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Research Article

PD-1 checkpoint blockade enhances adoptive immunotherapy by human Vγ2Vδ2 T cells against human prostate cancer

, , , & ORCID Icon
Article: 1989789 | Received 29 Mar 2021, Accepted 03 Oct 2021, Published online: 25 Oct 2021

References

  • Rast JP, Anderson MK, Strong SJ, Luer C, Litman RT, Litman GW. α, β, γ, and δ T cell antigen receptor genes arose early in vertebrate phylogeny. Immunity. 1997;6(1):1–17. doi:10.1016/s1074-7613(00)80237-x.
  • Morita CT, Mariuzza RA, Brenner MB. Antigen recognition by human γδ T cells: pattern recognition by the adaptive immune system. Springer Semin Immunopathol. 2000;22(3):191–217. doi:10.1007/s002810000042.
  • Morita CT, Jin C, Sarikonda G, Wang H. Nonpeptide antigens, presentation mechanisms, and immunological memory of human Vγ2Vδ2 T cells: discriminating friend from foe through the recognition of prenyl pyrophosphate antigens. Immunol Rev. 2007;215(1):59–76. doi:10.1111/j.1600-065X.2006.00479.x.
  • Tanaka Y, Morita CT, Tanaka Y, Nieves E, Brenner MB, Bloom BR. Natural and synthetic non-peptide antigens recognized by human γδ T cells. Nature. 1995;375(6527):155–158. doi:10.1038/375155a0.
  • Sandstrom A, Peigné C-M, Léger A, Crooks JE, Konczak F, Gesnel M-C, 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. doi:10.1016/j.immuni.2014.03.003.
  • Wang H, Morita CT. Sensor function for butyrophilin 3A1 in prenyl pyrophosphate stimulation of human Vγ2Vδ2 T cells. J Immunol. 2015;195(10):4583–4594. doi:10.4049/jimmunol.1500314.
  • Karunakaran MM, Willcox CR, Salim M, Paletta D, Fichtner AS, Noll A, Starick L, Nöhren A, Begley CR, Berwick KA, et al. Butyrophilin-2A1 directly binds germline-encoded regions of the Vγ9Vδ2 TCR and is essential for phosphoantigen sensing. Immunity. 2020;52(3):487–498 e6. doi:10.1016/j.immuni.2020.02.014.
  • Rigau M, Ostrouska S, Fulford TS, Johnson DN, Woods K, Ruan Z, McWilliam HEG, Hudson C, Tutuka C, Wheatley AK, et al. Butyrophilin 2A1 is essential for phosphoantigen reactivity by γδ T cells. Science. 2020;367(6478) :eaay5516. doi:10.1126/science.aay5516.
  • Tanaka Y, Iwasaki M, Murata-Hirai K, Matsumoto K, Hayashi K, Okamura H, Sugie T, Minato N, Morita CT, Toi M. Anti-tumor activity and immunotherapeutic potential of a bisphosphonate prodrug. Sci Rep. 2017;7(1):5987. doi:10.1038/s41598-017-05553-0.
  • Wang H, Sarikonda G, Puan K-J, Tanaka Y, Feng J, Giner J-L, 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):5099–5113. doi:10.4049/jimmunol.1002697.
  • Fisch P, Malkovsky M, Kovats S, Sturm E, Braakman E, Klein BS, Voss SD, Morrissey LW, DeMars R, Welch WJ, et al. Recognition by human Vγ9/Vδ2 T cells of a GroEL homolog on Daudi Burkitt’s lymphoma cells. Science. 1990;250(4985):1269–1273. doi:10.1126/science.1978758.
  • Bukowski JF, Morita CT, Tanaka Y, Bloom BR, Brenner MB, Band H. Vγ2Vδ2 TCR-dependent recognition of non-peptide antigens and Daudi cells analyzed by TCR gene transfer. J Immunol. 1995;154:998–1006.
  • Zheng B, Lam C, Im S, Huang J, Luk W, Lau SY, Yau KK, Wong C, Yao K, Ng MH. Distinct tumour specificity and IL-7 requirements of CD56− and CD56+ subsets of human γδ T cells. Scand J Immunol. 2001;53(1):40–48. doi:10.1046/j.1365-3083.2001.00827.x.
  • Harly C, Guillaume Y, Nedellec S, Peigné C-M, 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):2269–2279. doi:10.1182/blood-2012-05-430470.
  • Cano CE, Pasero C, De Gassart A, Kerneur C, Gabriac M, Fullana M, Granarolo E, Hoet R, Scotet E, Rafia C, et al. BTN2A1, an immune checkpoint targeting Vγ9Vδ2 T cell cytotoxicity against malignant cells. Cell Rep. 2021;36(2):109359. doi:10.1016/j.celrep.2021.109359.
  • Gober H-J, Kistowska M, Angman L, Jenö P, Mori L, De Libero G. Human T cell receptor γδ cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med. 2003;197(2):163–168. doi:10.1084/jem.20021500.
  • Li J, Herold MJ, Kimmel B, Müller I, Rincon-Orozco B, Kunzmann V, Herrmann T. Reduced expression of the mevalonate pathway enzyme farnesyl pyrophosphate synthase unveils recognition of tumor cells by Vγ9Vδ2 T cells. J Immunol. 2009;182(12):8118–8124. doi:10.4049/jimmunol.0900101.
  • Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, Nair VS, Xu Y, Khuong A, Hoang CD, et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med. 2015;21(8):938–945. doi:10.1038/nm.3909.
  • Vella M, Coniglio D, Abrate A, Scalici Gesolfo C, Lo Presti E, Meraviglia S, Serretta V, Simonato A. Characterization of human infiltrating and circulating gamma-delta T cells in prostate cancer. Investig Clin Urol. 2019;60(2):91–98. doi:10.4111/icu.2019.60.2.91.
  • Bennouna J, Bompas E, Neidhardt EM, Rolland F, Philip I, Galea C, Salot S, Saiagh S, Audrain M, Rimbert M, et al. Phase-I study of Innacell γδ, an autologous cell-therapy product highly enriched in γ9δ2 T lymphocytes, in combination with IL-2, in patients with metastatic renal cell carcinoma. Cancer Immunol Immunother. 2008;57(11):1599–1609. doi:10.1007/s00262-008-0491-8.
  • 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 Vγ9γδ T-cell-based immunotherapy for patients with multiple myeloma. Exp Hematol. 2009;37(8):956–968. doi:10.1016/j.exphem.2009.04.008.
  • 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. Br J Cancer. 2011;105(6):778–786. doi:10.1038/bjc.2011.293.
  • Kobayashi H, Tanaka Y, Yagi J, Minato N, Tanabe K. Phase I/II study of adoptive transfer of γδ T cells in combination with zoledronic acid and IL-2 to patients with advanced renal cell carcinoma. Cancer Immunol Immunother. 2011;60(8):1075–1084. doi:10.1007/s00262-011-1021-7.
  • 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):202–211. doi:10.1097/CJI.0b013e318207ecfb.
  • Noguchi A, Kaneko T, Kamigaki T, Fujimoto K, Ozawa M, Saito M, Ariyoshi N, Goto S. Zoledronate-activated Vγ9γδ T cell-based immunotherapy is feasible and restores the impairment of γδ T cells in patients with solid tumors. Cytotherapy. 2011;13(1):92–97. doi:10.3109/14653249.2010.515581.
  • Izumi T, Kondo M, Takahashi T, Fujieda N, Kondo A, Tamura N, Murakawa T, Nakajima J, Matsushita H, Kakimi K. Ex vivo characterization of γδ T-cell repertoire in patients after adoptive transfer of Vγ9Vδ2 T cells expressing the interleukin-2 receptor β-chain and the common γ-chain. Cytotherapy. 2013;15(4):481–491. doi:10.1016/j.jcyt.2012.12.004.
  • Wada I, Matsushita H, Noji S, Mori K, Yamashita H, Nomura S, Shimizu N, Seto Y, Kakimi K. Intraperitoneal injection of in vitro expanded Vγ9Vδ2 T cells together with zoledronate for the treatment of malignant ascites due to gastric cancer. Cancer Med. 2014;3(2):362–375. doi:10.1002/cam4.196.
  • Okawaki M, Hironaka K, Yamanura M, Yamaguchi Y. Adoptive immunotherapy using autologous lymphocytes activated ex vivo with antigen stimulation for patients with incurable cancer. Kawasaki Med J. 2014;40(1):33–39. doi:10.11482/-E40(1)33.
  • Yamaguchi Y, Katata Y, Okawaki M, Sawaki A, Yamamura M. A prospective observational study of adoptive immunotherapy for cancer using zoledronate-activated killer (ZAK) cells - an analysis for patients with incurable pancreatic cancer. Anticancer Res. 2016;36:2307–2313.
  • Aoki T, Matsushita H, Hoshikawa M, Hasegawa K, Kokudo N, Kakimi K. Adjuvant combination therapy with gemcitabine and autologous γδ T-cell transfer in patients with curatively resected pancreatic cancer. Cytotherapy. 2017;19(4):473–485. doi:10.1016/j.jcyt.2017.01.002.
  • Alnaggar M, Xu Y, Li J, He J, Chen J, Li M, Wu Q, Lin L, Liang Y, Wang X, et al. Allogenic Vγ9Vδ2 T cell as new potential immunotherapy drug for solid tumor: a case study for cholangiocarcinoma. J Immunother Cancer. 2019;7(1):36. doi:10.1186/s40425-019-0501-8.
  • Xu Y, Xiang Z, Alnaggar M, Kouakanou L, Li J, He J, Yang J, Hu Y, Chen Y, Lin L, et al. Allogeneic Vγ9Vδ2 T-cell immunotherapy exhibits promising clinical safety and prolongs the survival of patients with late-stage lung or liver cancer. Cell Mol Immunol. 2020;18(2):427–439. doi:10.1038/s41423-020-0515-7.
  • Kakimi K, Matsushita H, Masuzawa K, Karasaki T, Kobayashi Y, Nagaoka K, Hosoi A, Ikemura S, Kitano K, Kawada I, et al. Adoptive transfer of zoledronate-expanded autologous Vγ9Vδ2 T-cells in patients with treatment-refractory non-small-cell lung cancer: a multicenter, open-label, single-arm, phase 2 study. J Immunother Cancer. 2020;8(2):e001185. doi:10.1136/jitc-2020-001185.
  • Sato Y, Mori K, Hirano K, Yagi K, Kobayashi Y, Nagaoka K, Hosoi A, Matsushita H, Kakimi K, Seto Y. Adoptive γδT-cell transfer alone or combined with chemotherapy for the treatment of advanced esophageal cancer. Cytotherapy. 2021;23(5):423–432. doi:10.1016/j.jcyt.2021.02.002.
  • Kobayashi H, Tanaka Y, Shimmura H, Minato N, Tanabe K. Complete remission of lung metastasis following adoptive immunotherapy using activated autologous γδ T-cells in a patient with renal cell carcinoma. Anticancer Res. 2010;30(2):575–579.
  • Sharma P, Hu-Lieskovan S, Wargo JA, Ribas A. Primary, adaptive, and acquired resistance to cancer immunotherapy. Cell. 2017;168(4):707–723. doi:10.1016/j.cell.2017.01.017.
  • Andrews LP, Yano H, Vignali DAA. Inhibitory receptors and ligands beyond PD-1, PD-L1 and CTLA-4: breakthroughs or backups. Nat Immunol. 2019;20(11):1425–1434. doi:10.1038/s41590-019-0512-0.
  • Chihara N, Madi A, Kondo T, Zhang H, Acharya N, Singer M, Nyman J, Marjanovic ND, Kowalczyk MS, Wang C, et al. Induction and transcriptional regulation of the co-inhibitory gene module in T cells. Nature. 2018;558(7710):454–459. doi:10.1038/s41586-018-0206-z.
  • Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515(7528):568–571. doi:10.1038/nature13954.
  • Wherry EJ. T cell exhaustion. Nat Immunol. 2010;12(6):492–499. doi:10.1038/ni.2035.
  • Legat A, Speiser DE, Pircher H, Zehn D, Fuertes Marraco SA. Inhibitory receptor expression depends more dominantly on differentiation and activation than “exhaustion” of human CD8 T cells. Front Immunol. 2013;4(455). doi:10.3389/fimmu.2013.00455.
  • Grosser R, Cherkassky L, Chintala N, Adusumilli PS. Combination immunotherapy with CAR T cells and checkpoint blockade for the treatment of solid tumors. Cancer Cell. 2019;36(5):471–482. doi:10.1016/j.ccell.2019.09.006.
  • Gevensleben H, Dietrich D, Golletz C, Steiner S, Jung M, Thiesler T, Majores M, Stein J, Uhl B, Müller S, et al. The immune checkpoint regulator PD-L1 is highly expressed in aggressive primary prostate cancer. Clin Cancer Res. 2015;22(8):1969–1977. doi:10.1158/1078-0432.CCR-15-2042.
  • Schepisi G, Cursano MC, Casadei C, Menna C, Altavilla A, Lolli C, Cerchione C, Paganelli G, Santini D, Tonini G, et al. CAR-T cell therapy: a potential new strategy against prostate cancer. J Immunother Cancer. 2019;7(1):258. doi:10.1186/s40425-019-0741-7.
  • Nada MH, Wang H, Workalemahu G, Tanaka Y, Morita CT. Enhancing adoptive cancer immunotherapy with Vγ2Vδ2 T cells through pulse zoledronate stimulation. J Immunother Cancer. 2017;5(1):9. doi:10.1186/s40425-017-0209-6.
  • Santolaria T, Robard M, Léger A, Catros V, Bonneville M, Scotet E. Repeated systemic administrations of both aminobisphosphonates and human Vγ9Vδ2 T cells efficiently control tumor development in vivo. J Immunol. 2013;191(4):1993–2000. doi:10.4049/jimmunol.1300255.
  • Foreman O, Kavirayani AM, Griffey SM, Reader R, Shultz LD. Opportunistic bacterial infections in breeding colonies of the NSG mouse strain. Vet Pathol. 2011;48(2):495–499. doi:10.1177/0300985810378282.
  • Tanaka Y, Murata-Hirai K, Iwasaki M, Matsumoto K, Hayashi K, Kumagai A, Nada MH, Wang H, Kobayashi H, Kamitakahara H, et al. Expansion of human γδ T cells for adoptive immunotherapy using a bisphosphonate prodrug. Cancer Sci. 2018;109(3):587–599. doi:10.1111/cas.13491.
  • Klebanoff CA, Gattinoni L, Palmer DC, Muranski P, Ji Y, Hinrichs CS, Borman ZA, Kerkar SP, Scott CD, Finkelstein SE, et al. Determinants of successful CD8+ T-cell adoptive immunotherapy for large established tumors in mice. Clin Cancer Res. 2011;17(16):5343–5352. doi:10.1158/1078-0432.CCR-11-0503.
  • Iwasaki M, Tanaka Y, Kobayashi H, Murata-Hirai K, Miyabe H, Sugie T, Toi M, Minato N. Expression and function of PD-1 in human γδ T cells that recognize phosphoantigens. Eur J Immunol. 2011;41(2):345–355. doi:10.1002/eji.201040959.
  • Hsu H, Boudova S, Mvula G, Divala TH, Mungwira RG, Harman C, Laufer MK, Pauza CD, Cairo C. Prolonged PD1 expression on neonatal Vδ2 lymphocytes dampens proinflammatory responses: role of epigenetic regulation. J Immunol. 2016;197(5):1884–1892. doi:10.4049/jimmunol.1600284.
  • Zumwalde NA, Sharma A, Xu X, Ma S, Schneider CL, Romero-Masters JC, Hudson AW, Gendron-Fitzpatrick A, Kenney SC, Gumperz JE. Adoptively transferred Vγ9Vδ2 T cells show potent antitumor effects in a preclinical B cell lymphomagenesis model. JCI Insight. 2017;2(13):e93179. doi:10.1172/jci.insight.93179.
  • Carlsson B, Forsberg O, Bengtsson M, Tötterman TH, Essand M. Characterization of human prostate and breast cancer cell lines for experimental T cell-based immunotherapy. Prostate. 2007;67(4):389–395. doi:10.1002/pros.20498.
  • Sabatos-Peyton CA, Nevin J, Brock A, Venable JD, Tan DJ, Kassam N, Xu F, Taraszka J, Wesemann L, Pertel T, et al. Blockade of Tim-3 binding to phosphatidylserine and CEACAM1 is a shared feature of anti-Tim-3 antibodies that have functional efficacy. Oncoimmunology. 2018;7(2):e1385690. doi:10.1080/2162402X.2017.1385690.
  • DeKruyff RH, Bu X, Ballesteros A, Santiago C, Chim Y-LE, Lee H-H, Karisola P, Pichavant M, Kaplan GG, Umetsu DT, et al. T cell/transmembrane, Ig, and mucin-3 allelic variants differentially recognize phosphatidylserine and mediate phagocytosis of apoptotic cells. J Immunol. 2010;184(4):1918–1930. doi:10.4049/jimmunol.0903059.
  • Morita CT, Parker CM, Brenner MB, Band H. TCR usage and functional capabilities of human γδ T cells at birth. J Immunol. 1994;153(9):3979–3988.
  • Kato Y, Tanaka Y, Hayashi M, Okawa K, Minato N. Involvement of CD166 in the activation of human γδ T cells by tumor cells sensitized with nonpeptide antigens. J Immunol. 2006;177(2):877–884. doi:10.4049/jimmunol.177.2.877.
  • Das H, Groh V, Kuijl C, Sugita M, Morita CT, Spies T, Bukowski JF. MICA engagement by human Vγ2Vδ2 T cells enhances their antigen-dependent effector function. Immunity. 2001;15(1):83–93. doi:10.1016/s1074-7613(01)00168-6.
  • Rincon-Orozco B, Kunzmann V, Wrobel P, Kabelitz D, Steinle A, Herrmann T. Activation of Vγ9Vδ2 T Cells by NKG2D. J Immunol. 2005;175(4):2144–2151. doi:10.4049/jimmunol.175.4.2144.
  • Boissonnas A, Fetler L, Zeelenberg IS, Hugues S, Amigorena S. In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J Exp Med. 2007;204(2):345–356. doi:10.1084/jem.20061890.
  • Kabelitz D, Bender A, Schondelmaier S, da Silva Lobo ML, Janssen O. Human cytotoxic lymphocytes. V. Frequency and specificity of γδ+ cytotoxic lymphocyte precursors activated by allogeneic or autologous stimulator cells. J Immunol. 1990;145:2827–2832.
  • Li R, Johnson R, Yu G, McKenna DH, Hubel A. Preservation of cell-based immunotherapies for clinical trials. Cytotherapy. 2019;21(9):943–957. doi:10.1016/j.jcyt.2019.07.004.
  • Worsham DN, Reems J-A, Szczepiorkowski ZM, McKenna DH, Leemhuis T, Mathew AJ, Cancelas JA. Clinical methods of cryopreservation for donor lymphocyte infusions vary in their ability to preserve functional T-cell subpopulations. Transfusion (Paris). 2017;57(6):1555–1565. doi:10.1111/trf.14112.
  • Panch SR, Srivastava SK, Elavia N, McManus A, Liu S, Jin P, Highfill SL, Li X, Dagur P, Kochenderfer JN, et al. Effect of cryopreservation on autologous chimeric antigen receptor T cell characteristics. Mol Ther. 2019;27(7):1275–1285. doi:10.1016/j.ymthe.2019.05.015.
  • Xu H, Cao W, Huang L, Xiao M, Cao Y, Zhao L, Wang N, Zhou J. Effects of cryopreservation on chimeric antigen receptor T cell functions. Cryobiology. 2018;83:40–47. doi:10.1016/j.cryobiol.2018.06.007.
  • Garfall AL, Maus MV, Hwang WT, Lacey SF, Mahnke YD, Melenhorst JJ, Zheng Z, Vogl DT, Cohen AD, Weiss BM, et al. Chimeric antigen receptor T cells against CD19 for multiple myeloma. N Engl J Med. 2015;373(11):1040–1047. doi:10.1056/NEJMoa1504542.
  • Burnham RE, Tope D, Branella G, Williams E, Doering CB, Spencer HT. Human serum albumin and chromatin condensation rescue ex vivo expanded γδ T cells from the effects of cryopreservation. Cryobiology. 2021;99:78–87. doi:10.1016/j.cryobiol.2021.01.011.
  • Mimura K, Teh JL, Okayama H, Shiraishi K, Kua L-F, Koh V, Smoot DT, Ashktorab H, Oike T, Suzuki Y, et al. PD-L1 expression is mainly regulated by interferon gamma associated with JAK-STAT pathway in gastric cancer. Cancer Sci. 2017;109(1):43–53. doi:10.1111/cas.13424.
  • Garcia-Diaz A, Shin DS, Moreno BH, Saco J, Escuin-Ordinas H, Rodriguez GA, Zaretsky JM, Sun L, Hugo W, Wang X, et al. Interferon receptor signaling pathways regulating PD-L1 and PD-L2 expression. Cell Rep. 2017;19(6):1189–1201. doi:10.1016/j.celrep.2017.04.031.
  • Abiko K, Matsumura N, Hamanishi J, Horikawa N, Murakami R, Yamaguchi K, Yoshioka Y, Baba T, Konishi I, Mandai M. IFN-γ from lymphocytes induces PD-L1 expression and promotes progression of ovarian cancer. Br J Cancer. 2015;112(9):1501–1509. doi:10.1038/bjc.2015.101.
  • Chen S, Crabill GA, Pritchard TS, McMiller TL, Wei P, Pardoll DM, Pan F, Topalian SL. Mechanisms regulating PD-L1 expression on tumor and immune cells. J Immunother Cancer. 2019;7(1):305. doi:10.1186/s40425-019-0770-2.
  • Hoeres T, Holzmann E, Smetak M, Birkmann J, Wilhelm M. PD-1 signaling modulates interferon-γ production by Gamma Delta (γδ) T-Cells in response to leukemia. Oncoimmunology. 2019;8(3):1550618. doi:10.1080/2162402x.2018.1550618.
  • Hsu H, Boudova S, Mvula G, Divala TH, Rach D, Mungwira RG, Boldrin F, Degiacomi G, Manganelli R, Laufer MK, et al. Age-related changes in PD-1 expression coincide with increased cytotoxic potential in Vδ2 T cells during infancy. Cell Immunol. 2021;359:104244. doi:10.1016/j.cellimm.2020.104244.
  • Fuertes Marraco SA, Neubert NJ, Verdeil G, Speiser DE. Inhibitory receptors beyond T cell exhaustion. Front Immunol. 2015;6:310. doi:10.3389/fimmu.2015.00310.
  • DeLong JH, O’Hara Hall A, Rausch M, Moodley D, Perry J, Park J, Phan AT, Beiting DP, Kedl RM, Hill JA, et al. IL-27 and TCR stimulation promote T cell expression of multiple inhibitory receptors. Immunohorizons. 2019;3(1):13–25. doi:10.4049/immunohorizons.1800083.
  • Castella B, Foglietta M, Sciancalepore P, Rigoni M, Coscia M, Griggio V, Vitale C, Ferracini R, Saraci E, Omede P, et al. Anergic bone marrow Vγ9Vδ2 T cells as early and long-lasting markers of PD-1-targetable microenvironment-induced immune suppression in human myeloma. Oncoimmunology. 2015;4(11):e1047580. doi:10.1080/2162402X.2015.1047580.
  • Gestermann N, Saugy D, Martignier C, Tillé L, Fuertes Marraco SA, Zettl M, Tirapu I, Speiser DE, Verdeil G. LAG-3 and PD-1+LAG-3 inhibition promote anti-tumor immune responses in human autologous melanoma/T cell co-cultures. Oncoimmunology. 2020;9(1):1736792. doi:10.1080/2162402X.2020.1736792.
  • Rossi C, Gravelle P, Decaup E, Bordenave J, Poupot M, Tosolini M, Franchini D-M, Laurent C, Morin R, Lagarde J-M, et al. Boosting γδ T cell-mediated antibody-dependent cellular cytotoxicity by PD-1 blockade in follicular lymphoma. Oncoimmunology. 2019;8(3):1554175. doi:10.1080/2162402X.2018.1554175.
  • Kaighn ME, Narayan KS, Ohnuki Y, Lechner JF, Jones LW. Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol. 1979;17(1):16–23.
  • Tai S, Sun Y, Squires JM, Zhang H, Oh WK, Liang CZ, Huang J. PC3 is a cell line characteristic of prostatic small cell carcinoma. Prostate. 2011;71(15):1668–1679. doi:10.1002/pros.21383.
  • Wang J, Liu X, Wang Y, Ren G. Current trend of worsening prognosis of prostate small cell carcinoma: a population-based study. Cancer Med. 2019;8(15):6799–6806. doi:10.1002/cam4.2551.
  • Aggarwal R, Huang J, Alumkal JJ, Zhang L, Feng FY, Thomas GV, Weinstein AS, Friedl V, Zhang C, Witte ON, et al. Clinical and genomic characterization of treatment-emergent small-cell neuroendocrine prostate cancer: a multi-institutional prospective study. J Clin Oncol. 2018;36(24):2492–2503. doi:10.1200/JCO.2017.77.6880.
  • Venkatachalam S, McFarland TR, Agarwal N, Swami U. Immune checkpoint inhibitors in prostate cancer. Cancers (Basel). 2021;13(9):2187. doi:10.3390/cancers13092187.
  • Stultz J, Fong L. How to turn up the heat on the cold immune microenvironment of metastatic prostate cancer. Prostate Cancer Prostatic Dis. 2021;24(3):697–717. doi:10.1038/s41391-021-00340-5.
  • de Almeida DVP, Fong L, Rettig MB, Autio KA. Immune checkpoint blockade for prostate cancer: niche role or next breakthrough? Am Soc Clin Oncol Educ Book. 2020;40:e89-e106. doi:10.1200/EDBK_278853.
  • Sena LA, Fountain J, Isaacsson Velho P, Lim SJ, Wang H, Nizialek E, Rathi N, Nussenzveig R, Maughan BL, Velez MG, et al. Tumor frameshift mutation proportion predicts response to immunotherapy in mismatch repair-deficient prostate cancer. The Oncologist. 2021;26(2):e270–e278. doi:10.1002/onco.13601.
  • Ritch E, Fu SYF, Herberts C, Wang G, Warner EW, Schonlau E, Taavitsainen S, Murtha AJ, Vandekerkhove G, Beja K, et al. Identification of hypermutation and defective mismatch repair in ctDNA from metastatic prostate cancer. Clin Cancer Res. 2020;26(5):1114–1125. doi:10.1158/1078-0432.CCR-19-1623.
  • Abida W, Cheng ML, Armenia J, Middha S, Autio KA Vargas HA, Rathkopf D, Morris MJ, Danila DC, Slovin SF, et al. Analysis of the prevalence of microsatellite instability in prostate cancer and response to immune checkpoint blockade. JAMA Oncol. 2019;5(4):471–478. doi:10.1001/jamaoncol.2018.5801.
  • Moon EK, Ranganathan R, Eruslanov E, Kim S, Newick K, O’Brien S, Lo A, Liu X, Zhao Y, Albelda SM. Blockade of programmed death 1 augments the ability of human T cells engineered to target NY-ESO-1 to control tumor growth after adoptive transfer. Clin Cancer Res. 2016;22(2):436–447. doi:10.1158/1078-0432.CCR-15-1070.
  • Serganova I, Moroz E, Cohen I, Moroz M, Mane M, Zurita J, Shenker L, Ponomarev V, Blasberg R. Enhancement of PSMA-directed CAR adoptive immunotherapy by PD-1/PD-L1 blockade. Mol Ther Oncolytics. 2017;4:41–54. doi:10.1016/j.omto.2016.11.005.
  • John LB, Devaud C, Duong CP, Yong CS, Beavis PA, Haynes NM, Chow MT, Smyth MJ, Kershaw MH, Darcy PK. Anti-PD-1 antibody therapy potently enhances the eradication of established tumors by gene-modified T cells. Clin Cancer Res. 2013;19(20):5636–5646. doi:10.1158/1078-0432.CCR-13-0458.
  • Hu Z, Xia J, Fan W, Wargo J, Yang Y-G. Human melanoma immunotherapy using tumor antigen-specific T cells generated in humanized mice. Oncotarget. 2016;7(6):6448–6459. doi:10.18632/oncotarget.7044.
  • Rupp LJ, Schumann K, Roybal KT, Gate RE, Ye CJ, Lim WA, Marson A. CRISPR/Cas9-mediated PD-1 disruption enhances anti-tumor efficacy of human chimeric antigen receptor T cells. Sci Rep. 2017;7(1):737. doi:10.1038/s41598-017-00462-8.
  • Cherkassky L, Morello A, Villena-Vargas J, Feng Y, Dimitrov DS, Jones DR, Sadelain M, Adusumilli PS. Human CAR T cells with cell-intrinsic PD-1 checkpoint blockade resist tumor-mediated inhibition. J Clin Invest. 2016;126(8):3130–3144. doi:10.1172/JCI83092.
  • McGowan E, Lin Q, Ma G, Yin H, Chen S, Lin Y. PD-1 disrupted CAR-T cells in the treatment of solid tumors: promises and challenges. Biomed Pharmacother. 2020;121:109625. doi:10.1016/j.biopha.2019.109625.
  • Zacharakis N, Chinnasamy H, Black M, Xu H, Lu YC, Zheng Z, Pasetto A, Langhan M, Shelton T, Prickett T, et al. Immune recognition of somatic mutations leading to complete durable regression in metastatic breast cancer. Nat Med. 2018;24(6):724–730. doi:10.1038/s41591-018-0040-8.
  • Creelan BC, Wang C, Teer JK, Toloza EM, Yao J, Kim S, Landin AM, Mullinax JE, Saller JJ, Saltos AN, et al. Tumor-infiltrating lymphocyte treatment for anti-PD-1-resistant metastatic lung cancer: a phase 1 trial. Nat Med. 2021;27(8):1410–1418. doi:10.1038/s41591-021-01462-y.
  • Guo Q, Zhao P, Zhang Z, Zhang J, Zhang Z, Hua Y, Han B, Li N, Zhao X, Hou L. TIM-3 blockade combined with bispecific antibody MT110 enhances the anti-tumor effect of γδ T cells. Cancer Immunol Immunother. 2020;69(12):2571–2587. doi:10.1007/s00262-020-02638-0.
  • Anderson AC, Joller N, Kuchroo VK. Lag-3, Tim-3, and TIGIT: co-inhibitory receptors with specialized functions in immune regulation. Immunity. 2016;44(5):989–1004. doi:10.1016/j.immuni.2016.05.001.