Phosphostim-activated γδ T cells kill autologous metastatic renal cell carcinoma

Journal of Immunology

Volumn 174, Issue 3, 2005, Pages 1338-1347

  Viey, Emilie ^a,c   Fromont, Gaëlle ^b   Escudier, Bernard ^a   Morel, Yannis ^c   Da Rocha, Sylvie ^a   Chouaib, Salem ^a   Caignard, Anne ^a,d  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b INSTITUT MUTUALISTE MONTSOURIS   (France)

^c INNATE PHARMA   (France)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GRANZYME A; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL RECEPTOR NKG2D; PERFORIN; PHOSPHOSTIM; T LYMPHOCYTE ANTIGEN; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER INHIBITION; CELL KILLING; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; EFFECTOR CELL; EX VIVO STUDY; FEMALE; HUMAN; IN VITRO STUDY; KIDNEY CARCINOMA; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MEMORY CELL; METASTASIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TARGET CELL;

EID: 12444255107     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.174.3.1338     Document Type: Article

References (48)

1. Escudier, B., C. Chevreau, C. Lasset, J. Douillard, A. Ravaud, M. Fabbro, A. Caty, J. Rossi, P. Viens, J. Bergerat, J. Savary, and S. Negrier. 1999. Cytokines in metastatic renal cell carcinoma: is it useful to switch to interleukin-2 or interferon after failure of a first treatment? Groupe Francais d'Immunotherapie. J. Clin. Oncol. 17:2039.
2. Negrier, S., B. Escudier, F. Gomez, J. Douillard, A. Ravaud, C. Chevreau, M. Buclon, D. Perol, and C. Lasset. 2002. Prognostic factors of survival and rapid progression in 782 patients with metastatic renal carcinomas treated by cytokines: a report from the Groupe Francais d'Immunotherapie. Ann. Oncol. 13:1460.
3. Finke, J., A. Zea, J. Stanley, D. Longo, H. Mizoguchi, R. Tubbs, R. Wiltrout, J. O'Shea, S. Kudoh, and E. Klein. 1993. Loss of T-cell receptor ζ chain and p561ck in T-cells infiltrating human renal cell carcinoma. Cancer Res. 53:5613.
4. Rayman, P., R. Uzzo, V. Kolenko, T. Bloom, M. Cathcart, L. Molto, A. Novick, R. Bukowski, T. Hamilton, and J. Finke. 2000. Tumor-induced dysfunction in interleukin-2 production and interleukin-2 receptor signaling: a mechanism of immune escape. Cancer J. Sci. Am. 6(Suppl. 1):S81.
5. Uzzo, R., P. Clark, P. Rayman, T. Bloom, L. Rybicki, A. Novick, R. Bukowski, and J. Finke. 1999. Alterations in NFκB activation in T lymphocytes of patients with renal cell carcinoma. J. Natl Cancer Inst. 91:748.
6. Molto, L., P. Rayman, E. Paszkiewicz-Kozik, M. Thornton, L. Reese, S. Thomas, T. Das, D. Kudo, R. Bukowski, J. Finke, and C. Tannenbaum. 2003. The Bcl-2 transgene protects T cells from renal cell carcinoma-mediated apoptosis. Clin. Cancer Res. 11:4060.
7. Bukowski, R., P. Rayman, R. Uzzo, T. Bloom, K. Sandstrom, D. Peereboom, T. Olencki, G. Budd, D. McLain, P. Elson, A. Novick, and J. H. Finke. 1998. Signal transduction abnormalities in T lymphocytes from patients with advanced renal carcinoma: clinical relevance and effects of cytokine therapy. Clin. Cancer Res. 4:2337.
8. Mitropoulos, D., S. Kooi, J. Rodriguez-Villanueva, and C. Platsoucas. 1994. Characterization of fresh (uncultured) tumour-infiltrating lymphocytes (TIL) and TIL-derived T cell lines from patients with renal cell carcinoma. Clin. Exp. Immunol. 97:321.
9. Schendel, D., R. Oberneder, C. Falk, P. Jantzer, S. Kressenstein, B. Maget, A. Hofstetter, G. Riethmuller, and E. Nossner. 1997. Cellular and molecular analyses of major histocompatibility complex (MHC) restricted and non-MHC-restricted effector cells recognizing renal cell carcinomas: problems and perspectives for immunotherapy. J. Mol. Med. 75:400.
10. Schleypen, J., M. V. Geldern, E. Weiss, N. Kotzias, K. Rohrmann, D. Schendel, C. Falk, and H. Pohla. 2003. Renal cell carcinoma-infiltrating natural killer cells express differential repertoires of activating and inhibitory receptors and are inhibited by specific HLA class I allotypes. Int. J. Cancer. 106:905.
11. Gati, A., S. D. Rocha, N. Guerra, B. Escudier, A. Moretta, S. Chouaib, E. Angevin, and A. Caignard. 2004. Analysis of the natural killer mediated immune response in metastatic renal cell carcinoma patients. Int. J. Cancer. 109:393.
12. Escudier, B., F. Farace, E. Angevin, F. Charpentier, G. Nitenberg, F. Tribel, and T. Hercend. 1994. Immunotherapy with interleukin-2 (IL2) and lymphokine-activated natural killer cells: improvement of clinical responses in metastatic renal cell carcinoma patients previously treated with IL-2. Eur. J. Cancer 30:1078.
13. Kato, Y., Y. Tanaka, F. Miyagawa, S. Yamashita, and N. Minato. 2001. Targeting of tumor cells for human γδ T cells by nonpeptide antigens. J. Immunol. 167:5092.
14. Sicard, H., T. A. Saati, G. Delsol, and J. Fournie. 2001. Synthetic phosphoantigens enhance human Vγ9Vδ2 T lymphocytes killing of non-Hodgkin's B lymphoma. Mol. Med. 10:711.
15. Zheng, B., S. Ng, D. Chua, J. Sham, D. Kwong, C. Lam, and M. Ng. 2001. Peripheral γδ T-cell deficit in nasopharyngeal carcinoma. Int. J. Cancer. 99:213.
16. Wilhelm, M., V. Kunzmann, S. Eckstein, P. Reimer, F. Weissinger, T. Ruediger, and H. Tony. 2003. γδ T cells for immune therapy of patients with lymphoid malignancies. Blood 102:200.
17. Choudhary, A., F. Davodeau, A. Moreau, M. Peyrat, M. Bonneville, and F. Jotereau. 1995. Selective lysis of autologous tumor cells by recurrent γδ tumor-infiltrating lymphocytes from renal carcinoma. J. Immunol. 154:3932.
18. Kobayashi, H., Y. Tanaka, J. Yagi, H. Toma, and T. Uchiyama. 2001. γ/δ T cells provide innate immunity against renal cell carcinoma. Cancer Immunol. Immunother. 50:115.
19. Band, H., G. Panchamoorthy, J. Mclean, C. Morita, S. Ishikawa, R. Modlin, and M. Brenner. 1990. Recognition of mycobacterial antigens by γδ T cells. Res. Immunol. 141:645.
20. Poccia, F., S. Boullier, H. Lecoeur, M. Cochet, Y. Poquet, V. Colizzi, J. Fournie, and M. Gougeon. 1996. Peripheral Vγ9/Vδ2 T cell deletion and anergy to non-peptidic mycobacterial antigens in asymptomatic HIV-1-infected persons. J. Immunol.:449.
21. Wang, L., H. Das, A. Kamath, and J. Bukowski. 2001. Human Vγ2Vδ2 T cells produce IFN-γ and TNF-α with an on/off/on cycling pattern in response to live bacterial products. J. Immunol 167:6195.
22. Hara, T., Y. Mizuno, K. Takaki, H. Takada, H. Akeda, T. Aoki, M. Nagata, K. Veda, G. Matsuzaki, Y. Yoshikai, et al. 1992. Predominant activation and expansion of Vγ9-bearing γδ T cells in vivo as well as in vitro in Salmonella infection. J. Clin. Invest. 90:204.
23. + antigen receptors are present in increased proportions in a fraction of patients with tuberculosis or with sarcoidosis. Am. Rev. Respir. Dis. 148:1685.
24. Janis, E., S. Kaufmann, R. Schwartz, and D. Pardoll. 1989. Activation of γδ T cells in the primary immune response to Mycobacterium tuberculosis. Science 244:713.
25. Espinosa, E., C. Belmant, F. Pont, B. Luciani, R. Poupot, F. Romagne, H. Brailly, M. Bonneville, and J. Fournie. 2001. Chemical synthesis and biological activity of bromohydrin pyrophosphate, a potent stimulator of human γδ T cells. J. Biol. Chem. 276:18337.
26. Kunzmann, V., E. Bauer, J. Feurle, F. Weissinger, H. Tony, and M. Wilhelm. 2000. Stimulation of γδ T cells by aminobisphosphonates and induction of antiplasma cell activity in multiple myeloma. Blood 96:384.
27. Tanaka, Y., C. Morita, Y. Tanaka, E. Nieves, M. Brenner, and B. Bloom. 1995. Natural and synthetic non-peptide antigens recognized by human γδ T cells. 375:155.
28. Davodeau, F., M. Peyrat, M. Hallet, J. Gaschet, I. Houde, R. Vivien, H. Vie, and M. Bonneville. 1993. Close correlation between Daudi and mycobacterial antigen recognition by human γδ T cells and expression of V9JPC1γ/V2DJCδ-encoded T cell receptors. J. Immunol. 151:1214.
29. Lang, F., M. Peyrat, P. Constant, F. Davodeau, J. David-Ameline, Y. Poquet, H. Vie, J. Fournie, and M. Bonneville. 1995. Early activation of human Vγ9Vδ2 T cell broad cytotoxicity and TNF production by nonpeptidic mycobacterial ligands. J. Immunol. 154:5986.
30. Morita, C., E. Beckman, J. Bukowski, Y. Tanaka, H. Band, B. Bloom, D. Golan, and M. Brenner. 1995. Direct presentation of nonpeptide prenyl pyrophosphate antigens to human γδ T cells. Immunity 3:495.
31. Fisch, P., M. Malkovsky, E. Braakman, E. Sturm, R. Bolhuis, A. Prieve, J. Sosman, V. Lam, and P. Sondel. 1990. γδ T cell clones and natural killer cell clones mediate distinct patterns of non-major histocompatibility complex-restricted cytolysis. J. Exp. Med. 171:1567.
32. Fabrizio, L. D., Y. Kimura, R. Ware, L. Rogozinski, and L. Chess. 1991. Specific triggering of γδ T cells by K562 activates the γδ T cell receptor and may regulate natural killer-like function. J. Immunol. 146:2495.
33. Libero, G. D., G. Casorati, C. Giachino, C. Carbonara, N. Migone, P. Matzinger, and A. Lanzavecchia. 1991. Selection by two powerful antigens may account for the presence of the major population of human peripheral γδ T cells. J. Exp. Med. 173:1311.
34. Gober, H., M. Kistowska, L. Angman, P. Jeno, L. Mori, and G. D. Libero. 2003. Human T cell receptor γδ cells recognize endogenous mevalonate metabolites in tumor cells. J. Exp. Med. 197:163.
35. Guerra, N., F. Michel, A. Gati, C. Gaudin, Z. Mishal, B. Escudier, O. Acuto, S. Chouaib, and A. Caignard. 2002. Engagement of the inhibitory receptor CD158a interrupts TCR signaling, preventing dynamic membrane reorganization in CTL/tumor interaction. Blood 200:2874.
36. Das, H., L. Wang, A. Kamath, and J. Bukowski. 2001. Vγ2Vδ2 T-cell receptor-mediated recognition of aminobisphosphonates. Blood 98:1616.
37. Cosman, D. 2001. ULBPs novel MHC-cass-I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14:123.
38. Groh, W., J. Wu, C. Yee, and T. Spies. 2002. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419:734.
39. Fisch, P., E. Meuer, D. Pende, S. Rothenfusser, O. Viale, S. Kock, S. Ferrone, D. Fradelizi, G. Klein, L. Moretta, et al. 1997. Control of B cell lymphoma recognition via natural killer inhibitory receptors implies a role for human Vγ9/ Vδ2 T cells in tumor immunity. Eur. J. Immunol. 27:3368.
40. Halary, F., M. Peyrat, E. Champagne, M. Lopez-Botet, A. Moretta, L. Moretta, H. Vie, J. Fournie, and M. Bonneville. 1997. Control of self-reactive cytotoxic T lymphocytes expressing γδ T cell receptors by natural killer inhibitory receptors. Eur. J. Immunol. 27:2812.
41. + T cells during mycobacterial infections. Science 295:2255.
42. Hintzen, R., R. d. Jong, S. Lens, M. Brouwer, P. Baars, and R. v. Lier. 1993. Regulation of CD27 expression on subsets of mature T-lymphocytes. J. Immunol. 151:2426.
43. + T cells. J. Exp. Med. 194:953.
44. Poccia, F., B. Cipriani, S. Vendetti, V. Colizzi, Y. Poquet, L. Battistini, M. Lopez-Botet, J. J. Fournie, and M. Gougeon. 1997. CD94/NKG2 inhibitory receptor complex modulates both anti-viral and anti-tumoral responses of polyclonal phosphoantigen-reactive Vγ9Vδ2 T lymphocytes. J. Immunol. 159:6009.
45. Girardi, M., D. Oppenheim, C. Steele, J. Lewis, E. Glusac, R. Filler, P. Hobby, B. Sutton, R. Tigelaar, and A. Hayday. 2001. Regulation of cutaneous malignancy by γδ T cells. Science 294:605.
46. Bachelez, H., B. Flageul, L. Degos, L. Boumsell, and A. Bensussan. 1992. TCR γδ bearing T lymphocytes infiltrating human primary cutaneous melanomas. J. Invest. Dermatol. 98:369.
47. Nanno, M., H. Seki, C. Ioannides, K. Itoh, J. Morkowski, N. Day, R. Good, and C. Platsoucas. 1992. Disulfide-linked and non-disulfide-linked γδ T-cell antigen receptors: differential expression on T-cell lines and clones derived from normal donors and patients with primary immunodeficiency disorders. Anticancer Res. 12:1069.
48. Lozupone, F., D. Pende, V. Burgio, C. Castelli, M. Spada, M. Venditti, F. Luciani, L. Lugini, C. Federici, C. Ramoni, et al. 2004. Effect of human natural killer and γδ T cells on the growth of human autologous melanoma xenografts in SCID mice. Cancer Res. 64:378.