1,746
Views
36
CrossRef citations to date
0
Altmetric
Original Research

Zoledronate can induce colorectal cancer microenvironment expressing BTN3A1 to stimulate effector γδ T cells with antitumor activity

, , ORCID Icon, , , , ORCID Icon, , , , & show all
Article: e1278099 | Received 16 Aug 2016, Accepted 24 Dec 2016, Published online: 30 Mar 2017

References

  • Hayday AC. Gammadelta T cells and the lymphoid stress-surveillance response. Immunity 2009; 31(2):184-96; PMID:19699170; http://dx.doi.org/10.1016/j.immuni.2009.08.006
  • Bonneville M, O'Brien RL, Born WK. Gammadelta T cell effector functions: a blend of innate programming and acquired plasticity. Nat Rev Immunol 2010; 10(7):467-78; PMID:20539306; http://dx.doi.org/10.1038/nri2781
  • Poggi A, Zocchi MR. γδ T lymphocytes as a first line of immune defense: Old and new ways of antigen recognition and implications for cancer immunotherapy. Front Immunol 2014; 5:575; PMID:25426121; http://dx.doi.org/10.3389/fimmu.2014.00575. eCollection 2014; http://www.jem.org/cgi/doi/10.1084/jem.20021500
  • Gober HJ, Kistowska M, Angman L, Jenö P, Mori L, De Libero G. Human T cell receptor gammadelta cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med 2003; 197(2):163-8; PMID:12538656; http://www.jem.org/cgi/doi/10.1084/jem.20021500
  • Wang H, Sarikonda G, Puan KJ, Tanaka Y, Feng J, Giner JL, Cao R, Mönkkönen J, Oldfield E, Morita CT. Indirect stimulation of human Vγ2Vδ2 T cells through alterations in isoprenoid metabolism. J Immunol 2011; 187(10):5099-113; PMID:22013129; http://dx.doi.org/10.4049/jimmunol.1002697
  • Kabelitz D, Kalyan S, Oberg HH, Wesch D. Human Vδ2 versus non-Vδ2 γδ T cells in anti-tumor immunity. Oncoimmunology 2013; 2(3):e23304; PMID:23802074; http://dx.doi.org/10.4161/onci.23304
  • Corvaisier M, Moreau-Aubry A, Diez E, Bennouna J, Scotet E, Bonneville M, Jotereau F. Vgamma9 Vdelta2 T cell response to colon carcinoma cells. J Immunol 2005; 175(8):5481-8; PMID:16210656; http://doi.org/10.4049/jimmunol.175.8.5481
  • Bhat J, Kabelitz D. γδT cells and epigenetic drugs: A useful merger in cancer immunotherapy? Oncoimmunology 2015; 4(6):e1006088. eCollection 2015 Jun; PMID:26155411; http://dx.doi.org/10.1080/2162402X.2015.1006088
  • Tanaka Y, Kobayashi H, Terasaki T, Toma H, Aruga A, Uchiyama T, Mizutani K, Mikami B, Morita CT, Minato N. Synthesis of pyrophosphate-containing compounds that stimulate Vgamma2 Vdekta2 T cells: application to cancer immunotherapy. Med Chem 2007; 3(1):85-99; PMID:17266628; http://dx.doi.org/10.2174/157340607779317544
  • Burjanadzé M, Condomines M, Reme T, Quittet P, Latry P, Lugagne C, Romagne F, Morel Y, Rossi JF, Klein B et al. In vitro expansion of gammadelta T cells with anti-myeloma cells activity by Phosphostim and IL-2 in patients with multiple myeloma. Br J Haematol 2007; 139(2):206-16; PMID:17897296; http://dx.doi.org/10.1111/j.1365-2141.2007.06754.x
  • 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 bromohydrinpyrophosphate (BrHPP, IPH 1101) a Vgamma9 Vdelta2 T lymphocyte agonist in patients with solid tumors. Cancer Immunol Immunother 2010; 59(10):1521-30; PMID:20563721; http://dx.doi.org/10.1007/s00262-010-0879-0
  • Capietto AH, Martinet L, Cendron D, Fruchon S, Pont F, Fournié JJ. Phophoantigens overcome human TCRVgamma9+ gammadelta T cell immunosuppression by TGF-beta: relevance for cancer immunotherapy. J Immunol 2010; 184(12):6680-7; PMID:20483742; http://dx.doi.org/10.4049/jimmunol.1000681
  • Russell RG. Bisphosphonates: the first 40 years. Bone 2011; 49(1):2-19; PMID:21555003; http://dx.doi.org/10.1016/j.bone.2011.04.022
  • Das H, Wang L, Kamath A, Bukowski JF. Vgamma2Vdelta2 T-cell receptor-mediated recognition of aminobisphosphonates. Blood 2001; 98(5):1616-8; PMID:11520816; http://doi.org/10.1182/blood.V98.5.1616
  • Kunzmann V, Bauer E, Feurle J, Weissinger F, Tony HP, Wilhelm M. Stimulation of gammadelta T cells by aminobisphosphonates and induction of antiplasmacell activity in multiple myeloma. Blood 2000; 96(2):384-92; PMID:10887096
  • Dieli F, Gebbia N, Poccia F, Caccamo N, Montesano C, Fulfaro F, Arcara C, Valerio MR, Meraviglia S, Di Sano C et al. Induction of gammadelta T-lymphocyte effector functions by bisphosphonate zoledronic acid in cancer patients in vivo. Blood 2003; 102(6):2310-1; PMID:12959943; http://dx.doi.org/10.1182/blood-2003-05-1655
  • Santini D, Vespasiani Gentilucci U, Vincenzi B, Picardi A, Vasaturo F, La Cesa A, Onori N, Scarpa S, Tonini G. The antineoplastic role of bisphosphonates: from basic research to clinical evidence. Ann Oncol 2003; 14(10):1468-76; PMID:14504045
  • Clézardin P, Fournier P, Boissier S, Peyruchaud O. In vitro and in vivo anti-tumor effects of bisphopshonates. Curr Med Chem 2003; 10(2):173-80; PMID:12570716; http://dx.doi.org/10.2174/0929867033368529
  • Märten A, Lilienfeld-Toal MV, Büchler MW, Schmidt J. 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 2007; 30(4):370-7; PMID:17457212; http://dx.doi.org/10.1097/CJI.0b013e31802bff16
  • Todaro M, D'Asaro M, Caccamo N, Iovino F, Francipane MG, Meraviglia S, Orlando V, La Mendola C, Gulotta G, Salerno A et al. Efficient killing of human colon cancer stem cells by gammadelta T lymphocytes. J Immunol 2009; 182(11):7287-96; PMID:19454726; http://dx.doi.org/10.4049/jimmunol.0804288
  • Lang JM, Kaikobad MR, Wallace M, Staab MJ, Horvath DL, Wilding G, Liu G, Eickhoff JC, McNeel DG, Malkovsky M. Pilot trial of interleukin-2 and zoledronic acid to augment γδ T cells as treatment for patients with refractory renal cell carcinoma. Cancer Immunol Immunother 2011; 60(10):1447-60; PMID:21647691; http://dx.doi.org/10.1007/s00262-011-1049-8
  • Sakamoto M, Nakajima J, Murakawa T, Fukami T, Yoshida Y, Murayama T, Takamoto S, Matsushita H, Kakimi K. Adoptive immunotherapy for advanced non-small cell lung cancer using zoledronate-expanded γδT cells: a phase I clinical study. J Immunother 2011; 34(2):202-11; PMID:21304399; http://dx.doi.org/10.1097/CJI.0b013e318207ecfb
  • Meraviglia S, Eberl M, Vermijlen D, Todaro M, Buccheri S, Cicero G, La Mendola C, Guggino G, D'Asaro M, Orlando V 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(2):290-7; PMID:20491785; http://dx.doi.org/10.1111/j.1365-2249.2010.04167.x
  • Dieli F, Vermijlen D, Fulfaro F, Caccamo N, Meraviglia S, Cicero G, Roberts A, Buccheri S, D'Asaro M, Gebbia N et al. Targeting human gammadelta T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res 2007; 67(15):7450-7; PMID:17671215; http://dx.doi.org/10.1158/0008-5472.CAN-07-0199
  • Harly C, Guillaume Y, Nedellec S, Peigné CM, Mönkkönen H, Mönkkönen 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 γδ T-cell subset. Blood 2012; 120(11):2269-79; PMID:22767497; http://dx.doi.org/10.1182/blood-2012-05-430470
  • Palakodeti A, Sandstrom A, Sundaresan L, Harly C, Nedellec S, Olive D, Scotet E, Bonneville M, Adams EJ. The molecular basis for modulation of human Vγ9Vδ2 T cell responses by CD277/butyrophilin-3 (BTN3A)-specific antibodies. J Biol Chem 2012; 287(39):32780-90; PMID:22846996; http://dx.doi.org/10.1074/jbc.M112.384354
  • Arnett HA, Viney JL. Immune modulation by butyrophilins. Nat Rev Immunol 2014; 14(8):559-69; PMID:25060581; http://dx.doi.org/10.1038/nri3715
  • Kabelitz D. Critical role of butyrophilin 3A1 in presenting prenyl pyrophosphate antigens to human γδT cells. Cell Mol Immunol 2014; 11(2):117-9; PMID:24097034; http://dx.doi.org/10.1038/cmi.2013.50
  • Vavassori S, Kumar A, Wan GS, Ramanjaneyulu GS, Cavallari M, El Daker S, Beddoe T, Theodossis A, Williams NK, Gostick E et al. Butyrophilin 3A1 binds phosphorylated antigens and stimulates human γδ T cells. Nat Immunol 2013; 14(9):908-16; PMID:23872678; http://dx.doi.org/10.1038/ni.2665
  • Wang H, Henry O, Distefano MD, Wang YC, Räikkönen J, Mönkkönen J, Tanaka Y, Morita CT. Butyrophilin 3A1 plays an essential role in prenyl pyrophosphate stimulation of human Vγ2Vδ2 T cells. J Immunol 2013; 191(3):1029-42; PMID:23833237; http://dx.doi.org/10.4049/jimmunol.1300658
  • Sandstrom A, Peigné CM, Léger 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 Vγ9Vδ2 T cells. Immunity 2014; 40(4):490-500; PMID:24703779; http://dx.doi.org/10.1016/j.immuni.2014.03.003
  • Rhodes DA, Chen H-C, Price AJ, Keeble AH, Davey MS, James LC, Eberl M, Trowsdale J. Activation of human γδT cells by cytosolic interactions of BTN3A1 with soluble phosphoantigens and the cytoskeletal adaptor periplakin. J Immunol 2015:194(5):2390-2398; PMID:25637025; http://dx.doi.org/10.4049/Jimmunol.1401064
  • Sebestyen Z, Scheper W, Vyborova A, Gu S, Rychnavska Z, Schiffler M, Cleven A, Chéneau C, van Noorden M, Peigné CM et al. RhoB mediates phosphoantigen recognition by Vγ9Vδ2 T cell receptor. Cell Rep 2016; 15(9):1973-85; PMID:27210746; http://dx.doi.org/10.1016/j.celrep2016.04.081
  • Idrees ASM, Sugie T, Inoue C, Murata-Hirai K, Okamura H,Morita CT, Minato M, Toi M, Tanaka Y. Comparison of γδ T cell responsesand farnesyl diphosphate synthase inhibition in tunor cells pretreated with zoledronic acid. Cancer Sci 2013; 104(5):536-542; PMID:23387443; http://dx.doi.org/10.1111/cas.12124
  • Dieli F, Poccia F, Lipp M, Sireci G, Caccamo N, Di Sano C, Salerno A. Differentiation of effector/memory Vdelta2 T cells and migratory routes in lymph nodes or inflammatory sites. J ExpMed 2003; 198(3):391-397; PMID:12900516; http://dx.doi.org/10.1084/jem.20030235
  • Musso A, Catellani S, Canevali P, Tavella S, Venè R, Boero S, Pierri I, Gobbi M, Kunkl A, Ravetti JL et al. Aminobisphosphonate prevent the inhibitory effect exerted by lymph node stromal cells on anti-tumor Vδ2 T lymphocytes in non-Hodgkin lymphomas. Haematologica 2014; 99(1):131-9; PMID:24162786; http://dx.doi.org/10.3324/haematol.2013.097311
  • Arnett HA, Escobar SS, Gonzalez-Suarez E, Budelsky AL, Steffen LA, Boiani N, Zhang M, Siu G, Brewer AW, Viney JL. BTNL2, a butyrophilin/B7-like molecule, is a negative costimulatory molecule modulated in intestinal inflammation. J. Immunol 2007; 178(3):1523-33; PMID:17237401; http://doi.org/10.4049/jimmunol.178.3.1523
  • Jauhiainen M, Monkkonen H, Raikkonen J, Monkkonen J, Auriola S. Analysis of endogenous ATP analogs and mevalonate pathway mebolites in cancer cell cultures using liquid chromatography-electrospray ionization mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 2009; 877(27):2967-75; PMID:19665949; http://dx.doi.org/10.1016/j.jchromb.2009.07.010
  • Bouet-Toussaint F, Cabillic F, Toutirais O, Le Gallo M, Thomas de la Pintière C, Genetet N, Meunier B, Dupont-Bierre E, Boudjema K et al. Vγ9Vδ2 T cell-mediated recognition of human solid tumor. Potential for immunotherapy of hepatocellular and colorectal carcinomas. Cancer Immunol Immunother 2008; 57(4):531.539; PMID:17764010; http://dx.doi.org/10.1007/s00262-007-0391-3
  • Musso A, Zocchi MR, Poggi A. Relevance of the mevalonate biosynthetic pathway in the regulation of bone marrow mesenchymal stromal cell-mediated effects on T-cell proliferation and B-cell survival. Haematologica 2011; 96(1):16-23; PMID:20884711; http://dx.doi.org/10.3324/haematol.2010.031633
  • Fiore F, Castella B, Nuschak B, Bertieri R, Mariani S, Bruno B, Pantaleoni F, Foglietta M, Boccadoro M, Massaia M. Enhanced ability of dendritic cells to stimulate innate and adaptive immunity on short-term incubation with zoledronic acid. Blood 2007; 110(3):921-7; PMID:17403919; http://dx.doi.org/10.1182/blood-2006-09-044321
  • Zocchi MR, Camodeca C, Nuti E, Rossello A, Venè R, Tosetti F, Dapino I, Costa D, Musso A, Poggi A. ADAM10 new selective inhibitors reduce NKG2D ligand release sensitizing Hodgkin lymphoma cells to NKG2D-mediated killing. Oncoimmunol 2016; 5:5, e1123367; PMID:27467923; http://dx.doi.org/10.1080/2162402X.2015.1123367

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.