Combining inhibition of immune checkpoints and PARP: rationale and perspectives in cancer treatment

References

• Duffy MJ, Crown J. Biomarkers for predicting response to immunotherapy with immune checkpoint inhibitors in cancer patients. Clin Chem. 2019;65(10):1228–1238.
   PubMed Web of Science ®Google Scholar
• Yap TA, Parkes EE, Peng W, et al. Development of immunotherapy combination strategies in cancer. Cancer Discov. 2021;11(6):1368–1397.
   PubMed Web of Science ®Google Scholar
• Cortesi L, Rugo HS, Jackisch C. An overview of PARP inhibitors for the treatment of breast cancer. Target Oncol. 2021;16(3):255–282.
   PubMed Web of Science ®Google Scholar
• Armstrong DK Use of PARP inhibitors for ovarian cancer. In Proceedings of the JNCCN Journal of the National Comprehensive Cancer Network; Harborside Press, 2021; Vol. 19, pp. 636–638.
   Google Scholar
• Hammel P, Zhang C, Matile J, et al. PARP inhibition in treatment of pancreatic cancer. Expert Rev Anticancer Ther. 2020;20(11):939–945.
   PubMed Web of Science ®Google Scholar
• Nizialek E, Antonarakis ES. PARP inhibitors in metastatic prostate cancer: evidence to date. Cancer Manag Res. 2020;12:8105–8114.
   PubMed Web of Science ®Google Scholar
• Pilié PG, Gay CM, Byers LA, et al. PARP inhibitors: extending benefit beyond BRCA -mutant cancers. Clin Cancer Res. 2019;25(13):3759–3771.
   PubMed Web of Science ®Google Scholar
• Li Z, Pearlman AH, Hsieh P. DNA mismatch repair and the DNA damage response. DNA Repair (Amst). 2016;38:94–101.
   PubMed Web of Science ®Google Scholar
• Friedberg EC. DNA damage and repair. Nature. 2003;421(6921):436–440.
   PubMed Web of Science ®Google Scholar
• Pećina-Šlaus N, Kafka A, Salamon I, et al. Mismatch repair pathway, genome stability and cancer. Front Mol Biosci. 2020;7:122.
   PubMed Web of Science ®Google Scholar
• de la Chapelle A. Microsatellite instability. N Engl J Med. 2003;349(3):209–210.
   PubMed Web of Science ®Google Scholar
• MSS and MSI profiles using the pentaplex panel. (A) MSS profile of the … Download Scientific Diagram. [cited Apr 15, 2022]. Available from: https://www.researchgate.net/figure/MSS-and-MSI-profiles-using-the-pentaplex-panel-A-MSS-profile-of-the-five-consensus_fig2_336583432
   Google Scholar
• Shia J. Immunohistochemistry versus microsatellite instability testing for screening colorectal cancer patients at risk for hereditary nonpolyposis colorectal cancer syndrome: part I. The utility of immunohistochemistry. The Journal of Molecular Diagnostics. 2008;10(4):293–300.
   PubMed Web of Science ®Google Scholar
• Baudrin LG, Deleuze JF, How-Kit A. Molecular and computational methods for the detection of microsatellite instability in cancer. Front Oncol. 2018;8:621.
   PubMed Web of Science ®Google Scholar
• Bonneville R, Krook MA, Kautto EA, et al. Landscape of microsatellite instability across 39 cancer types. JCO Precis Oncol. 2017;2017(1):1–15.
   Google Scholar
• Wright WD, Shah SS, Heyer WD. Homologous recombination and the repair of DNA double-strand breaks. J Biol Chem. 2018;293(27):10524–10535.
   PubMed Web of Science ®Google Scholar
• Petrucelli N, Daly MB, Pal T. BRCA1- and BRCA2-associated hereditary breast and ovarian cancer. Seattle: University of Washington; 1993.
   Google Scholar
• Johnson ML, Cho BC, Luft A, et al. Durvalumab with or without tremelimumab in combination with chemotherapy as first-line therapy for metastatic non–small-cell lung cancer: the Phase III POSEIDON Study. J clin oncol. 2022. DOI:10.1200/jco.22.00975.
   Google Scholar
• Homologous recombination deficiency | target ovarian cancer. [cited Apr 15, 2022]. Available from: https://targetovariancancer.org.uk/about-ovarian-cancer/hereditary-ovarian-cancer/homologous-recombination-deficiency
   Google Scholar
• Javle M, Curtin NJ. The role of PARP in DNA repair and its therapeutic exploitation. Br J Cancer. 2011;105(8):1114–1122.
   PubMed Web of Science ®Google Scholar
• Rose M, Burgess JT, O’Byrne K, et al. PARP inhibitors: clinical relevance, mechanisms of action and tumor resistance. Front Cell Dev Biol. 2020;8:879.
   Web of Science ®Google Scholar
• Keung M, Wu Y, Vadgama J. PARP inhibitors as a therapeutic agent for homologous recombination deficiency in breast cancers. J Clin Med. 2019;8(435):435.
   PubMedGoogle Scholar
• Yi T, Feng Y, Sundaram R, et al. Antitumor efficacy of PARP inhibitors in homologous recombination deficient carcinomas. Int J Cancer. 2019;145(5):1209–1220.
   PubMed Web of Science ®Google Scholar
• Jackson SP. Sensing and repairing DNA double-strand breaks. Carcinogenesis. 2002;23(5):687–696.
   PubMed Web of Science ®Google Scholar
• Min A, Im S-A. PARP inhibitors as therapeutics: beyond modulation of parylation. Cancers (Basel). 2020;12(394):394.
   PubMedGoogle Scholar
• Golan T, Hammel P, Reni M, et al. Maintenance olaparib for germline BRCA -mutated metastatic pancreatic cancer. N Engl J Med. 2019;381(4):317–327.
   PubMed Web of Science ®Google Scholar
• McCabe N, Turner NC, Lord CJ, et al. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to Poly(ADP-Ribose) polymerase inhibition. Cancer Res. 2006;66(16):8109–8115.
   PubMed Web of Science ®Google Scholar
• Murai J, Huang SYN, Das BB, et al. Trapping of PARP1 and PARP2 by clinical PARP inhibitors. Cancer Res. 2012;72(21):5588–5599.
   PubMed Web of Science ®Google Scholar
• Lord CJ, Ashworth A. BRCAness revisited. Nat Rev Cancer. 2016;16(2):110–120.
   PubMed Web of Science ®Google Scholar
• Revythis A, Limbu A, Mikropoulos C, et al. Recent insights into PARP and immuno-checkpoint inhibitors in epithelial ovarian cancer. Int J Environ Res Public Health. 2022 Jul;19(14):8577.
   Google Scholar
• Peyraud F, Italiano A. Combined parp inhibition and immune checkpoint therapy in solid tumors. Cancers (Basel). 2020;12(6):1–28.
   Web of Science ®Google Scholar
• Brown JS, Sundar R, Lopez J. Combining DNA damaging therapeutics with immunotherapy: more haste, less speed. Br J Cancer. 2018;118(3):312–324.
   PubMed Web of Science ®Google Scholar
• Hsiehchen D, Hsieh A, Samstein RM, et al. DNA repair gene mutations as predictors of immune checkpoint inhibitor response beyond tumor mutation burden. Cell Reports Medicine. 2020;1. DOI:10.1016/j.xcrm.2020.100034
   Google Scholar
• Budczies J, Kluck K, Beck S, et al. Homologous recombination deficiency is inversely correlated with microsatellite instability and identifies immunologically cold tumors in most cancer types. J Pathology: Clin Res. 2022;8. doi:10.1002/cjp2.271
   Google Scholar
• Teo MY, Seier K, Ostrovnaya I, et al. Alterations in DNA damage response and repair genes as potential marker of clinical benefit from PD-1/PD-L1 blockade in advanced urothelial cancers. J clin oncol. 2018;36(17):1685–1694.
   PubMed Web of Science ®Google Scholar
• Willis JA, Reyes-Uribe L, Chang K, et al. Immune activation in mismatch repair–deficient carcinogenesis: more than just mutational rate. Clin Cancer Res. 2020;26(1):11–17.
   PubMed Web of Science ®Google Scholar
• Boland CR, Goel A. Microsatellite instability in colorectal cancer. Gastroenterology. 2010;138(6):2073.
   PubMed Web of Science ®Google Scholar
• Zhao P, Li L, Jiang X, et al. Mismatch repair deficiency/microsatellite instability-high as a predictor for anti-PD-1/PD-L1 immunotherapy efficacy. J Hematol Oncol. 2019;12(1):12.
   PubMedGoogle Scholar
• Sun W, Zhang Q, Wang R, et al. Targeting DNA damage Repair for immune checkpoint inhibition: mechanisms and potential clinical applications. Front Oncol. 2021;11:648687.
   Web of Science ®Google Scholar
• Hamanishi J, Mandai M, Ikeda T, et al. Safety and antitumor activity of Anti–PD-1 antibody, nivolumab, in patients with platinum-resistant ovarian cancer. J clin oncol. 2015;33(34):4015–4022.
   PubMed Web of Science ®Google Scholar
• Hugo W, Zaretsky JM, Sun L, et al. Genomic and transcriptomic features of response to Anti-PD-1 therapy in metastatic melanoma. Cell. 2016;165(1):35–44.
   PubMed Web of Science ®Google Scholar
• Rayner E, Van Gool IC, Palles C, et al. A panoply of errors: polymerase proofreading domain mutations in cancer. Nat Rev Cancer. 2016;16(2):71–81.
   PubMed Web of Science ®Google Scholar
• Rizvi NA, Hellmann MD, Snyder A, et al. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 2015;348(6230):124–128.
   PubMed Web of Science ®Google Scholar
• Bouffet E, Larouche V, Campbell BB, et al. Immune checkpoint inhibition for hypermutant glioblastoma multiforme resulting from germline biallelic mismatch repair deficiency. J clin oncol. 2016;34(19):2206–2211.
   PubMed Web of Science ®Google Scholar
• Boussios S, Rassy E, Shah S, et al. Aberrations of DNA repair pathways in prostate cancer: a cornerstone of precision oncology. Expert Opin Ther Targets. 2021;25(5):329–333.
   PubMed Web of Science ®Google Scholar
• Basit A, Cho MG, Kim EY, et al. The cGAS/STING/TBK1/IRF3 innate immunity pathway maintains chromosomal stability through regulation of p21 levels. Exp Mol Med. 2020;52(4):643–657.
   PubMed Web of Science ®Google Scholar
• Ma Z, Damania B. The cGAS-STING defense pathway and its counteraction by viruses. Cell Host Microbe. 2016;19(2):150–158.
   PubMed Web of Science ®Google Scholar
• Corrales L, McWhirter SM, Dubensky TW, et al. The host STING pathway at the interface of cancer and immunity. J Clin Investig. 2016;126(7):2404–2411.
   PubMed Web of Science ®Google Scholar
• Zitvogel L, Galluzzi L, Kepp O, et al. Type I interferons in anticancer immunity. Nat Rev Immunol. 2015;15(7):405–414.
   PubMed Web of Science ®Google Scholar
• Olabisi OA, Soto-Nieves N, Nieves E, et al. Regulation of transcription factor NFAT by ADP-ribosylation. Mol Cell Biol. 2008;28(9):2860–2871.
   PubMed Web of Science ®Google Scholar
• Mulligan AM, Raitman I, Feeley L, et al. Tumoral lymphocytic infiltration and expression of the chemokine CXCL10 in breast cancers from the Ontario familial breast cancer registry. Clin Cancer Res. 2013;19(2):336–346.
   PubMed Web of Science ®Google Scholar
• Rosado MM, Bennici E, Novelli F, et al. Beyond DNA repair, the immunological role of PARP-1 and its siblings. Immunology. 2013;139(4):428–437.
   PubMed Web of Science ®Google Scholar
• Strickland KC, Howitt BE, Shukla SA, et al. Association and prognostic significance of BRCA1/2-mutation status with neoantigen load, number of tumor-infiltrating lymphocytes and expression of PD-1/PD-L1 in high grade serous ovarian cancer. Oncotarget. 2016;7(12):13587–13598.
   PubMedGoogle Scholar
• Nolan E, Savas P, Policheni AN, et al. Combined immune checkpoint blockade as a therapeutic strategy for BRCA1 -mutated breast cancer. Sci Transl Med. 2017;9(393):11.
   Web of Science ®Google Scholar
• Connor AA, Denroche RE, Jang GH, et al. Association of distinct mutational signatures with correlates of increased immune activity in pancreatic ductal adenocarcinoma. JAMA Oncol. 2017;3(6):774–783.
   PubMed Web of Science ®Google Scholar
• Green AR, Aleskandarany MA, Ali R, et al. Clinical impact of tumor DNA repair expression and T-cell infiltration in breast cancers. Cancer Immunol Res. 2017;5(4):292–299.
   PubMed Web of Science ®Google Scholar
• Ghosh C, Luong G, Sun Y. A snapshot of the PD-1/PD-L1 pathway. J Cancer. 2021;12(9):2735–2746.
   PubMed Web of Science ®Google Scholar
• Yarchoan M, Albacker LA, Hopkins AC, et al. PD-L1 expression and tumor mutational burden are independent biomarkers in most cancers. JCI Insight. 2019;4. DOI:10.1172/jci.insight.126908.
   Web of Science ®Google Scholar
• Sato H, Niimi A, Yasuhara T, et al. DNA double-strand break repair pathway regulates PD-L1 expression in cancer cells. Nat Commun. 2017;8(1):8.
   PubMedGoogle Scholar
• Van Allen EM, Miao D, Schilling B, et al. Genomic correlates of response to CTLA-4 blockade in metastatic melanoma. Science. 2015;350(6257):207–211.
   PubMed Web of Science ®Google Scholar
• Anagnostou V, Smith KN, Forde PM, et al. Evolution of neoantigen landscape during immune checkpoint blockade in non-small cell lung cancer. Cancer Discov. 2017;7(3):264–276.
   PubMed Web of Science ®Google Scholar
• Boussios S, Rassy E, Samartzis E, et al. Melanoma of unknown primary: new perspectives for an old story. Crit Rev Oncol Hematol. 2021 Feb;158:103208.
   Google Scholar
• Goel S, Decristo MJ, Watt AC, et al. CDK4/6 inhibition triggers anti-tumour immunity. Nature. 2017;548(7668):471–475.
   PubMed Web of Science ®Google Scholar
• Dean JL, McClendon AK, Knudsen ES. Modification of the DNA damage response by therapeutic CDK4/6 inhibition. J Biol Chem. 2012;287(34):29075–29087.
   PubMed Web of Science ®Google Scholar
• McAlpine JN, Porter H, Köbel M, et al. BRCA1 and BRCA2 mutations correlate with TP53 abnormalities and presence of immune cell infiltrates in ovarian high-grade serous carcinoma. Mod Pathol. 2012;25(5):740–750.
   PubMed Web of Science ®Google Scholar
• Liu H, Wang S, Xin J, et al. Role of NKG2D and its ligands in cancer immunotherapy. Am J Cancer Res. 2019;9(10):2064–2078.
   PubMed Web of Science ®Google Scholar
• Fenerty KE, Padget M, Wolfson B, et al. Immunotherapy utilizing the combination of natural killer- and antibody dependent cellular cytotoxicity (ADCC)-mediating agents with poly (ADP-ribose) polymerase (PARP) inhibition 11. Medical and Health Sciences 1112 Oncology and Carcinogenesis 11 Medical and Health Sciences 1107 Immunology. Journal for ImmunoTherapy of Cancer. 2018; 6. DOI:10.1186/s40425-018-0445-4.
   Google Scholar
• Fenerty KE, Padget M, Wolfson B, et al. Immunotherapy utilizing the combination of natural killer- and antibody dependent cellular cytotoxicity (ADCC)-mediating agents with poly (ADP-ribose) polymerase (PARP) inhibition 11. Medical and Health Sciences 1112 Oncology and Carcinogenesis 11 Medical and Health Sciences 1107 Immunology. J ImmunoTher Cancer. 2018;6:1–14. 10.1186/s40425-018-0445-4.
   PubMed Web of Science ®Google Scholar
• Martí JM, Garcia-Diaz A, Delgado-Bellido D, et al. Selective modulation by PARP-1 of HIF-1α-recruitment to chromatin during hypoxia is required for tumor adaptation to hypoxic conditions. Redox Biol. 2021;41:101885.
   PubMed Web of Science ®Google Scholar
• Fridman WH, Zitvogel L, Sautès-Fridman C, et al. The immune contexture in cancer prognosis and treatment. Nat Rev Clin Oncol. 2017;14(12):717–734.
   PubMed Web of Science ®Google Scholar
• Crusz SM, Balkwill FR. Inflammation and cancer: advances and new agents. Nat Rev Clin Oncol. 2015;12(10):584–596.
   PubMed Web of Science ®Google Scholar
• Stewart RA, Pilie PG, Yap TA. Development of PARP and immune-checkpoint inhibitor combinations. Cancer Res. 2018;78(24):6717–6725.
   PubMed Web of Science ®Google Scholar
• Wu Z, Cui P, Tao H, et al. The Synergistic Effect of PARP Inhibitors and Immune Checkpoint Inhibitors. Clin Med Insights Oncol. 2021;15:1179554921996288.
   Web of Science ®Google Scholar
• Jiao S, Xia W, Yamaguchi H, et al. PARP inhibitor upregulates PD-L1 expression and enhances cancer-associated immunosuppression. Clin Cancer Res. 2017;23(14):3711–3720.
   PubMed Web of Science ®Google Scholar
• Wang Z, Sun K, Xiao Y, et al. Niraparib activates interferon signaling and potentiates anti-PD-1 antibody efficacy in tumor models. Sci Rep. 2019;9(1):1–12.
   PubMed Web of Science ®Google Scholar
• Shen J, Zhao W, Ju Z, et al. PARPI triggers the STING-dependent immune response and enhances the therapeutic efficacy of immune checkpoint blockade independent of BRCANEss. Cancer Res. 2019;79(2):311–319.
   PubMed Web of Science ®Google Scholar
• Robillard L, Nguyen M, Loehr A, et al. Abstract 3650: preclinical evaluation of the PARP inhibitor rucaparib in combination with PD-1 and PD-L1 inhibition in a syngeneic BRCA1 mutant ovarian cancer model. American Association for Cancer Research (AACR) Annual Meeting 2017, Washington, D.C., USA; 2017. p. 3650.
   Google Scholar
• Higuchi T, Flies DB, Marjon NA, et al. CTLA-4 blockade synergizes therapeutically with PARP Inhibition in BRCA1-deficient ovarian cancer. Cancer Immunol Res. 2015;3(11):1257–1268.
   PubMed Web of Science ®Google Scholar
• Konstantinopoulos PA, Waggoner SE, Vidal GA, et al. TOPACIO/Keynote-162 (NCT02657889): a phase 1/2 study of niraparib + pembrolizumab in patients (pts) with advanced triple-negative breast cancer or recurrent ovarian cancer (ROC)—Results from ROC cohort. J clin oncol. 2018;36:106.
   Web of Science ®Google Scholar
• Yap TA, Konstantinopoulos P, Telli ML, et al. Abstract P1-19-03: JAVELIN PARP Medley, a phase 1b/2 study of avelumab plus talazoparib: results from advanced breast cancer cohorts. Cancer Res. 2020;80(4_Supplement): 1–19-03-P1-19–03.
   Web of Science ®Google Scholar
• Rodriguez-Moreno JF, de Velasco G, Bravo Fernandez I, et al. Impact of the combination of durvalumab (MEDI4736) plus olaparib (AZD2281) administered prior to surgery in the molecular profile of resectable urothelial bladder cancer: NEODURVARIB Trial. J clin oncol. 2020;38(6_suppl):542.
   Web of Science ®Google Scholar
• Ramalingam SS, Thara E, Awad MM, et al. JASPER: phase 2 trial of first-line niraparib plus pembrolizumab in patients with advanced non–small cell lung cancer. Cancer. 2022;128(1):65–74.
   PubMedGoogle Scholar
• Domchek SM, Postel-Vinay S, Im SA, et al. Olaparib and durvalumab in patients with germline BRCA-mutated metastatic breast cancer (MEDIOLA): an open-label, multicentre, phase 1/2, basket study. Lancet Oncol. 2020;21(9):1155–1164.
   PubMed Web of Science ®Google Scholar
• Färkkilä A, Gulhan DC, Casado J, et al. Immunogenomic profiling determines responses to combined PARP and PD-1 inhibition in ovarian cancer. Nat Commun. 2020;11(1):1–13.
   PubMed Web of Science ®Google Scholar
• Bang Y-J, Kaufman B, Geva R, et al. An open-label, phase II basket study of olaparib and durvalumab (MEDIOLA): results in patients with relapsed gastric cancer. J clin oncol. 2019;37(4_suppl):140.
   Web of Science ®Google Scholar
• Kamel D, Gray C, Walia JS, et al. PARP inhibitor drugs in the treatment of breast, ovarian, prostate and pancreatic cancers: an update of clinical trials. Curr Drug Targets. 2018;19(1). DOI:10.2174/1389450118666170711151518
   PubMed Web of Science ®Google Scholar
• Konstantinopoulos PA, Waggoner S, Vidal GA, et al. Single-Arm Phases 1 and 2 trial of niraparib in combination with pembrolizumab in patients with recurrent platinum-resistant ovarian carcinoma. JAMA Oncol. 2019;5(8):1141–1149.
   PubMed Web of Science ®Google Scholar
• Vinayak S, Tolaney SM, Schwartzberg LS, et al. TOPACIO/Keynote-162: niraparib + pembrolizumab in patients (pts) with metastatic triple-negative breast cancer (TNBC), a phase 2 trial. J clin oncol. 2018;36(15_suppl):1011.
   Google Scholar
• Yu EY, Massard C, Retz M, et al. Keynote-365 cohort a: pembrolizumab (pembro) plus olaparib in docetaxel-pretreated patients (pts) with metastatic castrate-resistant prostate cancer (mCRPC). J clin oncol. 2019;37(7_suppl):145.
   Web of Science ®Google Scholar
• Thomas A, Vilimas R, Trindade C, et al. Durvalumab in combination with olaparib in patients with relapsed SCLC: results from a Phase II study. J Thorac Oncol. 2019;14(8):1447–1457.
   PubMed Web of Science ®Google Scholar
• A Phase I/II Study of MEDI4736 in Combination With Olaparib in Patients With Advanced Solid Tumors. - Full Text View - CLINICALTRIALS.gov. [cited Apr 15, 2022]. Available from: https://clinicaltrials.gov/ct2/show/NCT02734004
   Google Scholar
• Domchek SM, Postel-Vinay S, Im SA, et al. Olaparib and durvalumab in patients with germline BRCA-mutated metastatic breast cancer (MEDIOLA): an open-label, multicentre, phase 1/2, basket study. Lancet Oncol. 2020;21(9):1155–1164.
   PubMed Web of Science ®Google Scholar
• Drew Y, Kaufman B, Banerjee S, et al. Phase II study of olaparib + durvalumab (MEDIOLA): updated results in germline BRCA-mutated platinum-sensitive relapsed (PSR) ovarian cancer (OC). Ann Oncol. 2019;30:v485–v486.
   Web of Science ®Google Scholar
• Krebs M, Ross K, Kim S, et al. P1.15-004 an open-label, multitumor phase II basket study of olaparib and durvalumab (MEDIOLA): results in patients with relapsed SCLC. J Thorac Oncol. 2017;12(11):S2044–S2045.
   Web of Science ®Google Scholar
• An open-label, phase II basket study of olaparib and durvalumab (MEDIOLA): results in patients with relapsed gastric cancer. Journal of Clinical Oncology. [cited Apr 15, 2022]. Available from: https://ascopubs.org/doi/abs/10.1200/JCO.2019.37.4_suppl.140
   Google Scholar
• Lee J-M, Annunziata CM, Houston N, et al. A phase II study of durvalumab, a PD-L1 inhibitor and olaparib in recurrent ovarian cancer (OvCa). Ann Oncol. 2018;29(viii334):viii334.
   Google Scholar
• Karzai F, Vanderweele D, Madan RA, et al. Activity of durvalumab plus olaparib in metastatic castration-resistant prostate cancer in men with and without DNA damage repair mutations 11 medical and health sciences 1112 oncology and carcinogenesis. J Immunother Cancer. 2018;6(1):6.
   PubMedGoogle Scholar
• Friedlander M, Meniawy T, Markman B, et al. A phase 1b study of the anti-PD-1 monoclonal antibody BGB-A317 (A317) in combination with the PARP inhibitor BGB-290 (290) in advanced solid tumors. J clin oncol. 2018;36(5_suppl):48.
   Web of Science ®Google Scholar
• Friedlander M, Meniawy T, Markman B, et al. Pamiparib in combination with tislelizumab in patients with advanced solid tumours: results from the dose-escalation stage of a multicentre, open-label, phase 1a/b trial. Lancet Oncol. 2019;20(9):1306–1315.
   PubMed Web of Science ®Google Scholar
• Yap TA, Konstantinopoulos P, Telli ML, et al. Abstract P1-19-03: JAVELIN PARP Medley, a phase 1b/2 study of avelumab plus talazoparib: results from advanced breast cancer cohorts. Cancer Res. 2020;80: 1–19-03-P1-19–03.
   Web of Science ®Google Scholar
• Eskander RN, Ledermann JA, Birrer MJ, et al. JAVELIN ovarian PARP 100 study design: phase III trial of avelumab + chemotherapy followed by avelumab + talazoparib maintenance in previously untreated epithelial ovarian cancer. J clin oncol. 2019;37(8_suppl): TPS9–TPS9.
   Web of Science ®Google Scholar
• Rodriguez-Moreno JF, Ruiz-Llorente S, De Velasco G, et al. Comprehensive molecular characterization of muscle-invasive bladder cancer (MIBC) treated with durvalumab plus olaparib in the neoadjuvant setting: neodurvarib trial. J clin oncol. 2022;40(6_suppl):546.
   PubMed Web of Science ®Google Scholar
• Neelapu SS, Locke FL, Bartlett NL, et al. Axicabtagene ciloleucel CAR T-cell therapy in refractory large B-cell lymphoma. N Engl J Med. 2017;377(26):2531–2544.
   PubMed Web of Science ®Google Scholar
• Schuster SJ, Svoboda J, Chong EA, et al. Chimeric Antigen receptor T cells in refractory B-cell lymphomas. N Engl J Med. 2017;377(26):2545–2554.
   PubMed Web of Science ®Google Scholar
• Maude SL, Laetsch TW, Buechner J, et al. Tisagenlecleucel in children and young adults with B-Cell lymphoblastic leukemia. N Engl J Med. 2018;378(5):439–448.
   PubMed Web of Science ®Google Scholar
• Sadelain M, Brentjens R, Rivière I. The basic principles of chimeric antigen receptor design. Cancer Discov. 2013;3(4):388–398.
   PubMed Web of Science ®Google Scholar
• Sterner RC, Sterner RM. CAR-T cell therapy: current limitations and potential strategies. Blood Cancer J. 2021;11(4):69.
   PubMed Web of Science ®Google Scholar
• Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med. 2013;19(11):1423–1437.
   PubMed Web of Science ®Google Scholar
• Yin Y, Boesteanu AC, Binder ZA, et al. Checkpoint blockade reverses anergy in IL-13Rα2 humanized scFv-Based CAR T cells to treat murine and canine gliomas. Molecular Therapy - Oncolytics. 2018; 11: 20–38. 10.1016/j.omto.2018.08.002
   PubMed Web of Science ®Google Scholar
• Sun R, Luo H, Su J, et al. Olaparib suppresses MDSC recruitment via SDF1α/CXCR4 axis to improve the Anti-tumor Efficacy of CAR-T Cells on breast cancer in mice. Mol Ther. 2021;29(1):60–74.
   PubMed Web of Science ®Google Scholar
• Ji F, Zhang F, Zhang M, et al. Targeting the DNA damage response enhances CD70 CAR-T cell therapy for renal carcinoma by activating the cGAS-STING pathway. J Hematol Oncol. 2021;14(1):152.
   PubMed Web of Science ®Google Scholar
• D’Andrea AD. Mechanisms of PARP inhibitor sensitivity and resistance. DNA Repair (Amst). 2018;71:172–176.
   PubMed Web of Science ®Google Scholar
• Jenkins RW, Barbie DA, Flaherty KT. Mechanisms of resistance to immune checkpoint inhibitors. Br J Cancer. 2018;118(1):9–16.
   PubMed Web of Science ®Google Scholar
• Prolonged long-term survival with immunotherapy vs chemo in advanced NSCLC - The ASCO post. [cited Apr 17, 2022]. Available from: https://ascopost.com/issues/october-10-2019/prolonged-long-term-survival-with-immunotherapy-vs-chemo-in-advanced-nsclc
   Google Scholar
• McDermott D, Lebbé C, Hodi FS, et al. Durable benefit and the potential for long-term survival with immunotherapy in advanced melanoma. Cancer Treat Rev. 2014;40(9):1056–1064.
   PubMed Web of Science ®Google Scholar
• Wanderley CWS, Correa TS, Scaranti M, et al. Targeting PARP1 to enhance anticancer checkpoint immunotherapy response: rationale and clinical implications. Front Immunol. 2022 Apr 27;13:816642.
   Google Scholar
• Lau AY, Yates J, Wilson Z, et al. Abstract 2494: ATR inhibitor AZD6738 as monotherapy and in combination with olaparib or chemotherapy: defining pre-clinical dose-schedules and efficacy modelling. Cancer Res. 2017;77(13_Supplement):2494.
   Google Scholar
• Taniguchi H, Caeser R, Chavan SS, et al. WEE1 inhibition enhances the antitumor immune response to PD-L1 blockade by the concomitant activation of STING and STAT1 pathways in SCLC. Cell Rep. 2022;39(7):110814.
   PubMed Web of Science ®Google Scholar
• Dinavahi SS, Chen Y-C, Punnath K, et al. Targeting WEE1/AKT Restores p53-dependent natural killer–cell activation to induce immune checkpoint blockade responses in “cold” melanoma. Cancer Immunol Res. 2022;10(6):757–769.
   PubMed Web of Science ®Google Scholar
• Medina López RA, Rivero Belenchon I, Mazuecos-Quirós J, et al. Update on the treatment of metastatic renal cell carcinoma. World J Clin Oncol. 2022;13(1):1–8.
   PubMed Web of Science ®Google Scholar
• Haslam A, Prasad V. Estimation of the percentage of us patients with cancer who are eligible for and respond to checkpoint inhibitor immunotherapy drugs. JAMA Network Open. 2019 May 3;2(5):e192535.
   Web of Science ®Google Scholar
• Lord CJ, Ashworth A. PARP inhibitors: synthetic lethality in the clinic. Science. 2017;355(6330):1152–1158.
   PubMed Web of Science ®Google Scholar
• Helleday T. The underlying mechanism for the PARP and BRCA synthetic lethality: clearing up the misunderstandings. Mol Oncol. 2011;5(4):387–393.
   PubMed Web of Science ®Google Scholar
• Rosado MM, Bennici E, Novelli F, et al. Beyond DNA repair, the immunological role of PARP-1 and its siblings. Immunology. 2013;139(4):428–437.
   PubMed Web of Science ®Google Scholar
• Sisay M, Edessa D. PARP inhibitors as potential therapeutic agents for various cancers: focus on niraparib and its first global approval for maintenance therapy of gynecologic cancers. Gynecol Oncol Res Pract. 2017;4(1):18.
   PubMedGoogle Scholar
• Wu Z, Cui P, Tao H, et al. The synergistic effect of PARP Inhibitors and immune checkpoint inhibitors. Clic Medc Insights: Onc. 2021 Feb 25;15:1179554921996288.
   Google Scholar