Regulatory and effector functions of gamma-delta (γδ) T cells and their therapeutic potential in adoptive cellular therapy for cancer

International Journal of Cancer

Volumn 139, Issue 5, 2016, Pages 976-985

  Paul, Sourav ^a   Lal, Girdhari ^a  

^a NATIONAL CENTRE FOR CELL SCIENCE   (India)

Author keywords

Gamma delta T cells; inflammation; tolerance; tumor microenvironment

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; IMMUNOGLOBULIN RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

ADOPTIVE TRANSFER; CANCER CONTROL; CANCER IMMUNOTHERAPY; CYTOKINE RELEASE; GAMMA DELTA T LYMPHOCYTE; HUMAN; LYMPHOCYTE FUNCTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; ADOPTIVE IMMUNOTHERAPY; ANIMAL; IMMUNOLOGY; IMMUNOMODULATION; METABOLISM; NEOPLASMS; PROCEDURES; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; CYTOKINES; HUMANS; IMMUNOMODULATION; IMMUNOTHERAPY, ADOPTIVE; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTE SUBSETS;

EID: 84963620848     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.30109     Document Type: Review

References (122)

1. Born WK, Kemal Aydintug M, O'Brien RL., Diversity of gammadelta T-cell antigens. Cell Mol Immunol 2013; 10: 13-20.
2. Kabelitz D, Glatzel A, Wesch D., Antigen recognition by human gammadelta T lymphocytes. Int Arch Allergy Immunol 2000; 122: 1-7.
3. Born W, Hall L, Dallas A, et al., Recognition of a peptide antigen by heat shock-reactive gamma delta T lymphocytes. Science 1990; 249: 67-9.
4. Lawetzky A, Tiefenthaler G, Kubo R, et al., Identification and characterization of rat T cell subpopulations expressing T cell receptors alpha/beta and gamma/delta. Eur J Immunol 1990; 20: 343-9.
5. Stingl G, Koning F, Yamada H, et al., Thy-1+ dendritic epidermal cells express T3 antigen and the T-cell receptor gamma chain. Proc Natl Acad Sci USA 1987; 84: 4586-90.
6. Itohara S, Farr AG, Lafaille JJ, et al., Homing of a gamma delta thymocyte subset with homogeneous T-cell receptors to mucosal epithelia. Nature 1990; 343: 754-7.
7. Goodman T, Lefrancois L., Expression of the gamma-delta T-cell receptor on intestinal CD8+ intraepithelial lymphocytes. Nature 1988; 333: 855-8.
8. Asarnow DM, Kuziel WA, Bonyhadi M, et al., Limited diversity of gamma delta antigen receptor genes of Thy-1+ dendritic epidermal cells. Cell 1988; 55: 837-47.
9. Heilig JS, Tonegawa S., Diversity of murine gamma genes and expression in fetal and adult T lymphocytes. Nature 1986; 322: 836-40.
10. Crowley MP, Reich Z, Mavaddat N, et al., The recognition of the nonclassical major histocompatibility complex (MHC) class I molecule, T10, by the gammadelta T cell, G8. J Exp Med 1997; 185: 1223-30.
11. Rincon-Orozco B, Kunzmann V, Wrobel P, et al., Activation of V gamma 9V delta 2 T cells by NKG2D. J Immunol 2005; 175: 2144-51.
12. Rei M, Goncalves-Sousa N, Lanca T, et al., Murine CD27(-) Vgamma6(+) gammadelta T cells producing IL-17A promote ovarian cancer growth via mobilization of protumor small peritoneal macrophages. Proc Natl Acad Sci USA 2014; 111: E3562-70.
13. Kuhl AA, Pawlowski NN, Grollich K, et al., Human peripheral gammadelta T cells possess regulatory potential. Immunology 2009; 128: 580-8.
14. Ribot JC, deBarros A, Pang DJ, et al., CD27 is a thymic determinant of the balance between interferon-gamma- and interleukin 17-producing gammadelta T cell subsets. Nat Immunol 2009; 10: 427-36.
15. Sperling AI, Linsley PS, Barrett TA, et al., CD28-mediated costimulation is necessary for the activation of T cell receptor-gamma delta+ T lymphocytes. J Immunol 1993; 151: 6043-50.
16. Witherden DA, Verdino P, Rieder SE, et al., The junctional adhesion molecule JAML is a costimulatory receptor for epithelial gammadelta T cell activation. Science 2010; 329: 1205-10.
17. Sun X, Shibata K, Yamada H, et al., CD30L/CD30 is critical for maintenance of IL-17A-producing gammadelta T cells bearing Vgamma6 in mucosa-associated tissues in mice. Mucosal Immunol 2013; 6: 1191-201.
18. Bekiaris V, Sedy JR, Macauley MG, et al., The inhibitory receptor BTLA controls gammadelta T cell homeostasis and inflammatory responses. Immunity 2013; 39: 1082-94.
19. Gogoi D, Dar AA, Chiplunkar SV., Involvement of notch in activation and effector functions of gammadelta T cells. J Immunol 2014; 192: 2054-62.
20. Nedellec S, Sabourin C, Bonneville M, et al., NKG2D costimulates human V gamma 9V delta 2 T cell antitumor cytotoxicity through protein kinase C theta-dependent modulation of early TCR-induced calcium and transduction signals. J Immunol 2010; 185: 55-63.
21. Wang L, Kang N, Zhou J, et al., Downregulation of CD94/NKG2A inhibitory receptor on decreased gammadelta T cells in patients with systemic lupus erythematosus. Scand J Immunol 2012; 76: 62-9.
22. Collins C, Shi C, Russell JQ, et al., Activation of gamma delta T cells by Borrelia burgdorferi is indirect via a TLR- and caspase-dependent pathway. J Immunol 2008; 181: 2392-8.
23. Hedges JF, Lubick KJ, Jutila MA., Gamma delta T cells respond directly to pathogen-associated molecular patterns. J Immunol 2005; 174: 6045-53.
24. Otsuka A, Hanakawa S, Miyachi Y, et al., CD39: a new surface marker of mouse regulatory gammadelta T cells. J Allergy Clin Immunol 2013; 132: 1448-51.
25. Paul S, Singh AK, Shilpi Lal G., Phenotypic and functional plasticity of gamma-delta (yd) T cells in inflammation and tolerance. Int Rev Immunol 2014; 33: 537-58.
26. Paul S, Shilpi Lal G., Role of gamma-delta (gammadelta) T cells in autoimmunity. J Leukoc Biol 2015; 97: 259-71.
27. Brandes M, Willimann K, Moser B., Professional antigen-presentation function by human gammadelta T Cells. Science 2005; 309: 264-8.
28. Cordova A, Toia F, La Mendola C, et al., Characterization of human gammadelta T lymphocytes infiltrating primary malignant melanomas. PLoS One 2012; 7: e49878
29. Groh V, Rhinehart R, Secrist H, et al., Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci USA 1999; 96: 6879-84.
30. Ma C, Zhang Q, Ye J, et al., Tumor-infiltrating gammadelta T lymphocytes predict clinical outcome in human breast cancer. J Immunol 2012; 189: 5029-36.
31. Braza MS, Klein B., Anti-tumour immunotherapy with Vgamma9Vdelta2 T lymphocytes: from the bench to the bedside. Br J Haematol 2013; 160: 123-32.
32. Hannani D, Ma Y, Yamazaki T, et al., Harnessing gammadelta T cells in anticancer immunotherapy. Trends Immunol 2012; 33: 199-206.
33. Kunzmann V, Smetak M, Kimmel B, et al., Tumor-promoting versus tumor-antagonizing roles of gammadelta T cells in cancer immunotherapy: results from a prospective phase I/II trial. J Immunother 2012; 35: 205-13.
34. Nicol AJ, Tokuyama H, Mattarollo SR, et al., Clinical evaluation of autologous gamma delta T cell-based immunotherapy for metastatic solid tumours. Br J Cancer 2011; 105: 778-86.
35. Kobayashi H, Tanaka Y, Yagi J, et al., Phase I/II study of adoptive transfer of gammadelta T cells in combination with zoledronic acid and IL-2 to patients with advanced renal cell carcinoma. Cancer Immunol Immunother 2011; 60: 1075-84.
36. Ye J, Ma C, Hsueh EC, et al., Tumor-derived gammadelta regulatory T cells suppress innate and adaptive immunity through the induction of immunosenescence. J Immunol 2013; 190: 2403-14.
37. Saitoh A, Narita M, Watanabe N, et al., Anti-tumor cytotoxicity of gammadelta T cells expanded from peripheral blood cells of patients with myeloma and lymphoma. Med Oncol 2008; 25: 137-47.
38. Liu Z, Guo BL, Gehrs BC, et al., Ex vivo expanded human Vgamma9Vdelta2+ gammadelta-T cells mediate innate antitumor activity against human prostate cancer cells in vitro. J Urol 2005; 173: 1552-6.
39. Alexander AA, Maniar A, Cummings JS, et al., Isopentenyl pyrophosphate-activated CD56+ {gamma}{delta} T lymphocytes display potent antitumor activity toward human squamous cell carcinoma. Clin Cancer Res 2008; 14: 4232-40.
40. Corvaisier M, Moreau-Aubry A, Diez E, et al., V gamma 9V delta 2 T cell response to colon carcinoma cells. J Immunol 2005; 175: 5481-8.
41. Wu YL, Ding YP, Tanaka Y, et al., gammadelta T cells and their potential for immunotherapy. Int J Biol Sci 2014; 10: 119-35.
42. Roth SJ, Diacovo TG, Brenner MB, et al., Transendothelial chemotaxis of human alpha/beta and gamma/delta T lymphocytes to chemokines. Eur J Immunol 1998; 28: 104-13.
43. Cipriani B, Borsellino G, Poccia F, et al., Activation of C-C beta-chemokines in human peripheral blood gammadelta T cells by isopentenyl pyrophosphate and regulation by cytokines. Blood 2000; 95: 39-47.
44. Lanca T, Costa MF, Goncalves-Sousa N, et al., Protective role of the inflammatory CCR2/CCL2 chemokine pathway through recruitment of type 1 cytotoxic gammadelta T lymphocytes to tumor beds. J Immunol 2013; 190: 6673-80.
45. Zocchi MR, Ferrarini M, Rugarli C., Selective lysis of the autologous tumor by delta TCS1+ gamma/delta+ tumor-infiltrating lymphocytes from human lung carcinomas. Eur J Immunol 1990; 20: 2685-9.
46. Wang MH, Chen YQ, Gercken J, et al., Specific activation of human peripheral blood gamma/delta + lymphocytes by sonicated antigens of mycobacterium tuberculosis: role in vitro in killing human bladder carcinoma cell lines. Scand J Immunol 1993; 38: 239-46.
47. Viey E, Fromont G, Escudier B, et al., Phosphostim-activated gamma delta T cells kill autologous metastatic renal cell carcinoma. J Immunol 2005; 174: 1338-47.
48. Choudhary A, Davodeau F, Moreau A, et al., Selective lysis of autologous tumor cells by recurrent gamma delta tumor-infiltrating lymphocytes from renal carcinoma. J Immunol 1995; 154: 3932-40.
49. Zheng BJ, Ng SP, Chua DT, et al., Peripheral gamma delta T-cell deficit in nasopharyngeal carcinoma. Int J Cancer 2002; 99: 213-7.
50. Fisch P, Malkovsky M, Kovats S, et al., Recognition by human V gamma 9/V delta 2 T cells of a GroEL homolog on Daudi Burkitt's lymphoma cells. Science 1990; 250: 1269-73.
51. Fisch P, Meuer E, Pende D, et al., Control of B cell lymphoma recognition via natural killer inhibitory receptors implies a role for human Vgamma9/Vdelta2 T cells in tumor immunity. Eur J Immunol 1997; 27: 3368-79.
52. Van Acker HH, Anguille S, Van Tendeloo VF, et al., Empowering gamma delta T cells with antitumor immunity by dendritic cell-based immunotherapy. Oncoimmunology 2015; 4: e1021538
53. Shachaf CM, Perez OD, Youssef S, et al., Inhibition of HMGcoA reductase by atorvastatin prevents and reverses MYC-induced lymphomagenesis. Blood 2007; 110: 2674-84.
54. Goldstein JL, Brown MS., Regulation of the mevalonate pathway. Nature 1990; 343: 425-30.
55. Gober HJ, Kistowska M, Angman L, et al., Human T cell receptor gammadelta cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med 2003; 197: 163-8.
56. Mattarollo SR, Kenna T, Nieda M, et al., Chemotherapy and zoledronate sensitize solid tumour cells to Vgamma9Vdelta2 T cell cytotoxicity. Cancer Immunol Immunother 2007; 56: 1285-97.
57. Dhar S, Chiplunkar SV., Lysis of aminobisphosphonate-sensitized MCF-7 breast tumor cells by Vgamma9Vdelta2 T cells. Cancer Immun 2010; 10: 10
58. Bouet-Toussaint F, Cabillic F, Toutirais O, et al., Vgamma9Vdelta2 T cell-mediated recognition of human solid tumors. Potential for immunotherapy of hepatocellular and colorectal carcinomas. Cancer Immunol Immunother 2008; 57: 531-9.
59. Lanca T, Correia DV, Moita CF, et al., The MHC class Ib protein ULBP1 is a nonredundant determinant of leukemia/lymphoma susceptibility to gammadelta T-cell cytotoxicity. Blood 2010; 115: 2407-11.
60. Deniger DC, Maiti SN, Mi T, et al., Activating and propagating polyclonal gamma delta T cells with broad specificity for malignancies. Clin Cancer Res 2014; 20: 5708-19.
61. Kong Y, Cao W, Xi X, et al., The NKG2D ligand ULBP4 binds to TCRgamma9/delta2 and induces cytotoxicity to tumor cells through both TCRgammadelta and NKG2D. Blood 2009; 114: 310-7.
62. Toutirais O, Cabillic F, Le Friec G, et al., DNAX accessory molecule-1 (CD226) promotes human hepatocellular carcinoma cell lysis by Vgamma9Vdelta2 T cells. Eur J Immunol 2009; 39: 1361-8.
63. Lafont V, Liautard J, Liautard JP, et al., Production of TNF-alpha by human V gamma 9V delta 2 T cells via engagement of Fc gamma RIIIA, the low affinity type 3 receptor for the Fc portion of IgG, expressed upon TCR activation by nonpeptidic antigen. J Immunol 2001; 166: 7190-9.
64. Gertner-Dardenne J, Bonnafous C, Bezombes C, et al., Bromohydrin pyrophosphate enhances antibody-dependent cell-mediated cytotoxicity induced by therapeutic antibodies. Blood 2009; 113: 4875-84.
65. Tokuyama H, Hagi T, Mattarollo SR, et al., V gamma 9 V delta 2 T cell cytotoxicity against tumor cells is enhanced by monoclonal antibody drugs-rituximab and trastuzumab. Int J Cancer 2008; 122: 2526-34.
66. Aggarwal R, Lu J, Kanji S, et al., Human Vgamma2Vdelta2 T cells limit breast cancer growth by modulating cell survival-, apoptosis-related molecules and microenvironment in tumors. Int J Cancer 2013; 133: 2133-44.
67. He W, Hao J, Dong S, et al., Naturally activated V gamma 4 gamma delta T cells play a protective role in tumor immunity through expression of eomesodermin. J Immunol 2010; 185: 126-33.
68. Paul S, Singh AK, Shilpi Lal G., Phenotypic and functional plasticity of gamma-delta (γδ) T cells in inflammation and tolerance. Int Rev Immunol 2013; 33: 537-58.
69. Gao Y, Yang W, Pan M, et al., Gamma delta T cells provide an early source of interferon gamma in tumor immunity. J Exp Med 2003; 198: 433-42.
70. Riond J, Rodriguez S, Nicolau ML, et al., In vivo major histocompatibility complex class I (MHCI) expression on MHCI low tumor cells is regulated by gammadelta T and NK cells during the early steps of tumor growth. Cancer Immun 2009; 9: 10
71. Mattarollo SR, Loi S, Duret H, et al., Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res 2011; 71: 4809-20.
72. Ma Y, Aymeric L, Locher C, et al., Contribution of IL-17-producing gamma delta T cells to the efficacy of anticancer chemotherapy. J Exp Med 2011; 208: 491-503.
73. Takeuchi A, Dejima T, Yamada H, et al., IL-17 production by gammadelta T cells is important for the antitumor effect of mycobacterium bovis bacillus calmette-guerin treatment against bladder cancer. Eur J Immunol 2011; 41: 246-51.
74. von Lilienfeld-Toal M, Sievers E, Bodemuller V, et al., Coculture with dendritic cells promotes proliferation but not cytotoxic activity of gamma/delta T cells. Immunol Lett 2005; 99: 103-8.
75. Conti L, Casetti R, Cardone M, et al., Reciprocal activating interaction between dendritic cells and pamidronate-stimulated gammadelta T cells: role of CD86 and inflammatory cytokines. J Immunol 2005; 174: 252-60.
76. Devilder MC, Maillet S, Bouyge-Moreau I, et al., Potentiation of antigen-stimulated V gamma 9V delta 2 T cell cytokine production by immature dendritic cells (DC) and reciprocal effect on DC maturation. J Immunol 2006; 176: 1386-93.
77. Maniar A, Zhang X, Lin W, et al., Human gammadelta T lymphocytes induce robust NK cell-mediated antitumor cytotoxicity through CD137 engagement. Blood 2010; 116: 1726-33.
78. Lal G, Bromberg JS., Epigenetic mechanisms of regulation of Foxp3 expression. Blood 2009; 114: 3727-35.
79. Lal G, Zhang N, van der Touw W, et al., Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J Immunol 2009; 182: 259-73.
80. Kang N, Tang L, Li X, et al., Identification and characterization of Foxp3(+) gammadelta T cells in mouse and human. Immunol Lett 2009; 125: 105-13.
81. Casetti R, Agrati C, Wallace M, et al., Cutting edge: TGF-beta1 and IL-15 Induce FOXP3+ gammadelta regulatory T cells in the presence of antigen stimulation. J Immunol 2009; 183: 3574-7.
82. Li X, Kang N, Zhang X, et al., Generation of human regulatory gammadelta T cells by TCRgammadelta stimulation in the presence of TGF-beta and their involvement in the pathogenesis of systemic lupus erythematosus. J Immunol 2011; 186: 6693-700.
83. Peters C, Oberg HH, Kabelitz D, et al., Phenotype and regulation of immunosuppressive Vdelta2-expressing gammadelta T cells. Cell Mol Life Sci 2014; 71: 1943-60.
84. Tran DQ, Ramsey H, Shevach EM., Induction of FOXP3 expression in naive human CD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype. Blood 2007; 110: 2983-90.
85. Thornton AM, Korty PE, Tran DQ, et al., Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J Immunol 2010; 184: 3433-41.
86. Kabelitz D, Peters C, Wesch D, et al., Regulatory functions of gammadelta T cells. Int Immunopharmacol 2013; 16: 382-7.
87. Seo N, Tokura Y, Furukawa F, et al., Down-regulation of tumoricidal NK and NK T cell activities by MHC Kb molecules expressed on Th2-type gammadelta T and alphabeta T cells coinfiltrating in early B16 melanoma lesions. J Immunol 1998; 161: 4138-45.
88. Seo N, Tokura Y, Takigawa M, et al., Depletion of IL-10- and TGF-beta-producing regulatory gamma delta T cells by administering a daunomycin-conjugated specific monoclonal antibody in early tumor lesions augments the activity of CTLs and NK cells. J Immunol 1999; 163: 242-9.
89. Hao J, Dong S, Xia S, et al., Regulatory role of Vgamma1 gammadelta T cells in tumor immunity through IL-4 production. J Immunol 2011; 187: 4979-86.
90. Peng G, Wang HY, Peng W, et al., Tumor-infiltrating gammadelta T cells suppress T and dendritic cell function via mechanisms controlled by a unique toll-like receptor signaling pathway. Immunity 2007; 27: 334-48.
91. Ma S, Cheng Q, Cai Y, et al., IL-17A Produced by gammadelta T cells promotes tumor growth in hepatocellular carcinoma. Cancer Res 2014; 74: 1969-82.
92. Wu P, Wu D, Ni C, et al., gammadeltaT17 cells promote the accumulation and expansion of myeloid-derived suppressor cells in human colorectal cancer. Immunity 2014; 40: 785-800.
93. Carmi Y, Rinott G, Dotan S, et al., Microenvironment-derived IL-1 and IL-17 interact in the control of lung metastasis. J Immunol 2011; 186: 3462-71.
94. Wakita D, Sumida K, Iwakura Y, et al., Tumor-infiltrating IL-17-producing gammadelta T cells support the progression of tumor by promoting angiogenesis. Eur J Immunol 2010; 40: 1927-37.
95. Coffelt SB, Kersten K, Doornebal CW, et al., IL-17-producing gammadelta T cells and neutrophils conspire to promote breast cancer metastasis. Nature 2015; 522: 345-8.
96. Murugaiyan G, Saha B., Protumor vs antitumor functions of IL-17. J Immunol 2009; 183: 4169-75.
97. Zitvogel L, Apetoh L, Ghiringhelli F, et al., Immunological aspects of cancer chemotherapy. Nat Rev Immunol 2008; 8: 59-73.
98. Green DR, Ferguson T, Zitvogel L, et al., Immunogenic and tolerogenic cell death. Nat Rev Immunol 2009; 9: 353-63.
99. Yi Y, He HW, Wang JX, et al., The functional impairment of HCC-infiltrating gammadelta T cells, partially mediated by regulatory T cells in a TGFbeta- and IL-10-dependent manner. J Hepatol 2013; 58: 977-83.
100. Rey J, Veuillen C, Vey N, et al., Natural killer and gammadelta T cells in haematological malignancies: enhancing the immune effectors. Trends Mol Med 2009; 15: 275-84.
101. Gaafar A, Aljurf MD, Al-Sulaiman A, et al., Defective gammadelta T-cell function and granzyme B gene polymorphism in a cohort of newly diagnosed breast cancer patients. Exp Hematol 2009; 37: 838-48.
102. Meraviglia S, Eberl M, Vermijlen D, et al., In vivo manipulation of Vgamma9Vdelta2 T cells with zoledronate and low-dose interleukin-2 for immunotherapy of advanced breast cancer patients. Clin Exp Immunol 2010; 161: 290-7.
103. Naoe M, Ogawa Y, Takeshita K, et al., Zoledronate stimulates gamma delta T cells in prostate cancer patients. Oncol Res 2010; 18: 493-501.
104. Godder KT, Henslee-Downey PJ, Mehta J, et al., Long term disease-free survival in acute leukemia patients recovering with increased gammadelta T cells after partially mismatched related donor bone marrow transplantation. Bone Marrow Transplant 2007; 39: 751-7.
105. Saito A, Narita M, Yokoyama A, et al., Enhancement of anti-tumor cytotoxicity of expanded gammadelta T Cells by stimulation with monocyte-derived dendritic cells. J Clin Exp Hematop 2007; 47: 61-72.
106. Gomes AQ, Martins DS, Silva-Santos B., Targeting gammadelta T lymphocytes for cancer immunotherapy: from novel mechanistic insight to clinical application. Cancer Res 2010; 70: 10024-7.
107. Wilhelm M, Kunzmann V, Eckstein S, et al., Gammadelta T cells for immune therapy of patients with lymphoid malignancies. Blood 2003; 102: 200-6.
108. Lang JM, Kaikobad MR, Wallace M, et al., Pilot trial of interleukin-2 and zoledronic acid to augment gammadelta T cells as treatment for patients with refractory renal cell carcinoma. Cancer Immunol Immunother 2011; 60: 1447-60.
109. Dieli F, Vermijlen D, Fulfaro F, et al., Targeting human {gamma}delta} T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res 2007; 67: 7450-7.
110. Bennouna J, Levy V, Sicard H, et al., Phase I study of bromohydrin pyrophosphate (BrHPP, IPH 1101), a Vgamma9Vdelta2 T lymphocyte agonist in patients with solid tumors. Cancer Immunol Immunother 2010; 59: 1521-30.
111. Nakajima J, Murakawa T, Fukami T, et al., A phase I study of adoptive immunotherapy for recurrent non-small-cell lung cancer patients with autologous gammadelta T cells. Eur J Cardiothorac Surg 2010; 37: 1191-7.
112. Sakamoto M, Nakajima J, Murakawa T, et al., Adoptive immunotherapy for advanced non-small cell lung cancer using zoledronate-expanded gammadeltaTcells: a phase I clinical study. J Immunother 2011; 34: 202-11.
113. Abe Y, Muto M, Nieda M, et al., Clinical and immunological evaluation of zoledronate-activated Vgamma9gammadelta T-cell-based immunotherapy for patients with multiple myeloma. Exp Hematol 2009; 37: 956-68.
114. Qi J, Zhang J, Zhang S, et al., Immobilized MICA could expand human Vdelta1 gammadelta T cells in vitro that displayed major histocompatibility complex class I chain-related A-dependent cytotoxicity to human epithelial carcinomas. Scand J Immunol 2003; 58: 211-20.
115. Lamb LS, Jr., Bowersock J, Dasgupta A, et al., Engineered drug resistant gammadelta T cells kill glioblastoma cell lines during a chemotherapy challenge: a strategy for combining chemo- and immunotherapy. PLoS One 2013; 8: e51805
116. Hiasa A, Nishikawa H, Hirayama M, et al., Rapid alphabeta TCR-mediated responses in gammadelta T cells transduced with cancer-specific TCR genes. Gene Ther 2009; 16: 620-8.
117. van der Veken LT, Hagedoorn RS, van Loenen MM, et al., Alphabeta T-cell receptor engineered gammadelta T cells mediate effective antileukemic reactivity. Cancer Res 2006; 66: 3331-7.
118. Rischer M, Pscherer S, Duwe S, et al., Human gammadelta T cells as mediators of chimaeric-receptor redirected anti-tumour immunity. Br J Haematol 2004; 126: 583-92.
119. Wang H, Fang Z, Morita CT., Vgamma2Vdelta2 T cell receptor recognition of prenyl pyrophosphates is dependent on all CDRs. J Immunol 2010; 184: 6209-22.
120. Moser B., Tumor-killing gammadelta-TCRs take center stage. Blood 2012; 120: 5093-4.
121. Grunder C, van Dorp S, Hol S, et al., Gamma9 and delta2CDR3 domains regulate functional avidity of T cells harboring gamma9delta2TCRs. Blood 2012; 120: 5153-62.
122. Ke Y, Kapp LM, Kapp JA., Inhibition of tumor rejection by gammadelta T cells and IL-10. Cell Immunol 2003; 221: 107-14.