1887

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Volume 89, Issue 3

An MHC-restricted CD8 T-cell response is induced in cattle by foot-and-mouth disease virus (FMDV) infection and also following vaccination with inactivated FMDV Free

Abstract

Foot-and-mouth disease virus (FMDV) causes a highly contagious disease of cloven-hooved animals that carries enormous economic consequences. CD8 cytotoxic T lymphocytes play an important role in protection and disease outcome in viral infections but, to date, the role of the CD8 T-cell immune response to FMDV remains unclear. This study aimed to investigate major histocompatibility complex (MHC) class I-restricted CD8 T-cell responses to FMDV in vaccinated and in infected cattle. An assay was used to detect antigen-specific gamma interferon release by CD8 T cells in FMDV-infected cattle of known MHC class I genotypes. A significant MHC class I-restricted CD8 T-cell response was detected to both FMDV strain O1 BFS and a recombinant fowlpox virus expressing the structural proteins of FMDV. Antigen-specific MHC class I-restricted CD8 T-cell responses were also detected in cattle vaccinated with inactivated FMDV. These responses were shown to be directed, at least in part, to epitopes within the structural proteins (P12A region) of the virus. By using mouse cells expressing single cattle MHC class I alleles, it was possible to identify the restriction elements in each case. Identification of these epitopes will facilitate the quantitative and qualitative analysis of FMDV-specific memory CD8 T cells in cattle and help to ensure that potential vaccines induce a qualitatively appropriate CD8 T-cell response.

  • Received:
  • Accepted:
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2008-03-01
2024-04-18
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References

  1. Arguello J. R., Little A. M., Pay A. L., Gallardo D., Rojas I., Marsh S. G., Goldman J. M., Madrigal J. A. 1998; Mutation detection and typing of polymorphic loci through double-strand conformation analysis. Nat Genet 18:192–194 [CrossRef]
     [Google Scholar]
  2. Barteling S. J., Vreeswijk J. 1991; Developments in foot-and-mouth disease vaccines. Vaccine 9:75–88 [CrossRef]
     [Google Scholar]
  3. Bautista E. M., Ferman G. S., Golde W. T. 2003; Induction of lymphopenia and inhibition of T cell function during acute infection of swine with foot and mouth disease virus (FMDV). Vet Immunol Immunopathol 92:61–73 [CrossRef]
     [Google Scholar]
  4. Birch J., Murphy L., MacHugh N. D., Ellis S. A. 2006; Generation and maintenance of diversity in the cattle MHC class I region. Immunogenetics 58:670–679 [CrossRef]
     [Google Scholar]
  5. Blanco E., Garcia-Briones M., Sanz-Parra A., Gomes P., De Oliveira E., Valero M. L., Andreu D., Ley V., Sobrino F. 2001; Identification of T-cell epitopes in nonstructural proteins of foot-and-mouth disease virus. J Virol 75:3164–3174 [CrossRef]
     [Google Scholar]
  6. Bohm W., Schirmbeck R., Elbe A., Melber K., Diminky D., Kraal G., van Rooijen N., Barenholz Y., Reimann J. 1995; Exogenous hepatitis B surface antigen particles processed by dendritic cells or macrophages prime murine MHC class I-restricted cytotoxic T lymphocytes in vivo. J Immunol 155:3313–3321
     [Google Scholar]
  7. Bruce C. J., Howard C. J., Thomas L. H., Tempest P. R., Taylor G. 1999; Depletion of bovine CD8+ T cells with chCC63, a chimaeric mouse-bovine antibody. Vet Immunol Immunopathol 71:215–231 [CrossRef]
     [Google Scholar]
  8. Childerstone A. J., Cedillo-Baron L., Foster-Cuevas M., Parkhouse R. M. 1999; Demonstration of bovine CD8+ T-cell responses to foot-and-mouth disease virus. J Gen Virol 80:663–669
     [Google Scholar]
  9. Da Silva D. M., Fausch S. C., Verbeek J. S., Kast W. M. 2007; Uptake of human papillomavirus virus-like particles by dendritic cells is mediated by Fc γ receptors and contributes to acquisition of T cell immunity. J Immunol 178:7587–7597 [CrossRef]
     [Google Scholar]
  10. Davis W. C., Brown W. C., Hamilton M. J., Wyatt C. R., Orden J. A., Khalid A. M., Naessens J. 1996; Analysis of monoclonal antibodies specific for the γδ TcR. Vet Immunol Immunopathol 52:275–283 [CrossRef]
     [Google Scholar]
  11. Domingo E., Escarmis C., Baranowski E., Ruiz-Jarabo C. M., Carrillo E., Nunez J. I., Sobrino F. 2003; Evolution of foot-and-mouth disease virus. Virus Res 91:47–63 [CrossRef]
     [Google Scholar]
  12. Ellis S. A., Staines K. A., Morrison W. I. 1996; cDNA sequence of cattle MHC class I genes transcribed in serologically defined haplotypes A18 and A31. Immunogenetics 43:156–159
     [Google Scholar]
  13. Ellis S. A., Staines K. A., Stear M. J., Hensen E. J., Morrison W. I. 1998; DNA typing for BoLA class I using sequence-specific primers (PCR-SSP. Eur J Immunogenet 25:365–370 [CrossRef]
     [Google Scholar]
  14. Ellis S. A., Holmes E. C., Staines K. A., Smith K. B., Stear M. J., McKeever D. J., MacHugh N. D., Morrison W. I. 1999; Variation in the number of expressed MHC genes in different cattle class I haplotypes. Immunogenetics 50:319–328 [CrossRef]
     [Google Scholar]
  15. Fikri Y., Nyabenda J., Denis M., Pastoret P. P. 2000; Purification and characterisation of bovine WC1+ γδ T lymphocytes from peripheral blood. Vet Res 31:229–239 [CrossRef]
     [Google Scholar]
  16. Gaddum R. M., Ellis S. A., Willis A. C., Cook R. S., Staines K. A., Thomas L. H., Taylor G. 1996; Identification of potential CTL epitopes of bovine RSV using allele-specific peptide motifs from bovine MHC class I molecules. Vet Immunol Immunopathol 54:211–219 [CrossRef]
     [Google Scholar]
  17. Garcia-Briones M. M., Russell G. C., Oliver R. A., Tami C., Taboga O., Carrillo E., Palma E. L., Sobrino F., Glass E. J. 2000; Association of bovine DRB3 alleles with immune response to FMDV peptides and protection against viral challenge. Vaccine 19:1167–1171 [CrossRef]
     [Google Scholar]
  18. Garcia-Briones M. M., Blanco E., Chiva C., Andreu D., Ley V., Sobrino F. 2004; Immunogenicity and T cell recognition in swine of foot-and-mouth disease virus polymerase 3D. Virology 322:264–275 [CrossRef]
     [Google Scholar]
  19. Gerner W., Denyer M. S., Takamatsu H. H., Wileman T. E., Wiesmuller K. H., Pfaff E., Saalmuller A. 2006; Identification of novel foot-and-mouth disease virus specific T-cell epitopes in c/c and d/d haplotype miniature swine. Virus Res 121:223–228 [CrossRef]
     [Google Scholar]
  20. Glass E. J., Oliver R. A., Collen T., Doel T. R., Dimarchi R., Spooner R. L. 1991; MHC class II restricted recognition of FMDV peptides by bovine T cells. Immunology 74:594–599
     [Google Scholar]
  21. Grubman M. J., Baxt B. 2004; Foot-and-mouth disease. Clin Microbiol Rev 17:465–493 [CrossRef]
     [Google Scholar]
  22. Howard C. J., Sopp P., Parsons K. R., Finch J. 1989; In vivo depletion of BoT4 (CD4) and of non-T4/T8 lymphocyte subsets in cattle with monoclonal antibodies. Eur J Immunol 19:757–764 [CrossRef]
     [Google Scholar]
  23. Ilott M. C., Salt J. S., Gaskell R. M., Kitching R. P. 1997; Dexamethasone inhibits virus production and the secretory IgA response in oesophageal-pharyngeal fluid in cattle persistently infected with foot-and-mouth disease virus. Epidemiol Infect 118:181–187 [CrossRef]
     [Google Scholar]
  24. 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 [CrossRef]
     [Google Scholar]
  25. Laidlaw S. M., Skinner M. A. 2004; Comparison of the genome sequence of FP9, an attenuated, tissue culture-adapted European strain of fowlpox virus, with those of virulent American and European viruses. J Gen Virol 85:305–322 [CrossRef]
     [Google Scholar]
  26. MacHugh N. D., Bensaid A., Howard C. J., Davis W. C., Morrison W. I. 1991; Analysis of the reactivity of anti-bovine CD8 monoclonal antibodies with cloned T cell lines and mouse L-cells transfected with bovine CD8. Vet Immunol Immunopathol 27:169–172 [CrossRef]
     [Google Scholar]
  27. Mason P. W., Chinsangaram J., Moraes M. P., Mayr G. A., Grubman M. J. 2003; Engineering better vaccines for foot-and-mouth disease. Dev Biol (Basel 114:79–88
     [Google Scholar]
  28. Mbawuike I. N., Wyde P. R. 1993; Induction of CD8+ cytotoxic T cells by immunization with killed influenza virus and effect of cholera toxin B subunit. Vaccine 11:1205–1213 [CrossRef]
     [Google Scholar]
  29. McCullough K. C., De Simone F., Brocchi E., Capucci L., Crowther J. R., Kihm U. 1992; Protective immune response against foot-and-mouth disease. J Virol 66:1835–1840
     [Google Scholar]
  30. Mezencio J. M., Babcock G. D., Meyer R. F., Lubroth J., Salt J. S., Newman J. F., Brown F. 1998; Differentiating foot-and-mouth disease virus-infected from vaccinated animals with baculovirus-expressed specific proteins. Vet Q 20:Suppl. 2S11–S13 [CrossRef]
     [Google Scholar]
  31. Morrison W. I. 1996; Influence of host and parasite genotypes on immunological control of Theileria parasites. Parasitology 112:SupplS53–S66
     [Google Scholar]
  32. Morrison W. I., Howard C. J., Hinson C. J., MacHugh N. D., Sopp P. 1994; Identification of three distinct allelic forms of bovine CD4. Immunology 83:589–594
     [Google Scholar]
  33. Oem J. K., Chang B. S., Joo H. D., Yang M. Y., Kim G. J., Park J. Y., Ko Y. J., Kim Y. J., Park J. H., Joo Y. S. 2007; Development of an epitope-blocking-enzyme-linked immunosorbent assay to differentiate between animals infected with and vaccinated against foot-and-mouth disease virus. J Virol Methods 142:174–181 [CrossRef]
     [Google Scholar]
  34. Qingzhong Y., Barrett T., Brown T. D., Cook J. K., Green P., Skinner M. A., Cavanagh D. 1994; Protection against turkey rhinotracheitis pneumovirus (TRTV) induced by a fowlpox virus recombinant expressing the TRTV fusion glycoprotein (F). Vaccine 12:569–573 [CrossRef]
     [Google Scholar]
  35. Racaniello V. R. 2006; Picornaviridae : the viruses and their replication. In Fields Virology , 5th edn. pp 795–838Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams & Wilkins;
     [Google Scholar]
  36. Rodriguez A., Ley V., Ortuno E., Ezquerra A., Saalmuller A., Sobrino F., Saiz J. C. 1996; A porcine CD8+ T cell clone with heterotypic specificity for foot-and-mouth disease virus. J Gen Virol 77:2089–2096 [CrossRef]
     [Google Scholar]
  37. Schirmbeck R., Deml L., Melber K., Wolf H., Wagner R., Reimann J. 1995; Priming of class I-restricted cytotoxic T lymphocytes by vaccination with recombinant protein antigens. Vaccine 13:857–865 [CrossRef]
     [Google Scholar]
  38. Scudamore J. M., Harris D. M. 2002; Control of foot and mouth disease: lessons from the experience of the outbreak in Great Britain in 2001. Rev Sci Tech 21:699–710
     [Google Scholar]
  39. Sedlik C., Saron M., Sarraseca J., Casal I., Leclerc C. 1997; Recombinant parvovirus-like particles as an antigen carrier: a novel nonreplicative exogenous antigen to elicit protective antiviral cytotoxic T cells. Proc Natl Acad Sci U S A 94:7503–7508 [CrossRef]
     [Google Scholar]
  40. Sedlik C., Dridi A., Deriaud E., Saron M. F., Rueda P., Sarraseca J., Casal J. I., Leclerc C. 1999; Intranasal delivery of recombinant parvovirus-like particles elicits cytotoxic T-cell and neutralizing antibody responses. J Virol 73:2739–2744
     [Google Scholar]
  41. Shen F., Chen P. D., Walfield A. M., Ye J., House J., Brown F., Wang C. Y. 1999; Differentiation of convalescent animals from those vaccinated against foot-and-mouth disease by a peptide ELISA. Vaccine 17:3039–3049 [CrossRef]
     [Google Scholar]
  42. Sopp P., Howard C. J. 1997; Cross-reactivity of monoclonal antibodies to defined human leucocyte differentiation antigens with bovine cells. Vet Immunol Immunopathol 56:11–25 [CrossRef]
     [Google Scholar]
  43. Thompson D., Muriel P., Russell D., Osborne P., Bromley A., Rowland M., Creigh-Tyte S., Brown C. 2002; Economic costs of the foot and mouth disease outbreak in the United Kingdom in 2001. Rev Sci Tech 21:675–687
     [Google Scholar]
  44. Townsend A. R., Gotch F. M., Davey J. 1985; Cytotoxic T cells recognize fragments of the influenza nucleoprotein. Cell 42:457–467 [CrossRef]
     [Google Scholar]
  45. Townsend A. R., Rothbard J., Gotch F. M., Bahadur G., Wraith D., McMichael A. J. 1986; The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell 44:959–968 [CrossRef]
     [Google Scholar]
  46. Van Lierop M. J., Nilsson P. R., Wagenaar J. P., Van Noort J. M., Campbell J. D., Glass E. J., Joosten I., Hensen E. J. 1995; The influence of MHC polymorphism on the selection of T-cell determinants of FMDV in cattle. Immunology 84:79–85
     [Google Scholar]
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An MHC-restricted CD8+ T-cell response is induced in cattle by foot-and-mouth disease virus (FMDV) infection and also following vaccination with inactivated FMDV
J. Gen. Virol. 89, 667 (2008); https://doi.org/10.1099/vir.0.83417-0
/content/journal/jgv/10.1099/vir.0.83417-0
/content/journal/jgv/10.1099/vir.0.83417-0
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