Influenza epitope-specific CD8+ T cell avidity, but not cytokine polyfunctionality, can be determined by tcrβ clonotype

Journal of Immunology

Volumn 185, Issue 11, 2010, Pages 6850-6856

  Moffat, Jessica M ^a,d   Handel, Andreas ^b   Doherty, Peter C ^a,c   Turner, Stephen J ^a   Thomas, Paul G ^c   La Gruta, Nicole L ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF GEORGIA   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; D B NP 366 EPITOPE; D B PA 224 EPITOPE; EPITOPE; GAMMA INTERFERON; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR BETA CHAIN; TETRAMER; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; C57BL 6 MOUSE; CD8+ T LYMPHOCYTE; CELL CLONE; CELL SELECTION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; FEMALE; GENE SEQUENCE; INFLUENZA; INFLUENZA VIRUS A; LYMPHOCYTE SUBPOPULATION; MOLECULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; CELL ADHESION; CLONE CELLS; CYTOKINES; EPITOPES, T-LYMPHOCYTE; FEMALE; H-2 ANTIGENS; IMMUNODOMINANT EPITOPES; INFLUENZA A VIRUS, H1N1 SUBTYPE; INTERLEUKIN-2; MICE; MICE, INBRED C57BL; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; T-LYMPHOCYTES, CYTOTOXIC;

EID: 78650658949     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002025     Document Type: Article

References (43)

1. Faroudi, M., C. Utzny, M. Salio, V. Cerundolo, M. Guiraud, S. Müller, and S. Valitutti. 2003. Lytic versus stimulatory synapse in cytotoxic T lymphocyte/target cell interaction: manifestation of a dual activation threshold. Proc. Natl. Acad. Sci. USA 100:14145-14150.
2. Valitutti, S., S. Müller, M. Dessing, and A. Lanzavecchia. 1996. Different responses are elicited in cytotoxic T lymphocytes by different levels of T cell receptor occupancy. J. Exp. Med. 183:1917-1921.
3. Seder, R. A., P. A. Darrah, and M. Roederer. 2008. T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 8:247-258.
4. Betts, M. R., M. C. Nason, S. M. West, S. C. De Rosa, S. A. Migueles, J. Abraham, M. M. Lederman, J. M. Benito, P. A. Goepfert, M. Connors, et al. 2006. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107:4781-4789.
5. Duvall, M. G., M. L. Precopio, D. A. Ambrozak, A. Jaye, A. J. McMichael, H. C. Whittle, M. Roederer, S. L. Rowland-Jones, and R. A. Koup. 2008. Polyfunctional T cell responses are a hallmark of HIV-2 infection. Eur. J. Immunol. 38:350-363.
6. Almeida, J. R., D. A. Price, L. Papagno, Z. A. Arkoub, D. Sauce, E. Bornstein, T. E. Asher, A. Samri, A. Schnuriger, I. Theodorou, et al. 2007. Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J. Exp. Med. 204:2473-2485.
7. Almeida, J. R., D. Sauce, D. A. Price, L. Papagno, S. Y. Shin, A. Moris, M. Larsen, G. Pancino, D. C. Douek, B. Autran, et al. 2009. Antigen sensitivity is a major determinant of CD8+ T-cell polyfunctionality and HIV-suppressive activity. Blood 113:6351-6360.
8. Precopio, M. L., M. R. Betts, J. Parrino, D. A. Price, E. Gostick, D. R. Ambrozak, T. E. Asher, D. C. Douek, A. Harari, G. Pantaleo, et al. 2007. Immunization with vaccinia virus induces polyfunctional and phenotypically distinctive CD8 (+) T cell responses. J. Exp. Med. 204:1405-1416.
9. Darrah, P. A., D. T. Patel, P. M. De Luca, R. W. Lindsay, D. F. Davey, B. J. Flynn, S. T. Hoff, P. Andersen, S. G. Reed, S. L. Morris, et al. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13:843-850.
10. Imai, N., H. Ikeda, I. Tawara, and H. Shiku. 2009. Tumor progression inhibits the induction of multifunctionality in adoptively transferred tumor-specific CD8+ T cells. Eur. J. Immunol. 39:241-253.
11. Rizzuto, G. A., T. Merghoub, D. Hirschhorn-Cymerman, C. Liu, A. M. Lesokhin, D. Sahawneh, H. Zhong, K. S. Panageas, M. A. Perales, G. Altan-Bonnet, et al. 2009. Self-antigen-specific CD8+ T cell precursor frequency determines the quality of the antitumor immune response. J. Exp. Med. 206:849-866.
12. Lichterfeld, M., X. G. Yu, M. T. Waring, S. K. Mui, M. N. Johnston, D. Cohen, M. M. Addo, J. Zaunders, G. Alter, E. Pae, et al. 2004. HIV-1-specific cytotoxicity is preferentially mediated by a subset of CD8 (+) T cells producing both interferon-gamma and tumor necrosis factor-alpha. Blood 104:487-494.
13. Aagaard, C., T. T. Hoang, A. Izzo, R. Billeskov, J. Troudt, K. Arnett, A. Keyser, T. Elvang, P. Andersen, and J. Dietrich. 2009. Protection and polyfunctional T cells induced by Ag85B-TB10.4/IC31 against Mycobacterium tuberculosis is highly dependent on the antigen dose. PLoS One 4: e5930.
14. La Gruta, N. L., S. J. Turner, and P. C. Doherty. 2004. Hierarchies in cytokine expression profiles for acute and resolving influenza virus-specific CD8+ T cell responses: correlation of cytokine profile and TCR avidity. J. Immunol. 172:5553-5560.
15. Harari, A., C. Cellerai, F. B. Enders, J. Köstler, L. Codarri, G. Tapia, O. Boyman, E. Castro, S. Gaudieri, I. James, et al. 2007. Skewed association of polyfunctional antigen-specific CD8 T cell populations with HLA-B genotype. Proc. Natl. Acad. Sci. USA 104:16233-16238.
16. Doherty, P. C., and J. P. Christensen. 2000. Accessing complexity: the dynamics of virus-specific T cell responses. Annu. Rev. Immunol. 18:561-592.
17. Allan, W., Z. Tabi, A. Cleary, and P. C. Doherty. 1990. Cellular events in the lymph node and lung of mice with influenza. Consequences of depleting CD4+ T cells. J. Immunol. 144:3980-3986.
18. Belz, G. T., W. Xie, and P. C. Doherty. 2001. Diversity of epitope and cytokine profiles for primary and secondary influenza a virus-specific CD8+ T cell responses. J. Immunol. 166:4627-4633.
19. La Gruta, N. L., P. C. Doherty, and S. J. Turner. 2006. A correlation between function and selected measures of T cell avidity in influenza virus-specific CD8+ T cell responses. Eur. J. Immunol. 36:2951-2959.
20. Flynn, K. J., G. T. Belz, J. D. Altman, R. Ahmed, D. L. Woodland, and P. C. Doherty. 1998. Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity 8:683-691.
21. Kedzierska, K., N. L. La Gruta, M. P. Davenport, S. J. Turner, and P. C. Doherty. 2005. Contribution of T cell receptor affinity to overall avidity for virus-specific CD8+ T cell responses. Proc. Natl. Acad. Sci. USA 102:11432-11437.
22. Campbell, J. D. 2003. Detection and enrichment of antigen-specific CD4+ and CD8+ T cells based on cytokine secretion. Methods 31:150-159.
23. Kedzierska, K., S. J. Turner, and P. C. Doherty. 2004. Conserved T cell receptor usage in primary and recall responses to an immunodominant influenza virus nucleoprotein epitope. Proc. Natl. Acad. Sci. USA 101:4942-4947.
24. La Gruta, N. L., P. G. Thomas, A. I. Webb, M. A. Dunstone, T. Cukalac, P. C. Doherty, A. W. Purcell, J. Rossjohn, and S. J. Turner. 2008. Epitope-specific TCRbeta repertoire diversity imparts no functional advantage on the CD8+ T cell response to cognate viral peptides. Proc. Natl. Acad. Sci. USA 105:2034-2039.
25. Turner, S. J., G. Diaz, R. Cross, and P. C. Doherty. 2003. Analysis of clonotype distribution and persistence for an influenza virus-specific CD8+ T cell response. Immunity 18:549-559.
26. Venturi, V., K. Kedzierska, M. M. Tanaka, S. J. Turner, P. C. Doherty, and M. P. Davenport. 2008. Method for assessing the similarity between subsets of the T cell receptor repertoire. J. Immunol. Methods 329:67-80.
27. Kalergis, A. M., N. Boucheron, M. A. Doucey, E. Palmieri, E. C. Goyarts, Z. Vegh, I. F. Luescher, and S. G. Nathenson. 2001. Efficient T cell activation requires an optimal dwell-time of interaction between the TCR and the pMHC complex. Nat. Immunol. 2:229-234.
28. Deckhut, A. M., W. Allan, A. McMickle, M. Eichelberger, M. A. Blackman, P. C. Doherty, and D. L. Woodland. 1993. Prominent usage of V beta 8.3 T cells in the H-2Db-restricted response to an influenza A virus nucleoprotein epitope. J. Immunol. 151:2658-2666.
29. Belz, G. T., W. Xie, J. D. Altman, and P. C. Doherty. 2000. A previously unrecognized H-2D (b)-restricted peptide prominent in the primary influenza A virus-specific CD8 (+) T-cell response is much less apparent following secondary challenge. J. Virol. 74:3486-3493.
30. Farragher, S. M., A. Tanney, R. D. Kennedy, and D. Paul Harkin. 2008. RNA expression analysis from formalin fixed paraffin embedded tissues. Histochem. Cell Biol. 130:435-445.
31. Kristensen, N. N., A. N. Madsen, A. R. Thomsen, and J. P. Christensen. 2004. Cytokine production by virus-specific CD8 (+) T cells varies with activation state and localization, but not with TCR avidity. J. Gen. Virol. 85:1703-1712.
32. Neveu, B., E. Debeaupuis, K. Echasserieau, B. le Moullac-Vaidye, M. Gassin, L. Jegou, J. Decalf, M. Albert, N. Ferry, J. Gournay, et al. 2008. Selection of high-avidity CD8 T cells correlates with control of hepatitis C virus infection. Hepatology 48:713-722.
33. Alexander-Miller, M. A., G. R. Leggatt, and J. A. Berzofsky. 1996. Selective expansion of high-or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc. Natl. Acad. Sci. USA 93:4102-4107.
34. Gallimore, A., T. Dumrese, H. Hengartner, R. M. Zinkernagel, and H. G. Rammensee. 1998. Protective immunity does not correlate with the hierarchy of virus-specific cytotoxic T cell responses to naturally processed peptides. J. Exp. Med. 187:1647-1657.
35. Belyakov, I. M., V. A. Kuznetsov, B. Kelsall, D. Klinman, M. Moniuszko, M. Lemon, P. D. Markham, R. Pal, J. D. Clements, M. G. Lewis, et al. 2006. Impact of vaccine-induced mucosal high-avidity CD8+ CTLs in delay of AIDS viral dissemination from mucosa. Blood 107:3258-3264.
36. Valmori, D., V. Dutoit, V. Schnuriger, A. L. Quiquerez, M. J. Pittet, P. Guillaume, V. Rubio-Godoy, P. R. Walker, D. Rimoldi, D. Liénard, et al. 2002. Vaccination with a Melan-A peptide selects an oligoclonal T cell population with increased functional avidity and tumor reactivity. J. Immunol. 168:4231-4240.
37. Dutoit, V., V. Rubio-Godoy, P. Y. Dietrich, A. L. Quiqueres, V. Schnuriger, D. Rimoldi, D. Liénard, D. Speiser, P. Guillaume, P. Batard, et al. 2001. Heterogeneous T-cell response to MAGE-A10 (254-262): high avidity-specific cytolytic T lymphocytes show superior antitumor activity. Cancer Res. 61:5850-5856.
38. Zeh, H. J., III, D. Perry-Lalley, M. E. Dudley, S. A. Rosenberg, and J. C. Yang. 1999. High avidity CTLs for two self-antigens demonstrate superior in vitro and in vivo antitumor efficacy. J. Immunol. 162:989-994.
39. Jenkins, M. R., R. Webby, P. C. Doherty, and S. J. Turner. 2006. Addition of a prominent epitope affects influenza A virus-specific CD8+ T cell immunodominance hierarchies when antigen is limiting. J. Immunol. 177:2917-2925.
40. Pham, N. L., V. P. Badovinac, and J. T. Harty. 2009. A default pathway of memory CD8 T cell differentiation after dendritic cell immunization is deflected by encounter with inflammatory cytokines during antigen-driven proliferation. J. Immunol. 183:2337-2348.
41. Joshi, N. S., W. Cui, A. Chandele, H. K. Lee, D. R. Urso, J. Hagman, L. Gapin, and S. M. Kaech. 2007. Inflammation directs memory precursor and short-lived effector CD8 (+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27:281-295.
42. Pipkin, M. E., J. A. Sacks, F. Cruz-Guilloty, M. G. Lichtenheld, M. J. Bevan, and A. Rao. 2010. Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic T cells. Immunity 32:79-90.
43. Kalia, V., S. Sarkar, S. Subramaniam, W. N. Haining, K. A. Smith, and R. Ahmed. 2010. Prolonged interleukin-2Ralpha expression on virus-specific CD8+ T cells favors terminal-effector differentiation in vivo. Immunity 32:91-103.