Login Register Cart 0
Review Article

Research Progress of PARP Inhibitor Monotherapy and Combination Therapy for Endometrial Cancer

Author(s): Ke Shen, Li Yang*, Fei-Yan Li, Feng Zhang, Lei-Lei Ding, Jing Yang, Jie Lu, Nan-Nan Wang and Yan Wang

Volume 23, Issue 2, 2022

Published on: 13 July, 2021

Page: [145 - 155] Pages: 11

DOI: 10.2174/1389450122666210617111304

Price: $65

Abstract

Endometrial cancer is one of the three most common malignant tumors in the female reproductive system. Advanced and recurrent endometrial cancers have poor prognoses and lack effective treatments. Poly (ADP-ribose) polymerase (PARP) inhibitors have been applied to many different types of tumors, and they can selectively kill tumor cells that are defective in homologous recombination repair. Endometrial cancer is characterized by mutations in homologous recombination repair genes; accordingly, PARP inhibitors have achieved positive results in off-label treatments of endometrial cancer cases. Clinical trials of PARP inhibitors as monotherapies and within combination therapies for endometrial cancer are ongoing. For this review, we searched PubMed with “endometrial cancer” and “PARP inhibitor” as keywords, and we used “olaparib”, “rucaparib”, “niraparib” and “talazoparib” as search terms in clinicaltrials.gov for ongoing trials. The literature search ended in October 2020, and only English-language publications were selected. Multiple studies confirm that PARP inhibitors play an important role in killing tumor cells with defects in homologous recombination repair. Its combination with immune checkpoint inhibitors, PI3K/AKT/mTOR pathway inhibitors, cell cycle checkpoint inhibitors, and other drugs can improve the treatment of endometrial cancer.

Keywords: PARP inhibitor, endometrial cancer, homologous recombination deficiency, targeted therapy, combination therapy, immune checkpoint inhibitor, PI3K/AKT/mTOR pathway inhibitor.

« Previous Next »
Graphical Abstract

[1]
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68(6): 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[2]
Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin 2016; 66(2): 115-32.
[http://dx.doi.org/10.3322/caac.21338] [PMID: 26808342]
[3]
Colombo N, Preti E, Landoni F, et al. Endometrial cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 2013; 24(Suppl. 6): vi33-8.
[http://dx.doi.org/10.1093/annonc/mdt353] [PMID: 24078661]
[4]
Siegel R, Miller K, Jemal A. Cancer statistics, 2019. CA Cancer J Clin 2019; 69(1): 7-34.
[5]
Pujade-Lauraine E, Ledermann JA, Selle F, et al. Olaparib tablets as maintenance therapy in patients with platinum-sensitive, relapsed ovarian cancer and a BRCA1/2 mutation (SOLO2/ENGOT-Ov21): A double-blind, randomised, placebo-controlled, phase 3 trial. Lancet Oncol 2017; 18(9): 1274-84.
[http://dx.doi.org/10.1016/S1470-2045(17)30469-2] [PMID: 28754483]
[6]
González-Martín A, Pothuri B, Vergote I, et al. Niraparib in patients with newly diagnosed advanced ovarian cancer. N Engl J Med 2019; 381(25): 2391-402.
[http://dx.doi.org/10.1056/NEJMoa1910962] [PMID: 31562799]
[7]
Coleman RL, Oza AM, Lorusso D, et al. Rucaparib maintenance treatment for recurrent ovarian carcinoma after response to platinum therapy (ARIEL3): A randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 2017; 390(10106): 1949-61.
[http://dx.doi.org/10.1016/S0140-6736(17)32440-6] [PMID: 28916367]
[8]
Kandoth C, Schultz N, Cherniack AD, et al. Integrated genomic characterization of endometrial carcinoma. Nature 2013; 497(7447): 67-73.
[http://dx.doi.org/10.1038/nature12113] [PMID: 23636398]
[9]
Murali R, Soslow RA, Weigelt B. Classification of endometrial carcinoma: More than two types. Lancet Oncol 2014; 15(7): e268-78.
[http://dx.doi.org/10.1016/S1470-2045(13)70591-6] [PMID: 24872110]
[10]
van Gool IC, Eggink FA, Freeman-Mills L, et al. POLE proofreading mutations elicit an antitumor immune response in endometrial cancer. Clin Cancer Res 2015; 21(14): 3347-55.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-0057] [PMID: 25878334]
[11]
Gargiulo P, Della Pepa C, Berardi S, et al. Tumor genotype and immune microenvironment in POLE-ultramutated and msi-hypermutated endometrial cancers: New candidates for checkpoint blockade immunotherapy? Cancer Treat Rev 2016; 48: 61-8.
[http://dx.doi.org/10.1016/j.ctrv.2016.06.008] [PMID: 27362548]
[12]
Le Gallo M, Bell DW. The emerging genomic landscape of endometrial cancer. Clin Chem 2014; 60(1): 98-110.
[http://dx.doi.org/10.1373/clinchem.2013.205740] [PMID: 24170611]
[13]
Oda K, Stokoe D, Taketani Y, McCormick F. High frequency of coexistent mutations of PIK3CA and PTEN genes in endometrial carcinoma. Cancer Res 2005; 65(23): 10669-73.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-2620] [PMID: 16322209]
[14]
Wilczyński M, Danielska J, Wilczyński J. An update of the classical bokhman’s dualistic model of endometrial cancer. Przegl Menopauz 2016; 15(2): 63-8.
[http://dx.doi.org/10.5114/pm.2016.61186] [PMID: 27582678]
[15]
de Jonge MM, Auguste A, van Wijk LM, et al. Frequent homologous recombination deficiency in high-grade endometrial carcinomas. Clin Cancer Res 2019; 25(3): 1087-97.
[http://dx.doi.org/10.1158/1078-0432.CCR-18-1443] [PMID: 30413523]
[16]
Paleari L, Pesce S, Rutigliani M, et al. New insights into endometrial cancer. Cancers (Basel) 2021; 13(7): 1496.
[http://dx.doi.org/10.3390/cancers13071496] [PMID: 33804979]
[17]
Herceg Z, Wang ZQ. Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutat Res 2001; 477(1-2): 97-110.
[http://dx.doi.org/10.1016/S0027-5107(01)00111-7] [PMID: 11376691]
[18]
Mateo J, Lord CJ, Serra V, et al. A decade of clinical development of PARP inhibitors in perspective. Ann Oncol 2019; 30(9): 1437-47.
[http://dx.doi.org/10.1093/annonc/mdz192] [PMID: 31218365]
[19]
Murai J, Huang SY, Das BB, et al. Trapping of parp1 and parp2 by clinical parp inhibitors. Cancer Res 2012; 72(21): 5588-99.
[http://dx.doi.org/10.1158/0008-5472.CAN-12-2753] [PMID: 23118055]
[20]
Tomao F, Santangelo G, Musacchio L, et al. Targeting cervical cancer: Is there a role for poly (ADP-ribose) polymerase inhibition? J Cell Physiol 2020; 235(6): 5050-8.
[http://dx.doi.org/10.1002/jcp.29440] [PMID: 31912897]
[21]
Wurster S, Hennes F, Parplys AC, et al. PARP1 inhibition radiosensitizes HNSCC cells deficient in homologous recombination by disabling the DNA replication fork elongation response. Oncotarget 2016; 7(9): 9732-41.
[http://dx.doi.org/10.18632/oncotarget.6947] [PMID: 26799421]
[22]
Ashworth A. A synthetic lethal therapeutic approach: Poly(ADP) ribose polymerase inhibitors for the treatment of cancers deficient in DNA double-strand break repair. J Clin Oncol 2008; 26(22): 3785-90.
[http://dx.doi.org/10.1200/JCO.2008.16.0812] [PMID: 18591545]
[23]
Bryant HE, Schultz N, Thomas HD, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005; 434(7035): 913-7.
[http://dx.doi.org/10.1038/nature03443] [PMID: 15829966]
[24]
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): 8109-15.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-0140] [PMID: 16912188]
[25]
Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature 2001; 411(6835): 366-74.
[http://dx.doi.org/10.1038/35077232] [PMID: 11357144]
[26]
Bryant HE, Helleday T. Inhibition of poly (ADP-ribose) polymerase activates ATM which is required for subsequent homologous recombination repair. Nucleic Acids Res 2006; 34(6): 1685-91.
[http://dx.doi.org/10.1093/nar/gkl108] [PMID: 16556909]
[27]
Postel-Vinay S, Bajrami I, Friboulet L, et al. A high-throughput screen identifies PARP1/2 inhibitors as a potential therapy for ERCC1-deficient non-small cell lung cancer. Oncogene 2013; 32(47): 5377-87.
[http://dx.doi.org/10.1038/onc.2013.311] [PMID: 23934192]
[28]
Bajrami I, Frankum JR, Konde A, et al. Genome-wide profiling of genetic synthetic lethality identifies CDK12 as a novel determinant of PARP1/2 inhibitor sensitivity. Cancer Res 2014; 74(1): 287-97.
[http://dx.doi.org/10.1158/0008-5472.CAN-13-2541] [PMID: 24240700]
[29]
Yi T, Feng Y, Sundaram R, et al. Antitumor efficacy of PARP inhibitors in homologous recombination deficient carcinomas. Int J Cancer 2019; 145(5): 1209-20.
[http://dx.doi.org/10.1002/ijc.32143] [PMID: 30666631]
[30]
Jones P, Altamura S, Boueres J, et al. Discovery of 2-{4-[(3S)-piperidin-3-yl]phenyl}-2H-indazole-7-carboxamide (MK-4827): A novel oral poly(ADP-ribose)polymerase (PARP) inhibitor efficacious in BRCA-1 and -2 mutant tumors. J Med Chem 2009; 52(22): 7170-85.
[http://dx.doi.org/10.1021/jm901188v] [PMID: 19873981]
[31]
Shen Y, Rehman FL, Feng Y, et al. BMN 673, a novel and highly potent PARP1/2 inhibitor for the treatment of human cancers with DNA repair deficiency. Clin Cancer Res 2013; 19(18): 5003-15.
[http://dx.doi.org/10.1158/1078-0432.CCR-13-1391] [PMID: 23881923]
[32]
Wang B, Chu D, Feng Y, Shen Y, Aoyagi-Scharber M, Post LE. Discovery and Characterization of (8S,9R)-5-Fluoro-8-(4-fluorophenyl)-9-(1-methyl-1H-1,2,4-triazol-5-yl)-2,7,8,9-tetrahydro-3H-pyrido[4,3,2-de]phthalazin-3-one (BMN 673, Talazoparib), a Novel, Highly Potent, and Orally Efficacious Poly(ADP-ribose) Polymerase-1/2 Inhibitor, as an Anticancer Agent. J Med Chem 2016; 59(1): 335-57.
[http://dx.doi.org/10.1021/acs.jmedchem.5b01498] [PMID: 26652717]
[33]
Menear KA, Adcock C, Boulter R, et al. 4-[3-(4-cyclopropanecarbonylpiperazine-1-carbonyl)-4-fluorobenzyl]-2H-phthalazin-1-one: A novel bioavailable inhibitor of poly(ADP-ribose) polymerase-1. J Med Chem 2008; 51(20): 6581-91.
[http://dx.doi.org/10.1021/jm8001263] [PMID: 18800822]
[34]
Fong PC, Boss DS, Yap TA, et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 2009; 361(2): 123-34.
[http://dx.doi.org/10.1056/NEJMoa0900212] [PMID: 19553641]
[35]
Weaver AN, Yang ES. Beyond DNA Repair: Additional functions of parp-1 in cancer. Front Oncol 2013; 3: 290.
[http://dx.doi.org/10.3389/fonc.2013.00290] [PMID: 24350055]
[36]
Sonnenblick A, de Azambuja E, Azim HA Jr, Piccart M. An update on PARP inhibitors-moving to the adjuvant setting. Nat Rev Clin Oncol 2015; 12(1): 27-41.
[http://dx.doi.org/10.1038/nrclinonc.2014.163] [PMID: 25286972]
[37]
Mirza MR, Pignata S, Ledermann JA. Latest clinical evidence and further development of PARP inhibitors in ovarian cancer. Ann Oncol 2018; 29(6): 1366-76.
[http://dx.doi.org/10.1093/annonc/mdy174] [PMID: 29750420]
[38]
Keung MYT, Wu Y, Vadgama JV. PARP inhibitors as a therapeutic agent for homologous recombination deficiency in breast cancers. J Clin Med 2019; 8(4): E435.
[http://dx.doi.org/10.3390/jcm8040435] [PMID: 30934991]
[39]
Martinez-Useros J, Garcia-Foncillas J. The role of brca2 mutation status as diagnostic, predictive, and prognosis biomarker for pancreatic cancer. BioMed Res Int 2016; 2016: 1869304.
[http://dx.doi.org/10.1155/2016/1869304] [PMID: 28078281]
[40]
Pilié PG, Gay CM, Byers LA, O’Connor MJ, Yap TA. PARP inhibitors: Extending benefit beyond brca-mutant cancers. Clin Cancer Res 2019; 25(13): 3759-71.
[http://dx.doi.org/10.1158/1078-0432.CCR-18-0968] [PMID: 30760478]
[41]
Lim JSJ, Tan DSP. Understanding resistance mechanisms and expanding the therapeutic utility of parp inhibitors. Cancers (Basel) 2017; 9(8): E109.
[http://dx.doi.org/10.3390/cancers9080109] [PMID: 28829366]
[42]
Stewart RA, Pilié PG, Yap TA. Development of parp and immune-checkpoint inhibitor combinations. Cancer Res 2018; 78(24): 6717-25.
[http://dx.doi.org/10.1158/0008-5472.CAN-18-2652] [PMID: 30498083]
[43]
Mendes-Pereira AM, Martin SA, Brough R, et al. Synthetic lethal targeting of PTEN mutant cells with PARP inhibitors. EMBO Mol Med 2009; 1(6-7): 315-22.
[http://dx.doi.org/10.1002/emmm.200900041] [PMID: 20049735]
[44]
de Jonge MM, Ritterhouse LL, de Kroon CD, et al. Germline brca-associated endometrial carcinoma is a distinct clinicopathologic entity. Clin Cancer Res 2019; 25(24): 7517-26.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-0848] [PMID: 31492746]
[45]
Heeke AL, Pishvaian MJ, Lynce F, et al. Prevalence of homologous recombination-related gene mutations across multiple cancer types. JCO Precis Oncol 2018; 2018: PO.17.00286.
[http://dx.doi.org/10.1200/PO.17.00286]
[46]
Rodriguez-Freixinos V, Karakasis K, Oza AM. New targeted agents in endometrial cancer: Are we really making progress? Curr Oncol Rep 2016; 18(4): 23.
[http://dx.doi.org/10.1007/s11912-016-0507-z] [PMID: 26922329]
[47]
Sa JK, Hwang JR, Cho YJ, et al. Pharmacogenomic analysis of patient-derived tumor cells in gynecologic cancers. Genome Biol 2019; 20(1): 253.
[http://dx.doi.org/10.1186/s13059-019-1848-3] [PMID: 31771620]
[48]
Janzen DM, Paik DY, Rosales MA, et al. Low levels of circulating estrogen sensitize PTEN-null endometrial tumors to PARP inhibition in vivo. Mol Cancer Ther 2013; 12(12): 2917-28.
[http://dx.doi.org/10.1158/1535-7163.MCT-13-0572] [PMID: 24222661]
[49]
Lawrence LM, Russell R, Denning CE, et al. Expression of poly-ADP-ribose polymerase (PARP) in endometrial adenocarcinoma: Prognostic potential. Pathol Res Pract 2020; 216(6): 152965.
[http://dx.doi.org/10.1016/j.prp.2020.152965] [PMID: 32360251]
[50]
Dedes KJ, Wetterskog D, Mendes-Pereira AM, et al. PTEN deficiency in endometrioid endometrial adenocarcinomas predicts sensitivity to PARP inhibitors. Sci Transl Med 2010; 2(53): 53ra75.
[http://dx.doi.org/10.1126/scitranslmed.3001538] [PMID: 20944090]
[51]
Philip CA, Laskov I, Beauchamp MC, et al. Inhibition of PI3K-AKT-mTOR pathway sensitizes endometrial cancer cell lines to PARP inhibitors. BMC Cancer 2017; 17(1): 638.
[http://dx.doi.org/10.1186/s12885-017-3639-0] [PMID: 28886696]
[52]
Miyasaka A, Oda K, Ikeda Y, et al. Anti-tumor activity of olaparib, a poly (ADP-ribose) polymerase (PARP) inhibitor, in cultured endometrial carcinoma cells. BMC Cancer 2014; 14: 179.
[http://dx.doi.org/10.1186/1471-2407-14-179] [PMID: 24625059]
[53]
Gockley AA, Kolin DL, Awtrey CS, Lindeman NI, Matulonis UA, Konstantinopoulos PA. Durable response in a woman with recurrent low-grade endometrioid endometrial cancer and a germline BRCA2 mutation treated with a PARP inhibitor. Gynecol Oncol 2018; 150(2): 219-26.
[http://dx.doi.org/10.1016/j.ygyno.2018.05.028] [PMID: 29937315]
[54]
Forster MD, Dedes KJ, Sandhu S, et al. Treatment with olaparib in a patient with PTEN-deficient endometrioid endometrial cancer. Nat Rev Clin Oncol 2011; 8(5): 302-6.
[http://dx.doi.org/10.1038/nrclinonc.2011.42] [PMID: 21468130]
[55]
Dréan A, Lord CJ, Ashworth A. PARP inhibitor combination therapy. Crit Rev Oncol Hematol 2016; 108: 73-85.
[http://dx.doi.org/10.1016/j.critrevonc.2016.10.010] [PMID: 27931843]
[56]
Pilié PG, Tang C, Mills GB, Yap TA. State-of-the-art strategies for targeting the DNA damage response in cancer. Nat Rev Clin Oncol 2019; 16(2): 81-104.
[http://dx.doi.org/10.1038/s41571-018-0114-z] [PMID: 30356138]
[57]
Matulonis UA, Monk BJ. PARP inhibitor and chemotherapy combination trials for the treatment of advanced malignancies: Does a development pathway forward exist? Ann Oncol 2017; 28(3): 443-7.
[http://dx.doi.org/10.1093/annonc/mdw697] [PMID: 28057663]
[58]
Yap TA, Plummer R, Azad NS, Helleday T. The dna damaging revolution: PARP inhibitors and beyond. Am Soc Clin Oncol Educ Book 2019; 39: 185-95.
[http://dx.doi.org/10.1200/EDBK_238473] [PMID: 31099635]
[59]
Mirza MR, Monk BJ, Herrstedt J, et al. Niraparib maintenance therapy in platinum-sensitive, recurrent ovarian cancer. N Engl J Med 2016; 375(22): 2154-64.
[http://dx.doi.org/10.1056/NEJMoa1611310] [PMID: 27717299]
[60]
Swisher EM, Lin KK, Oza AM, et al. Rucaparib in relapsed, platinum-sensitive high-grade ovarian carcinoma (ARIEL2 Part 1): An international, multicentre, open-label, phase 2 trial. Lancet Oncol 2017; 18(1): 75-87.
[http://dx.doi.org/10.1016/S1470-2045(16)30559-9] [PMID: 27908594]
[61]
Moore K, Colombo N, Scambia G, et al. Maintenance olaparib in patients with newly diagnosed advanced ovarian cancer. N Engl J Med 2018; 379(26): 2495-505.
[http://dx.doi.org/10.1056/NEJMoa1810858] [PMID: 30345884]
[62]
Harding SM, Benci JL, Irianto J, Discher DE, Minn AJ, Greenberg RA. Mitotic progression following DNA damage enables pattern recognition within micronuclei. Nature 2017; 548(7668): 466-70.
[http://dx.doi.org/10.1038/nature23470] [PMID: 28759889]
[63]
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): 311-9.
[http://dx.doi.org/10.1158/0008-5472.CAN-18-1003] [PMID: 30482774]
[64]
Ding L, Kim HJ, Wang Q, et al. PARP inhibition elicits sting-dependent antitumor immunity in brca1-deficient ovarian cancer. Cell Rep 2018; 25(11): 2972-2980.e5.
[http://dx.doi.org/10.1016/j.celrep.2018.11.054] [PMID: 30540933]
[65]
Chabanon RM, Muirhead G, Krastev DB, et al. PARP inhibition enhances tumor cell-intrinsic immunity in ERCC1-deficient non-small cell lung cancer. J Clin Invest 2019; 129(3): 1211-28.
[http://dx.doi.org/10.1172/JCI123319] [PMID: 30589644]
[66]
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): 3711-20.
[http://dx.doi.org/10.1158/1078-0432.CCR-16-3215] [PMID: 28167507]
[67]
Drew Y, de Jonge M, Hong S. An open-label, Phase II basket study of olaparib and durvalumab (MEDIOLA): Results in germline BRCA-mutated (gBRCAm) platinum-sensitive relapsed (PSR) ovarian cancer (OC). Gynecol Oncol 2018; 149(Supplement 1): 246-7.
[68]
Mouw KW, Goldberg MS, Konstantinopoulos PA, D’Andrea AD. DNA damage and repair biomarkers of immunotherapy response. Cancer Discov 2017; 7(7): 675-93.
[http://dx.doi.org/10.1158/2159-8290.CD-17-0226] [PMID: 28630051]
[69]
Zimmer AS, Nichols E, Cimino-Mathews A, et al. A phase I study of the PD-L1 inhibitor, durvalumab, in combination with a PARP inhibitor, olaparib, and a VEGFR1-3 inhibitor, cediranib, in recurrent women’s cancers with biomarker analyses. J Immunother Cancer 2019; 7(1): 197.
[http://dx.doi.org/10.1186/s40425-019-0680-3] [PMID: 31345267]
[70]
Konstantinopoulos PA, et al. Phase 2, two-group, two-stage, open-label study of avelumab in patients with microsatellite stable,microsatellite instable and POLE-mutated recurrent or persistent endometrial cancer. J Clin Oncol 2017; 35(15_suppl): TPS5615-TPS5615.
[http://dx.doi.org/10.1200/JCO.2017.35.15_suppl.TPS5615]
[71]
Post CCB, Westermann AM, Bosse T, Creutzberg CL, Kroep JR. PARP and PD-1/PD-L1 checkpoint inhibition in recurrent or metastatic endometrial cancer. Crit Rev Oncol Hematol 2020; 152: 102973.
[http://dx.doi.org/10.1016/j.critrevonc.2020.102973] [PMID: 32497971]
[72]
Ibrahim YH, García-García C, Serra V, et al. PI3K inhibition impairs BRCA1/2 expression and sensitizes BRCA-proficient triple-negative breast cancer to PARP inhibition. Cancer Discov 2012; 2(11): 1036-47.
[http://dx.doi.org/10.1158/2159-8290.CD-11-0348] [PMID: 22915752]
[73]
Juvekar A, Burga LN, Hu H, et al. Combining a PI3K inhibitor with a PARP inhibitor provides an effective therapy for BRCA1-related breast cancer. Cancer Discov 2012; 2(11): 1048-63.
[http://dx.doi.org/10.1158/2159-8290.CD-11-0336] [PMID: 22915751]
[74]
Wang D, Li C, Zhang Y, et al. Combined inhibition of PI3K and PARP is effective in the treatment of ovarian cancer cells with wild-type PIK3CA genes. Gynecol Oncol 2016; 142(3): 548-56.
[http://dx.doi.org/10.1016/j.ygyno.2016.07.092] [PMID: 27426307]
[75]
Bian X, Gao J, Luo F, et al. PTEN deficiency sensitizes endometrioid endometrial cancer to compound PARP-PI3K inhibition but not PARP inhibition as monotherapy. Oncogene 2018; 37(3): 341-51.
[http://dx.doi.org/10.1038/onc.2017.326] [PMID: 28945226]
[76]
Kim H, George E, Ragland R, et al. Targeting the atr/chk1 axis with parp inhibition results in tumor regression in brca-mutant ovarian cancer models. Clin Cancer Res 2017; 23(12): 3097-108.
[http://dx.doi.org/10.1158/1078-0432.CCR-16-2273] [PMID: 27993965]
[77]
Yazinski SA, Comaills V, Buisson R, et al. ATR inhibition disrupts rewired homologous recombination and fork protection pathways in PARP inhibitor-resistant BRCA-deficient cancer cells. Genes Dev 2017; 31(3): 318-32.
[http://dx.doi.org/10.1101/gad.290957.116] [PMID: 28242626]
[78]
Haynes B, Murai J, Lee JM. Restored replication fork stabilization, a mechanism of PARP inhibitor resistance, can be overcome by cell cycle checkpoint inhibition. Cancer Treat Rev 2018; 71: 1-7.
[http://dx.doi.org/10.1016/j.ctrv.2018.09.003] [PMID: 30269007]
[79]
Lallo A, Frese KK, Morrow CJ, et al. The combination of the parp inhibitor olaparib and the wee1 inhibitor azd1775 as a new therapeutic option for small cell lung cancer. Clin Cancer Res 2018; 24(20): 5153-64.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-2805] [PMID: 29941481]
[80]
Parsels LA, Karnak D, Parsels JD, et al. PARP1 trapping and dna replication stress enhance radiosensitization with combined wee1 and parp inhibitors. Mol Cancer Res 2018; 16(2): 222-32.
[http://dx.doi.org/10.1158/1541-7786.MCR-17-0455] [PMID: 29133592]
[81]
Fang Y, McGrail DJ, Sun C, et al. Sequential therapy with parp and wee1 inhibitors minimizes toxicity while maintaining efficacy. Cancer Cell 2019; 35(6): 851-867.e7.
[http://dx.doi.org/10.1016/j.ccell.2019.05.001] [PMID: 31185210]
[82]
Lin X, Chen D, Zhang C, et al. Augmented antitumor activity by olaparib plus AZD1775 in gastric cancer through disrupting DNA damage repair pathways and DNA damage checkpoint. J Exp Clin Cancer Res 2018; 37(1): 129.
[http://dx.doi.org/10.1186/s13046-018-0790-7] [PMID: 29954437]
[83]
Meng X, Bi J, Li Y, et al. AZD1775 increases sensitivity to olaparib and gemcitabine in cancer cells with p53 mutations. Cancers (Basel) 2018; 10(5): E149.
[http://dx.doi.org/10.3390/cancers10050149] [PMID: 29783721]
[84]
Sun C, Fang Y, Yin J, et al. Rational combination therapy with PARP and MEK inhibitors capitalizes on therapeutic liabilities in RAS mutant cancers. Sci Transl Med 2017; 9(392): eaal5148.
[http://dx.doi.org/10.1126/scitranslmed.aal5148] [PMID: 28566428]
[85]
Sun C, Fang Y, Labrie M, Li X, Mills GB. Systems approach to rational combination therapy: PARP inhibitors. Biochem Soc Trans 2020; 48(3): 1101-8.
[http://dx.doi.org/10.1042/BST20191092] [PMID: 32379297]
[86]
Dinkic C, Jahn F, Zygmunt M, et al. PARP inhibition sensitizes endometrial cancer cells to paclitaxel-induced apoptosis. Oncol Lett 2017; 13(4): 2847-51.
[http://dx.doi.org/10.3892/ol.2017.5795] [PMID: 28454476]
[87]
Park Y, Chui MH, Suryo Rahmanto Y, et al. Loss of arid1a in tumor cells renders selective vulnerability to combined ionizing radiation and parp inhibitor therapy. Clin Cancer Res 2019; 25(18): 5584-94.
[http://dx.doi.org/10.1158/1078-0432.CCR-18-4222] [PMID: 31196855]
[88]
Tang L, Wang M, Jiang L, Zeng C. TRAF4 knockdown triggers synergistic lethality with simultaneous PARP1 inhibition in endometrial cancer. Hum Cell 2020; 33(3): 801-9.
[http://dx.doi.org/10.1007/s13577-020-00363-5] [PMID: 32388810]
[89]
Hensley ML, Chavan SS, Solit DB, et al. Genomic landscape of uterine sarcomas defined through prospective clinical sequencing. Clin Cancer Res 2020; 26(14): 3881-8.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-3959] [PMID: 32299819]

Rights & Permissions Print Cite
Article Metrics
68
3
© 2024 Bentham Science Publishers | Privacy Policy