Low dose gemcitabine increases the cytotoxicity of human Vγ9Vδ2 T cells in bladder cancer cells in vitro and in an orthotopic xenograft model

References

• Ghasemzadeh A, Bivalacqua TJ, Hahn NM, Drake CG. New Strategies in Bladder Cancer: A Second Coming for Immunotherapy. Clin Cancer Res. 2016;22:793–801. doi:10.1158/1078-0432.CCR-15-1135.
   PubMed Web of Science ®Google Scholar
• Barocas DA, Globe DR, Colayco DC, Onyenwenyi A, Bruno AS, Bramley TJ, Spear RJ. Surveillance and treatment of non-muscle-invasive bladder cancer in the USA. Advances in urology. 2012;2012:421709. doi:10.1155/2012/421709.
   PubMedGoogle Scholar
• Morales A, Eidinger D, Bruce AW. Intracavitary Bacillus Calmette-Guerin in the Treatment of Superficial Bladder Tumors. The Journal of urology. 2017;197:S142–s5. doi:10.1016/j.juro.2016.10.101.
   PubMed Web of Science ®Google Scholar
• Sylvester RJ. Bacillus Calmette-Guerin treatment of non-muscle invasive bladder cancer. International journal of urology: official journal of the Japanese Urological Association. 2011;18:113–20. doi:10.1111/j.1442-2042.2010.02678.x.
   PubMed Web of Science ®Google Scholar
• Zlotta AR, Fleshner NE, Jewett MA. The management of BCG failure in non-muscle-invasive bladder cancer: an update. Canadian Urological Association journal = Journal de l'Association des urologues du Canada. 2009;3:S199–205. doi:10.5489/cuaj.1196.
   PubMedGoogle Scholar
• Herr HW, Dalbagni G. Defining bacillus Calmette-Guerin refractory superficial bladder tumors. The Journal of urology. 2003;169:1706–8. doi:10.1097/01.ju.0000062605.92268.c6.
   PubMed Web of Science ®Google Scholar
• Kunzmann V, Bauer E, Wilhelm M. Gamma/delta T-cell stimulation by pamidronate. The New England journal of medicine. 1999;340:737–8. doi:10.1056/NEJM199903043400914.
   PubMed Web of Science ®Google Scholar
• Kunzmann V, Bauer E, Feurle J, Weissinger F, Tony HP, Wilhelm M. Stimulation of gammadelta T cells by aminobisphosphonates and induction of antiplasma cell activity in multiple myeloma. Blood. 2000;96:384–92.
   PubMed Web of Science ®Google Scholar
• Wilhelm M, Kunzmann V, Eckstein S, Reimer P, Weissinger F, Ruediger T, Tony HP. Gammadelta T cells for immune therapy of patients with lymphoid malignancies. Blood. 2003;102:200–6. doi:10.1182/blood-2002-12-3665.
   PubMed Web of Science ®Google Scholar
• Bonneville M, O'Brien RL, Born WK. Gammadelta T cell effector functions: A blend of innate programming and acquired plasticity. Nature reviews Immunology. 2010;10:467–78. doi:10.1038/nri2781.
   PubMed Web of Science ®Google Scholar
• Vantourout P, Hayday A. Six-of-the-best: unique contributions of gammadelta T cells to immunology. Nature reviews Immunology. 2013;13:88–100. doi:10.1038/nri3384.
   PubMed Web of Science ®Google Scholar
• Van Acker HH, Anguille S, Van Tendeloo VF, Lion E. Empowering gamma delta T cells with antitumor immunity by dendritic cell-based immunotherapy. Oncoimmunology. 2015;4:e1021538. doi:10.1080/2162402X.2015.1021538.
   PubMed Web of Science ®Google Scholar
• Rei M, Pennington DJ, Silva-Santos B. The emerging Protumor role of gammadelta T lymphocytes: implications for cancer immunotherapy. Cancer Res. 2015;75:798–802. doi:10.1158/0008-5472.CAN-14-3228.
   PubMed Web of Science ®Google Scholar
• Sandstrom A, Peigne CM, Leger A, Crooks JE, Konczak F, Gesnel MC, Breathnach R, Bonneville M, Scotet E, Adams EJ. The intracellular B30.2 domain of butyrophilin 3A1 binds phosphoantigens to mediate activation of human Vgamma9Vdelta2 T cells. Immunity. 2014;40:490–500. doi:10.1016/j.immuni.2014.03.003.
   PubMed Web of Science ®Google Scholar
• Hayday AC. Gammadelta T cells and the lymphoid stress-surveillance response. Immunity. 2009;31:184–96. doi:10.1016/j.immuni.2009.08.006.
   PubMed Web of Science ®Google Scholar
• Fisher JP, Flutter B, Wesemann F, Frosch J, Rossig C, Gustafsson K, Anderson J. Effective combination treatment of GD2-expressing neuroblastoma and Ewing's sarcoma using anti-GD2 ch14.18/CHO antibody with Vgamma9Vdelta2+ gammadeltaT cells. Oncoimmunology. 2016;5:e1025194. doi:10.1080/2162402X.2015.1025194.
   PubMed Web of Science ®Google Scholar
• Uchida R, Ashihara E, Sato K, Kimura S, Kuroda J, Takeuchi M, Kawata E, Taniguchi K, Okamoto M, Shimura K, et al. Gamma delta T cells kill myeloma cells by sensing mevalonate metabolites and ICAM-1 molecules on cell surface. Biochem Biophys Res Commun. 2007;354:613–8. doi:10.1016/j.bbrc.2007.01.031.
   PubMed Web of Science ®Google Scholar
• Ashihara E, Munaka T, Kimura S, Nakagawa S, Nakagawa Y, Kanai M, Hirai H, Abe H, Miida T, Yamato S, et al. Isopentenyl pyrophosphate secreted from Zoledronate-stimulated myeloma cells, activates the chemotaxis of gammadeltaT cells. Biochem Biophys Res Commun. 2015;463:650–5. doi:10.1016/j.bbrc.2015.05.118.
   PubMed Web of Science ®Google Scholar
• Chen G, Emens LA. Chemoimmunotherapy: Reengineering tumor immunity. Cancer Immunol Immunother. 2013;62:203–16 doi:10.1007/s00262-012-1388-0.
   PubMed Web of Science ®Google Scholar
• Green DR, Ferguson T, Zitvogel L, Kroemer G. Immunogenic and tolerogenic cell death. Nature reviews Immunology. 2009;9:353–63 doi:10.1038/nri2545.
   PubMed Web of Science ®Google Scholar
• Mattarollo SR, Kenna T, Nieda M, Nicol AJ. Chemotherapy and zoledronate sensitize solid tumour cells to Vgamma9Vdelta2 T cell cytotoxicity. Cancer Immunol Immunother. 2007;56:1285–97. doi:10.1007/s00262-007-0279-2.
   PubMed Web of Science ®Google Scholar
• Kabelitz D, Wesch D, He W. Perspectives of gammadelta T cells in tumor immunology. Cancer Res. 2007;67:5–8. doi:10.1158/0008-5472.CAN-06-3069.
   PubMed Web of Science ®Google Scholar
• Stresing V, Daubine F, Benzaid I, Monkkonen H, Clezardin P. Bisphosphonates in cancer therapy. Cancer Lett. 2007;257:16–35. doi:10.1016/j.canlet.2007.07.007.
   PubMed Web of Science ®Google Scholar
• Sato K, Kimura S, Segawa H, Yokota A, Matsumoto S, Kuroda J, Nogawa M, Yuasa T, Kiyono Y, Wada H, et al. Cytotoxic effects of gammadelta T cells expanded ex vivo by a third generation bisphosphonate for cancer immunotherapy. Int J Cancer. 2005;116:94–9. doi:10.1002/ijc.20987.
   PubMed Web of Science ®Google Scholar
• Chitadze G, Lettau M, Luecke S, Wang T, Janssen O, Furst D, Mytilineos J, Wesch D, Oberg HH, Held-Feindt J, et al. NKG2D- and T-cell receptor-dependent lysis of malignant glioma cell lines by human gammadelta T cells: Modulation by temozolomide and A disintegrin and metalloproteases 10 and 17 inhibitors. Oncoimmunology. 2016;5:e1093276. doi:10.1080/2162402X.2015.1093276.
   PubMed Web of Science ®Google Scholar
• Gruenbacher G, Nussbaumer O, Gander H, Steiner B, Leonhartsberger N, Thurnher M. Stress-related and homeostatic cytokines regulate Vgamma9Vdelta2 T-cell surveillance of mevalonate metabolism. Oncoimmunology. 2014;3:e953410. doi:10.4161/21624011.2014.953410.
   PubMed Web of Science ®Google Scholar
• Habu S, Fukui H, Shimamura K, Kasai M, Nagai Y, Okumura K, Tamaoki N. In vivo effects of anti-asialo GM1. I. Reduction of NK activity and enhancement of transplanted tumor growth in nude mice. Journal of immunology (Baltimore, Md: 1950). 1981;127:34–8.
   PubMed Web of Science ®Google Scholar
• Deniger DC, Moyes JS, Cooper LJ. Clinical applications of gamma delta T cells with multivalent immunity. Frontiers in immunology. 2014;5:636. doi:10.3389/fimmu.2014.00636.
   PubMed Web of Science ®Google Scholar
• Buccheri S, Guggino G, Caccamo N, Li Donni P, Dieli F. Efficacy and safety of gammadeltaT cell-based tumor immunotherapy: A meta-analysis. Journal of biological regulators and homeostatic agents. 2014;28:81–90.
   PubMed Web of Science ®Google Scholar
• Harly C, Guillaume Y, Nedellec S, Peigne CM, Monkkonen H, Monkkonen J, Li J, Kuball J, Adams EJ, Netzer S, et al. Key implication of CD277/butyrophilin-3 (BTN3A) in cellular stress sensing by a major human gammadelta T-cell subset. Blood. 2012;120:2269–79. doi:10.1182/blood-2012-05-430470.
   PubMed Web of Science ®Google Scholar
• Wang H, Henry O, Distefano MD, Wang YC, Raikkonen J, Monkkonen J, Tanaka Y, Morita CT. Butyrophilin 3A1 plays an essential role in prenyl pyrophosphate stimulation of human Vgamma2Vdelta2 T cells. Journal of immunology (Baltimore, Md: 1950). 2013;191:1029–42. doi:10.4049/jimmunol.1300658.
   PubMed Web of Science ®Google Scholar
• Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, Spies T. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science (New York, NY). 1999;285:727–9. doi:10.1126/science.285.5428.727.
   Google Scholar
• Nedellec S, Sabourin C, Bonneville M, Scotet E. 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. Journal of immunology (Baltimore, Md: 1950). 2010;185:55–63. doi:10.4049/jimmunol.1000373.
   PubMed Web of Science ®Google Scholar
• Rincon-Orozco B, Kunzmann V, Wrobel P, Kabelitz D, Steinle A, Herrmann T. Activation of V 9V 2 T Cells by NKG2D. The Journal of Immunology. 2005;175:2144–51. doi:10.4049/jimmunol.175.4.2144.
   PubMed Web of Science ®Google Scholar
• Wrobel P, Shojaei H, Schittek B, Gieseler F, Wollenberg B, Kalthoff H, Kabelitz D, Wesch D. Lysis of a broad range of epithelial tumour cells by human gamma delta T cells: involvement of NKG2D ligands and T-cell receptor- versus NKG2D-dependent recognition. Scand J Immunol. 2007;66:320–8. doi:10.1111/j.1365-3083.2007.01963.x.
   PubMed Web of Science ®Google Scholar
• Cerwenka A, Baron JL, Lanier LL. Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proceedings of the National Academy of Sciences of the United States of America. 2001;98:11521–6. doi:10.1073/pnas.201238598.
   PubMed Web of Science ®Google Scholar
• Waldhauer I, Steinle A. NK cells and cancer immunosurveillance. Oncogene. 2008;27:5932–43. doi:10.1038/onc.2008.267.
   PubMed Web of Science ®Google Scholar
• Gasser S, Raulet D. The DNA damage response, immunity and cancer. Seminars in cancer biology. 2006;16:344–7. doi:10.1016/j.semcancer.2006.07.004.
   PubMed Web of Science ®Google Scholar
• Krieg S, Ullrich E. Novel immune modulators used in hematology: Impact on NK cells. Frontiers in immunology. 2012;3:388.
   PubMed Web of Science ®Google Scholar
• Todaro M, Orlando V, Cicero G, Caccamo N, Meraviglia S, Stassi G, Dieli F. Chemotherapy sensitizes colon cancer initiating cells to Vgamma9Vdelta2 T cell-mediated cytotoxicity. PloS one. 2013;8:e65145. doi:10.1371/journal.pone.0065145.
   PubMed Web of Science ®Google Scholar
• Todaro M, Meraviglia S, Caccamo N, Stassi G, Dieli F. Combining conventional chemotherapy and gammadelta T cell-based immunotherapy to target cancer-initiating cells. Oncoimmunology. 2013; 2:e25821. doi:10.4161/onci.25821.
   PubMed Web of Science ®Google Scholar
• Raulet DH. Roles of the NKG2D immunoreceptor and its ligands. Nature reviews Immunology. 2003;3:781–90. doi:10.1038/nri1199.
   PubMed Web of Science ®Google Scholar
• Chiappinelli KB, Zahnow CA, Ahuja N, Baylin SB. Combining Epigenetic and Immunotherapy to Combat Cancer. Cancer Res. 2016;76:1683–9. doi:10.1158/0008-5472.CAN-15-2125.
   PubMed Web of Science ®Google Scholar
• Huang B, Sikorski R, Sampath P, Thorne SH. Modulation of NKG2D-ligand cell surface expression enhances immune cell therapy of cancer. J Immunother. 2011;34:289–96. doi:10.1097/CJI.0b013e31820e1b0d.
   PubMed Web of Science ®Google Scholar
• Skov S, Pedersen MT, Andresen L, Straten PT, Woetmann A, Odum N. Cancer cells become susceptible to natural killer cell killing after exposure to histone deacetylase inhibitors due to glycogen synthase kinase-3-dependent expression of MHC class I-related chain A and B. Cancer Res. 2005;65:11136–45. doi:10.1158/0008-5472.CAN-05-0599.
   PubMed Web of Science ®Google Scholar
• Yuasa T, Sato K, Ashihara E, Takeuchi M, Maita S, Tsuchiya N, Habuchi T, Maekawa T, Kimura S. Intravesical administration of gammadelta T cells successfully prevents the growth of bladder cancer in the murine model. Cancer Immunol Immunother. 2009;58:493–502. doi:10.1007/s00262-008-0571-9.
   PubMed Web of Science ®Google Scholar
• Kobayashi H, Tanaka Y, Yagi J, Minato N, Tanabe K. 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. doi:10.1007/s00262-011-1021-7.
   PubMed Web of Science ®Google Scholar
• Bennouna J, Levy V, Sicard H, Senellart H, Audrain M, Hiret S, Rolland F, Bruzzoni-Giovanelli H, Rimbert M, Galéa C, 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. doi:10.1007/s00262-010-0879-0.
   PubMed Web of Science ®Google Scholar
• Abe Y, Muto M, Nieda M, Nakagawa Y, Nicol A, Kaneko T, Goto S, Yokokawa K, Suzuki K. Clinical and immunological evaluation of zoledronate-activated Vgamma9gammadelta T-cell-based immunotherapy for patients with multiple myeloma. Experimental hematology. 2009;37:956–68. doi:10.1016/j.exphem.2009.04.008.
   PubMed Web of Science ®Google Scholar
• Nakajima J, Murakawa T, Fukami T, Goto S, Kaneko T, Yoshida Y, Takamoto S, Kakimi K. A phase I study of adoptive immunotherapy for recurrent non-small-cell lung cancer patients with autologous gammadelta T cells. European journal of cardio-thoracic surgery: official journal of the European Association for Cardio-thoracic Surgery. 2010;37:1191–7. doi:10.1016/j.ejcts.2009.11.051.
   PubMed Web of Science ®Google Scholar
• Nicol AJ, Tokuyama H, Mattarollo SR, Hagi T, Suzuki K, Yokokawa K, Nieda M. Clinical evaluation of autologous gamma delta T cell-based immunotherapy for metastatic solid tumours. British journal of cancer. 2011;105:778–86. doi:10.1038/bjc.2011.293.
   PubMed Web of Science ®Google Scholar