1887

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Volume 95, Issue 8

Immediate-early protein of equid herpesvirus type 1 as a target for cytotoxic T-lymphocytes in the Thoroughbred horse Free

Abstract

Cytotoxic T-lymphocytes (CTLs) are associated with protective immunity against disease caused by equid herpesvirus type 1 (EHV-1). However, the EHV-1 target proteins for CTLs are poorly defined. This limits the development of vaccine candidates designed to stimulate strong CTL immunity. Here, classical CTL assays using lymphocytes from horses of three defined MHC class I types that experienced natural infection with EHV-1 and a modified vaccinia virus construct containing an EHV-1 gene encoding the immediate-early (IE) protein are reported. Horses homozygous for the equine leukocyte antigen (ELA)-A2 haplotype, but not the ELA-A5 haplotype, produced MHC-restricted CTL responses against the IE protein. Previously, horses homozygous for the ELA-A3 haplotype also mounted CTL responses against the IE protein. Both haplotypes are common in major horse breeds, including the Thoroughbred. Thus, the IE protein is an attractive candidate molecule for future studies of T-cell immunity to EHV-1 in the horse.

  • Received:
  • Accepted:
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© 2014 The Authors
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2014-08-01
2024-04-24
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References

  1. Allen G. P. 2008; Risk factors for development of neurologic disease after experimental exposure to equine herpesvirus-1 in horses. Am J Vet Res 69:1595–1600 [View Article][PubMed]
     [Google Scholar]
  2. Allen G., Yeargan M., Costa L. R., Cross R. 1995; Major histocompatibility complex class I-restricted cytotoxic T-lymphocyte responses in horses infected with equine herpesvirus 1. J Virol 69:606–612[PubMed]
     [Google Scholar]
  3. Ambagala A. P., Solheim J. C., Srikumaran S. 2005; Viral interference with MHC class I antigen presentation pathway: the battle continues. Vet Immunol Immunopathol 107:1–15 [View Article][PubMed]
     [Google Scholar]
  4. Antczak D. F., Bailey E., Barger B., Bell T. K., Bernoco D., Bull R. W., Byrns G., Guerin G., Lazary S.other authors 1986; Joint report of the Third International Workshop on Lymphocyte Alloantigens of the Horse, Kennett Square, Pennsylvania, 25–27 April 1984. Anim Genet 17:363–373 [View Article][PubMed]
     [Google Scholar]
  5. Arvin A. M., Sharp M., Smith S., Koropchak C. M., Diaz P. S., Kinchington P., Ruyechan W., Hay J. 1991; Equivalent recognition of a varicella-zoster virus immediate early protein (IE62) and glycoprotein I by cytotoxic T lymphocytes of either CD4+ or CD8+ phenotype. J Immunol 146:257–264[PubMed]
     [Google Scholar]
  6. Bergen R. E., Sharp M., Sanchez A., Judd A. K., Arvin A. M. 1991; Human T cells recognize multiple epitopes of an immediate early/tegument protein (IE62) and glycoprotein I of varicella zoster virus. Viral Immunol 4:151–166 [View Article][PubMed]
     [Google Scholar]
  7. Chung C., Leib S. R., Fraser D. G., Ellis S. A., McGuire T. C. 2003; Novel classical MHC class I alleles identified in horses by sequencing clones of reverse transcription-PCR products. Eur J Immunogenet 30:387–396 [View Article][PubMed]
     [Google Scholar]
  8. Goehring L. S., Wagner B., Bigbie R., Hussey S. B., Rao S., Morley P. S., Lunn D. P. 2010; Control of EHV-1 viremia and nasal shedding by commercial vaccines. Vaccine 28:5203–5211 [View Article][PubMed]
     [Google Scholar]
  9. Griffin B. D., Verweij M. C., Wiertz E. J. 2010; Herpesviruses and immunity: the art of evasion. Vet Microbiol 143:89–100 [View Article][PubMed]
     [Google Scholar]
  10. Gustafson A. L., Tallmadge R. L., Ramlachan N., Miller D., Bird H., Antczak D. F., Raudsepp T., Chowdhary B. P., Skow L. C. 2003; An ordered BAC contig map of the equine major histocompatibility complex. Cytogenet Genome Res 102:189–195 [View Article][PubMed]
     [Google Scholar]
  11. Hannant D., Jessett D. M., O’Neill T., Dolby C. A., Cook R. F., Mumford J. A. 1993; Responses of ponies to equid herpesvirus-1 ISCOM vaccination and challenge with virus of the homologous strain. Res Vet Sci 54:299–305 [View Article][PubMed]
     [Google Scholar]
  12. Hart J., MacHugh N. D., Morrison W. I. 2011; Theileria annulata-transformed cell lines are efficient antigen-presenting cells for in vitro analysis of CD8 T cell responses to bovine herpesvirus-1. Vet Res 42:119 [View Article][PubMed]
     [Google Scholar]
  13. Heldens J. G., Hannant D., Cullinane A. A., Prendergast M. J., Mumford J. A., Nelly M., Kydd J. H., Weststrate M. W., van den Hoven R. 2001; Clinical and virological evaluation of the efficacy of an inactivated EHV1 and EHV4 whole virus vaccine (Duvaxyn EHV1,4). Vaccination/challenge experiments in foals and pregnant mares. Vaccine 19:4307–4317 [View Article][PubMed]
     [Google Scholar]
  14. Holmes M. A., Townsend H. G., Kohler A. K., Hussey S., Breathnach C., Barnett C., Holland R., Lunn D. P. 2006; Immune responses to commercial equine vaccines against equine herpesvirus-1, equine influenza virus, eastern equine encephalomyelitis, and tetanus. Vet Immunol Immunopathol 111:67–80 [View Article][PubMed]
     [Google Scholar]
  15. Kern F., Bunde T., Faulhaber N., Kiecker F., Khatamzas E., Rudawski I. M., Pruss A., Gratama J. W., Volkmer-Engert R.other authors 2002; Cytomegalovirus (CMV) phosphoprotein 65 makes a large contribution to shaping the T cell repertoire in CMV-exposed individuals. J Infect Dis 185:1709–1716 [View Article][PubMed]
     [Google Scholar]
  16. Kydd J. H., Wattrang E., Hannant D. 2003; Pre-infection frequencies of equine herpesvirus-1 specific, cytotoxic T lymphocytes correlate with protection against abortion following experimental infection of pregnant mares. Vet Immunol Immunopathol 96:207–217 [View Article][PubMed]
     [Google Scholar]
  17. Kydd J. H., Davis-Poynter N. J., Birch J., Hannant D., Minke J., Audonnet J. C., Antczak D. F., Ellis S. A. 2006; A molecular approach to the identification of cytotoxic T-lymphocyte epitopes within equine herpesvirus 1. J Gen Virol 87:2507–2515 [View Article][PubMed]
     [Google Scholar]
  18. Lazary S., Antczak D. F., Bailey E., Bell T. K., Bernoco D., Byrns G., McClure J. J. 1988; Joint Report of the Fifth International Workshop on Lymphocyte Alloantigens of the Horse, Baton Rouge, Louisiana, 31 October–1 November 1987. Anim Genet 19:447–456 [View Article][PubMed]
     [Google Scholar]
  19. Levings R. L., Roth J. A. 2013; Immunity to bovine herpesvirus 1: II. Adaptive immunity and vaccinology. Anim Health Res Rev 14:103–123 [View Article][PubMed]
     [Google Scholar]
  20. Ma G., Azab W., Osterrieder N. 2013; Equine herpesviruses type 1 (EHV-1) and 4 (EHV-4) – masters of co-evolution and a constant threat to equids and beyond. Vet Microbiol 167:123–134 [View Article][PubMed]
     [Google Scholar]
  21. McLaughlin-Taylor E., Pande H., Forman S. J., Tanamachi B., Li C. R., Zaia J. A., Greenberg P. D., Riddell S. R. 1994; Identification of the major late human cytomegalovirus matrix protein pp65 as a target antigen for CD8+ virus-specific cytotoxic T lymphocytes. J Med Virol 43:103–110 [View Article][PubMed]
     [Google Scholar]
  22. Mealey R. H., Lee J. H., Leib S. R., Littke M. H., McGuire T. C. 2006; A single amino acid difference within the alpha-2 domain of two naturally occurring equine MHC class I molecules alters the recognition of Gag and Rev epitopes by equine infectious anemia virus-specific CTL. J Immunol 177:7377–7390 [View Article][PubMed]
     [Google Scholar]
  23. Minke J. M., Audonnet J. C., Fischer L. 2004; Equine viral vaccines: the past, present and future. Vet Res 35:425–443 [View Article][PubMed]
     [Google Scholar]
  24. O’Neill T., Kydd J. H., Allen G. P., Wattrang E., Mumford J. A., Hannant D. 1999; Determination of equid herpesvirus 1-specific, CD8+, cytotoxic T lymphocyte precursor frequencies in ponies. Vet Immunol Immunopathol 70:43–54 [View Article][PubMed]
     [Google Scholar]
  25. Paillot R., Ellis S. A., Daly J. M., Audonnet J. C., Minke J. M., Davis-Poynter N., Hannant D., Kydd J. H. 2006; Characterisation of CTL and IFN-gamma synthesis in ponies following vaccination with a NYVAC-based construct coding for EHV-1 immediate early gene, followed by challenge infection. Vaccine 24:1490–1500 [View Article][PubMed]
     [Google Scholar]
  26. Ramsay J. D., Leib S. R., Orfe L., Call D. R., Tallmadge R. L., Fraser D. G., Mealey R. H. 2010; Development of a DNA microarray for detection of expressed equine classical MHC class I sequences in a defined population. Immunogenetics 62:633–639 [View Article][PubMed]
     [Google Scholar]
  27. Rappocciolo G., Birch J., Ellis S. A. 2003; Down-regulation of MHC class I expression by equine herpesvirus-1. J Gen Virol 84:293–300 [View Article][PubMed]
     [Google Scholar]
  28. Sadzot-Delvaux C., Kinchington P. R., Debrus S., Rentier B., Arvin A. M. 1997; Recognition of the latency-associated immediate early protein IE63 of varicella-zoster virus by human memory T lymphocytes. J Immunol 159:2802–2806[PubMed]
     [Google Scholar]
  29. Said A., Azab W., Damiani A., Osterrieder N. 2012; Equine herpesvirus type 4 UL56 and UL49.5 proteins downregulate cell surface major histocompatibility complex class I expression independently of each other. J Virol 86:8059–8071 [View Article][PubMed]
     [Google Scholar]
  30. Soboll G., Whalley J. M., Koen M. T., Allen G. P., Fraser D. G., Macklin M. D., Swain W. F., Lunn D. P. 2003; Identification of equine herpesvirus-1 antigens recognized by cytotoxic T lymphocytes. J Gen Virol 84:2625–2634 [View Article][PubMed]
     [Google Scholar]
  31. Soboll G., Breathnach C. C., Kydd J. H., Hussey S. B., Mealey R. M., Lunn D. P. 2010; Vaccination of ponies with the IE gene of EHV-1 in a recombinant modified live vaccinia vector protects against clinical and virological disease. Vet Immunol Immunopathol 135:108–117 [View Article][PubMed]
     [Google Scholar]
  32. Splitter G. A., Eskra L., Abruzzini A. F. 1988; Cloned bovine cytolytic T cells recognize bovine herpes virus-1 in a genetically restricted, antigen-specific manner. Immunology 63:145–150[PubMed]
     [Google Scholar]
  33. Tallmadge R. L., Lear T. L., Antczak D. F. 2005; Genomic characterization of MHC class I genes of the horse. Immunogenetics 57:763–774 [View Article][PubMed]
     [Google Scholar]
  34. Tallmadge R. L., Campbell J. A., Miller D. C., Antczak D. F. 2010; Analysis of MHC class I genes across horse MHC haplotypes. Immunogenetics 62:159–172 [View Article][PubMed]
     [Google Scholar]
  35. Tseng C. T., Miller D., Cassano J., Bailey E., Antczak D. F. 2010; Identification of equine major histocompatibility complex haplotypes using polymorphic microsatellites. Anim Genet 41:Suppl. 2150–153 [View Article][PubMed]
     [Google Scholar]
  36. van der Meulen K. M., Favoreel H. W., Pensaert M. B., Nauwynck H. J. 2006; Immune escape of equine herpesvirus 1 and other herpesviruses of veterinary importance. Vet Immunol Immunopathol 111:31–40 [View Article][PubMed]
     [Google Scholar]
  37. Wills M. R., Carmichael A. J., Mynard K., Jin X., Weekes M. P., Plachter B., Sissons J. G. 1996; The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J Virol 70:7569–7579[PubMed]
     [Google Scholar]
  38. Zhang W., Lonning S. M., McGuire T. C. 1998; Gag protein epitopes recognized by ELA-A-restricted cytotoxic T lymphocytes from horses with long-term equine infectious anemia virus infection. J Virol 72:9612–9620[PubMed]
     [Google Scholar]
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Immediate-early protein of equid herpesvirus type 1 as a target for cytotoxic T-lymphocytes in the Thoroughbred horse
J. Gen. Virol. 95, 1783 (2014); https://doi.org/10.1099/vir.0.065888-0
/content/journal/jgv/10.1099/vir.0.065888-0
/content/journal/jgv/10.1099/vir.0.065888-0
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