Potential of human γδ T cells for immunotherapy of osteosarcoma

Molecular Biology Reports

Volumn 40, Issue 1, 2013, Pages 427-437

  Li, Zhaoxu ^a  

^a GUILIN MEDICAL UNIVERSITY   (China)

Author keywords

Adoptive; Antigen; Gamma delta; Immunotherapy; Neoplasms; Osteosarcoma; Receptors; T cell

Indexed keywords

1 DEOXY DEXTRO XYLULOSE 5 PHOSPHATE; ANTIGEN; APOLIPOPROTEIN A1; BISPHOSPHONIC ACID DERIVATIVE; CYTOKINE; GAMMA INTERFERON; GRANZYME; HLA ANTIGEN CLASS 1; INTERCELLULAR ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 2; INTERLEUKIN 5; LIPOSOMAL MURAMYL TRIPEPTIDE PHOSPHATIDYLETHANOLAMINE; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 3; MAJOR HISTOCOMPATIBILITY ANTIGEN; MEVALONIC ACID; MURAMYL DIPEPTIDE DERIVATIVE; NATURAL KILLER CELL RECEPTOR NKG2D; NONPEPTIDE PRENYL PYROPHOSPHATE; PERFORIN; PROTEIN KINASE C THETA; PROTEIN MSH2; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RECOMBINANT INTERLEUKIN 2; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; ZOLEDRONIC ACID;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ADVERSE OUTCOME; ALPHA BETA T LYMPHOCYTE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ANTINEOPLASTIC ACTIVITY; B CELL LYMPHOMA; BREAST CANCER; CALCIUM SIGNALING; CANCER COMBINATION CHEMOTHERAPY; CANCER GRADING; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER PREVENTION; CANCER RECURRENCE; CANCER STEM CELL; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CELL CONTACT; CELL EXPANSION; CELL KILLING; CELL PROLIFERATION; CELL SURVIVAL; CELL THERAPY; CELLULAR DISTRIBUTION; CHRONIC MYELOID LEUKEMIA; CLINICAL TRIAL (TOPIC); CYTOLYSIS; CYTOTOXICITY; DISEASE PREDISPOSITION; DRUG EFFICACY; DRUG PULSE THERAPY; ENZYME RELEASE; EX VIVO STUDY; FLU LIKE SYNDROME; GAMMA DELTA T LYMPHOCYTE; GASTROINTESTINAL DISEASE; HUMAN; HYPOTENSION; IMMUNOSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; KIDNEY CARCINOMA; LEUKEMIA; LOW DRUG DOSE; LUNG CARCINOMA; LUNG METASTASIS; LUNG NON SMALL CELL CANCER; LYMPHOCYTE FUNCTION; LYMPHOMA; METASTASIS POTENTIAL; MULTIPLE CYCLE TREATMENT; MYELOMA; NATURAL KILLER CELL; NEUROBLASTOMA; NONHUMAN; OSTEOSARCOMA; OVARY CANCER; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; PROTEIN FUNCTION; RECURRENT CANCER; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TACHYCARDIA; TREATMENT DURATION; TREATMENT OUTCOME; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR VOLUME; TUMOR XENOGRAFT; UPREGULATION;

ANIMALS; BONE NEOPLASMS; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MICE; MICE, SCID; OSTEOSARCOMA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTES;

EID: 84871266778     PISSN: 03014851     EISSN: 15734978     Source Type: Journal    
DOI: 10.1007/s11033-012-2077-y     Document Type: Review

References (114)

1. Ritter J, Bielack SS (2010) Osteosarcoma. Ann Oncol 21(Suppl 7):vii320-vii325
2. Bidwell J, McCabe R, Rougraff B, Feister H, Fey E, Onyia J, Holden J, Hock J (1997) Tissue matrix protein expression in human osteoblasts, osteosarcoma tumors, and osteosarcoma cell lines. Mol Biol Rep 24(4):271-282
3. Eyre R, Feltbower RG, James PW, Blakey K, Mubwandarikwa E, Forman D, McKinney PA, Pearce MS, McNally RJ (2010) The epidemiology of bone cancer in 0-39year olds in northern England, 1981-2002. BMC Cancer 10:357. doi: 10.1186/1471-2407-10-357
4. Messerschmitt PJ, Garcia RM, Abdul-Karim FW, Greenfield EM, Getty PJ (2009) Osteosarcoma. J Am Acad Orthop Surg 17(8):515-527
5. Meyers PA, Healey JH, Chou AJ, Wexler LH, Merola PR, Morris CD, Laquaglia MP, Kellick MG, Abramson SJ, Gorlick R (2011) Addition of pamidronate to chemotherapy for the treatment of osteosarcoma. Cancer 117(8):1736-1744. doi: 10.1002/cncr.25744
6. Zhao H, Guo W, Peng C, Ji T, Lu X (2010) Arsenic trioxide inhibits the growth of adriamycin resistant osteosarcoma cells through inducing apoptosis. Mol Biol Rep 37(5):2509-2515. doi: 10.1007/s11033-009-9765-2
7. Bielack SS, Carrle D (2008) State-of-the-art approach in selective curable tumors: bone sarcoma. Ann Oncol 19(Suppl 7):vii155-vii160
8. Fagioli F, Biasin E, Mereuta OM, Muraro M, Luksch R, Ferrari S, Aglietta M, Madon E (2008) Poor prognosis osteosarcoma: new therapeutic approach. Bone Marrow Transplant 41(Suppl 2):S131-S134
9. Li Y, Flores R, Yu A, Okcu MF, Murray J, Chintagumpala M, Hicks J, Lau CC, Man TK (2011) Elevated expression of CXC chemokines in pediatric osteosarcoma patients. Cancer 117(1):207-217. doi: 10.1002/cncr.25563
10. Picci P, Mercuri M, Ferrari S, Alberghini M, Briccoli A, Ferrari C, Pignotti E, Bacci G (2010) Survival in high-grade osteosarcoma: improvement over 21years at a single institution. Ann Oncol 21(6):1366-1373
11. Andreou D, Bielack SS, Carrle D, Kevric M, Kotz R, Winkelmann W, Jundt G, Werner M, Fehlberg S, Kager L, Kuhne T, Lang S, Dominkus M, Exner GU, Hardes J, Hillmann A, Ewerbeck V, Heise U, Reichardt P, Tunn PU (2011) The influence of tumor- and treatment-related factors on the development of local recurrence in osteosarcoma after adequate surgery. An analysis of 1355 patients treated on neoadjuvant cooperative osteosarcoma study group protocols. Ann Oncol 22(5):1228-1235
12. Moore C, Eslin D, Levy A, Roberson J, Giusti V, Sutphin R (2010) Prognostic significance of early lymphocyte recovery in pediatric osteosarcoma. Pediatr Blood Cancer 55(6):1096-1102. doi: 10.1002/pbc.22673
13. Merchant MS, Melchionda F, Sinha M, Khanna C, Helman L, Mackall CL (2007) Immune reconstitution prevents metastatic recurrence of murine osteosarcoma. Cancer Immunol Immunother 56(7):1037-1046. doi: 10.1007/s00262-006-0257-0
14. Loeb DM (2009) Is there a role for immunotherapy in osteosarcoma? Cancer Treat Res 152:447-457. doi: 10.1007/978-1-4419-0284-9-25
15. Gomes AQ, Martins DS, Silva-Santos B (2010) Targeting gammadelta T lymphocytes for cancer immunotherapy: from novel mechanistic insight to clinical application. Cancer Res 70(24):10024-10027
16. Bonneville M, Scotet E (2006) Human Vgamma9Vdelta2 T cells: promising new leads for immunotherapy of infections and tumors. Curr Opin Immunol 18(5):539-546
17. Marina N, Gorlick R (2009) Immune approaches to treating osteosarcoma. Cancer Biol Ther 8(10):981-983
18. Mori K, Redini F, Gouin F, Cherrier B, Heymann D (2006) Osteosarcoma: current status of immunotherapy and future trends (Review). Oncol Rep 15(3):693-700
19. Gorlick R, Anderson P, Andrulis I, Arndt C, Beardsley GP, Bernstein M, Bridge J, Cheung NK, Dome JS, Ebb D, Gardner T, Gebhardt M, Grier H, Hansen M, Healey J, Helman L, Hock J, Houghton J, Houghton P, Huvos A, Khanna C, Kieran M, Kleinerman E, Ladanyi M, Lau C, Malkin D, Marina N, Meltzer P, Meyers P, Schofield D, Schwartz C, Smith MA, Toretsky J, Tsokos M, Wexler L, Wigginton J, Withrow S, Schoenfeldt M, Anderson B (2003) Biology of childhood osteogenic sarcoma and potential targets for therapeutic development: meeting summary. Clin Cancer Res 9(15):5442-5453
20. Mori K, Ando K, Heymann D (2008) Liposomal muramyl tripeptide phosphatidyl ethanolamine: a safe and effective agent against osteosarcoma pulmonary metastases. Expert Rev Anticancer Ther 8(2):151-159. doi: 10.1586/14737140.8.2.151
21. Ando K, Mori K, Corradini N, Redini F, Heymann D (2011) Mifamurtide for the treatment of nonmetastatic osteosarcoma. Expert Opin Pharmacother 12(2):285-292. doi: 10.1517/14656566.2011.543129
22. Kleinerman ES, Gano JB, Johnston DA, Benjamin RS, Jaffe N (1995) Efficacy of liposomal muramyl tripeptide (CGP 19835A) in the treatment of relapsed osteosarcoma. Am J Clin Oncol 18(2):93-99
23. Rosenberg SA, Dudley ME (2009) Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr Opin Immunol 21(2):233-240
24. Knutson KL, Wagner W, Disis ML (2006) Adoptive T cell therapy of solid cancers. Cancer Immunol Immunother 55(1):96-103. doi: 10.1007/s00262-005-0706-1
25. Martinet L, Poupot R, Fournie JJ (2009) Pitfalls on the roadmap to gammadelta T cell-based cancer immunotherapies. Immunol Lett 124(1):1-8
26. Cho D, Shook DR, Shimasaki N, Chang YH, Fujisaki H, Campana D (2010) Cytotoxicity of activated natural killer cells against pediatric solid tumors. Clin Cancer Res 16(15):3901-3909. doi: 10.1158/1078-0432.CCR-10-0735
27. Pahl JH, Ruslan SE, Buddingh EP, Santos SJ, Szuhai K, Serra M, Gelderblom H, Hogendoorn PC, Egeler RM, Schilham MW, Lankester AC (2012) Anti-EGFR antibody cetuximab enhances the cytolytic activity of natural killer cells toward osteosarcoma. Clin Cancer Res 18(2):432-441. doi: 10.1158/1078-0432.CCR- 11-2277
28. Buddingh EP, Schilham MW, Ruslan SE, Berghuis D, Szuhai K, Suurmond J, Taminiau AH, Gelderblom H, Egeler RM, Serra M, Hogendoorn PC, Lankester AC (2011) Chemotherapy-resistant osteosarcoma is highly susceptible to IL-15-activated allogeneic and autologous NK cells. Cancer Immunol Immunother 60(4):575-586. doi: 10.1007/s00262-010-0965-3
29. Muraro M, Mereuta OM, Saglio F, Carraro F, Cravero C, Fagioli F (2011) Tumor-associated-antigens or osteosarcoma cell line lysates: two efficient methods for in vitro generation of CTLs with special regard to MHC-I restriction. Cell Immunol 266(2):123-129. doi: 10.1016/j.cellimm.2010.09.007
30. Rainusso N, Brawley VS, Ghazi A, Hicks MJ, Gottschalk S, Rosen JM, Ahmed N (2012) Immunotherapy targeting HER2 with genetically modified T cells eliminates tumor-initiating cells in osteosarcoma. Cancer Gene Ther 19(3):212-217
31. Todaro M, D'Asaro M, Caccamo N, Iovino F, Francipane MG, Meraviglia S, Orlando V, La Mendola C, Gulotta G, Salerno A, Dieli F, Stassi G (2009) Efficient killing of human colon cancer stem cells by gammadelta T lymphocytes. J Immunol 182(11):7287-7296
32. Rivoltini L, Arienti F, Orazi A, Cefalo G, Gasparini M, Gambacorti-Passerini C, Fossati-Bellani F, Parmiani G (1992) Phenotypic and functional analysis of lymphocytes infiltrating paediatric tumours, with a characterization of the tumour phenotype. Cancer Immunol Immunother 34(4):241-251
33. Theoleyre S, Mori K, Cherrier B, Passuti N, Gouin F, Redini F, Heymann D (2005) Phenotypic and functional analysis of lymphocytes infiltrating osteolytic tumors: use as a possible therapeutic approach of osteosarcoma. BMC Cancer 5:123. doi: 10.1186/1471-2407-5-123
34. Yabe H, Tsukahara T, Kawaguchi S, Wada T, Torigoe T, Sato N, Terai C, Aoki M, Hirose S, Morioka H (2011) Prognostic significance of HLA class I expression in Ewing's sarcoma family of tumors. J Surg Oncol 103(5):380-385. doi: 10.1002/jso.21829
35. Berghuis D, Santos SJ, Baelde HJ, Taminiau AH, Egeler RM, Schilham MW, Hogendoorn PC, Lankester AC (2011) Pro-inflammatory chemokine-chemokine receptor interactions within the Ewing sarcoma microenvironment determine CD8(+) T-lymphocyte infiltration and affect tumour progression. J Pathol 223(3):347-357. doi: 10.1002/path.2819
36. Tsukahara T, Kawaguchi S, Torigoe T, Asanuma H, Nakazawa E, Shimozawa K, Nabeta Y, Kimura S, Kaya M, Nagoya S, Wada T, Yamashita T, Sato N (2006) Prognostic significance of HLA class I expression in osteosarcoma defined by anti-pan HLA class I monoclonal antibody, EMR8-5. Cancer Sci 97(12):1374-1380
37. Chodaczek G, Papanna V, Zal MA, Zal T (2012) Body-barrier surveillance by epidermal gammadelta TCRs. Nat Immunol 13(3):272-282
38. Lamb LS Jr, Lopez RD (2005) Gammadelta T cells: a new frontier for immunotherapy? Biol Blood Marrow Transplant 11(3):161-168. doi: 10.1016/j.bbmt.2004.11.015
39. Bonneville M, O'Brien RL, Born WK (2010) Gammadelta T cell effector functions: a blend of innate programming and acquired plasticity. Nat Rev Immunol 10(7):467-478
40. Casetti R, Martino A (2008) The plasticity of gamma delta T cells: innate immunity, antigen presentation and new immunotherapy. Cell Mol Immunol 5(3):161-170. doi: 10.1038/cmi.2008.20
41. Kabelitz D (2011) Gammadelta T-cells: cross-talk between innate and adaptive immunity. Cell Mol Life Sci 68(14):2331-2333. doi: 10.1007/s00018-011- 0696-4
42. Champagne E (2011) Gammadelta T cell receptor ligands and modes of antigen recognition. Arch Immunol Ther Exp (Warsz) 59(2):117-137. doi: 10.1007/s00005-011-0118-1
43. Kato Y, Tanaka Y, Miyagawa F, Yamashita S, Minato N (2001) Targeting of tumor cells for human gammadelta T cells by nonpeptide antigens. J Immunol 167(9):5092-5098
44. Dai Y, Chen H, Mo C, Cui L, He W (2012) Ectopically-expressed human tumor biomarker MutS homologue 2 is a novel endogenous ligand that is recognized by human gammadelta T cells to induce innate anti-tumor/virus immunity. J Biol Chem. doi: 10.1074/jbc.M111.327650
45. Scotet E, Martinez LO, Grant E, Barbaras R, Jeno P, Guiraud M, Monsarrat B, Saulquin X, Maillet S, Esteve JP, Lopez F, Perret B, Collet X, Bonneville M, Champagne E (2005) Tumor recognition following Vgamma9Vdelta2 T cell receptor interactions with a surface F1-ATPase-related structure and apolipoprotein A-I. Immunity 22(1):71-80
46. Morita CT, Beckman EM, Bukowski JF, Tanaka Y, Band H, Bloom BR, Golan DE, Brenner MB (1995) Direct presentation of nonpeptide prenyl pyrophosphate antigens to human gamma delta T cells. Immunity 3(4):495-507. doi: 10.1016/1074-7613(95)90178-7
47. Wang H, Fang Z, Morita CT (2010) Vgamma2Vdelta2 T Cell Receptor recognition of prenyl pyrophosphates is dependent on all CDRs. J Immunol 184(11):6209-6222
48. Nedellec S, Sabourin C, Bonneville M, Scotet E (2010) 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 185(1):55-63
49. DeBarros A, Chaves-Ferreira M, d'Orey F, Ribot JC, Silva-Santos B (2011) CD70-CD27 interactions provide survival and proliferative signals that regulate T cell receptor-driven activation of human gammadelta peripheral blood lymphocytes. Eur J Immunol 41(1):195-201. doi: 10.1002/eji.201040905
50. Ferrarini M, Delfanti F, Gianolini M, Rizzi C, Alfano M, Lazzarin A, Biswas P (2008) NF-kappa B modulates sensitivity to apoptosis, proinflammatory and migratory potential in short- versus long-term cultured human gamma delta lymphocytes. J Immunol 181(9):5857-5864
51. Witherden DA, Verdino P, Rieder SE, Garijo O, Mills RE, Teyton L, Fischer WH, Wilson IA, Havran WL (2010) The junctional adhesion molecule JAML is a costimulatory receptor for epithelial gammadelta T cell activation. Science 329(5996):1205-1210
52. Liu Z, Guo B, Lopez RD (2009) Expression of intercellular adhesion molecule (ICAM)-1 or ICAM-2 is critical in determining sensitivity of pancreatic cancer cells to cytolysis by human gammadelta-T cells: implications in the design of gammadelta-T-cell-based immunotherapies for pancreatic cancer. J Gastroenterol Hepatol 24(5):900-911
53. Ribot JC, debarros A, Silva-Santos B (2011) Searching for "signal 2": costimulation requirements of gammadelta T cells. Cell Mol Life Sci 68(14):2345-2355. doi: 10.1007/s00018-011-0698-2
54. Alexander AA, Maniar A, Cummings JS, Hebbeler AM, Schulze DH, Gastman BR, Pauza CD, Strome SE, Chapoval AI (2008) Isopentenyl pyrophosphate-activated CD56+ {gamma}{delta} T lymphocytes display potent antitumor activity toward human squamous cell carcinoma. Clin Cancer Res 14(13):4232-4240
55. Braza MS, Klein B, Fiol G, Rossi JF (2011) Gammadelta T-cell killing of primary follicular lymphoma cells is dramatically potentiated by GA101, a type II glycoengineered anti-CD20 monoclonal antibody. Haematologica 96(3):400-407
56. Chattopadhyay PK, Betts MR, Price DA, Gostick E, Horton H, Roederer M, De Rosa SC (2009) The cytolytic enzymes granyzme A, granzyme B, and perforin: expression patterns, cell distribution, and their relationship to cell maturity and bright CD57 expression. J Leukoc Biol 85(1):88-97
57. Caldwell SA, Ryan MH, McDuffie E, Abrams SI (2003) The Fas/Fas ligand pathway is important for optimal tumor regression in a mouse model of CTL adoptive immunotherapy of experimental CMS4 lung metastases. J Immunol 171(5):2402-2412
58. Eberl M, Roberts GW, Meuter S, Williams JD, Topley N, Moser B (2009) A rapid crosstalk of human gammadelta T cells and monocytes drives the acute inflammation in bacterial infections. PLoS Pathog 5(2):e1000308. doi: 10.1371/journal.ppat.1000308
59. Schnurr M, Scholz C, Rothenfusser S, Galambos P, Dauer M, Robe J, Endres S, Eigler A (2002) Apoptotic pancreatic tumor cells are superior to cell lysates in promoting cross-priming of cytotoxic T cells and activate NK and gammadelta T cells. Cancer Res 62(8):2347-2352
60. Castella B, Riganti C, Fiore F, Pantaleoni F, Canepari ME, Peola S, Foglietta M, Palumbo A, Bosia A, Coscia M, Boccadoro M, Massaia M (2011) Immune modulation by zoledronic acid in human myeloma: an advantageous cross-talk between Vgamma9Vdelta2 T cells, alphabeta CD8+ T cells, regulatory T cells, and dendritic cells. J Immunol 187(4):1578-1590
61. Huber SA (2010) Gammadelta T lymphocytes kill T regulatory cells through CD1d. Immunology 131(2):202-209. doi: 10.1111/j.1365-2567.2010.03292.x
62. Capietto AH, Martinet L, Fournie JJ (2011) Stimulated gammadelta T cells increase the in vivo efficacy of trastuzumab in HER-2+ breast cancer. J Immunol 187(2):1031-1038
63. Brandes M, Willimann K, Moser B (2005) Professional antigen-presentation function by human gammadelta T Cells. Science 309(5732):264-268
64. Brandes M, Willimann K, Bioley G, Levy N, Eberl M, Luo M, Tampe R, Levy F, Romero P, Moser B (2009) Cross-presenting human gammadelta T cells induce robust CD8+ alphabeta T cell responses. Proc Natl Acad Sci USA 106(7):2307-2312
65. Maniar A, Zhang X, Lin W, Gastman BR, Pauza CD, Strome SE, Chapoval AI (2010) Human gammadelta T lymphocytes induce robust NK cell-mediated antitumor cytotoxicity through CD137 engagement. Blood 116(10):1726-1733. doi: 10.1182/blood-2009-07-234211
66. Fisch P, Malkovsky M, Braakman E, Sturm E, Bolhuis RL, Prieve A, Sosman JA, Lam VA, Sondel PM (1990) Gamma/delta T cell clones and natural killer cell clones mediate distinct patterns of non-major histocompatibility complex-restricted cytolysis. J Exp Med 171(5):1567-1579
67. Burjanadze M, Condomines M, Reme T, Quittet P, Latry P, Lugagne C, Romagne F, Morel Y, Rossi JF, Klein B, Lu ZY (2007) In vitro expansion of gamma delta T cells with anti-myeloma cell activity by Phosphostim and IL-2 in patients with multiple myeloma. Br J Haematol 139(2):206-216
68. Corvaisier M, Moreau-Aubry A, Diez E, Bennouna J, Mosnier JF, Scotet E, Bonneville M, Jotereau F (2005) V gamma 9V delta 2 T cell response to colon carcinoma cells. J Immunol 175(8):5481-5488
69. Liu Z, Guo BL, Gehrs BC, Nan L, Lopez RD (2005) Ex vivo expanded human Vgamma9Vdelta2+ gammadelta-T cells mediate innate antitumor activity against human prostate cancer cells in vitro. J Urol 173(5):1552-1556
70. Guo BL, Liu Z, Aldrich WA, Lopez RD (2005) Innate anti-breast cancer immunity of apoptosis-resistant human gammadelta-T cells. Breast Cancer Res Treat 93(2):169-175. doi: 10.1007/s10549-005-4792-8
71. Kang N, Zhou J, Zhang T, Wang L, Lu F, Cui Y, Cui L, He W (2009) Adoptive immunotherapy of lung cancer with immobilized anti-TCR gammadelta antibody-expanded human gammadelta T-cells in peripheral blood. Cancer Biol Ther 8(16):1540-1549
72. Bryant NL, Gillespie GY, Lopez RD, Markert JM, Cloud GA, Langford CP, Arnouk H, Su Y, Haines HL, Suarez-Cuervo C, Lamb LS Jr (2011) Preclinical evaluation of ex vivo expanded/activated gammadelta T cells for immunotherapy of glioblastoma multiforme. J Neurooncol 101(2):179-188. doi: 10.1007/s11060-010- 0245-2
73. Saitoh A, Narita M, Watanabe N, Tochiki N, Satoh N, Takizawa J, Furukawa T, Toba K, Aizawa Y, Shinada S, Takahashi M (2008) Anti-tumor cytotoxicity of gammadelta T cells expanded from peripheral blood cells of patients with myeloma and lymphoma. Med Oncol 25(2):137-147. doi: 10.1007/s12032-007-9004-4
74. D'Asaro M, La Mendola C, Di Liberto D, Orlando V, Todaro M, Spina M, Guggino G, Meraviglia S, Caccamo N, Messina A, Salerno A, Di Raimondo F, Vigneri P, Stassi G, Fournie JJ, Dieli F (2010) V gamma 9V delta 2 T lymphocytes efficiently recognize and kill zoledronate-sensitized, imatinib-sensitive, and imatinib-resistant chronic myelogenous leukemia cells. J Immunol 184(6):3260-3268
75. Bouet-Toussaint F, Cabillic F, Toutirais O, Le Gallo M, de la Pintiere CT, Daniel P, Genetet N, Meunier B, Dupont-Bierre E, Boudjema K, Catros V (2008) Vgamma9Vdelta2 T cell-mediated recognition of human solid tumors. Potential for immunotherapy of hepatocellular and colorectal carcinomas. Cancer Immunol Immunother 57(4):531-539. doi: 10.1007/s00262-007-0391-3
76. Murayama M, Tanaka Y, Yagi J, Uchiyama T, Ogawa K (2008) Antitumor activity and some immunological properties of gammadelta T-cells from patients with gastrointestinal carcinomas. Anticancer Res 28(5B):2921-2931
77. Siegers GM, Felizardo TC, Mathieson AM, Kosaka Y, Wang XH, Medin JA, Keating A (2011) Anti-leukemia activity of in vitro-expanded human gamma delta T cells in a xenogeneic Ph+ leukemia model. PLoS ONE 6(2):e16700. doi: 10.1371/journal.pone.0016700
78. Lozupone F, Pende D, Burgio VL, Castelli C, Spada M, Venditti M, Luciani F, Lugini L, Federici C, Ramoni C, Rivoltini L, Parmiani G, Belardelli F, Rivera P, Marcenaro S, Moretta L, Fais S (2004) Effect of human natural killer and gammadelta T cells on the growth of human autologous melanoma xenografts in SCID mice. Cancer Res 64(1):378-385
79. Benzaid I, Monkkonen H, Stresing V, Bonnelye E, Green J, Monkkonen J, Touraine JL, Clezardin P (2011) High phosphoantigen levels in bisphosphonate-treated human breast tumors promote Vgamma9Vdelta2 T-cell chemotaxis and cytotoxicity in vivo. Cancer Res 71(13):4562-4572. doi: 10.1158/0008-5472.CAN-10-3862
80. Otto M, Barfield RC, Martin WJ, Iyengar R, Leung W, Leimig T, Chaleff S, Gillies SD, Handgretinger R (2005) Combination immunotherapy with clinical-scale enriched human gammadelta T cells, hu14.18 antibody, and the immunocytokine Fc-IL7 in disseminated neuroblastoma. Clin Cancer Res 11(23):8486-8491
81. Lai D, Wang F, Chen Y, Wang C, Liu S, Lu B, Ge X, Guo L (2011) Human ovarian cancer stem-like cells can be efficiently killed by gammadelta T lymphocytes. Cancer Immunol Immunother. doi: 10.1007/s00262-011-1166-4
82. Li H, Wang Y, Zhou F (2010) Effect of ex vivo-expanded gammadelta-T cells combined with galectin-1 antibody on the growth of human cervical cancer xenografts in SCID mice. Clin Invest Med 33(5):E280-E289
83. Bennouna J, Bompas E, Neidhardt EM, Rolland F, Philip I, Galea C, Salot S, Saiagh S, Audrain M, Rimbert M, Lafaye-de SM, Tiollier J, Negrier S (2008) Phase-I study of Innacell gammadelta, an autologous cell-therapy product highly enriched in gamma9delta2 T lymphocytes, in combination with IL-2, in patients with metastatic renal cell carcinoma. Cancer Immunol Immunother 57(11):1599-1609. doi: 10.1007/s00262-008-0491-8
84. Kobayashi H, Tanaka Y, Yagi J, Osaka Y, Nakazawa H, Uchiyama T, Minato N, Toma H (2007) Safety profile and anti-tumor effects of adoptive immunotherapy using gamma-delta T cells against advanced renal cell carcinoma: a pilot study. Cancer Immunol Immunother 56(4):469-476. doi: 10.1007/s00262-006-0199-6
85. Kobayashi H, Tanaka Y, Shimmura H, Minato N, Tanabe K (2010) Complete remission of lung metastasis following adoptive immunotherapy using activated autologous gammadelta T-cells in a patient with renal cell carcinoma. Anticancer Res 30(2):575-579
86. Kobayashi H, Tanaka Y, Yagi J, Minato N, Tanabe K (2011) 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 60(8):1075-1084. doi: 10.1007/s00262-011-1021-7
87. Nakajima J, Murakawa T, Fukami T, Goto S, Kaneko T, Yoshida Y, Takamoto S, Kakimi K (2010) A phase I study of adoptive immunotherapy for recurrent non-small-cell lung cancer patients with autologous gammadelta T cells. Eur J Cardiothorac Surg 37(5):1191-1197
88. Sakamoto M, Nakajima J, Murakawa T, Fukami T, Yoshida Y, Murayama T, Takamoto S, Matsushita H, Kakimi K (2011) Adoptive immunotherapy for advanced non-small cell lung cancer using zoledronate-expanded gammadeltaTcells: a phase I clinical study. J Immunother 34(2):202-211. doi: 10.1097/CJI.0b013e318207ecfb
89. Nicol AJ, Tokuyama H, Mattarollo SR, Hagi T, Suzuki K, Yokokawa K, Nieda M (2011) Clinical evaluation of autologous gamma delta T cell-based immunotherapy for metastatic solid tumours. Br J Cancer 105(6):778-786
90. Meraviglia S, Eberl M, Vermijlen D, Todaro M, Buccheri S, Cicero G, La Mendola C, Guggino G, D'Asaro M, Orlando V, Scarpa F, Roberts A, Caccamo N, Stassi G, Dieli F, Hayday AC (2010) In vivo manipulation of Vgamma9Vdelta2 T cells with zoledronate and low-dose interleukin-2 for immunotherapy of advanced breast cancer patients. Clin Exp Immunol 161(2):290-297
91. Dieli F, Vermijlen D, Fulfaro F, Caccamo N, Meraviglia S, Cicero G, Roberts A, Buccheri S, D'Asaro M, Gebbia N, Salerno A, Eberl M, Hayday AC (2007) Targeting human {gamma}{delta} T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res 67(15):7450-7457
92. Lang JM, Kaikobad MR, Wallace M, Staab MJ, Horvath DL, Wilding G, Liu G, Eickhoff JC, McNeel DG, Malkovsky M (2011) 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 60(10):1447-1460. doi: 10.1007/s00262-011-1049-8
93. Bennouna J, Levy V, Sicard H, Senellart H, Audrain M, Hiret S, Rolland F, Bruzzoni-Giovanelli H, Rimbert M, Galea C, Tiollier J, Calvo F (2010) Phase I study of bromohydrin pyrophosphate (BrHPP, IPH 1101), a Vgamma9Vdelta2 T lymphocyte agonist in patients with solid tumors. Cancer Immunol Immunother 59(10):1521-1530. doi: 10.1007/s00262-010-0879-0
94. Muraro M, Mereuta OM, Carraro F, Madon E, Fagioli F (2007) Osteosarcoma cell line growth inhibition by zoledronate-stimulated effector cells. Cell Immunol 249(2):63-72
95. Li Z, Xu Q, Peng H, Cheng R, Sun Z, Ye Z (2011) IFN-gamma enhances HOS and U2OS cell lines susceptibility to gammadelta T cell-mediated killing through the Fas/Fas ligand pathway. Int Immunopharmacol 11(4):496-503
96. Jiang H, Xu Q, Yang C, Cao ZG, Li ZX, Ye ZM (2010) Gammadelta T cells stimulated by zoledronate kill osteosarcoma cells. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 26(12):1195-1197
97. Li Z, Peng H, Xu Q, Ye Z (2012) Sensitization of human osteosarcoma cells to Vgamma9Vdelta2 T-cell-mediated cytotoxicity by zoledronate. J Orthop Res 30(5):824-830. doi: 10.1002/jor.21579
98. Rosenberg SA, Restifo NP, Yang JC, Morgan RA, Dudley ME (2008) Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer 8(4):299-308
99. Gnant M, Dubsky P, Hadji P (2012) Bisphosphonates: prevention of bone metastases in breast cancer. Recent Results Cancer Res 192:65-91. doi: 10.1007/978-3-642-21892-7-3
100. Heymann D, Ory B, Blanchard F, Heymann MF, Coipeau P, Charrier C, Couillaud S, Thiery JP, Gouin F, Redini F (2005) Enhanced tumor regression and tissue repair when zoledronic acid is combined with ifosfamide in rat osteosarcoma. Bone 37(1):74-86
101. Ory B, Heymann MF, Kamijo A, Gouin F, Heymann D, Redini F (2005) Zoledronic acid suppresses lung metastases and prolongs overall survival of osteosarcoma-bearing mice. Cancer 104(11):2522-2529. doi: 10.1002/cncr.21530
102. Russell RG (2011) Bisphosphonates: the first 40years. Bone 49(1):2-19. doi: 10.1016/j.bone.2011.04.022
103. Gober HJ, Kistowska M, Angman L, Jeno P, Mori L, De Libero G (2003) Human T cell receptor gammadelta cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med 197(2):163-168
104. June CH, Blazar BR, Riley JL (2009) Engineering lymphocyte subsets: tools, trials and tribulations. Nat Rev Immunol 9(10):704-716
105. Ahmed N, Salsman VS, Yvon E, Louis CU, Perlaky L, Wels WS, Dishop MK, Kleinerman EE, Pule M, Rooney CM, Heslop HE, Gottschalk S (2009) Immunotherapy for osteosarcoma: genetic modification of T cells overcomes low levels of tumor antigen expression. Mol Ther 17(10):1779-1787
106. Schumacher TN (2002) T-cell-receptor gene therapy. Nat Rev Immunol 2(7):512-519. doi: 10.1038/nri841
107. Hiasa A, Hirayama M, Nishikawa H, Kitano S, Nukaya I, Yu SS, Mineno J, Kato I, Shiku H (2008) Long-term phenotypic, functional and genetic stability of cancer-specific T-cell receptor (TCR) alphabeta genes transduced to CD8+ T cells. Gene Ther 15(9):695-699
108. Coccoris M, Swart E, de Witte MA, van Heijst JW, Haanen JB, Schepers K, Schumacher TN (2008) Long-term functionality of TCR-transduced T cells in vivo. J Immunol 180(10):6536-6543
109. Uckert W, Schumacher TN (2009) TCR transgenes and transgene cassettes for TCR gene therapy: status in 2008. Cancer Immunol Immunother 58(5):809-822. doi: 10.1007/s00262-008-0649-4
110. van der Veken LT, Hagedoorn RS, van Loenen MM, Willemze R, Falkenburg JH, Heemskerk MH (2006) Alphabeta T-cell receptor engineered gammadelta T cells mediate effective antileukemic reactivity. Cancer Res 66(6):3331-3337
111. van der Veken LT, Coccoris M, Swart E, Falkenburg JH, Schumacher TN, Heemskerk MH (2009) Alpha beta T cell receptor transfer to gamma delta T cells generates functional effector cells without mixed TCR dimers in vivo. J Immunol 182(1):164-170
112. Hanagiri T, Shigematsu Y, Kuroda K, Baba T, Shiota H, Ichiki Y, Nagata Y, Yasuda M, So T, Takenoyama M, Tanaka F (2012) Anti-tumor activity of human gammadelta T cells transducted with CD8 and with T cell receptors of tumor-specific cytotoxic T lymphocytes. Cancer Sci. doi: 10.1111/j.1349-7006. 2012.02337.x
113. Hiasa A, Nishikawa H, Hirayama M, Kitano S, Okamoto S, Chono H, Yu SS, Mineno J, Tanaka Y, Minato N, Kato I, Shiku H (2009) Rapid alphabeta TCR-mediated responses in gammadelta T cells transduced with cancer-specific TCR genes. Gene Ther 16(5):620-628
114. Sudo T, Kuramoto T, Komiya S, Inoue A, Itoh K (1997) Expression of MAGE genes in osteosarcoma. J Orthop Res 15(1):128-132. doi: 10.1002/jor.1100150119