Assessment of the phenotype and functionality of porcine cd8 t cell responses following vaccination with live attenuated classical swine fever virus (CSFV) and virulent CSFV challenge

Clinical and Vaccine Immunology

Volumn 20, Issue 10, 2013, Pages 1604-1616

  Franzoni, Giulia ^a,b   Kurkure, Nitin V ^a,c   Edgar, Daniel S ^a,b   Everett, Helen E ^a   Gerner, Wilhelm ^d   Bodman Smith, Kikki B ^b   Crooke, Helen R ^a   Grahama, Simon P ^a  

^a VETERINARY LABORATORIES AGENCY   (United Kingdom)

^b UNIVERSITY OF SURREY   (United Kingdom)

^c NAGPUR VETERINARY COLLEGE   (India)

^d UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; HERMES ANTIGEN; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; L SELECTIN; LIVE VACCINE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MEDIATED CYTOTOXICITY; CELLULAR IMMUNITY; CLASSICAL SWINE FEVER; CONTROLLED STUDY; FLOW CYTOMETRY; IMMUNOLOGICAL MEMORY; INFECTION PREVENTION; LYMPHOCYTE FUNCTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; T LYMPHOCYTE SUBPOPULATION; VIRUS STRAIN;

ANIMALS; ANTIGENS, CD; CD8-POSITIVE T-LYMPHOCYTES; CLASSICAL SWINE FEVER; CLASSICAL SWINE FEVER VIRUS; FLOW CYTOMETRY; IMMUNOPHENOTYPING; SWINE; T-LYMPHOCYTE SUBSETS; VIRAL VACCINES;

EID: 84886730383     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00415-13     Document Type: Article

References (53)

1. Moennig V. 2000. Introduction to classical swine fever: virus, disease and control policy. Vet. Microbiol. 73:93-102.
2. van Oirschot JT. 2003. Emergency vaccination against classical swine fever. Dev. Biol. (Basel) 114:259-267.
3. van Oirschot JT. 2003. Vaccinology of classical swine fever: from lab to field. Vet. Microbiol. 96:367-384.
4. Beer M, Reimann I, Hoffmann B, Depner K. 2007. Novel marker vaccines against classical swine fever. Vaccine 25:5665-5670.
5. Suradhat S, Intrakamhaeng M, Damrongwatanapokin S. 2001. The correlation of virus-specific interferon-gamma production and protection against classical swine fever virus infection. Vet. Immunol. Immunopathol. 83:177-189.
6. Graham SP, Everett HE, Haines FJ, Johns HL, Sosan OA, Salguero FJ, Clifford DJ, Steinbach F, Drew TW, Crooke HR. 2012. Challenge of pigs with classical swine fever viruses after C-strain vaccination reveals remarkably rapid protection and insights into early immunity. PLoS One 7:e29310. doi:10.1371/journal.pone.0029310.
7. Graham SP, Haines F, Johns H, Sosan OA, La Rocca SA, Lamp B, Rumenapf T, Everett H, Crooke H. 2012. Characterization of vaccine-induced, broadly cross-reactive IFN-γ secreting T cell responses that correlate with rapid protection against classical swine fever virus. Vaccine 30:2742-2748.
8. Ceppi M, de Bruin MG, Seuberlich T, Balmelli C, Pascolo S, Ruggli N, Wienhold D, Tratschin JD, McCullough KC, Summerfield A. 2005. Identification of classical swine fever virus protein E2 as a target for cytotoxic T cells by using mRNA-transfected antigen presenting cells. J. Gen. Virol. 86:2525-2534.
9. Rau H, Reverts H, Balmelli C, McCullough K, Summerfield A. 2006. Immunological properties of recombinant classical swine fever virus NS3 protein in vitro and in vivo. Vet. Res. 37:155-168.
10. Pauly T, Elbers K, Konig M, Lengsfeld T, Saalmuller A, Thiel HJ. 1995. Classical swine fever virus-specific cytotoxic T lymphocytes and identification of a T cell epitope. J. Gen. Virol. 76:3039-3049.
11. Suradhat S, Sada W, Buranapradiktun S, Damrongwatanapokin S. 2005. The kinetics of cytokine production and CD25 expression by porcine lymphocyte subpopulations following exposure to classical swine fever virus (CSFV). Vet. Immunol. Immunopathol. 106:197-208.
12. Tarradas J, Argilaguet JM, Rosell R, Nofrarias M, Crisci E, Córdoba L, Pérez-Martín E, Díaz I, Rodríguez F, Domingo M, Montoya M, Ganges L. 2010. Interferon-gamma induction correlates with protection by DNA vaccine expressing E2 glycoprotein against classical swine fever virus infection in domestic pigs. Vet. Microbiol. 142:51-58.
13. Tarradas J, Monsó M, Fraile L, de la Torre BG, Muñoz M, Rosell R, Riquelme C, Pérez LJ, Nofrarías M, Domingo M, Sobrino F, Andreu D, Ganges L. 2012. A T-cell epitope on NS3 non-structural protein enhances the B and T cell responses elicited by dendrimeric constructions against CSFV in domestic pigs. Vet. Immunol. Immunopathol. 150:36-46.
14. Kaech SM, Wherry EJ, Ahmed R. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2:251-262.
15. Thakur A, Pedersen L, Jungersen G. 2012. Immune markers and correlates of protection for vaccine induced immune responses. Vaccine 30:4907-4920.
16. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708-712.
17. Wiesel M, Walton S, Richer K, Oxenius A. 2009. Virus-specific CD8 T cells: activation, differentiation and memory formation. APMIS 117:356-381.
18. Larsen M, Sauce D, Arnaud L, Fastenackels S, Appay V. 2012. Evaluating cellular polyfunctionality with a novel polyfunctionality index. PLoS One 7:e42403. doi:10.1371/journal.pone.0042403.
19. Barnes E, Folgori A, Capone S, Swadling L, Aston S, Kurioka A, Meyer J, Huddart R, Smith K, Townsend R, Brown A, Antrobus R, Ammendola V, Naddeo M, O'Hara G, Willberg C, Harrison A, Grazioli F, Esposito ML, Siani L, Traboni C, Oo Y, Adams D, Hill A, Colloca S, Nicosia A, Cortese R, Klenerman P. 2012. Novel adenovirus-based vaccines induce broad and sustained T cell responses to HCV in man. Sci. Transl. Med. 4:115ra1. doi:10.1126/scitranslmed.3003155.
20. Mikkelsen M, Holst PJ, Bukh J, Thomsen AR, Christensen JP. 2011. Enhanced and sustained CD8+ T cell responses with an adenoviral vector-based hepatitis C virus vaccine encoding NS3 linked to the MHC class II chaperone protein invariant chain. J. Immunol. 186:2355-2364.
21. Urbani S, Boni C, Missale G, Elia G, Cavallo C, Massari M, Raimondo G, Ferrari C. 2002. Virus-specific CD8+ lymphocytes share the same effector-memory phenotype but exhibit functional differences in acute hepatitis B and C. J. Virol. 76:12423-12434.
22. Akondy RS, Monson ND, Miller JD, Edupuganti S, Teuwen D, Wu H, Quyyumi F, Garg S, Altman JD, Del Rio C, Keyserling HL, Ploss A, Rice CM, Orenstein WA, Mulligan MJ, Ahmed R. 2009. The yellow fever virus vaccine induces a broad and polyfunctional human memory CD8+T cell response. J. Immunol. 183:7919-7930.
23. Kaden V, Lange E, Küster H, Müller T, Lange B. 2010. An update on safety studies on the attenuated "RIEMSER Schweinepestoralvakzine" for vaccination of wild boar against classical swine fever. Vet. Microbiol. 143:133-138.
24. Gladue DP, Holinka LG, Largo E, Fernandez Sainz I, Carrillo C, O'Donnell V, Baker-Branstetter R, Lu Z, Ambroggio X, Risatti GR, Nieva JL, Borca MV. 2012. Classical swine fever virus p7 protein is a viroporin involved in virulence in swine. J. Virol. 86:6778-6791.
25. Fernandez-Sainz I, Gladue DP, Holinka LG, O'Donnell V, Gudmundsdottir I, Prarat MV, Patch JR, Golde WT, Lu Z, Zhu J, Carrillo C, Risatti GR, Borca MV. 2010. Mutations in classical swine fever virus NS4B affect virulence in swine. J. Virol. 84:1536-1549.
26. Weesendorp E, Stegeman A, Loeffen WL. 2009. Quantification of classical swine fever virus in aerosols originating from pigs infected with strains of high, moderate or low virulence. Vet. Microbiol. 135:222-230.
27. Drew TW. 2008. Classical swine fever (hog cholera), p 1092-1106. In OIE manual of diagnostic test and vaccines for terrestrial animals (mammals, birds and bees), 6th ed. World Organization for Animal Health (OIE), Paris, France.
28. Graham SP, Everett HE, Johns HE, Haines FJ, La Rocca SA, Khatri M, Wright IK, Drew R, Crooke HR. 2010. Characterisation of virus-specific blood cell cytokine responses following vaccination or infection with classical swine fever viruses. Vet. Microbiol. 142:34-40.
29. Everett HE, Salguero FJ, Graham SP, Haines FJ, Johns H, Clifford D, Nunez A, La Rocca SA, Parchariyanon S, Steinbach F, Drew TW, Crooke H. 2010. Characterization of experimental infection of pigs with genotype 2.1 and 3.3 isolates of classical swine fever virus. Vet. Microbiol. 142:26-33.
30. Hoffmann B, Beer M, Schelp C, Schirrmeier H, Depner K. 2005. Validation of a real-time RT-PCR assay for sensitive and specific detection of classical swine fever. J. Virol. Methods 130:36-44.
31. Reutner K, Leitner J, Essler SE, Witter K, Patzl M, Steinberger P, Saalmuller A, Gerner W. 2012. Porcine CD27: identification, expression and functional aspects in lymphocyte subset in swine. Dev. Comp. Immunol. 38:321-331.
32. Costantini A, Mancini S, Giuliodoro S, Butini L, Regnery CM, Silvestri G, Montroni M. 2003. Effects of cryopreservation on lymphocyte immunophenotype and function. J. Immunol. Methods 278:145-155.
33. Gerner W, Käser T, Saalmüller A. 2009. Porcine T lymphocytes and NK cells - an update. Dev. Comp. Immunol. 33:310-320.
34. Betts MR, Brenchley JM, Price DA, De Rosa SC, Douke DC, Roeder M, Koup RA. 2003. Sensitive and viable identification of antigen-specific CD8+T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281:65-78.
35. Toka FN, Nfon C, Dawson H, Golde WT. 2009. Natural killer cell dysfunction during acute infection with foot-and-mouth disease virus. Clin. Vaccine Immunol. 16:1738-1749.
36. Hendriks J, Xiao Y, Borst J. 2003. CD27 promotes survival of activated T cells and complements CD28 in generation and establishment of the effector T cell pool. J. Exp. Med. 198:1369-1380.
37. Kobayashi N, Kondo T, Takata H, Yokota S, Takiguchi M. 2006. Functional and phenotypic analysis of human memory CD8+ T cells expressing CXCR3. J. Leukoc. Biol. 80:320-329.
38. Tomiyama H, Takata H, Matsuda T, Takiguchi M. 2004. Phenotypic classification of human CD8+ T cells reflecting their function: inverse correlation between quantitative expression of CD27 and cytotoxic effector function. Eur. J. Immunol. 34:999-1010.
39. Reutner K, Leitner J, Müllebner A, Ladinig A, Essler SE, Duvigneau JC, Ritzmann M, Steinberger P, Saalmüller A, Gerner W. 2013. CD27 expression discriminates porcine T helper cells with functionally distinct properties. Vet. Res. 44:18.
40. Talker SC, Käser T, Reutner K, Sedlak C, Mair KH, Koinig H, Graage R, Viehmann M, Klingler E, Ladinig A, Ritzmann M, Saalmüller A, Gerner W. 2013. Phenotypic maturation of porcine NK- and T-cell subsets. Dev. Comp. Immunol. 40:51-68.
41. Minami Y, Kono T, Miyazaki T, Taniguchi T. 1993. The IL-2 receptor complex: its structure, function and target genes. Annu. Rev. Immunol. 11:245-267.
42. Piriou L, Chevallier S, Hutet E, Charley B, Le Potier MF, Albina E. 2003. Humoral and cell-mediated immune responses of d/d histocompatible pigs against classical swine fever (CSF) virus. Vet. Res. 34:389-404.
43. Kalia V, Sarkar S, Subramaniam S, Haining WN, Smith KA, Ahmed R. 2010. Prolonged interleukin-2Ralpha expression on virus-specific CD8+ T cells favours terminal-effector differentiation in vivo. Immunity 32:91-103.
44. Patch JR, Pedersen LE, Toka FN, Moraes M, Grubman MJ, Nielsen M, Jungersen G, Buus S, Golde WT. 2011. Induction of foot-and-mouth disease virus-specific cytotoxic T cell killing by vaccination. Clin. Vaccine Immunol. 18:280-288.
45. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, Flynn BJ, Hoff ST, Andersen P, Reed SG, Morris SL, Roederer M, Seder RA. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania. Nat. Med. 13:843-850.
46. Lumsden JM, Schwenk RJ, Rein LE, Moris P, Janssens M, Ofori-Anyinam O, Cohen J, Kester KE, Heppner DG, Krzych U. 2011. Protective immunity induced with the RTS, S/AS vaccine is associated with IL-2 and TNF-α producing effector and central memory CD4 T cells. PLoS One 6:e20775. doi:10.1371/journal. pone.0020775.
47. Burgers WA, Chege GK, Muller TL, van Harmelen JH, Khoury G, Shephard EG, Gray CM, Williamson C, Williamson AL. 2009. Broad, high-magnitude and multifunctional CD4+ and CD8+ T-cell responses elicited by a DNA and modified vaccinia Ankara vaccine containing human immunodeficiency virus type I subtype C genes in baboons. J. Gen. Virol. 90:468-480.
48. Kaveh DA, Bachy VS, Hewinson RG, Hogarth PJ. 2011. Systemic BCG immunization induces persistent lung mucosal multifunctional CD4 TEMcells which expand following virulent mycobacterial challenge. PLoS One 6:e21566. doi:10.1371/journal.pone.0021566.
49. Berchtold C, Panthel K, Jellbauer S, Kohn B, Roider E, Partilla M, Heesemann J, Endres S, Bourquin C, Russmann H. 2009. Superior protective immunity against murine listeriosis by combined vaccination with CpG DNA and recombinant Salmonella enteric serovar Typhimurium. Infect. Immun. 77:5501-5508.
50. Reyes-Sandoval A, Wyllie DH, Bauza K, Milicic A, Forbes EK, Rollier CS, Hill AV. 2011. CD8+ T effector memory cells protect against liver-stage malaria. J. Immunol. 187:1347-1357.
51. Hansen SG, Ford JC, Lewis MS, Ventura AB, Hughes CM, Coyne-Johnson L, Whizin N, Oswald K, Shoemaker R, Swanson T, Legasse AW, Chiuchiolo MJ, Parks CL, Axthelm MK, Nelson JA, Jarvis MA, Piatak M, Lifson JD, Picker LJ. 2011. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473:523-527.
52. EM cells in cattle naturally infected with bovine tuberculosis. PLoS One 6:e29194. doi:10.1371/journal.pone.0029194.
53. Seder RA, Darrah PA, Roederer M. 2008. T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 8:247-258.