Characterization of tumor reactivity of human Vγ9Vδ2 γδ T cells in vitro and in SCID mice in vivo

Journal of Immunology

Volumn 173, Issue 11, 2004, Pages 6767-6776

  Kabelitz, Dieter ^a,c   Wesch, Daniela ^a   Pitters, Elke ^a   Zöller, Margot ^b  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALENDRONIC ACID; AMINOBISPHOSPHONATE ALENDRONATE; BISPHOSPHONIC ACID DERIVATIVE; INTERLEUKIN 2; RECOMBINANT INTERLEUKIN 2; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER SURVIVAL; CELL INTERACTION; CONTROLLED STUDY; EFFECTOR CELL; HUMAN; HUMAN CELL; MELANOMA; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR CELL DESTRUCTION; TUMOR IMMUNOLOGY;

EID: 9144241718     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.11.6767     Document Type: Article

References (66)

1. Van der Bruggen, P., Y. Zhang, P. Chaux, V. Stroobant, C. Panichelli, E. S. Schultz, J. Chapiro, B. J. van den Eynde, F. Brasseur, and T. Boon. 2002. Tumor-specific shared antigenic peptides recognized by human T cells. Immunol. Rev. 188:51.
2. Finn, O. J. 2003. Cancer vaccines: between the idea and the reality. Nat. Rev. Immunol. 3:630.
3. Dudley, M. E., J. R. Wunderlich, T. E. Shelton, J. Even, and S. A. Rosenberg. 2003. Generation of tumor-infiltrating lymphocyte cultures for use in adoptive transfer therapy for melanoma patients. J. Immunother. 26:332.
4. Dudley, M. E., and S. A. Rosenberg. 2003. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat. Rev. Cancer 3:666.
5. Hayday, A. 2000. γδ T cells: a right time and a right place for a conserved third way of protection. Annu. Rev. Immunol. 18:975.
6. Porcelli, S., M. B. Brenner, and H. Band. 1991. Biology of the human γδ T-cell receptor. Immunol. Rev. 120:137.
7. Hinz, T., D. Wesch, F. Halary, S. Marx, A. Choudhary, B. Arden, O. Janssen, M. Bonneville, and D. Kabeltz. 1997. Identification of the complete expressed human T-cell receptor Vγ repertoire by flow cytometry. Int. Immunol. 9:1065.
8. Deusch, K., F. Luling, K. Reich, M. Classen, H. Wagner, and K. Pfeffer. 1991. A major fraction of human intraepithelial lymphocytes simultaneously expresses the γδ receptor, the CD8 accessory molecule and preferentially uses the Vδ1 gene segment. Eur. J. Immunol. 21:1053.
9. Constant, P., F. Davodeau, M. A. Peyrat, Y. Poquet, G. Puzo, M. Bonneville, and J. J. Fournié. 1994. Stimulation of human γδ T-cells by nonpeptidic mycobacterial ligands. Science 264:267.
10. Jomaa, H., J. Feurle, K. Luhs, V. Kunzmann, H. P. Tony, M. Herderich, and W. Wilhelm. 1999. Vγ9/Vδ2 T cell activation induced by bacterial low molecular mass compounds depends on the 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis. FEMS Immunol. Med. Microbiol. 25:371.
11. Altincicek, B., J. Moll, N. Campos, G. Foerster, E. Beck, J. F. Hoeffler, C. Grosdemange-Billiatd, M. Rodriguez-Concepcion, M. Rohmer, A. Boron, et al. 2001. Cutting edge: human γδ T cells are activated by intermediates of the 2-C-methyl-D-erythritol 4-phosphate pathway of isoprenoid biosynthesis. J. Immunol. 166:3655.
12. Belmant, C., E. Espinosa, R. Poupot, M. Guiraud, Y. Poquet, M. Bonneville, and J. J. Fournié. 1999. 3-Formyl-1-butyl pyrophosphate: a novel mycobacterial metabolite activating human γδ T cells. J. Biol. Chem. 274:32079.
13. Kabelitz, D., A. Glatzel, and D. Wesch. 2000. Antigen recognition by human γδ T lymphocytes. Int. Arch. Allergy Immunol. 122:1.
14. Fisch, P., M. Malkovsky, S. Kovats, E. Sturm, E. Braakman, B. S. Klein, S. D. Voss, L. W. Morissey, R. DeMars, W. J. Welch, et al. 1990. Recognition by human Vγ9/Vδ2 T cells of a GroEL homolog on Daudi Burkitt's lymphoma cells. Science 250:1269.
15. Groh, V., A. Steinle, S. Bauer, and T. Spies. 1998. Recognition of stress-induced MHC molecules by intestinal epithelial γδ T cells. Science 279:1737.
16. Bauer, S., V. Groh, J. Wu, A. Steinle, J. H. Philipps, L. L. Lanier, and T. Spies. 1999. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285:727.
17. Das, H., V. Groh, C. Kuijl, M. Sugita, C. T. Morita, T. Spies, and J. F. Bukowski. 2001. MICA engagement by human Vγ2Vδ2 T cells enhances their antigen-dependent effector function. Immunity 15:83.
18. Wu, J., V. Groh, and T. Spies. 2002. T cell antigen receptor engagement and specificity in the recognition of stress-inducible MHC class I-related chains by human epithelial γδ T cells. J. Immunol. 169:1236.
19. Spada, F. M., E. P. Grant, P. J. Peters, M. Sugita, A. Melián, D. S. Leslie, H. K. Lee, E. van Donselar, D. A. Hanson, A. M. Krensky, et al. 2000. Self recognition of CD1 by γδ T cells: implications for innate immunity. J. Exp. Med. 191:937.
20. Boismenu, R., and W. L. Havran. 1994. Modulation of epithelial cell growth by γδ T cells. Science 266:1253.
21. Workalemahu, G., M. Foerster, and C. Kroegel. 2004. Expression and synthesis of fibroblast growth factor-9 in human γδ T-lymphocytes: response to isopentenyl pyrophosphate and TGF-β/IL-15. J. Leukocyte Biol. 75:657.
22. Hayday, A., and R. Tigelaar. 2003. Immunoregulation in the tissues by γδ T cells. Nat. Rev. Immunol. 3:233.
23. Girardi, M., D. E. Oppenheim, C. R. Steele, J. M. Lewis, E. Glusac, R. Filler, P. Hobby, B. Sutton, R. E. Tigelaar, and A. C. Hayday. 2001. Regulation of cutaneous malignancy by γδ T cells. Science 294:605.
24. Gao, Y., W. Yang, M. Pan, E. Scully, M. Girardi, L. H. Augenlicht, J. Craft, and Z. Yin. 2003. γδ T cells provide an early source of interferon γ in tumor immunity. J. Exp. Med. 198:433.
25. Street, S. E. A., Y. Hayakawa, Y. Zhan, A. M. Lew, D. MacGregor, A. M. Jamieson, A. Diefenbach, H. Yagita, D. I. Godfrey, and M. J. Smyth. 2004. Innate immune surveillance of spontaneous B cell lymphomas by natural killer cells and γδ T cells. J. Exp. Med. 199:879.
26. Choudhary, A., F. Davodeau, A. Moreau, M. A. 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.
27. + lymphocytes recognize tumor cells of epithelial origin. J. Exp. Med. 183:1681.
28. + γδ tumor infiltrating lymphocytes from human lung carcinomas. Eur. J. Immunol. 20:2685.
29. + T-cell receptors. J. Natl. Cancer Inst. 88:436.
30. Dolstra, H., H. Fredrix, A. van der Meer, T. de Witte, C. Figdor, and E. van de Weil-van Kemenade. 2001. TCRγδ cytotoxic T lymphocytes expressing the killer cell-inhibitory receptor p58.2 (CD158b) selectively lyse acute myeloid leukaemia cells. Bone Marrow Transplant. 27:1087.
31. Zheng, B. J., K. W. Chan, S. Im, D. Chua, J. S. T. Sham, P. C. Tin, Z. M. He, and M. H. Ng. 2001. Anti-tumor effects of human peripheral γδ T cells in a mouse tumor model. Int. J. Cancer 92:421.
32. Lozupone, F., D. Pende, V. L. 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 xenograft in SCID mice. Cancer Res. 64:378.
33. Malkovska, V., F. K. Cigel, N. Armstrong, B. Storere, and R. Hong. 1992. Antilymphoma activity of human γδ T-cells in mice with severe combined immune deficiency. Cancer Res. 52:5610.
34. Espinosa, E., C. Belmant, F. Pont, B. Lucani, R. Poupot, F. Romagné, H. Brailly, M. Bonneville, and J. J. Fournié. 2001. Chemical synthesis and biological activity of bromohydrin pyrophosphate, a potent stimulator of human γδ T cells. J. Biol. Chem. 276:18337.
35. Kunzmann, V., E. Bauer, and M. Wilhelm. 1999. γ/δ T-cell stimulation by pamidronate. N. Engl. J. Med. 340:737 (Lett.).
36. Kunzmann, V., E. Bauer, J. Feurle, F. Weißinger, H. P. Tony, and M. Wilhelm. 2000. Stimulation of γδ T cells by aminobisphosphonates and induction of antiplasma cell activity in multiple myeloma. Blood 96:384.
37. Das, H., L. Wang, A. Kamath, and J. F. Bukowski. 2001. Vγ2Vδ2 T-cell receptor-mediated recognition of aminobisphosphonates. Blood 98:1616.
38. Miyagawa, F., Y. Tanaka, S. Yamashita, and N. Minato. 2001. Essential requirement of antigen presentation by monocyte lineage cells for the activation of primary human γδ T cells by aminobisphosphonate antigen. J. Immunol. 166:5508.
39. Wilhelm, M., V. Kunzmann, S. Eckstein, P. Reimer, F. Weissinger, T. Ruediger, and H. P. Tony. 2003. γδ T cells for immune therapy of patients with lymphoid malignancy. Blood 102:200.
40. Dieli, F., N. Gebbia, F. Poccia, N. Caccamo, C. Montesano, F. Fulfaro, C. Arcara, M. R. Valerio, S. Meraviglia, C. Di Sano, et al. 2003. Induction of γδ T-lymphocyte effector functions by bisphosphonate zoledronic acid in cancer patients in vivo. Blood 102:2310 (Lett.).
41. + antigen-presenting cells. Int. Immunol. 4:1381.
42. Pechhold, K., N. Craighead, D. Wesch, and D. Kabelitz. 2002. Measurement of cellular proliferation. In Methods in Microbiology, Vol. 32: Immunology of Infection, 2nd Ed. S. H. E. Kaufmann and D. Kabelitz, eds. Academic Press, London, p. 77.
43. Janssen, O., S. Wesselborg, B. Heckl-Östreicher, A. Bender, S. Schondelmaier, K. Pechhold, G. Moldenhauer, and D. Kabelitz. 1991. T-cell receptor/CD3-signalling induces death by apoptosis in human T-cell receptor γδ-positive T-cells. J. Immunol. 146:35.
44. Koch, N., G. Hämmerling, N. Tada, S. Kimura, and U. Hämmerling. 1982. Cross-blocking studies with monoclonal antibodies against I-A molecules of haplotypes b, days and k. Eur. J. Immunol. 12:909.
45. Wesch, D., A. Glatzel, and D. Kabelitz. 2001. Differentiation of resting human peripheral blood γδ T cells towards Th1- or Th2-phenotype. Cell. Immunol. 212:110.
46. Shpitz, B., B. J. Fernandes, J. B. Mullen, J. C. Roder, and S. Gallinger. 1994. Improved engraftment of human tumours in SCID mice pretreated with radiation and anti-asialo GM1. Anticancer Res. 14:1927.
47. Pechhold, K., D. Wesch, S. Schondelmaier, and D. Kabelitz. 1994. Primary activation of Vγ9 expressing γδ T cells by mycobacterium tuberculosis: requirement for Th1-type CD4 T cell help and inhibition by interleukin-10. J. Immunol. 152:4984.
48. Ungefroren, H., M. Voss, M. Jansen, C. Röder, D. Henne-Bruns, B. Kremer, and H. Kalthoff. 1998. Human pancreatic adenocarcinomas express Fas and Fas ligand yet are resistant to Fas-mediated apoptosis. Cancer Res. 58:1741.
49. Sicard, H., T. Al Saati, G. Delsol, and J. J. Fournié. 2001. Synthetic phosphoantigens enhance human Vγ9Vδ2 T lymphocytes killing of non-Hodgkin's lymphoma. Mol. Med. 7:711.
50. 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.
51. Shipman, C. M., M. J. Rogers, J. F. Apperley, R. G. G. Russell, and P. I. Croucher. 1997. Bisphosphonates induce apoptosis in human myeloma cell lines: a novel anti-tumour activity. Br. J. Haematol. 98:665.
52. Riedle, S., M. Rösel, S. Seiter, and M. Zöller. 1998. Effector cell targeting by bispecific antibodies in the therapy of human malignant melanoma: evaluation in the SCID mouse model. Int. J. Cancer. 75:908.
53. 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.
54. Ferrarini, M., E. Ferrero, L. Dagna, A. Poggi, and M. R. Zocchi. 2002. Human γδ T cells: a nonredundant system in the immune-surveillance against cancer. Trends Immunol. 23:14.
55. Angelini, D. F., G. Borsellino, M. Poupot, A. Diamantini, R. Poupot, G. Bernardi, F. Poccia, J. J. Fournié, and L. Battistini. 2004. FcγRIII discriminates between two subsets of Vγ9Vδ2 effector cells with different responses and activation pathways. Blood 104:1801.
56. Lafont, V., J. Liautard, J. P. Liautard, and J. Favero. 2001. Production of TNF-α by human Vγ9Vδ2 T cells via engagement of FcγRIIIA, the low affinity type 3 receptor for the Fc portion of IgG, expressed upon TCR activation by nonpeptidic antigen. J. Immunol. 166:7190.
57. Cooper, M. A., T. A. Fehniger, and M. A. Caliguri. 2001. The biology of human natural killer-cell subsets. Trends Immunol. 22:633.
58. Gober, H. J., M. Kistowska, L. Angman, P. Jenö, L. Mori, and G. de Libero. 2003. Human T cell receptor γδ T cells recognize endogenous mevalonate metabolites in tumor cells. J. Exp. Med. 197:163.
59. Bergstrom, J. D., R. G. Bostedor, P. J. Masarachia, A. A. Reszka, and G. Rodan. 2000. Alendronate is a specific, nanomolar inhibitor of farnesyl diphosphate synthase. Arch. Biochem. Biophys. 373:231.
60. Borrego, F., J. Kabat, T. B. Sanni, and J. E. Coligan. 2002. NK cell CD94/NKG2A inhibitory receptors are internalized and recycle independently of inhibitory signaling processes. J. Immunol. 169:6102.
61. Zhu, H., H. O. Fearnhead, and G. M. Cohen. 1995. An ICE-like protease is a common mediator of apoptosis induced by diverse stimuli in human monocytic THP. 1 cells. FEBS Lett. 374:303.
62. Koizumi, H., C. C. Liu, L. M. Zheng, S. V. Joag, N. K. Bayne, J. Holoshitz, and J. D. Young. 1991. Expression of perform and serine esterases by human γδ T-cells. J. Exp. Med. 173:499.
63. Pardo, J., P. Perez-Galan, S. Gamen, I. Marzo, I. Monleon, A. A. Kaspar, S. A. Susin, G. Kroemer, A. M. Krensky, J. Naval, et al. 2001. A role of the mitochondrial apoptosis-inducing factor in granulysin-induced apoptosis. J. Immunol. 167:1222.
64. Kabelitz, D., and D. Wesch. 2003. Features and functions of γδ T lymphocytes: focus on chemokines and their receptors. Crit. Rev. Immunol. 25:339.
65. Bukowski, J. F., C. T. Morita, Y. Tanaka, B. R. Bloom, M. B. Brenner, and H. Band. 1995. Vγ2Vδ2 TCR-dependent recognition of non-peptide antigens and Daudi cells analyzed by TCR gene transfer. J. Immunol. 154:998.
66. Fisch, P., A. Moris, H. G. Rammensee, and R. Handgretinger. 2000. Inhibitory MHC class I receptors on γδ T cells in tumour immunity and autoimmunity. Trends Immunol. 21:187.