Clinical evaluation of autologous gamma delta T cell-based immunotherapy for metastatic solid tumours

British Journal of Cancer

Volumn 105, Issue 6, 2011, Pages 778-786

  Nicol, A J ^a   Tokuyama, H ^a,b   Mattarollo, S R ^a   Hagi, T ^a   Suzuki, K ^c   Yokokawa, K ^d   Nieda, M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b TOKYO MEDICAL UNIVERSITY   (Japan)

^c Japanese Red Cross ^*  (Japan)

^d MEDINET Co Ltd   (Japan)

Author keywords

clinical trial; gamma delta T cells; immunotherapy; V 9Vd2 T cells

Indexed keywords

8 QUINOLINOL INDIUM IN 111; ZOLEDRONIC ACID;

ADOPTIVE TRANSFER; ARTICLE; BILE DUCT CARCINOMA; BONE METASTASIS; CANCER IMMUNOTHERAPY; CLINICAL ARTICLE; CLINICAL PROTOCOL; COLON CANCER; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; CYTOTOXICITY; DIGESTIVE SYSTEM CANCER; DISTANT METASTASIS; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; ISOTOPE LABELING; LIVER METASTASIS; LUNG METASTASIS; MELANOMA; METASTASIS; OVARY CANCER; PATIENT SAFETY; PHASE 1 CLINICAL TRIAL; PRIORITY JOURNAL; REMISSION; REPEATED DRUG DOSE; SOLID TUMOR; T LYMPHOCYTE; TREATMENT RESPONSE;

AGED; DIPHOSPHONATES; FEASIBILITY STUDIES; FEMALE; HUMANS; IMIDAZOLES; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; NEOPLASM METASTASIS; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES; TREATMENT OUTCOME;

EID: 80052446521     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2011.293     Document Type: Article

References (50)

1. Abe Y, Muto M, Nieda M, Nakagawa Y, Nicol A, Kaneko T, Goto S, Yokogawa K, Suzuki K (2009) Clinical and immunological evaluation of zolendronate- activated Vgamma9Vdelta2 T cell-based immunotherapy for patients with multiple myeloma. Exp Hematol 37: 956-968
2. Bennouna J, Bompas E, Neidhardt EM, Rolland F, Philip I, Galea C, Salot S, Saiagh S, Audrain M, Rimbert M, Lafaye-de Micheaux S, 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: 1599-1609
3. Bonneville M, Scotet E (2006) Human Vgamma9Vdelta2 T cells: promising new leads for immunotherapy of infections and tumours. Curr Opin Immunol 18: 539-546 (Pubitemid 44311448)
4. Bouet-Toussaint F, Cabillac F, Toutirais O, Le Gallo M, Thomas de la Pintiere C, 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: 531-539 (Pubitemid 351170536)
5. Braakman E, van de Winkel JG, van Krimpen BA, Jansze M, Bolhuis RL (1992) CD16 on human gd T lymphocytes: expression, function, and specificity for mouse IgG isotypes. Cell Immunol 143: 97-107
6. Brandes M, Willimann K, Lang AB, Nam KH, Jin C, Brenner MB, Morita CT, Moser B (2003) Flexible migration program regulates gamma delta T-cell involvement in humoral immunity. Blood 102: 3693-3701 (Pubitemid 37409390)
7. Carding SR, Egan PJ (2002) Gammadelta T cells: functional plasticity and heterogeneity. Nat Rev Immunol 2: 336-345 (Pubitemid 37328756)
8. Cendron D, Ingoure S, Martino A, Casetti R, Horand F, Romagne F, Sicard H, Fournie JJ, Poccia F (2007) A tuberculosis vaccine based on phosphoantigens and fusion proteins induces distinct gammadelta and alphabeta T cell responses in primates. Eur J Immunol 37: 549-565 (Pubitemid 46915593)
9. Cesana GC, DeRaffele G, Cohen S, Moroziewicz D, Mitcham J, Stoutenburg J, Cheung K, Hesdorffer C, Kim-Schulze S, Kaufman HL (2006) Characterization of CD4+CD25+ regulatory T cells in patients treated with high-dose interleukin-2 for metastatic melanoma or renal cell carcinoma. J Clin Oncol 24: 1169-1177 (Pubitemid 46638815)
10. Chen ZW, Letvin NL (2003) Adaptive immune response of Vgamma2V-delta2 T cells: a new paradigm. Trends Immunol 24: 213-219 (Pubitemid 36412110)
11. Clezardin P (2005) Anti-tumour activity of zoledronic acid. Cancer Treat Rev 31(Suppl 3): 1-8
12. Das H, Wang L, Kamath A, Bukowski JF (2001) Vgamma2Vdelta2 T-cell receptor-mediated recognition of aminobisphosphonates. Blood 98: 1616-1618
13. 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. Cancer Res 67: 7450-7457
14. Ensslin AS, Formby B (1991) Comparison of cytolytic and proliferative activities of human gamma delta and alpha beta T cells from peripheral blood against various human tumor cell lines. J Natl Cancer Inst 83: 1564-1569
15. Fisher B, Packard BS, Read EJ, Carrasquillo JA, Carter CS, Topalian SL, Yang JC, Yolles P, Larson SM, Rosenberg SA (1989) Tumor localization of adoptively transferred indium-111 labelled tumor infiltrating lymphocytes in patients with metastatic melanoma. J Clin Oncol 7: 250-261 (Pubitemid 19048459)
16. Gallimore A, Godkin A (2008) Regulatory T cells and tumour immunity-observations in mice and men. Immunology 123: 157-163
17. Gertner-Dardenne J, Bonnafous C, Bezombes C, Capietto AH, Scaglione V, Ingoure S, Cendron D, Gross E, Lepage JF, Quillet-Mary A, Ysebaert L, Laurent G, Sicard H, Fournie JJ (2009) Bromohydrin pyrophosphate enhances antibody-dependent cell-mediated cytoxicity induced by therapeutic antibodies. Blood 113: 4875-4884
18. Giraudo E, Inoue M, Hanahan D (2004) An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J Clin Invest 114: 623-633 (Pubitemid 39578752)
19. Glatzel A, Wesch D, Schiemann F, Brandt E, Janssen O, Kabelitz D (2002) Patterns of chemokine receptor expression on peripheral blood gamma delta T lymphocytes: strong expression of CCR5 is a selective feature of V delta 2/V gamma 9 gamma delta T cells. J Immunol 168: 4920-4929 (Pubitemid 34498305)
20. Gober HJ, Kistowska M, Angman L, Jeno P, Mori L, De Libero G (2003) Human T cell receptor gamma delta cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med 197: 163-168 (Pubitemid 36152311)
21. Green AE, Lissina A, Hutchinson SL, Hewitt RE, Temple B, James D, Boulter JM, Price DA, Sewell AK (2004) Recognition of nonpeptide antigens by human V gamma 9V delta 2 T cells requires contact with cells of human origin. Clin Exp Immunol 136: 472-482 (Pubitemid 38703681)
22. 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: 169-175 (Pubitemid 41396778)
23. Kabelitz D, Wesch D, He W (2007) Perspectives of gammadelta T cells in tumor immunology. Cancer Res 67: 5-8 (Pubitemid 46142752)
24. Kabelitz D, Wesch D, Pitters E, Zoller M (2004) Characterization of tumor reactivity of human V gamma 9V delta 2 gamma delta T cells in vitro and in SCID mice in vivo. J Immunol 173: 6767-6776 (Pubitemid 39541063)
25. Kato Y, Tanaka Y, Miyagawa F, Yamashita S, Minato N (2001) Targeting of tumor cells for human gamma delta T cells by nonpeptide antigens. J Immunol 167: 5092-5098 (Pubitemid 33009743)
26. Knight LA, Conroy M, Fernando A, Polak M, Kurbacher CM, Cree IA (2005) Pilot studies of the effect of zoledronic acid (Zometa) on tumor-derived cells ex vivo in the ATP-based tumor chemosensitivity assay. Anticancer Drugs 16: 969-976 (Pubitemid 41416087)
27. 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: 469-476 (Pubitemid 46204533)
28. Kondo M, Sakuta K, Noguchi A, Ariyoshi N, Sato K, Sato S, Sao K, Hosoi A, Nakjima J, Yoshida Y, Shiraishi K, Nakagawa K, Kakimi K (2008) Zoledronate facilitates large-scale ex vivo expansion of functional gd T cells from cancer patients for use in adoptive immunotherapy. Cytotherapy 10: 842-856
29. Kunzmann V, Kimmel B, Herrmann T, Einsele H, Wilhelm M (2009) Inhibition of phosphoantigen-mediated gammadelta T-cell proliferation by CD4+ CD25+ FoxP3+ regulatory T cells. Immunology 126: 256-267
30. Lanier LL, Kipps TJ, Phillips JH (1985) Functional properties of a unique subset of cytotoxic CD3+ T lymphocytes that express Fc receptors for IgG (CD16/Leu-11 antigen). J Exp Med 162: 2089-2106 (Pubitemid 16149696)
31. 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: 1552-1556 (Pubitemid 40524770)
32. Lopez RD, Xu S, Guo B, Negrin RS, Waller EK (2000) CD2-mediated IL-12-dependent signals render human gamma delta-T cells resistant to mitogen-induced apoptosis, permitting the large-scale ex vivo expansion of functionally distinct lymphocytes: implications for the development of adoptive immunotherapy strategies. Blood 96: 3827-3837
33. Marten A, von Lilienfeld-Toal M, Buchler MW, Schmidt J (2007) Zoledronic acid has direct antiproliferative and antimetastatic effect on pancreatic carcinoma cells and acts as an antigen for delta2 gamma/delta T cells. J Immunother 30: 370-377 (Pubitemid 46684427)
34. Mattarollo SR, Kenna T, Nieda M, Nicol AJ (2007) Chemotherapy and zoledronate sensitize solid tumour cells to Vgamma9Vdelta2 T cell cytotoxicity. Cancer Immunol Immunother 56: 1285-1297 (Pubitemid 46763941)
35. Meidenbauer N, Marienhagen J, Laumer M, Vogl S, Heymann J, Andreesen R, Mackensen A (2003) Survival and tumor localization of adoptively transferred Melan-A-specific T cells in melanoma patients. J Immunol 170: 2161-2169 (Pubitemid 36197440)
36. Moser B, Loetscher P (2001) Lymphocyte traffic control by chemokines. Nat Immunol 2: 123-128 (Pubitemid 33707929)
37. Nieda M, Okai M, Tazbirkova A, Lin H, Yamaura A, Ide K, Abraham R, Juji T, Macfarlane DJ, Nicol AJ (2004) Therapeutic activation of Valpha24+Vbeta11+ NKT cells in human subjects results in highly coordinated secondary activation of acquired and innate immunity. Blood 103: 383-389 (Pubitemid 38140063)
38. Noguchi A, Kaneko T, Kamigaki T, Fujimoto K, Ozawa M, Saito M, Ariyoshi N, Goto S (2011) Zoledronate-activated Vg9gd T cell-based immunotherapy is feasible and restores the impairment of gd T cells in patients with solid tumors. Cytotherapy 13: 92-97
39. Santini D, Vincenzi B, Dicuonzo G, Avvisati G, Massacesi C, Battistoni F, Gavasci M, Rocci L, Tirindelli MC, Altomare V, Tocchini M, Bonsignori M, Tonini G (2003) Zoledronic acid induces significant and long-lasting modifications of circulating angiogenic factors in cancer patients. Clin Cancer Res 9: 2893-2897 (Pubitemid 36993246)
40. Sato K, Kimura S, Segawa H, Yokota A, Matsumoto S, Kuroda J, Nogawa M, Yuasa T, Kiyono Y, Wada H, Maekawa T (2005) Cytotoxic effects of gamma delta T cells expanded ex vivo by a third generation bisphosphonate for cancer immunotherapy. Int J Cancer 116: 94-99 (Pubitemid 40827760)
41. Senaratne SG, Pirianov G, Mansi JL, Arnett TR, Colston KW (2000) Bisphosphonates induce apoptosis in human breast cancer cell lines. Br J Cancer 82: 1459-1468 (Pubitemid 30175914)
42. Tassone P, Forciniti S, Galea E, Morrone G, Turco MC, Martinelli V, Tagliaferri P, Venuta S (2000) Growth inhibition and synergistic induction of apoptosis by zoledronate and dexamethasone in human myeloma cell lines. Leukemia 14: 841-844 (Pubitemid 30235061)
43. Thedrez A, Harly C, Morice A, Salot S, Bonneville M, Scotet E (2009) IL-21-mediated potentiation of antitumor cytolytic and proinflammatory responses of human Vg9Vd2 T cells for adoptive immunotherapy. J Immunol 182: 3423-3431
44. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, van Oosterom AT, Christian MC, Gwyther SG (2000) New guidelines to evaluate the response to treatment in solid tumors. J Natl Cancer Inst 92: 205-216 (Pubitemid 30099779)
45. 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 gamma delta T lymphocytes. J Immunol 182: 7287-7296
46. Tokuyama H, Hagi T, Mattarollo SR, Morley J, Wang Q, Fai-So H, Moriyasu F, Nieda M, Nicol AJ (2008) Vg9Vd2 T cell cytotoxicity against tumor cells is enhanced by monoclonal antibody drugs-rituximab and trastuzumab. Int J Cancer 122: 2526-2534 (Pubitemid 351590486)
47. Urban EM, Li H, Armstrong C, Focaccetti C, Cairo C, Pauza CD (2009) Control of CD56 expression and tumor cell cytotoxicity in human Vgamma2Vdelta2 T cells. BMC Immunol 21: 10-50
48. Viey E, Fromont G, Escudier B, Morel Y, Da Rocha S, Chouaib S, Caignard A (2005) Phosphostim-activated gamma delta T cells kill autologous metastatic renal cell carcinoma. J Immunol 174: 1338-1347
49. Wilhelm M, Kunzmann V, Eckstein S, Reimer P, Weissinger F, Ruediger T, Tony HP (2003) Gammadelta T cells for immune therapy of patients with lymphoid malignancies. Blood 102: 200-206 (Pubitemid 36759655)
50. Zou W (2006) Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 6: 295-307