Human antitumor CD8+ T cells producing Th1 polycytokines show superior antigen sensitivity and tumor recognition

Journal of Immunology

Volumn 189, Issue 2, 2012, Pages 598-605

  Wilde, Susanne ^a   Sommermeyer, Daniel ^b   Leisegang, Matthias ^b   Frankenberger, Bernhard ^a   Mosetter, Barbara ^a   Uckert, Wolfgang ^b,c   Schendel, Dolores J ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAMMA INTERFERON; INTERLEUKIN 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN; TUMOR NECROSIS FACTOR ALPHA; TYROSINE PHENOL LYASE;

ANTIGEN RECOGNITION; ARTICLE; CD8+ T LYMPHOCYTE; CELL CLONE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; ENZYME IMMOBILIZATION; GENE TRANSFER; HUMAN; HUMAN CELL; LYMPHOCYTE; MELANOMA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECRETION; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; TH1 CELL; TRANSGENE;

ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; CELL ADHESION; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; CLONE CELLS; COCULTURE TECHNIQUES; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; TH1 CELLS;

EID: 84863607641     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102165     Document Type: Article

References (40)

1. Rooney, C. M., C. A. Smith, C. Y. Ng, S. Loftin, C. Li, R. A. Krance, M. K. Brenner, and H. E. Heslop. 1995. Use of gene-modified virus-specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet 345: 9-13.
2. Walter, E. A., P. D. Greenberg, M. J. Gilbert, R. J. Finch, K. S. Watanabe, E. D. Thomas, and S. R. Riddell. 1995. Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N. Engl. J. Med. 333: 1038-1044.
3. Berger, C., C. J. Turtle, M. C. Jensen, and S. R. Riddell. 2009. Adoptive transfer of virus-specific and tumor-specific T cell immunity. Curr. Opin. Immunol. 21: 224-232.
4. Kolb, H. J. 2008. Graft-versus-leukemia effects of transplantation and donor lymphocytes. Blood 112: 4371-4383.
5. Geiger, C., E. Nössner, B. Frankenberger, C. S. Falk, H. Pohla, and D. J. Schendel. 2009. Harnessing innate and adaptive immunity for adoptive cell therapy of renal cell carcinoma. J. Mol. Med. 87: 595-612.
6. Besser, M. J., R. Shapira-Frommer, A. J. Treves, D. Zippel, O. Itzhaki, L. Hershkovitz, D. Levy, A. Kubi, E. Hovav, N. Chermoshniuk, et al. 2010. Clinical responses in a phase II study using adoptive transfer of short-term cultured tumor infiltration lymphocytes in metastatic melanoma patients. Clin. Cancer Res. 16: 2646-2655.
7. Rosenberg, S. A., J. C. Yang, R. M. Sherry, U. S. Kammula, M. S. Hughes, G. Q. Phan, D. E. Citrin, N. P. Restifo, P. F. Robbins, J. R. Wunderlich, et al. 2011. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin. Cancer Res. 17: 4550-4557.
8. Schumacher, T. N. 2002. T-cell-receptor gene therapy. Nat. Rev. Immunol. 2: 512-519. (Pubitemid 37328742)
9. Morgan, R. A., M. E. Dudley, J. R. Wunderlich, M. S. Hughes, J. C. Yang, R. M. Sherry, R. E. Royal, S. L. Topalian, U. S. Kammula, N. P. Restifo, et al. 2006. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314: 126-129. (Pubitemid 44547756)
10. Johnson, L. A., R. A. Morgan, M. E. Dudley, L. Cassard, J. C. Yang, M. S. Hughes, U. S. Kammula, R. E. Royal, R. M. Sherry, J. R. Wunderlich, et al. 2009. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114: 535-546.
11. Offringa, R. 2009. Antigen choice in adoptive T-cell therapy of cancer. Curr. Opin. Immunol. 21: 190-199.
12. Theobald, M., J. Biggs, J. Hernández, J. Lustgarten, C. Labadie, and L. A. Sherman. 1997. Tolerance to p53 by A2.1-restricted cytotoxic T lymphocytes. J. Exp. Med. 185: 833-841. (Pubitemid 27119867)
13. Davis, J. L., M. R. Theoret, Z. Zheng, C. H. Lamers, S. A. Rosenberg, and R. A. Morgan. 2010. Development of human anti-murine T-cell receptor antibodies in both responding and nonresponding patients enrolled in TCR gene therapy trials. Clin. Cancer Res. 16: 5852-5861.
14. Li, L. P., J. C. Lampert, X. Chen, C. Leitao, J. Popović, W. Mü ller, and T. Blankenstein. 2010. Transgenic mice with a diverse human T cell antigen receptor repertoire. Nat. Med. 16: 1029-1034.
15. Richman, S. A., and D. M. Kranz. 2007. Display, engineering, and applications of antigen-specific T cell receptors. Biomol. Eng. 24: 361-373. (Pubitemid 47391576)
16. Kuball, J., B. Hauptrock, V. Malina, E. Antunes, R. H. Voss, M. Wolfl, R. Strong, M. Theobald, and P. D. Greenberg. 2009. Increasing functional avidity of TCR- redirected T cells by removing defined N-glycosylation sites in the TCR constant domain. J. Exp. Med. 206: 463-475.
17. Stauss, H. J. 1999. Immunotherapy with CTLs restricted by nonself MHC. Immunol. Today 20: 180-183.
18. Savage, P., L. Gao, K. Vento, P. Cowburn, S. Man, N. Steven, G. Ogg, A. McMichael, A. Epenetos, E. Goulmy, and H. J. Stauss. 2004. Use of B cellbound HLA-A2 class I monomers to generate high-avidity, allo-restricted CTLs against the leukemia-associated protein Wilms tumor antigen. Blood 103: 4613-4615. (Pubitemid 38745991)
19. Wilde, S., D. Sommermeyer, B. Frankenberger, M. Schiemann, S. Milosevic, S. Spranger, H. Pohla, W. Uckert, D. H. Busch, and D. J. Schendel. 2009. Dendritic cells pulsed with RNA encoding allogeneic MHC and antigen induce T cells with superior antitumor activity and higher TCR functional avidity. Blood 114: 2131-2139.
20. 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. (Pubitemid 26134333)
21. 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. (Pubitemid 26144250)
22. 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.
23. Yee, C., P. A. Savage, P. P. Lee, M. M. Davis, and P. D. Greenberg. 1999. Isolation of high avidity melanoma-reactive CTL from heterogeneous populations using peptide-MHC tetramers. J. Immunol. 162: 2227-2234. (Pubitemid 29288845)
24. Dutoit, V., V. Rubio-Godoy, M. A. Doucey, P. Batard, D. Liénard, D. Rimoldi, D. Speiser, P. Guillaume, J. C. Cerottini, P. Romero, and D. Valmori. 2002. Functional avidity of tumor antigen-specific CTL recognition directly correlates with the stability of MHC/peptide multimer binding to TCR. J. Immunol. 168: 1167-1171. (Pubitemid 34094481)
25. 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. (Pubitemid 38542057)
26. Rivoltini, L., K. C. Barracchini, V. Viggiano, Y. Kawakami, A. Smith, A. Mixon, N. P. Restifo, S. L. Topalian, T. B. Simonis, S. A. Rosenberg, et al. 1995. Quantitative correlation between HLA class I allele expression and recognition of melanoma cells by antigen-specific cytotoxic T lymphocytes. Cancer Res. 55: 3149-3157.
27. Wölfl, M., S. Schalk, M. Hellmich, K. M. Huster, D. H. Busch, and F. Berthold. 2004. Quantitation of MHC tetramer-positive cells from whole blood: evaluation of a single-platform, six-parameter flow cytometric method. Cytometry A 57: 120-130. (Pubitemid 38197603)
28. Braun, M., B. Müller, D. ter Meer, S. Raffegerst, B. Simm, S.Wilde, S. Spranger, J. Ellwart, B. Mosetter, L. Umansky, et al. 2011. The CD6 scavenger receptor is differentially expressed on a CD56 natural killer cell subpopulation and contributes to natural killer-derived cytokine and chemokine secretion. J. Innate Immun. 3: 420-434.
29. Leisegang, M., A. Turqueti-Neves, B. Engels, T. Blankenstein, D. J. Schendel, W. Uckert, and E. Noessner. 2010. T-cell receptor gene-modified T cells with shared renal cell carcinoma specificity for adoptive T-cell therapy. Clin. Cancer Res. 16: 2333-2343.
30. Leisegang, M., B. Engels, P. Meyerhuber, E. Kieback, D. Sommermeyer, S. A. Xue, S. Reuss, H. Stauss, and W. Uckert. 2008. Enhanced functionality of T cell receptor-redirected T cells is defined by the transgene cassette. J. Mol. Med. 86: 573-583.
31. Matsui, K., J. J. Boniface, P. Steffner, P. A. Reay, and M. M. Davis. 1994. Kinetics of T-cell receptor binding to peptide/I-Ek complexes: correlation of the dissociation rate with T-cell responsiveness. Proc. Natl. Acad. Sci. USA 91: 12862-12866.
32. Lyons, D. S., S. A. Lieberman, J. Hampl, J. J. Boniface, Y. Chien, L. J. Berg, and M. M. Davis. 1996. A TCR binds to antagonist ligands with lower affinities and faster dissociation rates than to agonists. Immunity 5: 53-61. (Pubitemid 26254784)
33. Rubio-Godoy, V., V. Dutoit, D. Rimoldi, D. Lienard, F. Lejeune, D. Speiser, P. Guillaume, J. C. Cerottini, P. Romero, and D. Valmori. 2001. Discrepancy between ELISPOT IFN-gamma secretion and binding of A2/peptide multimers to TCR reveals interclonal dissociation of CTL effector function from TCRpeptide/ MHC complexes half-life. Proc. Natl. Acad. Sci. USA 98: 10302-10307. (Pubitemid 32803015)
34. Derby, M. A., J. Wang, D. H. Margulies, and J. A. Berzofsky. 2001. Two intermediate-avidity cytotoxic T lymphocyte clones with a disparity between functional avidity and MHC tetramer staining. Int. Immunol. 13: 817-824. (Pubitemid 32514707)
35. Dutoit, V., P. Guillaume, J. C. Cerottini, P. Romero, and D. Valmori. 2002. Dissecting TCR-MHC/peptide complex interactions with A2/peptide multimers incorporating tumor antigen peptide variants: crucial role of interaction kinetics on functional outcomes. Eur. J. Immunol. 32: 3285-3293. (Pubitemid 35414886)
36. Lyons, G. E., J. J. Roszkowski, S. Man, C. Yee,W. M. Kast, and M. I. Nishimura. 2006. T-cell receptor tetramer binding or the lack there of does not necessitate antigen reactivity in T-cell receptor transduced T cells. Cancer Immunol. Immunother. 55: 1142-1150. (Pubitemid 43800729)
37. Leitenberg, D., and K. Bottomly. 1999. Regulation of naive T cell differentiation by varying the potency of TCR signal transduction. Semin. Immunol. 11: 283-292. (Pubitemid 29401502)
38. Blander, J. M., D. B. Sant'Angelo, K. Bottomly, and C. A. Janeway, Jr. 2000. Alteration at a single amino acid residue in the T cell receptor alpha chain complementarity determining region 2 changes the differentiation of naive CD4 T cells in response to antigen from T helper cell type 1 (Th1) to Th2. J. Exp. Med. 191: 2065-2074.
39. Brogdon, J. L., D. Leitenberg, and K. Bottomly. 2002. The potency of TCR signaling differentially regulates NFATc/p activity and early IL-4 transcription in naive CD4+ T cells. J. Immunol. 168: 3825-3832. (Pubitemid 34298383)
40. Hersperger, A. R., F. Pereyra, M. Nason, K. Demers, P. Sheth, L. Y. Shin, C. M. Kovacs, B. Rodriguez, S. F. Sieg, L. Teixeira-Johnson, et al. 2010. Perforin expression directly ex vivo by HIV-specific CD8 T-cells is a correlate of HIV elite control. PLoS Pathog. 6: e1000917.