. The nsp1alpha and nsp1 papain-like autoproteinases are essential for porcine reproductive and respiratory syndrome virus RNA synthesis.. J. Gen. Virol. 2008;89:494–499.
    pubmed: 18198380
  49. Lu Z., Zhang J., Huang C.M., Go Y.Y., Faaberg K.S., Rowland R.R., Timoney P.J., Balasuriya U.B.. Chimeric viruses containing the N-terminal ectodomains of GP5 and M proteins of porcine reproductive and respiratory syndrome virus do not change the cellular tropism of equine arteritis virus.. Virology 2012;432:99–109.
    pubmed: 22739441
  50. MacLachlan N.J., Balasuriya U.B.. Equine viral arteritis.. Adv. Exp. Med. Biol. 2006;581:429–433.
    pmc: PMC7123899pubmed: 17037573
  51. MacLachlan N.J., Balasuriya U.B., Rossitto P.V., Hullinger P.A., Patton J.F., Wilson W.D.. Fatal experimental equine arteritis virus infection of a pregnant mare: immunohistochemical staining of viral antigens.. J. Vet. Diagn. Investig. 1996;8:367–374.
    pubmed: 8844583
  52. Maess J., Reczko E., Bohm H.O.. Equine arteritis virus: multiplication in BHK 21-cells buoyant density and electron microscopical demonstration.. Arch. Ges. Virusforsch. 1970;30:47–58.
    pubmed: 4194811
  53. McCollum W.H.. Vaccination for equine viral arteritis.. Proceedings of the Second International Conference on Equine Infectious Diseases 1970a;pp. 143–151.
  54. McCollum W.H.. Development of a modified virus strain and vaccine for equine viral arteritis.. J. Am. Vet. Med. Assoc. 1969;155:318–322.
    pubmed: 4978804
  55. McCollum W.H.. Vaccination for equine viral arteritis.. Proceedings of the Second International Conference on Equine Infectious Diseases, Paris 1969 1970b;pp. 143–151.
  56. McCollum W.H., Doll E.R., Wilson J.C., Cheatham J.. Isolation and propagation of equine arteritis virus in monolayer cell cultures of rabbit kidney.. Cornell Vet. 1962;52:452–458.
    pubmed: 14007366
  57. McCollum W.H., Doll E.R., Wilson J.C.. The recovery of virus from horses with experimental cases of equine artertis using monolayer cell cultures of rabbit kidney.. Am. J. Vet. Res. 1961;23:465–469.
  58. McCollum W.H., Doll E.R., Wilson J.C., Johnson C.B.. Propagation of equine arteritis virus in monolayer cultures of equine kidney.. Am. J. Vet. Res. 1961;22:731–735.
  59. McCollum W.H., Timoney P.J.. Experimental observations on the virulence of isolates of equine arteritis virus.. Proceedings of the Eigth International Conference Equine Infectious Diseases 1999;pp. 558–559.
  60. McKinnon A.O., Colbern G.T., Collins J.K., Bowen R.A., Voss J.L., Umphenour J.W.. Vaccination of stallions with a modified live equine arteritis virus vaccine.. J. Equine Vet. Sci. 1986;6:66–69.
  61. Meulenberg J.J., Hulst M.M., de Meijer E.J., Moonen P.L., den Besten A., de Kluyver E.P., Wensvoort G., Moormann R.J.. Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV.. Virology 1993;192:62–72.
    pmc: PMC7173055pubmed: 8517032
  62. Miszczak F., Legrand L., Balasuriya U.B., Ferry-Abitbol B., Zhang J., Hans A., Fortier G., Pronost S., Vabret A.. Emergence of novel equine arteritis virus (EAV) variants during persistent infection in the stallion: origin of the 2007 French EAV outbreak was linked to an EAV strain present in the semen of a persistently infected carrier stallion.. Virology 2012;423:165–174.
    pubmed: 22209234
  63. Molenkamp R., van Tol H., Rozier B.C., van der Meer Y., Spaan W.J., Snijder E.J.. The arterivirus replicase is the only viral protein required for genome replication and subgenomic mRNA transcription.. J. Gen. Virol. 2000;81:2491–2496.
    pubmed: 10993938
  64. Mullis K.B., Faloona F.A.. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction.. Method Enzymol. 1987;155:335–350.
    pubmed: 3431465
  65. Nugent J., Sinclair R., deVries A.A.. Development and evaluation of ELISA procedures to detect antibodies against the major envelope protein (G(L)) of equine arteritis virus.. J. Virol. Methods. 2000;90:167–183.
    pubmed: 11064117
  66. Pasternak A.O., Spaan W.J., Snijder E.J.. Nidovirus transcription: how to make sense…?. J. Gen. Virol. 2006;87:1403–1421.
    pubmed: 16690906
  67. Patton J.F., Balasuriya U.B., Hedges J.F., Schweidler T.M., Hullinger P.J., MacLachlan N.J.. Phylogenetic characterization of a highly attenuated strain of equine arteritis virus from the semen of a persistently infected standardbred stallion.. Arch. Virol. 1999;144:817–827.
    pubmed: 10365172
  68. Pirzadeh B., Gagnon C.A., Dea S.. Genomic and antigenic variations of porcine reproductive and respiratory syndrome virus major envelope GP5 glycoprotein.. Can. J. Vet. Res. 1998;62:170–177.
    pmc: PMC1189472pubmed: 9684045
  69. Plagemann P.G.. Complexity of the single linear neutralization epitope of the mouse arterivirus lactate dehydrogenase-elevating virus.. Virology 2001;290:11–20.
    pubmed: 11882995
  70. Plagemann P.G., Chen Z., Li K.. Replication competition between lactate dehydrogenase-elevating virus quasispecies in mice. Implications for quasispecies selection and evolution.. Arch. Virol. 2001;146:1283–1296.
    pubmed: 11556706
  71. Plagemann P.G., Jones Q.A., Cafruny W.A.. Polyclonal activation of B cells by lactate dehydrogenase-elevating virus is mediated by N-glycans on the short ectodomain of the primary envelope glycoprotein.. Adv. Exp. Med. Biol. 2001;494:375–384.
    pubmed: 11774496
  72. Pronost S., Pitel P.H., Miszczak F., Legrand L., Marcillaud-Pitel C., Hamon M., Tapprest J., Balasuriya U.B., Freymuth F., Fortier G.. Description of the first recorded major occurrence of equine viral arteritis in France.. Equine Vet. J. 2010;42:713–720.
    pubmed: 21039801
  73. Racaniello V.R., Baltimore D.. Cloned poliovirus complementary DNA is infectious in mammalian cells.. Science 1981;214:916–919.
    pubmed: 6272391
  74. Racaniello V.R., Baltimore D.. Molecular cloning of poliovirus cDNA and determination of the complete nucleotide sequence of the viral genome.. Proc. Natl. Acad. Sci. USA. 1981;78:4887–4891.
    pmc: PMC320284pubmed: 6272282
  75. Radwan A.I., Burger D.. The complement-requiring neutralization of equine arteritis virus by late antisera.. Virology 1973;51:71–77.
    pubmed: 4630828
  76. Siddell S.G., Ziebuhr J., Snijder E.J.. Coronaviruses, toroviruses and arteriviruses.. Topley and Wilson׳s Microbiology and Microbial Infections; Virology Volume 2005;pp. 823–856.
  77. Smits S.L., Snijder E.J., de Groot R.J.. Characterization of a torovirus main proteinase.. J. Virol. 2006;80:4157–4167.
    pmc: PMC1440467pubmed: 16571831
  78. Snijder E., Wassenaar A.L., den Boon J.A., Spaan W.J.. Proteolytic processing of the arterivirus replicase.. Adv. Exp. Med. Biol. 1995;380:443–451.
    pubmed: 8830522
  79. Snijder E.J.. The arterivirus replicase. The road from RNA to protein(s), and back again.. Adv. Exp. Med. Biol. 1998;440:97–108.
    pubmed: 9782270
  80. Snijder E.J.. Arterivirus RNA synthesis dissected. Nucleotides, membranes, amino acids, and a bit of zinc.. Adv. Exp. Med. Biol. 2001;494:241–253.
    pubmed: 11774476
  81. Snijder E.J., Spann W.J.M.. Arteriviruses.. Fields Virology 2007;pp. 1337–1355.
  82. Snijder E.J., Kikkert M., Fang Y.. Arterivirus molecular biology and pathogenesis.. J. Gen. Virol. 2013;94:2141–2163.
    pubmed: 23939974
  83. Snijder E.J., Kikkert M.. Arteriviruses.. Fields Virology 2013.
  84. Snijder E.J., Siddell S.G., Gorbalenya A.E.. The Order Nidovirales.. Topley and Wilson׳s Microbiology and Microbial Infections; Virology Volume 2005;pp. 390–404.
  85. Snijder E.J., van der Meer Y., Zevenhoven-Dobbe J., Onderwater J.J., van der Meulen J., Koerten H.K., Mommaas A.M.. Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex.. J. Virol. 2006;80:5927–5940.
    pmc: PMC1472606pubmed: 16731931
  86. Snijder E.J., van Tol H., Pedersen K.W., Raamsman M.J., de Vries A.A.. Identification of a novel structural protein of arteriviruses.. J. Virol. 1999;73:6335–6345.
    pmc: PMC112712pubmed: 10400725
  87. Snijder E.J., van Tol H., Roos N., Pedersen K.W.. Non-structural proteins 2 and 3 interact to modify host cell membranes during the formation of the arterivirus replication complex.. J. Gen. Virol. 2001;82:985–994.
    pubmed: 11297673
  88. Summers-Lawyer K.A., Go Y.Y., Lu Z., Timoney P.J., McCue P.M., Zhang J., Shuck K.M., Bruemmer J.. Response of stallions to primary immunization with a modified live equine viral arteritis vaccine.. J. Equine Vet. Sci. 2011;31:10.
  89. Tian D., Wei Z., Zevenhoven-Dobbe J.C., Liu R., Tong G., Snijder E.J., Yuan S.. Arterivirus minor envelope proteins are a major determinant of viral tropism in cell culture.. J. Virol. 2012;86:3701–3712.
    pmc: PMC3302522pubmed: 22258262
  90. Tijms M.A., Nedialkova D.D., Zevenhoven-Dobbe J.C., Gorbalenya A.E., Snijder E.J.. Arterivirus subgenomic mRNA synthesis and virion biogenesis depend on the multifunctional nsp1 autoprotease.. J. Virol. 2007;81:10496–10505.
    pmc: PMC2045461pubmed: 17626105
  91. Tijms M.A., Snijder E.J.. Equine arteritis virus non-structural protein 1, an essential factor for viral subgenomic mRNA synthesis, interacts with the cellular transcription co-factor p100.. J. Gen. Virol. 2003;84:2317–2322.
    pubmed: 12917451
  92. Tijms M.A., van Dinten L.C., Gorbalenya A.E., Snijder E.J.. A zinc finger-containing papain-like protease couples subgenomic mRNA synthesis to genome translation in a positive-stranded RNA virus.. Proc. Natl. Acad. Sci. USA. 2001;98:1889–1894.
    pmc: PMC29352pubmed: 11172046
  93. Timoney P.J.. Equine viral arteritis: epidemiology and control.. J. Equine Vet. Sci. 1988;8:54–59.
  94. Timoney P.J., Fallon L., Shuck K., McCollum W.H., Zhang J., Williams N.. The outcome of vaccinating five pregnant mares with a commercial equine viral arteritis vaccine.. Equine Vet. Educ. 2007;19:6.
  95. Timoney P.J., McCollum W.H.. Equine viral arteritis.. Vet. Clin. N. Am. Equine Pract. 1993;9:295–309.
    pmc: PMC7134676pubmed: 8395325
  96. Vairo S., Vandekerckhove A., Steukers L., Glorieux S., Van den Broeck W., Nauwynck H.. Clinical and virological outcome of an infection with the Belgian equine arteritis virus strain 08P178.. Vet. Microbiol. 2012;157:12.
    pubmed: 22306037
  97. van Aken D., Benckhuijsen W.E., Drijfhout J.W., Wassenaar A.L., Gorbalenya A.E., Snijder E.J.. Expression, purification, and in vitro activity of an arterivirus main proteinase.. Virus Res. 2006;120:97–106.
    pmc: PMC7114227pubmed: 16527369
  98. van Aken D., Snijder E.J., Gorbalenya A.E.. Mutagenesis analysis of the nsp4 main proteinase reveals determinants of arterivirus replicase polyprotein autoprocessing.. J. Virol. 2006;80:3428–3437.
    pmc: PMC1440411pubmed: 16537610
  99. Van Breedam W., Delputte P.L., Van Gorp H., Misinzo G., Vanderheijden N., Duan X., Nauwynck H.J.. Porcine reproductive and respiratory syndrome virus entry into the porcine macrophage.. J. Gen. Virol. 2010;91:1659–1667.
    pubmed: 20410315
  100. van den Born E., Posthuma C.C., Gultyaev A.P., Snijder E.J.. Discontinuous subgenomic RNA synthesis in arteriviruses is guided by an RNA hairpin structure located in the genomic leader region.. J. Virol. 2005;79:6312–6324.
    pmc: PMC1091703pubmed: 15858015
  101. van der Zeijst B.A., Horzinek M.C.. The genome of equine arteritis virus.. Virology 1975;68:418–425.
    pubmed: 173077
  102. van Dinten L.C., den Boon J.A., Wassenaar A.L., Spaan W.J., Snijder E.J.. An infectious arterivirus cDNA clone: identification of a replicase point mutation that abolishes discontinuous mRNA transcription.. Proc. Natl. Acad. Sci. USA. 1997;94:991–996.
    pmc: PMC19627pubmed: 9023370
  103. van Dinten L.C., Rensen S., Gorbalenya A.E., Snijder E.J.. Proteolytic processing of the open reading frame 1b-encoded part of arterivirus replicase is mediated by nsp4 serine protease and is essential for virus replication.. J. Virol. 1999;73:2027–2037.
    pmc: PMC104445pubmed: 9971783
  104. van Dinten L.C., van Tol H., Gorbalenya A.E., Snijder E.J.. The predicted metal-binding region of the arterivirus helicase protein is involved in subgenomic mRNA synthesis, genome replication, and virion biogenesis.. J. Virol. 2000;74:5213–5223.
    pmc: PMC110875pubmed: 10799597
  105. van Marle G., Dobbe J.C., Gultyaev A.P., Luytjes W., Spaan W.J., Snijder E.J.. Arterivirus discontinuous mRNA transcription is guided by base pairing between sense and antisense transcription-regulating sequences.. Proc. Natl. Acad. Sci. USA. 1999;96:12056–12061.
    pmc: PMC18411pubmed: 10518575
  106. van Marle G., van Dinten L.C., Spaan W.J., Luytjes W., Snijder E.J.. Characterization of an equine arteritis virus replicase mutant defective in subgenomic mRNA synthesis.. J. Virol. 1999;73:5274–5281.
    pmc: PMC112582pubmed: 10364273
  107. Weiland E., Bolz S., Weiland F.. Monoclonal antibodies directed against conserved epitopes on the nucleocapsid protein and the major envelope glycoprotein of equine arteritis virus.. J. Clin. Microbiol. 2000;38:2065–2075.
    pmc: PMC86730pubmed: 10834955
  108. Zevenhoven-Dobbe J.C., Greve S., van Tol H., Spaan W.J., Snijder E.J.. Rescue of disabled infectious single-cycle (DISC) equine arteritis virus by using complementing cell lines that express minor structural glycoproteins.. J. Gen. Virol. 2004;85:3709–3714.
    pubmed: 15557244
  109. Zhang J., Go Y.Y., Huang C.M., Meade B.J., Lu Z., Snijder E.J., Timoney P.J., Balasuriya U.B.. Development and characterization of an infectious cDNA clone of the modified live virus vaccine strain of equine arteritis virus.. Clin. Vaccin. Immunol. 2012;19:1312–1321.
    pmc: PMC3416077pubmed: 22739697
  110. Zhang J., Go Y.Y., MacLachlan N.J., Meade B.J., Timoney P.J., Balasuriya U.B.. Amino acid substitutions in the structural or nonstructural proteins of a vaccine strain of equine arteritis virus are associated with its attenuation.. Virology 2008;378:355–362.
    pubmed: 18619638
  111. Zhang J., Timoney P.J., MacLachlan N.J., Balasuriya U.B.. Identification of an additional neutralization determinant of equine arteritis virus.. Virus Res. 2008;138:150–153.
    pubmed: 18851997
  112. Zhang J., Timoney P.J., MacLachlan N.J., McCollum W.H., Balasuriya U.B.. Persistent equine arteritis virus infection in HeLa cells.. J. Virol. 2008;82:8456–8464.
    pmc: PMC2519626pubmed: 18579588
  113. Zhang J., Timoney P.J., Shuck K.M., Seoul G., Go Y.Y., Lu Z., Powell D.G., Meade B.J., Balasuriya U.B.. Molecular epidemiology and genetic characterization of equine arteritis virus isolates associated with the 2006-2007 multi-state disease occurrence in the USA.. J. Gen. Virol. 2010;91:2286–2301.
    pubmed: 20444993