Anti-tumour immunotherapy with Vγ9Vδ2 T lymphocytes: From the bench to the bedside

British Journal of Haematology

Volumn 160, Issue 2, 2013, Pages 123-132

  Braza, Mounia S ^a   Klein, Bernard ^a,b,c  

^a INSERM   (France)

^b MONTPELLIER UNIVERSITY HOSPITAL   (France)

^c UNIV MONTPELLIER   (France)

Author keywords

Cancer; Gamma delta T lymphocytes; Haematological oncology; Immunotherapy; Monoclonal antibodies

Indexed keywords

2 METHYL 3 BUTENYL 1 PYROPHOSPHATE; BCG VACCINE; DENDRITIC CELL VACCINE; GAMMA INTERFERON; IMMUNOSTIMULATING AGENT; INTERLEUKIN 17; INTERLEUKIN 2; PAMIDRONIC ACID; PHOSPHORYLATED BROMOHYDRIN; PHOSPHOSTIMTM; RECOMBINANT INTERLEUKIN 2; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ZOLEDRONIC ACID;

ADOPTIVE TRANSFER; ANTINEOPLASTIC ACTIVITY; BLADDER CANCER; BREAST METASTASIS; CANCER IMMUNOTHERAPY; CD4+ CD25+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INTERACTION; COLORECTAL CARCINOMA; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; GAMMA DELTA T LYMPHOCYTE; HUMAN; KIDNEY CARCINOMA; LIVER CELL CARCINOMA; LIVER METASTASIS; LOW DRUG DOSE; LYMPHOCYTE PROLIFERATION; MESENCHYMAL STEM CELL; METASTASIS; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; REGULATORY T LYMPHOCYTE; REVIEW; SOLID TUMOR; T LYMPHOCYTE ACTIVATION;

ADAPTIVE IMMUNITY; ADJUVANTS, IMMUNOLOGIC; ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CLINICAL TRIALS AS TOPIC; DENDRITIC CELLS; DIPHOSPHONATES; GENE REARRANGEMENT, DELTA-CHAIN T-CELL ANTIGEN RECEPTOR; GENE REARRANGEMENT, GAMMA-CHAIN T-CELL ANTIGEN RECEPTOR; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC SURVEILLANCE; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; MESENCHYMAL STROMAL CELLS; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, REGULATORY; TRANSLATIONAL MEDICAL RESEARCH; TUMOR ESCAPE;

EID: 84872275227     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.12090     Document Type: Review

References (93)

1. Alexander, A.A., Maniar, A., Cummings, J.S., Hebbeler, A.M., Schulze, D.H., Gastman, B.R., Pauza, C.D., Strome, S.E. & Chapoval, A.I. (2008) Isopentenyl pyrophosphate-activated CD56+ {gamma}{delta} T lymphocytes display potent antitumor activity toward human squamous cell carcinoma. Clinical Cancer Research, 14, 4232-4240.
2. Ali, Z., Yan, L., Plagman, N., Reichenberg, A., Hintz, M., Jomaa, H., Villinger, F. & Chen, Z.W. (2009) Gammadelta T cell immune manipulation during chronic phase of simian-human immunodeficiency virus infection [corrected] confers immunological benefits. Journal of Immunology, 183, 5407-5417.
3. Argentati, K., Re, F., Serresi, S., Tucci, M.G., Bartozzi, B., Bernardini, G. & Provinciali, M. (2003) Reduced number and impaired function of circulating gamma delta T cells in patients with cutaneous primary melanoma. The Journal of Investigative Dermatology, 120, 829-834.
4. Banchereau, J. & Steinman, R.M. (1998) Dendritic cells and the control of immunity. Nature, 392, 245-252.
5. Bauer, S., Groh, V., Wu, J., Steinle, A., Phillips, J.H., Lanier, L.L. & Spies, T. (1999) Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science, 285, 727-729.
6. Bennouna, J., Bompas, E., Neidhardt, E.M., Rolland, F., Philip, I., Galea, C., Salot, S., Saiagh, S., Audrain, M., Rimbert, M., Lafaye-de Micheaux, S., Tiollier, J. & Négrier, 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 Immunology, Immunotherapy, 57, 1599-1609.
7. Benzaid, I., Monkkonen, H., Stresing, V., Bonnelye, E., Green, J., Monkkonen, J., Touraine, J.L. & Clezardin, P. (2011) High phosphoantigen levels in bisphosphonate-treated human breast tumors promote Vgamma9Vdelta2 T-cell chemotaxis and cytotoxicity in vivo. Cancer Research, 71, 4562-4572.
8. Beyer, M. & Schultze, J.L. (2006) Regulatory T cells in cancer. Blood, 108, 804-811.
9. Born, W.K., Reardon, C.L. & O'Brien, R.L. (2006) The function of gammadelta T cells in innate immunity. Current Opinion in Immunology, 18, 31-38.
10. Brandes, M., Willimann, K. & Moser, B. (2005) Professional antigen-presentation function by human gammadelta T cells. Science, 309, 264-268.
11. 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. Proceedings of the National Academy of Sciences of the United States of America, 106, 2307-2312.
12. Braza, M.S., Caraux, A., Rousset, T., Lafaye de Micheaux, S., Sicard, H., Squiban, P., Costes, V., Klein, B. & Rossi, J.F. (2010) gammadelta T lymphocytes count is normal and expandable in peripheral blood of patients with follicular lymphoma, whereas it is decreased in tumor lymph nodes compared with inflammatory lymph nodes. Journal of Immunology, 184, 134-140.
13. Braza, M.S., Klein, B., Fiol, G. & Rossi, J.F. (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, 400-407.
14. Bui, J.D., Uppaluri, R., Hsieh, C.S. & Schreiber, R.D. (2006) Comparative analysis of regulatory and effector T cells in progressively growing versus rejecting tumors of similar origins. Cancer Research, 66, 7301-7309.
15. Burjanadze, M., Condomines, M., Reme, T., Quittet, P., Latry, P., Lugagne, C., Romagne, F., Morel, Y., Rossi, J.F., Klein, B. & Lu, Z.Y. (2007) In vitro expansion of gamma delta T cells with anti-myeloma cell activity by Phosphostim and IL-2 in patients with multiple myeloma. British Journal of Haematology, 139, 206-216.
16. Cabillic, F., Toutirais, O., Lavoue, V., de La Pintiere, C.T., Daniel, P., Rioux-Leclerc, N., Turlin, B., Monkkonen, H., Monkkonen, J., Boudjema, K., Catros, V. & Bouet-Toussait, F. (2010) Aminobisphosphonate-pretreated dendritic cells trigger successful Vgamma9Vdelta2 T cell amplification for immunotherapy in advanced cancer patients. Cancer Immunology, Immunotherapy, 59, 1611-1619.
17. Caccamo, N., La Mendola, C., Orlando, V., Meraviglia, S., Todaro, M., Stassi, G., Sireci, G., Fournie, J.J. & Dieli, F. (2011) Differentiation, phenotype, and function of interleukin-17-producing human Vgamma9Vdelta2 T cells. Blood, 118, 129-138.
18. Casetti, R., Martino, A., Sacchi, A., Agrati, C., Goletti, D. & Martini, F. (2008) Do human gammadelta T cells respond to M tuberculosis protein antigens? Blood, 112, 4776-4777; author reply 4777.
19. Castella, B., Riganti, C., Fiore, F., Pantaleoni, F., Canepari, M.E., Peola, S., Foglietta, M., Palumbo, A., Bosia, A., Coscia, M., Baccadoro, 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. Journal of Immunology, 187, 1578-1590.
20. Cendron, D., Ingoure, S., Martino, A., Casetti, R., Horand, F., Romagne, F., Sicard, H., Fournie, J.J. & Poccia, F. (2007) A tuberculosis vaccine based on phosphoantigens and fusion proteins induces distinct gammadelta and alphabeta T cell responses in primates. European Journal of Immunology, 37, 549-565.
21. Chien, Y.H. & Konigshofer, Y. (2007) Antigen recognition by gammadelta T cells. Immunological Reviews, 215, 46-58.
22. Conti, L., Casetti, R., Cardone, M., Varano, B., Martino, A., Belardelli, F., Poccia, F. & Gessani, S. (2005) Reciprocal activating interaction between dendritic cells and pamidronate-stimulated gammadelta T cells: role of CD86 and inflammatory cytokines. Journal of Immunology, 174, 252-260.
23. Corvaisier, M., Moreau-Aubry, A., Diez, E., Bennouna, J., Mosnier, J.F., Scotet, E., Bonneville, M. & Jotereau, F. (2005) V gamma 9V delta 2 T cell response to colon carcinoma cells. Journal of Immunology, 175, 5481-5488.
24. 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., Fournié, J.J. & 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. Journal of Immunology, 184, 3260-3268.
25. Devilder, M.C., Maillet, S., Bouyge-Moreau, I., Donnadieu, E., Bonneville, M. & Scotet, E. (2006) Potentiation of antigen-stimulated V gamma 9V delta 2 T cell cytokine production by immature dendritic cells (DC) and reciprocal effect on DC maturation. Journal of Immunology, 176, 1386-1393.
26. 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, A.C. (2007) Targeting human {gamma}delta} T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Research, 67, 7450-7457.
27. Do, J.S. & Min, B. (2009) IL-15 produced and trans-presented by DCs underlies homeostatic competition between CD8 and {gamma} {delta} T cells in vivo. Blood, 113, 6361-6371.
28. D'Ombrain, M.C., Hansen, D.S., Simpson, K.M. & Schofield, L. (2007) gammadelta-T cells expressing NK receptors predominate over NK cells and conventional T cells in the innate IFN-gamma response to Plasmodium falciparum malaria. European Journal of Immunology, 37, 1864-1873.
29. Eagle, R.A. & Trowsdale, J. (2007) Promiscuity and the single receptor: NKG2D. Nature Reviews Immunology, 7, 737-744.
30. French, J.D., Roark, C.L., Born, W.K. & O'Brien, R.L. (2005) {gamma}{delta} T cell homeostasis is established in competition with {alpha}{beta} T cells and NK cells. Proceedings of the National Academy of Sciences of the United States of America, 102, 14741-14746.
31. Galluzzo, S., Santini, D., Vincenzi, B., Caccamo, N., Meraviglia, F., Salerno, A., Dieli, F. & Tonini, G. (2007) Immunomodulating role of bisphosphonates on human gamma delta T cells: an intriguing and promising aspect of their antitumour activity. Expert Opinion on Therapeutic Targets, 11, 941-954.
32. Gao, Q., Qiu, S.J., Fan, J., Zhou, J., Wang, X.Y., Xiao, Y.S., Xu, Y., Li, Y.W. & Tang, Z.Y. (2007) Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. Journal of Clinical Oncology, 25, 2586-2593.
33. Gertner-Dardenne, J., Bonnafous, C., Bezombes, C., Capietto, A.H., Scaglione, V., Ingoure, S., Cendron, D., Gross, E., Lepage, J.F., Quillet-Mary, A., Ysebaert, L., Laurent, G., Sicard, H. & Fournié, J.J. (2009) Bromohydrin pyrophosphate enhances antibody-dependent cell-mediated cytotoxicity induced by therapeutic antibodies. Blood, 113, 4875-4884.
34. Girardi, M. (2006) Immunosurveillance and immunoregulation by gammadelta T cells. The Journal of Investigative Dermatology, 126, 25-31.
35. Gober, H.J., 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. Journal of Experimental Medicine, 197, 163-168.
36. Groh, V., Steinle, A., Bauer, S. & Spies, T. (1998) Recognition of stress-induced MHC molecules by intestinal epithelial gammadelta T cells. Science, 279, 1737-1740.
37. Groh, V., Rhinehart, R., Secrist, H., Bauer, S., Grabstein, K.H. & Spies, T. (1999) Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proceedings of the National Academy of Sciences of the United States of America, 96, 6879-6884.
38. Hall, B., Andreeff, M. & Marini, F. (2007) The participation of mesenchymal stem cells in tumor stroma formation and their application as targeted-gene delivery vehicles. Handbook of Experimental Pharmacology, 180, 263-283.
39. Hayes, S.M. & Laird, R.M. (2012) Genetic requirements for the development and differentiation of interleukin-17-producing gammadelta T cells. Critical Reviews in Immunology, 32, 81-95.
40. Henry, T., Kirimanjeswara, G.S., Ruby, T., Jones, J.W., Peng, K., Perret, M., Ho, L., Sauer, J.D., Iwakura, Y., Metzger, D.W. & Monack, D.M. (2010) Type I IFN signaling constrains IL-17A/F secretion by {gamma} {delta} T cells during bacterial infections. Journal of Immunology, 184, 3755-3767.
41. Himoudi, N., Morgenstern, D.A., Yan, M., Vernay, B., Saraiva, L., Wu, Y., Cohen, C.J., Gustafsson, K. & Anderson, J. (2012) Human gammadelta T lymphocytes are licensed for professional antigen presentation by interaction with opsonized target cells. Journal of Immunology, 188, 1708-1716.
42. Hori, S., Nomura, T. & Sakaguchi, S. (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science, 299, 1057-1061.
43. Iovino, F., Meraviglia, S., Spina, M., Orlando, V., Saladino, V., Dieli, F., Stassi, G. & Todaro, M. (2011) Immunotherapy targeting colon cancer stem cells. Immunotherapy, 3, 97-106.
44. Jiang, H. & Chess, L. (2004) An integrated view of suppressor T cell subsets in immunoregulation. The Journal of Clinical Investigation, 114, 1198-1208.
45. 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-TCRgammadelta antibody-expanded human gammadelta T-cells in peripheral blood. Cancer Biology & Therapy, 8, 1540-1549.
46. Karnoub, A.E., Dash, A.B., Vo, A.P., Sullivan, A., Brooks, M.W., Bell, G.W., Richardson, A.L., Polyak, K., Tubo, R. & Weinberg, R.A. (2007) Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature, 449, 557-563.
47. 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 Immunology, Immunotherapy, 56, 469-476.
48. 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 Immunology, Immunotherapy, 60, 1075-1084.
49. Kondo, M., Sakuta, K., Noguchi, A., Ariyoshi, N., Sato, K., Sato, S., Sato, K., Hosoi, A., Nakajima, J., Yoshida, Y., Shiraishi, K., Nakagawa, K. & Kakimi, K. (2008) Zoledronate facilitates large-scale ex vivo expansion of functional gammadelta T cells from cancer patients for use in adoptive immunotherapy. Cytotherapy, 10, 842-856.
50. Konigshofer, Y. & Chien, Y.H. (2006) Gammadelta T cells - innate immune lymphocytes? Current Opinion in Immunology, 18, 527-533.
51. Kunzmann, V., Bauer, E., Feurle, J., Weissinger, F., Tony, H.P. & Wilhelm, M. (2000) Stimulation of gammadelta T cells by aminobisphosphonates and induction of antiplasma cell activity in multiple myeloma. Blood, 96, 384-392.
52. 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.
53. Li, J., Herold, M.J., Kimmel, B., Muller, I., Rincon-Orozco, B., Kunzmann, V. & Herrmann, T. (2009) Reduced expression of the mevalonate pathway enzyme farnesyl pyrophosphate synthase unveils recognition of tumor cells by Vgamma9Vdelta2 T cells. Journal of Immunology, 182, 8118-8124.
54. von Lilienfeld-Toal, M., Sievers, E., Bodemuller, V., Mihailescu, C., Marten, A., Gorschluter, M. & Schmidt-Wolf, I.G. (2005) Coculture with dendritic cells promotes proliferation but not cytotoxic activity of gamma/delta T cells. Immunology Letters, 99, 103-108.
55. Liu, Z., Guo, B.L., Gehrs, B.C., Nan, L. & Lopez, R.D. (2005) Ex vivo expanded human Vgamma9Vdelta2+ gammadelta-T cells mediate innate antitumor activity against human prostate cancer cells in vitro. The Journal of Urology, 173, 1552-1556.
56. Liu, Z., Eltoum, I.E., Guo, B., Beck, B.H., Cloud, G.A. & Lopez, R.D. (2008) Protective immunosurveillance and therapeutic antitumor activity of gammadelta T cells demonstrated in a mouse model of prostate cancer. Journal of Immunology, 180, 6044-6053.
57. Lockhart, E., Green, A.M. & Flynn, J.L. (2006) IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. Journal of Immunology, 177, 4662-4669.
58. Ma, Y., Aymeric, L., Locher, C., Mattarollo, S.R., Delahaye, N.F., Pereira, P., Boucontet, L., Apetoh, L., Ghiringhelli, F., Casares, N., Lasarte, J.J., Matsuzaki, G., Ikuta, K., Ryffel, B., Benlagha, K., Tesnière, A., Ibrahim, N., Déchanet-Merville, J., Chaput, N., Smyth, M.J., Kroemer, G. & Zitvogel, L. (2011) Contribution of IL-17-producing gamma delta T cells to the efficacy of anticancer chemotherapy. Journal of Experimental Medicine, 208, 491-503.
59. Maniar, A., Zhang, X., Lin, W., Gastman, B.R., Pauza, C.D., Strome, S.E. & Chapoval, A.I. (2010) Human gammadelta T lymphocytes induce robust NK cell-mediated antitumor cytotoxicity through CD137 engagement. Blood, 116, 1726-1733.
60. Marcu-Malina, V., Heijhuurs, S., van Buuren, M., Hartkamp, L., Strand, S., Sebestyen, Z., Scholten, K., Martens, A. & Kuball, J. (2011) Redirecting alphabeta T cells against cancer cells by transfer of a broadly tumor-reactive gammadeltaT-cell receptor. Blood, 118, 50-59.
61. Martinet, L., Fleury-Cappellesso, S., Gadelorge, M., Dietrich, G., Bourin, P., Fournie, J.J. & Poupot, R. (2009) A regulatory cross-talk between Vgamma9Vdelta2 T lymphocytes and mesenchymal stem cells. European Journal of Immunology, 39, 752-762.
62. Martinet, L., Jean, C., Dietrich, G., Fournie, J.J. & Poupot, R. (2010) PGE2 inhibits natural killer and gamma delta T cell cytotoxicity triggered by NKR and TCR through a cAMP-mediated PKA type I-dependent signaling. Biochemical Pharmacology, 80, 838-845.
63. 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, A.C. (2010) In vivo manipulation of Vgamma9Vdelta2 T cells with zoledronate and low-dose interleukin-2 for immunotherapy of advanced breast cancer patients. Clinical and Experimental Immunology, 161, 290-297.
64. Meuter, S., Eberl, M. & Moser, B. (2010) Prolonged antigen survival and cytosolic export in cross-presenting human gammadelta T cells. Proceedings of the National Academy of Sciences of the United States of America, 107, 8730-8735.
65. Moser, B. & Eberl, M. (2007) gammadelta T cells: novel initiators of adaptive immunity. Immunological Reviews, 215, 89-102.
66. Noguchi, A., Kaneko, T., Kamigaki, T., Fujimoto, K., Ozawa, M., Saito, M., Ariyoshi, N. & Goto, S. (2011) Zoledronate-activated Vgamma9gammadelta T cell-based immunotherapy is feasible and restores the impairment of gammadelta T cells in patients with solid tumors. Cytotherapy, 13, 92-97.
67. Nussbaumer, O., Gruenbacher, G., Gander, H. & Thurnher, M. (2011) DC-like cell-dependent activation of human natural killer cells by the bisphosphonate zoledronic acid is regulated by gammadelta T lymphocytes. Blood, 118, 2743-2751.
68. Pende, D., Rivera, P., Marcenaro, S., Chang, C.C., Biassoni, R., Conte, R., Kubin, M., Cosman, D., Ferrone, S., Moretta, L. & Moretta, A. (2002) Major histocompatibility complex class I-related chain A and UL16-binding protein expression on tumor cell lines of different histotypes: analysis of tumor susceptibility to NKG2D-dependent natural killer cell cytotoxicity. Cancer Research, 62, 6178-6186.
69. Prigione, I., Benvenuto, F., Bocca, P., Battistini, L., Uccelli, A. & Pistoia, V. (2009) Reciprocal interactions between human mesenchymal stem cells and gammadelta T cells or invariant natural killer T cells. Stem Cells (Dayton, Ohio), 27, 693-702.
70. Qin, G., Liu, Y., Zheng, J., Ng, I.H., Xiang, Z., Lam, K.T., Mao, H., Li, H., Peiris, J.S., Lau, Y.L. & Tu, W. (2011) Type 1 responses of human Vgamma9Vdelta2 T cells to influenza A viruses. Journal of Virology, 85, 10109-10116.
71. Ribot, J.C., deBarros, A., Pang, D.J., Neves, J.F., Peperzak, V., Roberts, S.J., Girardi, M., Borst, J., Hayday, A.C., Pennington, D.J. & Silva-Santos, B. (2009) CD27 is a thymic determinant of the balance between interferon-gamma- and interleukin 17-producing gammadelta T cell subsets. Nature Immunology, 10, 427-436.
72. Ribot, J.C., Chaves-Ferreira, M., d'Orey, F., Wencker, M., Goncalves-Sousa, N., Decalf, J., Simas, J.P., Hayday, A.C. & Silva-Santos, B. (2010) Cutting edge: adaptive versus innate receptor signals selectively control the pool sizes of murine IFN-gamma- or IL-17-producing gammadelta T cells upon infection. Journal of Immunology, 185, 6421-6425.
73. Roelofs, A.J., Jauhiainen, M., Monkkonen, H., Rogers, M.J., Monkkonen, J. & Thompson, K. (2009) Peripheral blood monocytes are responsible for gammadelta T cell activation induced by zoledronic acid through accumulation of IPP/DMAPP. British Journal of Haematology, 144, 245-250.
74. Ryan, J.M., Barry, F., Murphy, J.M. & Mahon, B.P. (2007) Interferon-gamma does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clinical and Experimental Immunology, 149, 353-363.
75. 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. Medical Oncology, 25, 137-147.
76. Salot, S., Laplace, C., Saiagh, S., Bercegeay, S., Tenaud, I., Cassidanius, A., Romagne, F., Dreno, B. & Tiollier, J. (2007) Large scale expansion of gamma 9 delta 2 T lymphocytes: Innacell gamma delta cell therapy product. Journal of Immunological Methods, 326, 63-75.
77. Scotet, E., Martinez, L.O., Grant, E., Barbaras, R., Jeno, P., Guiraud, M., Monsarrat, B., Saulquin, X., Maillet, S., Esteve, J.P., 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, 71-80.
78. Shi, C., Sahay, B., Russell, J.Q., Fortner, K.A., Hardin, N., Sellati, T.J. & Budd, R.C. (2011) Reduced immune response to Borrelia burgdorferi in the absence of gammadelta T cells. Infection and Immunity, 79, 3940-3946.
79. Sicard, H., Ingoure, S., Luciani, B., Serraz, C., Fournie, J.J., Bonneville, M., Tiollier, J. & Romagne, F. (2005) In vivo immunomanipulation of V gamma 9V delta 2 T cells with a synthetic phosphoantigen in a preclinical nonhuman primate model. Journal of Immunology, 175, 5471-5480.
80. Simoni, D., Gebbia, N., Invidiata, F.P., Eleopra, M., Marchetti, P., Rondanin, R., Baruchello, R., Provera, S., Marchioro, C., Tolomeo, M., Marinelli, L., Limongelli, V., Novellino, E., Kwaasi, A., Dunford, J., Buccheri, S., Caccamo, N. & Dieli, F. (2008) Design, synthesis, and biological evaluation of novel aminobisphosphonates possessing an in vivo antitumor activity through a gammadelta-T lymphocytes-mediated activation mechanism. Journal of Medicinal Chemistry, 51, 6800-6807.
81. Spencer, C.T., Abate, G., Blazevic, A. & Hoft, D.F. (2008) Only a subset of phosphoantigen-responsive gamma9delta2 T cells mediate protective tuberculosis immunity. Journal of Immunology, 181, 4471-4484.
82. Sutton, C.E., Lalor, S.J., Sweeney, C.M., Brereton, C.F., Lavelle, E.C. & Mills, K.H. (2009) Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity, 31, 331-341.
83. Takeuchi, A., Dejima, T., Yamada, H., Shibata, K., Nakamura, R., Eto, M., Nakatani, T., Naito, S. & Yoshikai, Y. (2011) IL-17 production by gammadelta T cells is important for the antitumor effect of Mycobacterium bovis bacillus Calmette-Guerin treatment against bladder cancer. European Journal of Immunology, 41, 246-251.
84. Thedrez, A., Sabourin, C., Gertner, J., Devilder, M.C., Allain-Maillet, S., Fournie, J.J., Scotet, E. & Bonneville, M. (2007) Self/non-self discrimination by human gammadelta T cells: simple solutions for a complex issue? Immunological Reviews, 215, 123-135.
85. 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 V gamma 9V delta 2 T cells for adoptive immunotherapy. Journal of Immunology, 182, 3423-3431.
86. Thompson, K., Rojas-Navea, J. & Rogers, M.J. (2006) Alkylamines cause Vgamma9Vdelta2 T-cell activation and proliferation by inhibiting the mevalonate pathway. Blood, 107, 651-654.
87. Tokuyama, H., Hagi, T., Mattarollo, S.R., Morley, J., Wang, Q., Fai-So, H., Moriyasu, F., Nieda, M. & Nicol, A.J. (2008) V gamma 9 V delta 2 T cell cytotoxicity against tumor cells is enhanced by monoclonal antibody drugs-rituximab and trastuzumab. International Journal of Cancer, 122, 2526-2534.
88. 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. Journal of Immunology, 174, 1338-1347.
89. Viey, E., Lucas, C., Romagne, F., Escudier, B., Chouaib, S. & Caignard, A. (2008) Chemokine receptors expression and migration potential of tumor-infiltrating and peripheral-expanded Vgamma9Vdelta2 T cells from renal cell carcinoma patients. Journal of Immunotherapy, 31, 313-323.
90. Vivier, E., Raulet, D.H., Moretta, A., Caligiuri, M.A., Zitvogel, L., Lanier, L.L., Yokoyama, W.M. & Ugolini, S. (2011) Innate or adaptive immunity? The example of natural killer cells. Science, 331, 44-49.
91. Wilhelm, M., Kunzmann, V., Eckstein, S., Reimer, P., Weissinger, F., Ruediger, T. & Tony, H.P. (2003) Gammadelta T cells for immune therapy of patients with lymphoid malignancies. Blood, 102, 200-206.
92. Zhang, R., Zheng, X., Li, B., Wei, H. & Tian, Z. (2006) Human NK cells positively regulate gammadelta T cells in response to Mycobacterium tuberculosis. Journal of Immunology, 176, 2610-2616.
93. Zheng, B.J., Ng, S.P., Chua, D.T., Sham, J.S., Kwong, D.L., Lam, C.K. & Ng, M.H. (2002) Peripheral gamma delta T-cell deficit in nasopharyngeal carcinoma. International Journal of Cancer, 99, 213-217.