FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Virus Res / Studying longitudinal neutralising antibody levels against E...
Virus research2023; 339; 199262; doi: 10.1016/j.virusres.2023.199262

Studying longitudinal neutralising antibody levels against Equid herpesvirus 1 in experimentally infected horses using a novel pseudotype based assay.

Abstract: Infection with equid herpesvirus 1 (EHV-1), a DNA virus of the Herpesviridae family represents a significant welfare issue in horses and a great impact on the equine industry. During EHV-1 infection, entry of the virus into different cell types is complex due to the presence of twelve glycoproteins (GPs) on the viral envelope. To investigate virus entry mechanisms, specific combinations of GPs were pseudotyped onto lentiviral vectors. Pseudotyped virus (PV) particles bearing gB, gD, gH and gL were able to transduce several target cell lines (HEK293T/17, RK13, CHO-K1, FHK-Tcl3, MDCK I & II), demonstrating that these four EHV-1 glycoproteins are both essential and sufficient for cell entry. The successful generation of an EHV-1 PV permitted development of a PV neutralisation assay (PVNA). The efficacy of the PVNA was tested by measuring the level of neutralising serum antibodies from EHV-1 experimentally infected horses (n = 52) sampled in a longitudinal manner. The same sera were assessed using a conventional EHV-1 virus neutralisation (VN) assay, exhibiting a strong correlation (r = 0.82) between the two assays. Furthermore, PVs routinely require -80 °C for long term storage and a dry ice cold-chain during transport, which can impede dissemination and utilisation in other stakeholder laboratories. Consequently, lyophilisation of EHV-1 PVs was conducted to address this issue. PVs were lyophilised and pellets either reconstituted immediately or stored under various temperature conditions for different time periods. The recovery and functionality of these lyophilised PVs was compared with standard frozen aliquots in titration and neutralisation tests. Results indicated that lyophilisation could be used to stably preserve such complex herpesvirus pseudotypes, even after weeks of storage at room temperature, and that reconstituted EHV-1 PVs could be successfully employed in antibody neutralisation tests.
Copyright © 2023. Published by Elsevier B.V.
Get Full Text
Publication Date: 2023-11-17 PubMed ID: 37931881PubMed Central: PMC10694342DOI: 10.1016/j.virusres.2023.199262Google 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

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 study researched the levels of neutralising antibodies against Equid herpesvirus 1 (EHV-1) in horses by using a new pseudotype-based test. The research found that a set of glycoproteins are crucial for the virus to enter cells and that the level of neutralising antibodies can be effectively measured using the new test. The study also explored the possibilities of preserving and transporting the pseudoviruses through lyophilisation.

Investigation of Virus Entry Mechanisms

  • The study used pseudotyped viruses (PVs), which are retroviruses bearing specific combinations of glycoproteins (GPs) from EHV-1, to study how the virus enters cells.
  • It was found that PVs containing the glycoproteins gB, gD, gH, and gL could infect various cell types indicating that these GPs are both necessary and adequate to facilitate the virus’s entry into cells.

    • Development of a Pseudotype Virus Neutralisation Assay (PVNA)

    • A PVNA was developed to measure the levels of neutralising antibodies in serum from experimentally infected horses.
    • The PVNA was tested against a conventional virus neutralisation (VN) assay, echoing a strong correlation between the two methods, demonstrating the PVNA’s effectiveness.

      • Lyophilisation of Pseudoviruses

      • One of the downsides of pseudoviruses is that they usually need to be stored at very cold temperatures (-80°C) and require a cold chain for transport.
      • To overcome this, a lyophilisation process, or freeze-drying, was performed on the PVs, and the resulting pellets were tested for their viability after being reconstituted or stored under various conditions for different periods.
      • The results showed that lyophilised PVs can be preserved for weeks at room temperature and can be used in antibody neutralisation tests once they have been reconstituted, simplifying transport and storage requirements.

Cite This Article

APA
Di Genova C, Sutton G, Paillot R, Temperton N, Pronost S, Scott SD. (2023). Studying longitudinal neutralising antibody levels against Equid herpesvirus 1 in experimentally infected horses using a novel pseudotype based assay. Virus Res, 339, 199262. https://doi.org/10.1016/j.virusres.2023.199262

Publication

Virus research
ISSN: 1872-7492
NlmUniqueID: 8410979
Country: Netherlands
Language: English
Volume: 339
Pages: 199262

Researcher Affiliations

Di Genova, Cecilia
  • Viral Pseudotype Unit, Medway School of Pharmacy, Universities of Kent and Greenwich, Chatham Maritime, Kent ME4 4 TB, United Kingdom; Animal and Plant Health Agency (APHA), Weybridge, Surrey KT15 3NB, United Kingdom.
Sutton, Gabrielle
  • LABÉO Frank Duncombe, 14280 Saint-Contest, France; BIOTARGEN, Normandie Univ, UNICAEN, 14000 Caen, France; Université de Montréal, H3C 3J7 Montreal, Q, Canada.
Paillot, Romain
  • LABÉO Frank Duncombe, 14280 Saint-Contest, France; BIOTARGEN, Normandie Univ, UNICAEN, 14000 Caen, France; School of Equine and Veterinary Physiotherapy, Writtle University College, Writtle, Chelmsford, Essex CM1 3RR, United Kingdom.
Temperton, Nigel
  • Viral Pseudotype Unit, Medway School of Pharmacy, Universities of Kent and Greenwich, Chatham Maritime, Kent ME4 4 TB, United Kingdom.
Pronost, Stéphane
  • LABÉO Frank Duncombe, 14280 Saint-Contest, France; BIOTARGEN, Normandie Univ, UNICAEN, 14000 Caen, France.
Scott, Simon D
  • Viral Pseudotype Unit, Medway School of Pharmacy, Universities of Kent and Greenwich, Chatham Maritime, Kent ME4 4 TB, United Kingdom. Electronic address: s.d.scott@kent.ac.uk.

MeSH Terms

  • Humans
  • Animals
  • Horses
  • Herpesvirus 1, Equid / genetics
  • HEK293 Cells
  • Antibodies, Viral
  • Antibodies, Neutralizing
  • Herpesviridae Infections / veterinary
  • Glycoproteins
  • Horse Diseases
  • Herpesvirus 4, Equid / genetics

Conflict of Interest Statement

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References

This article includes 77 references
  1. Abousenna M, Khafagy H, Shafik N, Abdelmotilib N, Yahia IS. Detection of humoral immune response induced in horses vaccinated with inactivated Equine Herpes Virus Vaccine. Revis Bionatura 2022;7(1):21.
    doi: 10.21931/RB/2022.07.01.21google scholar: lookup
  2. Allen GP. Respiratory infections by equine herpesvirus types 1 and 4. Equine Respiratory Diseases 2002.
  3. Allen GP, Kydd JH, Slater JD, Smith KC. Equid Herpesvirus-1 (EHV-1) and -4 (EHV-4) Infections. Infectious Diseases of Livestock 2004;pp. 829–859.
  4. Azab W, Lehmann MJ, Osterrieder N. Glycoprotein H and ?4?1 integrins determine the entry pathway of alphaherpesviruses. J. Virol. 2013;87(10):5937–5948.
    doi: 10.1128/JVI.03522-12pmc: PMC3648174pubmed: 23514881google scholar: lookup
  5. Azab W, Osterrieder N. Glycoproteins D of equine herpesvirus type 1 (EHV-1) and EHV-4 determine cellular tropism independently of integrins. J. Virol. 2012;86(4):2031–2044.
    doi: 10.1128/JVI.06555-11pmc: PMC3302398pubmed: 22171258google scholar: lookup
  6. Azab W, Zajic L, Osterrieder N. The role of glycoprotein H of equine herpesviruses 1 and 4 (EHV-1 and EHV-4) in cellular host range and integrin binding. Vet. Res. 2012;43(1):61.
    doi: 10.1186/1297-9716-43-61pmc: PMC3522555pubmed: 22909178google scholar: lookup
  7. Balasuriya UB, Crossley BM, Timoney PJ. A review of traditional and contemporary assays for direct and indirect detection of Equid herpesvirus 1 in clinical samples. J. Vet. Diagn. Invest. 2015;27(6):673–687.
    doi: 10.1177/1040638715605558pubmed: 26472746google scholar: lookup
  8. Bannai H, Tsujimura K, Nemoto M, Ohta M, Yamanaka T, Kokado H, Matsumura T. Epizootiological investigation of equine herpesvirus type 1 infection among Japanese racehorses before and after the replacement of an inactivated vaccine with a modified live vaccine. BMC Vet. Res. 2019;15(1):280.
    doi: 10.1186/s12917-019-2036-0pmc: PMC6683523pubmed: 31387602google scholar: lookup
  9. Bresgen C, Lämmer M, Wagner B, Osterrieder N, Damiani AM. Serological responses and clinical outcome after vaccination of mares and foals with equine herpesvirus type 1 and 4 (EHV-1 and EHV-4) vaccines. Vet. Microbiol. 2012;160(1):9–16.
    doi: 10.1016/j.vetmic.2012.04.042pubmed: 22633483google scholar: lookup
  10. Bryant NA, Wilkie GS, Russell CA, Compston L, Grafham D, Clissold L, McLay K, Medcalf L, Newton R, Davison AJ, Elton DM. Genetic diversity of equine herpesvirus 1 isolated from neurological, abortigenic and respiratory disease outbreaks. Transbound. Emerg. Dis. 2018;65(3):817–832.
    doi: 10.1111/tbed.12809pmc: PMC5947664pubmed: 29423949google scholar: lookup
  11. Campadelli-Fiume GM. Entry of alphaherpesviruses into the cell. Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis 2007;pp. Chapter-7.
    pubmed: 21348071
  12. Carnell GW, Ferrara F, Grehan K, Thompson CP, Temperton NJ. Pseudotype-Based Neutralization Assays for Influenza: A Systematic Analysis. Front. Immunol. 2015;6:161.
    doi: 10.3389/fimmu.2015.00161pmc: PMC4413832pubmed: 25972865google scholar: lookup
  13. Carvelli A, Nielsen SS, Paillot R, Broglia A, Kohnle L. Clinical impact, diagnosis and control of Equine Herpesvirus-1 infection in Europe. EFSA J. 2022;20(4):e07230.
    doi: 10.2903/j.efsa.2022.7230pmc: PMC8985062pubmed: 35414834google scholar: lookup
  14. Cepko C. Large-Scale Preparation and Concentration of Retrovirus Stocks. Curr. Protoc. Mol. Biol. 1997;37(1):9.12.11–19.12.16.
    doi: 10.1002/0471142727.mb0912s37pubmed: 18265280google scholar: lookup
  15. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, Jarrossay D, Vachieri SG, Pinna D, Minola A, Vanzetta F, Silacci C, Fernandez-Rodriguez BM, Agatic G, Bianchi S, Giacchetto-Sasselli I, Calder L, Sallusto F, Collins P, Haire LF, Lanzavecchia A. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 2011;333(6044):850–856.
    doi: 10.1126/science.1205669pubmed: 21798894google scholar: lookup
  16. Couroucé A, Normand C, Tessier C, Pomares R, Thévenot J, Marcillaud-Pitel C, Legrand L, Pitel PH, Pronost S, Lupo C. Equine Herpesvirus-1 Outbreak During a Show-Jumping Competition: A Clinical and Epidemiological Study. J. Equin. Veter. Sci. 2023;128.
    doi: 10.1016/j.jevs.2023.104869pubmed: 37339699google scholar: lookup
  17. Crabb BS, MacPherson CM, Reubel GH, Browning GF, Studdert MJ, Drummer HE. A type-specific serological test to distinguish antibodies to equine herpesviruses 4 and 1. Arch. Virol. 1995;140(2):245–258.
    doi: 10.1007/BF01309860pubmed: 7710353google scholar: lookup
  18. Crabb BS, Nagesha HS, Studdert MJ. Identification of equine herpesvirus 4 glycoprotein G: a type-specific, secreted glycoprotein. Virology 1992;190(1):143–154.
    doi: 10.1016/0042-6822(92)91200-epubmed: 1529525google scholar: lookup
  19. Crabb BS, Studdert MJ. Epitopes of glycoprotein G of equine herpesviruses 4 and 1 located near the C termini elicit type-specific antibody responses in the natural host. J. Virol. 1993;67(10):6332–6338.
    doi: 10.1128/JVI.67.10.6332-6338.1993pmc: PMC238063pubmed: 7690425google scholar: lookup
  20. Csellner H, Walker C, Wellington JE, McLure LE, Love DN, Whalley JM. EHV-1 glycoprotein D (EHV-1 gD) is required for virus entry and cell-cell fusion, and an EHV-1 gD deletion mutant induces a protective immune response in mice. Arch. Virol. 2000;145(11):2371–2385.
    doi: 10.1007/s007050070027pubmed: 11205124google scholar: lookup
  21. Darling D, Hughes C, Galea-Lauri J, Gäken J, Trayner ID, Kuiper M, Farzaneh F. Low-speed centrifugation of retroviral vectors absorbed to a particulate substrate: a highly effective means of enhancing retroviral titre. Gene Ther. 2000;7(11):914–923.
    doi: 10.1038/sj.gt.3301201pubmed: 10849550google scholar: lookup
  22. Davison AJ, Eberle R, Ehlers B, Hayward GS, McGeoch DJ, Minson AC, Pellett PE, Roizman B, Studdert MJ, Thiry E. The order Herpesvirales. Arch. Virol. 2009;154(1):171–177.
    doi: 10.1007/s00705-008-0278-4pmc: PMC3552636pubmed: 19066710google scholar: lookup
  23. Di Genova C, Sampson A, Scott S, Cantoni D, Mayora-Neto M, Bentley E, Mattiuzzo G, Wright E, Derveni M, Auld B, Ferrara BT, Harrison D, Said M, Selim A, Thompson E, Thompson C, Carnell G, Temperton N. Production, Titration, Neutralisation, Storage and Lyophilisation of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Lentiviral Pseudotypes. Bio. Protoc. 2021;11(21):e4236.
    doi: 10.21769/BioProtoc.4236pmc: PMC8595416pubmed: 34859134google scholar: lookup
  24. Dunowska M, Gopakumar G, Perrott MR, Kendall AT, Waropastrakul S, Hartley CA, Carslake HB. Virological and serological investigation of Equid herpesvirus 1 infection in New Zealand. Vet. Microbiol. 2015;176(3):219–228.
    doi: 10.1016/j.vetmic.2015.01.016pubmed: 25666453google scholar: lookup
  25. Edington N, Bridges CG, Patel JR. Endothelial cell infection and thrombosis in paralysis caused by equid herpesvirus-1: equine stroke. Arch. Virol. 1986;90(1-2):111–124.
    doi: 10.1007/BF01314149pubmed: 3015074google scholar: lookup
  26. Edington N, Smyth B, Griffiths L. The role of endothelial cell infection in the endometrium, placenta and foetus of equid herpesvirus 1 (EHV-1) abortions. J. Comp. Pathol. 1991;104(4):379–387.
    doi: 10.1016/s0021-9975(08)80148-xpubmed: 1651960google scholar: lookup
  27. El Brini Z, Fassi Fihri O, Paillot R, Lotfi C, Amraoui F, El Ouadi H, Dehhaoui M, Colitti B, Alyakine H, Piro M. Seroprevalence of Equine Herpesvirus 1 (EHV-1) and Equine Herpesvirus 4 (EHV-4) in the Northern Moroccan Horse Populations. Animal Open Access J. MDPI 2021;11(10):2851.
    doi: 10.3390/ani11102851pmc: PMC8532652pubmed: 34679874google scholar: lookup
  28. Ferrara F, Molesti E, Böttcher-Friebertshäuser E, Cattoli G, Corti D, Scott SD, Temperton NJ. The human Transmembrane Protease Serine 2 is necessary for the production of Group 2 influenza A virus pseudotypes. J. Mol. Genet. Med. 2012;7:309–314.
    pmc: PMC3614188pubmed: 23577043doi: ma14/14google scholar: lookup
  29. Ferrara F, Molesti E, Temperton N. The application of pseudotypes to Influenza pandemic preparedness. Future Virol. 2015;10(6):731–749.
    doi: 10.2217/fvl.15.36google scholar: lookup
  30. Ferrara F, Temperton N. Pseudotype Neutralization Assays: From Laboratory Bench to Data Analysis. Methods Protoc. 2018;1(1):8.
    doi: 10.3390/mps1010008pmc: PMC6526431pubmed: 31164554google scholar: lookup
  31. Frampton AR, Goins WF, Cohen JB, von Einem J, Osterrieder N, O'Callaghan DJ, Glorioso JC. Equine herpesvirus 1 utilizes a novel herpesvirus entry receptor. J. Virol. 2005;79(5):3169–3173.
    doi: 10.1128/JVI.79.5.3169-3173.2005pmc: PMC548480pubmed: 15709036google scholar: lookup
  32. Frampton AR, Stolz DB, Uchida H, Goins WF, Cohen JB, Glorioso JC. Equine herpesvirus 1 enters cells by two different pathways, and infection requires the activation of the cellular kinase ROCK1. J. Virol. 2007;81(20):10879–10889.
    doi: 10.1128/JVI.00504-07pmc: PMC2045510pubmed: 17670830google scholar: lookup
  33. Galvin P, Gildea S, Arkins S, Walsh C, Cullinane A. The evaluation of a nucleoprotein ELISA for the detection of equine influenza antibodies and the differentiation of infected from vaccinated horses (DIVA). Influenza Other Respir. Viruses 2013;7(s4):73–80.
    doi: 10.1111/irv.12195pmc: PMC5655885pubmed: 24224822google scholar: lookup
  34. Gilkerson JR, Love DN, Whalley JM. Incidence of equine herpesvirus 1 infection in Thoroughbred weanlings on two stud farms. Aust. Vet. J. 2000;78(4):277–278.
    doi: 10.1111/j.1751-0813.2000.tb11757.xpubmed: 10840577google scholar: lookup
  35. Gilkerson JR, Whalley JM, Drummer HE, Studdert MJ, Love DN. Epidemiological studies of equine herpesvirus 1 (EHV-1) in Thoroughbred foals: a review of studies conducted in the Hunter Valley of New South Wales between 1995 and 1997. Vet. Microbiol. 1999;68(1-2):15–25.
    doi: 10.1016/s0378-1135(99)00057-7pubmed: 10501158google scholar: lookup
  36. Haid S, Grethe C, Bankwitz D, Grunwald T, Pietschmann T, Lyles DS. Identification of a Human Respiratory Syncytial Virus Cell Entry Inhibitor by Using a Novel Lentiviral Pseudotype System. J. Virol. 2016;90(6):3065–3073.
    doi: 10.1128/JVI.03074-15pmc: PMC4810627pubmed: 26719246google scholar: lookup
  37. Harald G, GK B, Walter F, Jutta V, Nikolaus O, CM T. Egress of Alphaherpesviruses: Comparative Ultrastructural Study. J. Virol. 2001;75(8):3675–3684.
    doi: 10.1128/JVI.75.8.3675-3684.2001pmc: PMC114859pubmed: 11264357google scholar: lookup
  38. Hartley CA, Wilks CR, Studdert MJ, Gilkerson JR. Comparison of antibody detection assays for the diagnosis of equine herpesvirus 1 and 4 infections in horses. Am. J. Vet. Res. 2005;66(5):921–928.
    doi: 10.2460/ajvr.2005.66.921pubmed: 15934623google scholar: lookup
  39. Jiang W, Hua R, Wei M, Li C, Qiu Z, Yang X, Zhang C. An optimized method for high-titer lentivirus preparations without ultracentrifugation. Sci. Rep. 2015;5(1):13875.
    doi: 10.1038/srep13875pmc: PMC4562269pubmed: 26348152google scholar: lookup
  40. Kemenesi G, Tóth GE, Mayora-Neto M, Scott S, Temperton N, Wright E, Mühlberger E, Hume AJ, Suder EL, Zana B, Boldogh SA, Görföl T, Estók P, Szentiványi T, Lanszki Z, Somogyi BA, Nagy Á, Pereszlényi CI, Dudás G, Jakab F. Isolation of infectious Lloviu virus from Schreiber's bats in Hungary. Nat. Commun. 2022;13(1):1706.
    doi: 10.1038/s41467-022-29298-1pmc: PMC8971391pubmed: 35361761google scholar: lookup
  41. King B, Temperton N, Grehan K, Scott S, Wright E, Tarr A, Daly J. Troubleshooting methods for the generation of novel pseudotyped viruses. Future Virol. 2016;11(1):47–59.
    doi: 10.2217/fvl.15.106google scholar: lookup
  42. Kinsley R, Pronost S, De Bock M, Temperton N, Daly JM, Paillot R, Scott S. Evaluation of a Pseudotyped Virus Neutralisation Test for the Measurement of Equine Influenza Virus-Neutralising Antibody Responses Induced by Vaccination and Infection. Vaccines 2020;8(3):466.
    doi: 10.3390/vaccines8030466pmc: PMC7565038pubmed: 32825702google scholar: lookup
  43. Kurtz BM, Singletary LB, Kelly SD, Frampton AR. Equus caballus Major Histocompatibility Complex Class I Is an Entry Receptor for Equine Herpesvirus Type 1. J. Virol. 2010;84(18):9027.
    doi: 10.1128/JVI.00287-10pmc: PMC2937649pubmed: 20610718google scholar: lookup
  44. Kydd JH, Smith KC, Hannant D, Livesay GJ, Mumford JA. Distribution of equid herpesvirus-1 (EHV-1) in respiratory tract associated lymphoid tissue: implications for cellular immunity. Equine Vet. J. 1994;26(6):470–473.
    doi: 10.1111/j.2042-3306.1994.tb04052.xpubmed: 7889921google scholar: lookup
  45. Lunn DP, Davis-Poynter N, Flaminio MJ, Horohov DW, Osterrieder K, Pusterla N, Townsend HG. Equine herpesvirus-1 consensus statement. J. Vet. Intern. Med. 2009;23(3):450–461.
    doi: 10.1111/j.1939-1676.2009.0304.xpubmed: 19645832google scholar: lookup
  46. Maclachlan Dubovi EJBSWSD E, Winton NJ. Chapter 9 - Herpesvirales. Fenner's Veterinary Virology (Fifth Edition) 2017;pp. 189–216.
  47. Mather ST, Wright E, Scott SD, Temperton NJ. Lyophilisation of influenza, rabies and Marburg lentiviral pseudotype viruses for the development and distribution of a neutralisation -assay-based diagnostic kit. J. Virol. Methods 2014;210:51–58.
    pubmed: 25286181
  48. Mayora-Neto M, Wright E, Temperton N, Soema P, ten Have R, Ploemen I, Scott S. Application and comparison of lyophilisation protocols to enhance stable long-term storage of filovirus pseudotypes for use in antibody neutralisation tests. J. Appl. Microbiol. 2023;134(2):lxac067.
    doi: 10.1093/jambio/lxac067pubmed: 36724296google scholar: lookup
  49. Neubauer A, Braun B, Brandmuller C, Kaaden OR, Osterrieder N. Analysis of the contributions of the equine herpesvirus 1 glycoprotein gB homolog to virus entry and direct cell-to-cell spread. Virology 1997;227(2):281–294.
    doi: 10.1006/viro.1996.8336pubmed: 9018127google scholar: lookup
  50. Nielsen SS, Alvarez J, Bicout DJ, Calistri P, Canali E, Drewe JA, Garin-Bastuji B, Gonzales Rojas JL, Gortázar C, Herskin M, Michel V, Miranda Chueca MÁ, Roberts HC, Padalino B, Pasquali P, Spoolder H, Ståhl K, Calvo AV, Viltrop A, Van der Stede Y. Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): infection with Equine Herpesvirus-1. EFSA J. 2022;20(1):e07036.
    doi: 10.2903/j.efsa.2022.7036pmc: PMC8753587pubmed: 35035581google scholar: lookup
  51. Niwa H, Yamamura K, Miyazaki J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 1991;108(2):193–199.
    doi: 10.1016/0378-1119(91)90434-dpubmed: 1660837google scholar: lookup
  52. Nugent J, Birch-Machin I, Smith KC, Mumford JA, Swann Z, Newton JR, Bowden RJ, Allen GP, Davis-Poynter N. Analysis of equid herpesvirus 1 strain variation reveals a point mutation of the DNA polymerase strongly associated with neuropathogenic versus nonneuropathogenic disease outbreaks. J. Virol. 2006;80(8):4047–4060.
    doi: 10.1128/JVI.80.8.4047-4060.2006pmc: PMC1440451pubmed: 16571821google scholar: lookup
  53. OIE. Equine rhinopneumonitis (Infection with equid herpesvirus-1 and -4). Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2018;pp. 1320–1332.
  54. Osterrieder N. Construction and characterization of an equine herpesvirus 1 glycoprotein C negative mutant. Virus Res. 1999;59(2):165–177.
    doi: 10.1016/s0168-1702(98)00134-8pubmed: 10082388google scholar: lookup
  55. Paillot R, Case R, Ross J, Newton R, Nugent J. Equine Herpes Virus-1: Virus, Immunity and Vaccines. Open Veter. Sci. J. 2008;2:68–91.
    doi: 10.2174/1874318808002010068google scholar: lookup
  56. Patel JR, Edington N, Mumford JA. Variation in cellular tropism between isolates of equine herpesvirus-1 in foals. Arch. Virol. 1982;74(1):41–51.
    doi: 10.1007/BF01320781pubmed: 6297429google scholar: lookup
  57. Peterson RB, Goyal SM. Propagation and quantitation of animal herpesviruses in eight cell culture systems. Comp. Immunol. Microbiol. Infect. Dis. 1988;11(2):93–98.
    doi: 10.1016/0147-9571(88)90023-9pubmed: 2846231google scholar: lookup
  58. Prion S, Haerling K. Making Sense of Methods and Measurement: Pearson Product-Moment Correlation Coefficient. Clin. Simulat. Nurs. 2014;10:587–588.
    doi: 10.1016/j.ecns.2014.07.010google scholar: lookup
  59. Pusterla N, Mapes S, Madigan JE, Maclachlan NJ, Ferraro GL, Watson JL, Spier SJ, Wilson WD. Prevalence of EHV-1 in adult horses transported over long distances. Vet. Rec. 2009;165(16):473–475.
    doi: 10.1136/vr.165.16.473pubmed: 19850855google scholar: lookup
  60. Rogalin HB, Heldwein EE. Characterization of Vesicular Stomatitis Virus Pseudotypes Bearing Essential Entry Glycoproteins gB, gD, gH, and gL of Herpes Simplex Virus 1. J. Virol. 2016;90(22):10321–10328.
    doi: 10.1128/JVI.01714-16pmc: PMC5105666pubmed: 27605677google scholar: lookup
  61. Sasaki M, Hasebe R, Makino Y, Suzuki T, Fukushi H, Okamoto M, Matsuda K, Taniyama H, Sawa H, Kimura T. Equine major histocompatibility complex class I molecules act as entry receptors that bind to equine herpesvirus-1 glycoprotein D. Gene Cell Devot. Mol. Cell. Mech. 2011;16(4):343–357.
    doi: 10.1111/j.1365-2443.2011.01491.xpmc: PMC3118799pubmed: 21306483google scholar: lookup
  62. Scott S, Molesti E, Temperton N, Ferrara F, Böttcher-Friebertshäuser E, Daly J. The use of equine influenza pseudotypes for serological screening. J. Mol. Genet. Med. 2012;6:304–308.
    doi: 10.4172/1747-0862.1000054pmc: PMC3601075pubmed: 23515229google scholar: lookup
  63. Scott SD, Kinsley R, Temperton N, Daly JM. The Optimisation of Pseudotyped Viruses for the Characterisation of Immune Responses to Equine Influenza Virus. Pathogens 2016;5(4):68.
    doi: 10.3390/pathogens5040068pmc: PMC5198168pubmed: 27983716google scholar: lookup
  64. Sušac L, Vuong MT, Thomas C, von Bülow S, O'Brien-Ball C, Santos AM, Fernandes RA, Hummer G, Tampé R, Davis SJ. Structure of a fully assembled tumor-specific T cell receptor ligated by pMHC. Cell 2022;185(17):3201–3213.
    doi: 10.1016/j.cell.2022.07.010pmc: PMC9630439pubmed: 35985289google scholar: lookup
  65. Sutton G, Garvey M, Cullinane A, Jourdan M, Fortier C, Moreau P, Foursin M, Gryspeerdt A, Maisonnier V, Marcillaud-Pitel C, Legrand L, Paillot R, Pronost S. Molecular Surveillance of EHV-1 Strains Circulating in France during and after the Major 2009 Outbreak in Normandy Involving Respiratory Infection, Neurological Disorder, and Abortion. Viruses 2019;11(10):916.
    doi: 10.3390/v11100916pmc: PMC6832873pubmed: 31590336google scholar: lookup
  66. Sutton G, Thieulent C, Fortier C, Hue ES, Marcillaud-Pitel C, Pléau A, Deslis A, Guitton E, Paillot R, Pronost S. Identification of a New Equid Herpesvirus 1 DNA Polymerase (ORF30) Genotype with the Isolation of a C(2254)/H(752) Strain in French Horses Showing no Major Impact on the Strain Behaviour. Viruses 2020;12(10):1160.
    doi: 10.3390/v12101160pmc: PMC7650556pubmed: 33066315google scholar: lookup
  67. Tearle JP, Smith KC, Platt AJ, Hannant D, Davis-Poynter NJ, Mumford JA. In vitro characterisation of high and low virulence isolates of equine herpesvirus-1 and -4. Res. Vet. Sci. 2003;75(1):83–86.
    doi: 10.1016/S0034-5288(03)00031-6pubmed: 12801466google scholar: lookup
  68. Telford EA, Watson MS, McBride K, Davison AJ. The DNA sequence of equine herpesvirus-1. Virology 1992;189(1):304–316.
    doi: 10.1016/0042-6822(92)90706-upubmed: 1318606google scholar: lookup
  69. Temperton NJ, Hoschler K, Major D, Nicolson C, Manvell R, Hien VM, Ha DQ, De Jong M, Zambon M, Takeuchi Y, Weiss RA. A sensitive retroviral pseudotype assay for influenza H5N1-neutralizing antibodies. Influenza Other Respir. Viruses 2007;1(3):105–112.
    doi: 10.1111/j.1750-2659.2007.00016.xpmc: PMC4941878pubmed: 19453415google scholar: lookup
  70. Temperton NJ, Wright E, Scott SD. Retroviral Pseudotypes – From Scientific Tools to Clinical Utility. ELS 2015;pp. 1–11.
    doi: 10.1002/9780470015902.a0021549.pub2google scholar: lookup
  71. Thieulent CJ, Sutton G, Toquet MP, Fremaux S, Hue E, Fortier C, Pléau A, Deslis A, Abrioux S, Guitton E, Pronost S, Paillot R. Oral Administration of Valganciclovir Reduces Clinical Signs, Virus Shedding and Cell-Associated Viremia in Ponies Experimentally Infected with the Equid Herpesvirus-1 C2254 Variant. Pathogens 2022;11(5).
    doi: 10.3390/pathogens11050539pmc: PMC9148010pubmed: 35631060google scholar: lookup
  72. Thomson GR, Mumford JA, Campbell J, Griffiths L, Clapham P. Serological detection of equid herpesvirus 1 infections of the respiratory tract. Equine Vet. J. 1976;8(2):58–65.
    doi: 10.1111/j.2042-3306.1976.tb03291.xpubmed: 177281google scholar: lookup
  73. USDA-APHIS. Equine herpesvirus Myeloencephalopathy: a potentially emerging disease. 2007.
  74. Wang P, Chen J, Zheng A, Nie Y, Shi X, Wang W, Wang G, Luo M, Liu H, Tan L, Song X, Wang Z, Yin X, Qu X, Wang X, Qing T, Ding M, Deng H. Expression cloning of functional receptor used by SARS coronavirus. Biochem. Biophys. Res. Commun. 2004;315(2):439–444.
    doi: 10.1016/j.bbrc.2004.01.076pmc: PMC7111169pubmed: 14766227google scholar: lookup
  75. Wang W, Xie H, Ye Z, Vassell R, Weiss CD. Characterization of lentiviral pseudotypes with influenza H5N1 hemagglutinin and their performance in neutralization assays. J. Virol. Methods 2010;165(2):305–310.
    doi: 10.1016/j.jviromet.2010.02.009pubmed: 20153374google scholar: lookup
  76. Warda FF, Ahmed HES, Shafik NG, Mikhael CA, Abd-ElAziz HMG, Mohammed WA, Shosha EA. Application of equine herpesvirus-1 vaccine inactivated by both formaldehyde and binary ethylenimine in equine. Vet. World 2021;14(7):1815–1821.
    doi: 10.14202/vetworld.2021.1815-1821pmc: PMC8404127pubmed: 34475703google scholar: lookup
  77. Whalley JM, Ruitenberg KM, Sullivan K, Seshadri L, Hansen K, Birch D, Gilkerson JR, Wellington JE. Host cell tropism of equine herpesviruses: glycoprotein D of EHV-1 enables EHV-4 to infect a non-permissive cell line. Arch. Virol. 2007;152(4):717–725.
    doi: 10.1007/s00705-006-0885-xpubmed: 17171298google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.