Functional avidity-driven activation-induced cell death shapes CTL immunodominance

Journal of Immunology

Volumn 193, Issue 9, 2014, Pages 4704-4711

  Dalla Santa, Silvia ^a   Merlo, Anna ^a   Bobisse, Sara ^b   Ronconi, Elisa ^c   Boldrin, Daniela ^a   Milan, Gabriella ^d   Barbieri, Vito ^d   Marin, Oriano ^d   Facchinetti, Antonella ^d   Biasi, Giovanni ^e   Dolcetti, Riccardo ^f   Zanovello, Paola ^a,d   Rosato, Antonio ^a,d  

^a VENETO INSTITUTE OF ONCOLOGY IOV IRCCS   (Italy)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY OF FLORENCE   (Italy)

^d UNIVERSITY OF PADOVA   (Italy)

^e UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^f CENTRO DI RIFERIMENTO ONCOLOGICO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; T LYMPHOCYTE RECEPTOR; VIRUS ENVELOPE PROTEIN; EPITOPE; VIRUS ANTIGEN;

ADOPTIVE TRANSFER; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINDING AFFINITY; CD8+ T LYMPHOCYTE; CELL DEATH; CELL EXPANSION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FEMALE; IMMUNITY; IMMUNODOMINANCE; IN VITRO STUDY; IN VIVO STUDY; MOLONEY LEUKEMIA ONCOVIRUS; MOLONEY MURINE SARCOMA ONCOVIRUS; MOUSE; NONHUMAN; SARCOMA; T LYMPHOCYTE ACTIVATION; THERAPY EFFECT; TUMOR GROWTH; VIRUS IMMUNITY; ANIMAL; CELL LINE; CYTOTOXICITY; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; RETROVIRUS; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, VIRAL; APOPTOSIS; CELL LINE; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; GENE PRODUCTS, ENV; GENE PRODUCTS, GAG; HUMANS; IMMUNODOMINANT EPITOPES; LYMPHOCYTE ACTIVATION; MICE; RETROVIRIDAE; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84908123708     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303203     Document Type: Article

References (42)

1. Yewdell, J. W., and J. R. Bennink. 1999. Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu. Rev. Immunol. 17: 51-88.
2. Chen, W., and J. McCluskey. 2006. Immunodominance and immunodomination: critical factors in developing effective CD8+ T-cell-based cancer vaccines. Adv. Cancer Res. 95: 203-247.
3. Probst, H. C., K. Tschannen, A. Gallimore, M. Martinic, M. Basler, T. Dumrese, E. Jones, and M. F. van den Broek. 2003. Immunodominance of an antiviral cytotoxic T cell response is shaped by the kinetics of viral protein expression. J. Immunol. 171: 5415-5422.
4. van der Most, R. G., K. Murali-Krishna, J. G. Lanier, E. J. Wherry, M. T. Puglielli, J. N. Blattman, A. Sette, and R. Ahmed. 2003. Changing immunodominance patterns in antiviral CD8 T-cell responses after loss of epitope presentation or chronic antigenic stimulation. Virology 315: 93-102.
5. Brett, S. J., K. B. Cease, and J. A. Berzofsky. 1988. Influences of antigen processing on the expression of the T cell repertoire. Evidence for MHC-specific hindering structures on the products of processing. J. Exp. Med. 168: 357-373.
6. Tenzer, S., E. Wee, A. Burgevin, G. Stewart-Jones, L. Friis, K. Lamberth, C. H. Chang, M. Harndahl, M. Weimershaus, J. Gerstoft, et al. 2009. Antigen processing influences HIV-specific cytotoxic T lymphocyte immunodominance. Nat. Immunol. 10: 636-646.
7. Rodriguez, F., S. Harkins, M. K. Slifka, and J. L. Whitton. 2002. Immunodominance in virus-induced CD8(+) T-cell responses is dramatically modified by DNA immunization and is regulated by gamma interferon. J. Virol. 76: 4251-4259.
8. Kedl, R. M., J. W. Kappler, and P. Marrack. 2003. Epitope dominance, competition and T cell affinity maturation. Curr. Opin. Immunol. 15: 120-127.
9. van der Most, R. G., A. Sette, C. Oseroff, J. Alexander, K. Murali-Krishna, L. L. Lau, S. Southwood, J. Sidney, R. W. Chesnut, M. Matloubian, and R. Ahmed. 1996. Analysis of cytotoxic T cell responses to dominant and subdominant epitopes during acute and chronic lymphocytic choriomeningitis virus infection. J. Immunol. 157: 5543-5554.
10. Chen, W., S. Khilko, J. Fecondo, D. H. Margulies, and J. McCluskey. 1994. Determinant selection of major histocompatibility complex class I-restricted antigenic peptides is explained by class I-peptide affinity and is strongly influenced by nondominant anchor residues. J. Exp. Med. 180: 1471-1483.
11. ∗3501-restricted human cytomegalovirus epitope. J. Virol. 81: 7269-7273.
12. Brawand, P., G. Biasi, C. Horvath, J. C. Cerottini, and H. R. MacDonald. 1998. Flow-microfluorometric monitoring of oligoclonal CD8+ T cell responses to an immunodominant Moloney leukemia virus-encoded epitope in vivo. J. Immunol. 160: 1659-1665.
13. Pion, S., G. J. Christianson, P. Fontaine, D. C. Roopenian, and C. Perreault. 1999. Shaping the repertoire of cytotoxic T-lymphocyte responses: explanation for the immunodominance effect whereby cytotoxic T lymphocytes specific for immunodominant antigens prevent recognition of nondominant antigens. Blood 93: 952-962.
14. La Gruta, N. L., W. T. Rothwell, T. Cukalac, N. G. Swan, S. A. Valkenburg, K. Kedzierska, P. G. Thomas, P. C. Doherty, and S. J. Turner. 2010. Primary CTL response magnitude in mice is determined by the extent of naive T cell recruitment and subsequent clonal expansion. J. Clin. Invest. 120: 1885-1894.
15. Alexander-Miller, M. A. 2005. High-avidity CD8+ T cells: optimal soldiers in the war against viruses and tumors. Immunol. Res. 31: 13-24.
16. Viganò, S., D. T. Utzschneider, M. Perreau, G. Pantaleo, D. Zehn, and A. Harari. 2012. Functional avidity: a measure to predict the efficacy of effector T cells? Clin. Dev. Immunol. 2012: 153863.
17. Chieco-Bianchi, L., D. Collavo, and G. Biasi. 1988. Immunologic unrespon-siveness to murine leukemia virus antigens: mechanisms and role in tumor development. Adv. Cancer Res. 51: 277-306.
18. Milan, G., A. Zambon, M. Cavinato, P. Zanovello, A. Rosato, and D. Collavo. 1999. Dissecting the immune response to moloney murine sarcoma/leukemia virus-induced tumors by means of a DNA vaccination approach. J. Virol. 73: 2280-2287.
19. Schepers, K., M. Toebes, G. Sotthewes, F. A. Vyth-Dreese, T. A. Dellemijn, C. J. Melief, F. Ossendorp, and T. N. Schumacher. 2002. Differential kinetics of antigen-specific CD4+ and CD8+ T cell responses in the regression of retrovirus-induced sarcomas. J. Immunol. 169: 3191-3199.
20. Rosato, A., S. Dalla Santa, A. Zoso, S. Giacomelli, G. Milan, B. Macino, V. Tosello, P. Dellabona, P. L. Lollini, C. De Giovanni, and P. Zanovello. 2003. The cytotoxic T-lymphocyte response against a poorly immunogenic mammary adenocarcinoma is focused on a single immunodominant class I epitope derived from the gp70 Env product of an endogenous retrovirus. Cancer Res. 63: 2158-2163.
21. Rosato, A., S. Mandruzzato, V. Bronte, A. Zambon, B. Macino, F. Calderazzo, P. Zanovello, and D. Collavo. 1995. Role of anti-LFA-1 and anti-ICAM-1 combined MAb treatment in the rejection of tumors induced by Moloney mu-rine sarcoma virus (M-MSV). Int. J. Cancer 61: 355-362.
22. Rosato, A., A. Zoso, S. Dalla Santa, G. Milan, P. Del Bianco, G. L. De Salvo, and P. Zanovello. 2006. Predicting tumor outcome following cancer vaccination by monitoring quantitative and qualitative CD8+ T cell parameters. J. Immunol. 176: 1999-2006.
23. Derby, M. A., J. T. Snyder, R. Tse, M. A. Alexander-Miller, and J. A. Berzofsky. 2001. An abrupt and concordant initiation of apoptosis: antigen-dependent death of CD8+ CTL. Eur. J. Immunol. 31: 2951-2959.
24. Camporeale, A., A. Boni, G. Iezzi, E. Degl'Innocenti, M. Grioni, A. Mondino, and M. Bellone. 2003. Critical impact of the kinetics of dendritic cells activation on the in vivo induction of tumor-specific T lymphocytes. Cancer Res. 63: 3688-3694.
25. Zanovello, P., A. Rosato, V. Bronte, V. Cerundolo, S. Treves, F. Di Virgilio, T. Pozzan, G. Biasi, and D. Collavo. 1989. Interaction of lymphokine-activated killer cells with susceptible targets does not induce second messenger generation and cytolytic granule exocytosis. J. Exp. Med. 170: 665-677.
26. Lipford, G. B., S. Bauer, H. Wagner, and K. Heeg. 1995. In vivo CTL induction with point-substituted ovalbumin peptides: immunogenicity correlates with peptide-induced MHC class I stability. Vaccine 13: 313-320.
27. Alexander-Miller, M. A., G. R. Leggatt, A. Sarin, and J. A. Berzofsky. 1996. Role of antigen, CD8, and cytotoxic T lymphocyte (CTL) avidity in high dose antigen induction of apoptosis of effector CTL. J. Exp. Med. 184: 485-492.
28. Derby, M., M. Alexander-Miller, R. Tse, and J. Berzofsky. 2001. High-avidity CTL exploit two complementary mechanisms to provide better protection against viral infection than low-avidity CTL. J. Immunol. 166: 1690-1697.
29. Laugel, B., H. A. van den Berg, E. Gostick, D. K. Cole, L. Wooldridge, J. Boulter, A. Milicic, D. A. Price, and A. K. Sewell. 2007. Different T cell receptor affinity thresholds and CD8 coreceptor dependence govern cytotoxic T lymphocyte activation and tetramer binding properties. J. Biol. Chem. 282: 23799-23810.
30. 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.
31. Kitazono, T., T. Okazaki, N. Araya, Y. Yamano, Y. Yamada, T. Nakamura, Y. Tanaka, M. Inoue, and S. Ozaki. 2011. Advantage of higher-avidity CTL specific for Tax against human T-lymphotropic virus-1 infected cells and tumors. Cell. Immunol. 272: 11-17.
32. 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.
33. Luciani, F., M. T. Sanders, S. Oveissi, K. C. Pang, and W. Chen. 2013. Increasing viral dose causes a reversal in CD8+ T cell immunodominance during primary influenza infection due to differences in antigen presentation, T cell avidity, and precursor numbers. J. Immunol. 190: 36-47.
34. Viganò, S., F. Bellutti Enders, I. Miconnet, C. Cellerai, A. L. Savoye, V. Rozot, M. Perreau, M. Faouzi, K. Ohmiti, M. Cavassini, et al. 2013. Rapid perturbation in viremia levels drives increases in functional avidity of HIV-specific CD8 T cells. PLoS Pathog. 9: e1003423.
35. Holbrook, B. C., R. D. Yammani, L. K. Blevins, and M. A. Alexander-Miller. 2013. In vivo modulation of avidity in highly sensitive CD8(+) effector T cells following viral infection. Viral Immunol. 26: 302-313.
36. Lichterfeld, M., X. G. Yu, S. K. Mui, K. L. Williams, A. Trocha, M. A. Brockman, R. L. Allgaier, M. T. Waring, T. Koibuchi, M. N. Johnston, et al. 2007. Selective depletion of high-avidity human immunodeficiency virus type 1 (HIV-1)-specific CD8+ T cells after early HIV-1 infection. J. Virol. 81: 4199-4214.
37. Molldrem, J. J., P. P. Lee, S. Kant, E. Wieder, W. Jiang, S. Lu, C. Wang, and M. M. Davis. 2003. Chronic myelogenous leukemia shapes host immunity by selective deletion of high-avidity leukemia-specific T cells. J. Clin. Invest. 111: 639-647.
38. Kim, M., H. B. Moon, K. Kim, and K. Y. Lee. 2006. Antigen dose governs the shaping of CTL repertoires in vitro and in vivo. Int. Immunol. 18: 435-444.
39. Lin, L. C., I. E. Flesch, and D. C. Tscharke. 2013. Immunodomination during peripheral vaccinia virus infection. PLoS Pathog. 9: e1003329.
40. Brentville, V. A., R. L. Metheringham, B. Gunn, and L. G. Durrant. 2012. High avidity cytotoxic T lymphocytes can be selected into the memory pool but they are exquisitely sensitive to functional impairment. PLoS ONE 7: e41112.
41. Hailemichael, Y., Z. Dai, N. Jaffarzad, Y. Ye, M. A. Medina, X. F. Huang, S. M. Dorta-Estremera, N. R. Greeley, G. Nitti, W. Peng, et al. 2013. Persistent antigen at vaccination sites induces tumor-specific CD8+ T cell sequestration, dysfunction and deletion. Nat. Med. 19: 465-472.
42. Zhong, S., K. Malecek, L. A. Johnson, Z. Yu, E. Vega-Saenz de Miera, F. Darvishian, K. McGary, K. Huang, J. Boyer, E. Corse, et al. 2013. T-cell receptor affinity and avidity defines antitumor response and autoimmunity in T-cell immunotherapy. Proc. Natl. Acad. Sci. USA 110: 6973-6978.