Characterization of the human CD4+ T-cell repertoire specific for major histocompatibility class I-restricted antigens

European Journal of Immunology

Volumn 43, Issue 12, 2013, Pages 3244-3253

  Legoux, François ^a,c   Gautreau, Laetitia ^a,b   Hesnard, Leslie ^a   Leger, Alexandra ^a   Moyon, Melinda ^a   Devilder, Marie Claire ^a   Bonneville, Marc ^a   Saulquin, Xavier ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Human; Major histocompatibility (MHC); T cell receptor

Indexed keywords

HLA A2 ANTIGEN; T LYMPHOCYTE RECEPTOR; TUMOR ANTIGEN; VIRUS ANTIGEN; HLA A*02:01 ANTIGEN; HLA-A*02:01 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR;

ADAPTIVE IMMUNITY; ALLELE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ISOLATION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE RESPONSE; CYTOTOXICITY; EX VIVO STUDY; HELPER CELL; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE RESPONSE; MELANOMA CELL; PRIORITY JOURNAL; TARGET CELL; TH1 CELL; VIRUS; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; FEMALE; IMMUNOLOGY; MAJOR HISTOCOMPATIBILITY (MHC); MALE; T-CELL RECEPTOR;

CD4+ T CELLS; HUMAN; MAJOR HISTOCOMPATIBILITY (MHC); T-CELL RECEPTOR;

ANTIGENS, NEOPLASM; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; FEMALE; HLA-A2 ANTIGEN; HUMANS; MALE; RECEPTORS, ANTIGEN, T-CELL; TH1 CELLS;

EID: 84896979192     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343726     Document Type: Article

References (38)

1. Engelhard, V. H., Structure of peptides associated with class I and class II MHC molecules. Annu. Rev. Immunol. 1994. 12: 181-207.
2. Arstila, T. P., Casrouge, A., Baron, V., Even, J., Kanellopoulos, J. and Kourilsky, P., A direct estimate of the human alphabeta T cell receptor diversity. Science 1999. 286: 958-961.
3. Golding, H., Mizuochi, T., McCarthy, S. A., Cleveland, C. A. and Singer, A., Relationship among function, phenotype, and specificity in primary allospecific T cell populations: identification of phenotypically identical but functionally distinct primary T cell subsets that differ in their recognition of MHC class I and class II allodeterminants. J. Immunol. 1987. 138: 10-17.
4. Shinohara, N., Hozumi, N., Watanabe, M., Bluestone, J. A., Johnson-Leva, R. and Sachs, D. H., Class II antigen-specific murine cytolytic T lymphocytes (CTL). II. Genuine class II specificity of Lyt-2+ CTL clones. J. Immunol. 1988. 140: 30-36.
5. Darrow, T. L., Abdel-Wahab, Z., Quinn-Allen, M. A. and Seigler, H. F., Recognition and lysis of human melanoma by a CD3+, CD4+, CD8- T-cell clone restricted by HLA-A2. Cell Immunol. 1996. 172: 52-59.
6. Kobayashi, H., Kimura, S., Aoki, N., Sato, K., Celis, E. and Katagiri, M., Existence of MHC class I-restricted alloreactive CD4+ T cells reacting with peptide transporter-deficient cells. Immunogenetics 2001. 53: 626-633.
7. Nishimura, M. I., Avichezer, D., Custer, M. C., Lee, C. S., Chen, C., Parkhurst, M. R., Diamond, R. A. et al., MHC class I-restricted recognition of a melanoma antigen by a human CD4+ tumor infiltrating lymphocyte. Cancer Res. 1999. 59: 6230-6238.
8. Boyle, L. H., Goodall, J. C., Opat, S. S. and Gaston, J. S., The recognition of HLA-B27 by human CD4(+) T lymphocytes. J. Immunol. 2001. 167: 2619-2624.
9. Legoux, F., Debeaupuis, E., Echasserieau, K., De La Salle, H., Saulquin, X. and Bonneville, M., Impact of TCR reactivity and HLA phenotype on naive CD8 T cell frequency in humans. J. Immunol. 2010. 184: 6731-6738.
10. Pittet, M. J., Rubio-Godoy, V., Bioley, G., Guillaume, P., Batard, P., Speiser, D., Luescher, I. et al., Alpha 3 domain mutants of peptide/MHC class I multimers allow the selective isolation of high avidity tumor-reactive CD8 T cells. J. Immunol. 2003. 171: 1844-1849.
11. Holler, P. D. and Kranz, D. M., Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 2003. 18: 255-264.
12. Labarriere, N., Diez, E., Pandolfino, M. C., Viret, C., Guilloux, Y., Le Guiner, S., Fonteneau, J. F. et al., Optimal T cell activation by melanoma cells depends on a minimal level of antigen transcription. J. Immunol. 1997. 158: 1238-1245.
13. Pittet, M. J., Valmori, D., Dunbar, P. R., Speiser, D. E., Lienard, D., Lejeune, F., Fleischhauer, K. et al., High frequencies of naive Melan-A/MART-1-specific CD8(+) T cells in a large proportion of human histocompatibility leukocyte antigen (HLA)-A2 individuals. J. Exp. Med. 1999. 190: 705-715.
14. Voelkl, S., Moore, T. V., Rehli, M., Nishimura, M. I., Mackensen, A. and Fischer, K., Characterization of MHC class-I restricted TCR alphabeta+ CD4- CD8- double negative T cells recognizing the gp100 antigen from a melanoma patient after gp100 vaccination. Cancer Immunol. Immunother. 2009. 58: 709-718.
15. Wang, P., Vanky, F. and Klein, E., MHC class-I-restricted auto-tumor-specific CD4+CD8- T-cell clones established from autologous mixed lymphocyte-tumor-cell culture (MLTC). Int. J. Cancer 1992. 51: 962-967.
16. Somasundaram, R., Robbins, P., Moonka, D., Loh, E., Marincola, F., Patel, A., Guerry, D. and Herlyn, D., CD4(+), HLA class I-restricted, cytolytic T-lymphocyte clone against primary malignant melanoma cells. Int. J. Cancer 2000. 85: 253-259.
17. Roddis, M., Carter, R. W., Sun, M. Y., Weissensteiner, T., McMichael, A. J., Bowness, P. and Bodmer, H. C., Fully functional HLA B27-restricted CD4+ as well as CD8+ T cell responses in TCR transgenic mice. J. Immunol. 2004. 172: 155-161.
18. Yang, Y. and Wilson, J. M., Clearance of adenovirus-infected hepatocytes by MHC class I-restricted CD4 +CTLs in vivo. J. Immunol. 1995. 155: 2564-2570.
19. Mehrotra, S., Al-Khami, A. A., Klarquist, J., Husain, S., Naga, O., Eby, J. M., Murali, A. K. et al., A coreceptor-independent transgenic human TCR mediates anti-tumor and anti-self immunity in mice. J. Immunol. 2012. 189: 1627-1638.
20. Allen, R. L., O'Callaghan, C. A., McMichael, A. J. and Bowness, P., Cutting edge: HLA-B27 can form a novel beta 2-microglobulin-free heavy chain homodimer structure. J. Immunol. 1999. 162: 5045-5048.
21. Tanaka, Y., Koido, S., Xia, J., Ohana, M., Liu, C., Cote, G. M., Sawyer, D. B. et al., Development of antigen-specific CD8+ CTL in MHC class I-deficient mice through CD4 to CD8 conversion. J. Immunol. 2004. 172: 7848-7858.
22. Alexander-Miller, M. A., Leggatt, G. R. and Berzofsky, J. A., Selective expansion of high- or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc. Natl. Acad. Sci. USA 1996. 93: 4102-4107.
23. Zeh, H. J., 3rd, Perry-Lalley, D., Dudley, M. E., Rosenberg, S. A. and Yang, J. C., High avidity CTLs for two self-antigens demonstrate superior in vitro and in vivo antitumor efficacy. J. Immunol. 1999. 162: 989-994.
24. Falkenburg, W. J., Melenhorst, J. J., van de Meent, M., Kester, M. G., Hombrink, P., Heemskerk, M. H., Hagedoorn, R. S. et al., Allogeneic HLA-A*02-restricted WT1-specific T cells from mismatched donors are highly reactive but show off-target promiscuity. J. Immunol. 2011. 187: 2824-2833.
25. Holler, P. D., Holman, P. O., Shusta, E. V., O'Herrin, S., Wittrup, K. D. and Kranz, D. M., In vitro evolution of a T cell receptor with high affinity for peptide/MHC. Proc. Natl. Acad. Sci. USA 2000. 97: 5387-5392.
26. Kessels, H. W., Schepers, K., van den Boom, M. D., Topham, D. J. and Schumacher, T. N., Generation of T cell help through a MHC class I-restricted TCR. J. Immunol. 2006. 177: 976-982.
27. Morris, E. C., Tsallios, A., Bendle, G. M., Xue, S. A. and Stauss, H. J., A critical role of T cell antigen receptor-transduced MHC class I-restricted helper T cells in tumor protection. Proc. Natl. Acad. Sci. USA 2005. 102: 7934-7939.
28. Engels, B., Chervin, A. S., Sant, A. J., Kranz, D. M. and Schreiber, H., Long-term persistence of CD4(+) but rapid disappearance of CD8(+) T cells expressing an MHC class I-restricted TCR of nanomolar affinity. Mol. Ther. 2012. 20: 652-660.
29. Clay, T. M., Custer, M. C., Sachs, J., Hwu, P., Rosenberg, S. A. and Nishimura, M. I., Efficient transfer of a tumor antigen-reactive TCR to human peripheral blood lymphocytes confers anti-tumor reactivity. J. Immunol. 1999. 163: 507-513.
30. Roszkowski, J. J., Lyons, G. E., Kast, W. M., Yee, C., Van Besien, K. and Nishimura, M. I., Simultaneous generation of CD8+ and CD4+ melanoma-reactive T cells by retroviral-mediated transfer of a single T-cell receptor. Cancer Res. 2005. 65: 1570-1576.
31. Zhao, Y., Zheng, Z., Robbins, P. F., Khong, H. T., Rosenberg, S. A. and Morgan, R. A., Primary human lymphocytes transduced with NY-ESO-1 antigen-specific TCR genes recognize and kill diverse human tumor cell lines. J. Immunol. 2005. 174: 4415-4423.
32. Chhabra, A., Yang, L., Wang, P., Comin-Anduix, B., Das, R., Chakraborty, N. G., Ray, S. et al., CD4+CD25- T cells transduced to express MHC class I-restricted epitope-specific TCR synthesize Th1 cytokines and exhibit MHC class I-restricted cytolytic effector function in a human melanoma model. J. Immunol. 2008. 181: 1063-1070.
33. Ray, S., Chhabra, A., Chakraborty, N. G., Hegde, U., Dorsky, D. I., Chodon, T., von Euw, E. et al., MHC-I-restricted melanoma antigen specific TCR-engineered human CD4+ T cells exhibit multifunctional effector and helper responses, in vitro. Clin. Immunol. 2010. 136: 338-347.
34. Le Drean, E., Gervois, N., Diez, E., Semana, G., Dreno, B. and Jotereau, F., HLA class II-restricted recognition of common tumor epitopes on human melanoma cells by CD4+ melanoma-infiltrating lymphocytes. Eur. J. Immunol. 1995. 25: 2732-2736.
35. Bodinier, M., Peyrat, M. A., Tournay, C., Davodeau, F., Romagne, F., Bonneville, M. and Lang, F., Efficient detection and immunomagnetic sorting of specific T cells using multimers of MHC class I and peptide with reduced CD8 binding. Nat. Med. 2000. 6: 707-710.
36. Neveu, B., Echasserieau, K., Hill, T., Kuus-Reichel, K., Houssaint, E., Bonneville, M. and Saulquin, X., Impact of CD8-MHC class I interaction in detection and sorting efficiencies of antigen-specific T cells using MHC class I/peptide multimers: contribution of pMHC valency. Int. Immunol. 2006. 18: 1139-1145.
37. Moon, J. J., Chu, H. H., Hataye, J., Pagan, A. J., Pepper, M., McLachlan, J. B., Zell, T. et al., Tracking epitope-specific T cells. Nat. Protoc. 2009. 4: 565-581.
38. Neveu, B., Debeaupuis, E., Echasserieau, K., le Moullac-Vaidye, B., Gassin, M., Jegou, L., Decalf, J. et al., Selection of high-avidity CD8 T cells correlates with control of hepatitis C virus infection. Hepatology 2008. 48: 713-722.