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Review

Targeting deficient DNA damage repair in gastric cancer

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Pages 1757-1766 | Received 18 Apr 2016, Accepted 25 Jul 2016, Published online: 08 Aug 2016

References

  • Ferlay J, Soerjomataram I I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–E386. doi:10.1002/ijc.29210.
  • Cunningham D, Allum WH, Stenning SP, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med. 2006;355(1):11–20. doi:10.1056/NEJMoa055531.
  • Ychou M, Boige V, Pignon JP, et al. Perioperative chemotherapy compared with surgery alone for resectable gastroesophageal adenocarcinoma: an FNCLCC and FFCD multicenter phase III trial. J Clin Oncol. 2011;29(13):1715–1721. doi:10.1200/JCO.2010.33.0597.
  • Wagner AD, Grothe W, Haerting J, et al. Chemotherapy in advanced gastric cancer: a systematic review and meta-analysis based on aggregate data. J Clin Oncol. 2006;24(18):2903–2909. doi:10.1200/JCO.2005.05.0245.
  • Ajani JA, Moiseyenko VM, Tjulandin S, et al. Quality of life with docetaxel plus cisplatin and fluorouracil compared with cisplatin and fluorouracil from a phase III trial for advanced gastric or gastroesophageal adenocarcinoma: the V-325 study group. J Clin Oncol. 2007;25(22):3210–3216. doi:10.1200/JCO.2006.08.3956.
  • Cunningham D, Starling N, Rao S, et al. Capecitabine and oxaliplatin for advanced esophagogastric cancer. N Engl J Med. 2008;358(1):36–46. doi:10.1056/NEJMoa073149.
  • Bang Y-J, Van Cutsem E, Feyereislova A, et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet. 2010;376(9742):687–697. doi:10.1016/S0140-6736(10)61121-X.
  • Fuchs CS, Tomasek J, Yong CJ, et al. Ramucirumab monotherapy for previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (REGARD): an international, randomised, multicentre, placebo-controlled, phase 3 trial. Lancet. 2014;383(9911):31–39. doi:10.1016/S0140-6736(13)61719-5.
  • Wilke H, Muro K, Van Cutsem E, et al. Ramucirumab plus paclitaxel versus placebo plus paclitaxel in patients with previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (RAINBOW): a double-blind, randomised phase 3 trial. Lancet Oncol. 2014;15(11):1224–1235. doi:10.1016/S1470-2045(14)70420-6.
  • Li J, Qin S, Xu J, et al. Randomized, double-blind, placebo-controlled phase III trial of apatinib in patients with chemotherapy-refractory advanced or metastatic adenocarcinoma of the stomach or gastroesophageal junction. J Clin Oncol. 2016. doi:10.1200/JCO.2015.63.5995.
  • Kang JH, Lee SI, Lim DH, et al. Salvage chemotherapy for pretreated gastric cancer: a randomized phase III trial comparing chemotherapy plus best supportive care with best supportive care alone. J Clin Oncol. 2012;30(13):1513–1518. doi:10.1200/JCO.2011.39.4585.
  • Thuss-Patience PC, Kretzschmar A, Bichev D, et al. Survival advantage for irinotecan versus best supportive care as second-line chemotherapy in gastric cancer –a randomised phase III study of the Arbeitsgemeinschaft Internistische Onkologie (AIO). Eur J Cancer. 2011;47(15):2306–2314. doi:10.1016/j.ejca.2011.06.002.
  • Ford HER, Marshall A, Bridgewater JA, et al. Docetaxel versus active symptom control for refractory oesophagogastric adenocarcinoma (COUGAR-02): an open-label, phase 3 randomised controlled trial. Lancet Oncol. 2014;15(1):78–86. doi:10.1016/S1470-2045(13)70549-7.
  • Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature. 2001;411(6835):366–374. doi:10.1038/35077232.
  • Jiricny J. The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol. 2006;7(5):335–346. doi:10.1038/nrm1907.
  • Maynard S, Schurman SH, Harboe C, et al. Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis. 2009;30(1):2–10. doi:10.1093/carcin/bgn250.
  • De Boer J. Nucleotide excision repair and human syndromes. Carcinogenesis. 2000;21(3):453–460 [cited 2000 Mar 5]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10688865.
  • Esteller M, Hamilton SR, Burger PC, et al. Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res. 1999;59(4):793–797 [cited 2016 Mar 10]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10029064
  • Sung P, Klein H. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat Rev Mol Cell Biol. 2006;7(10):739–750. doi:10.1038/nrm2008.
  • Lieber MR. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem. 2010;79:181–211. doi:10.1146/annurev.biochem.052308.093131.
  • Ander M, Subramaniam S, Fahmy K, et al. A single-strand annealing protein clamps DNA to detect and secure homology. PLoS Biol. 2015;13(8):e1002213. doi:10.1371/journal.pbio.1002213.
  • Peltomaki P. Role of DNA mismatch repair defects in the pathogenesis of human cancer. J Clin Oncol. 2003;21(6):1174–1179 [cited 2003 Jan 8]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12637487
  • Gudmundsdottir K, Ashworth A. The roles of BRCA1 and BRCA2 and associated proteins in the maintenance of genomic stability. Oncogene. 2006;25(43):5864–5874. doi:10.1038/sj.onc.1209874.
  • 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):3785–3790. doi:10.1200/JCO.2008.16.0812.
  • Lord CJ, Tutt ANJ, Ashworth A. Synthetic lethality and cancer therapy: lessons learned from the development of PARP inhibitors. Annu Rev Med. 2015;66:455–470. doi:10.1146/annurev-med-050913-022545.
  • Moeller BJ, Pasqualini R, Arap W. Targeting cancer-specific synthetic lethality in double-strand DNA break repair. Cell Cycle. 2009;8(12):1872–1876. doi:10.4161/cc.8.12.8743.
  • Heitz F, Harter P, Ewald-Riegler N, et al. Poly(ADP-ribosyl)ation polymerases: mechanism and new target of anticancer therapy. Expert Rev Anticancer Ther. 2010;10(7):1125–1136. doi:10.1586/era.10.53.
  • Aguilar-Quesada R, Muñoz-Gámez JA, Martín-Oliva D, et al. Interaction between ATM and PARP-1 in response to DNA damage and sensitization of ATM deficient cells through PARP inhibition. BMC Mol Biol. 2007;8:29. doi:10.1186/1471-2199-8-29.
  • 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):123–134. doi:10.1056/NEJMoa0900212.
  • Fong PC, Yap TA, Boss DS, et al. Poly(ADP)-ribose polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval. J Clin Oncol. 2010;28(15):2512–2519. doi:10.1200/JCO.2009.26.9589.
  • Tutt A, Robson M, Garber JE, et al. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. Lancet (London, England). 2010;376(9737):235–244. doi:10.1016/S0140-6736(10)60892-6.
  • Audeh MW, Carmichael J, Penson RT, et al. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet (London, England). 2010;376(9737):245–251. doi:10.1016/S0140-6736(10)60893-8.
  • Ledermann J, Harter P, Gourley C, et al. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N Engl J Med. 2012;366(15):1382–1392. doi:10.1056/NEJMoa1105535.
  • Ledermann J, Harter P, Gourley C, et al. Olaparib maintenance therapy in patients with platinum-sensitive relapsed serous ovarian cancer: a preplanned retrospective analysis of outcomes by BRCA status in a randomised phase 2 trial. Lancet Oncol. 2014;15(8):852–861. doi:10.1016/S1470-2045(14)70228-1.
  • Mateo J, Carreira S, Sandhu S, et al. DNA-repair defects and olaparib in metastatic prostate cancer. N Engl J Med. 2015;373(18):1697–1708. doi:10.1056/NEJMoa1506859.
  • Turner N, Tutt A, Ashworth A. Hallmarks of “BRCAness” in sporadic cancers. Nat Rev Cancer. 2004;4(10):814–819. doi:10.1038/nrc1457.
  • Pederson HJ, Padia SA, May M, et al. Managing patients at genetic risk of breast cancer. Cleve Clin J Med. 2016;83(3):199–206. doi:10.3949/ccjm.83a.14057.
  • Kehoe SM, Kauff ND. Screening and prevention of hereditary gynecologic cancers. Semin Oncol. 2007;34(5):406–410. doi:10.1053/j.seminoncol.2007.07.004.
  • Klein AP. Genetic susceptibility to pancreatic cancer. Mol Carcinog. 2012;51(1):14–24. doi:10.1002/mc.20855.
  • Robinson D, Van Allen EM, Wu Y-M, et al. Integrative clinical genomics of advanced prostate cancer. Cell. 2015;161(5):1215–1228. doi:10.1016/j.cell.2015.05.001.
  • Lord CJ, Ashworth A. BRCAness revisited. Nat Rev Cancer. 2016. doi:10.1038/nrc.2015.21.
  • 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):315–322. doi:10.1002/emmm.200900041.
  • Shen J, Peng Y, Wei L, et al. ARID1A deficiency impairs the DNA damage checkpoint and sensitizes cells to PARP inhibitors. Cancer Discov. 2015;5(7):752–767. doi:10.1158/2159-8290.CD-14-0849.
  • Kubota E, Williamson CT, Ye R, et al. Low ATM protein expression and depletion of p53 correlates with olaparib sensitivity in gastric cancer cell lines. Cell Cycle. 2014;13(13):2129–2137. doi:10.4161/cc.29212.
  • Results of ARIEL2: A Phase 2 trial to prospectively identify ovarian cancer patients likely to respond to rucaparib using tumor genetic analysis. ASCO Annual Meeting |Abstracts |Meeting Library; 2015 [cited 2016 Mar 24]. Available from: http://meetinglibrary.asco.org/content/150121-156
  • Alexandrov LB, Nik-Zainal S, Wedge DC, et al. Signatures of mutational processes in human cancer. Nature. 2013;500(7463):415–421. doi:10.1038/nature12477.
  • Birkbak NJ, Kochupurakkal B, Izarzugaza JMG. Tumor mutation burden forecasts outcome in ovarian cancer with BRCA1 or BRCA2 mutations. PLoS One. 2013;8(11):e80023. doi:10.1371/journal.pone.0080023.
  • Konstantinopoulos PA, Spentzos D, Karlan BY, et al. Gene expression profile of BRCAness that correlates with responsiveness to chemotherapy and with outcome in patients with epithelial ovarian cancer. J Clin Oncol. 2010;28(22):3555–3561. doi:10.1200/JCO.2009.27.5719.
  • Prime JE, Unwin L, Hunter J, et al. Abstract A119: A proteomics-based approach to identify biomarker profiles of homologous recombination deficiency (HRD) in breast cancer cell lines. Mol Cancer Ther. 2009;8(Supplement 1):A119–A119. doi:10.1158/1535-7163.TARG-09-A119.
  • Lee J-M, Hays JL, Annunziata CM, et al. Phase I/Ib study of olaparib and carboplatin in BRCA1 or BRCA2 mutation-associated breast or ovarian cancer with biomarker analyses. J Natl Cancer Inst. 2014;106(6):dju089. doi:10.1093/jnci/dju089.
  • Farmer H, McCabe N, Lord CJ, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature. 2005;434(7035):917–921. doi:10.1038/nature03445.
  • Shah MM, Dobbin ZC, Nowsheen S, et al. An ex vivo assay of XRT-induced Rad51 foci formation predicts response to PARP-inhibition in ovarian cancer. Gynecol Oncol. 2014;134(2):331–337. doi:10.1016/j.ygyno.2014.05.009.
  • O′Donnell RL, McCormick A, Mukhopadhyay A, et al. The use of ovarian cancer cells from patients undergoing surgery to generate primary cultures capable of undergoing functional analysis. PLoS One. 2014;9(3):e90604. doi:10.1371/journal.pone.0090604.
  • Hodgson D, Mason H, Oplustilova L, et al. Abstract 2398: activity of the PARP inhibitor olaparib in ATM-deficient gastric cancer: from preclinical models to the clinic. Cancer Res. 2014;74(19 Supplement):2398–2398. doi:10.1158/1538-7445.AM2014-2398.
  • Cremona CA, Behrens A. ATM signalling and cancer. Oncogene. 2014;33(26):3351–3360. doi:10.1038/onc.2013.275.
  • Weber AM, Ryan AJ. ATM and ATR as therapeutic targets in cancer. Pharmacol Ther. 2015;149:124–138. doi:10.1016/j.pharmthera.2014.12.001.
  • Kim HS, Choi SI, Min HL, et al. Mutation at intronic repeats of the ataxia-telangiectasia mutated (ATM) gene and ATM protein loss in primary gastric cancer with microsatellite instability. PLoS One. 2013;8(12):e82769. doi:10.1371/journal.pone.0082769.
  • Kang B, Guo R-F, Tan X-H, et al. Expression status of ataxia-telangiectasia-mutated gene correlated with prognosis in advanced gastric cancer. Mutat Res. 2008;638(1–2):17–25. doi:10.1016/j.mrfmmm.2007.08.013.
  • Guo X, Shen D, Cheng W, et al. Abstract B42: ATM deficiency sensitizes gastric cancer cells to the PARP inhibitior olaparib. Mol Cancer Ther. 2009;8(Supplement 1):B42–B42. doi:10.1158/1535-7163.TARG-09-B42.
  • Fenoglio-Preiser CM, Wang J, Stemmermann GN, et al. TP53 and gastric carcinoma: a review. Hum Mutat. 2003;21(3):258–270. doi:10.1002/humu.10180.
  • Bass AJ, Thorsson V, Shmulevich I, et al. Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014;513(7517):202–209. doi:10.1038/nature13480.
  • Zhang L, Jia G, Li W-M, et al. Alteration of the ATM gene occurs in gastric cancer cell lines and primary tumors associated with cellular response to DNA damage. Mutat Res. 2004;557(1):41–51 [cited 2004 Mar 28]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/14706517.
  • Huang D-S, Tao H-Q, He X-J, et al. Prevalence of deleterious ATM germline mutations in gastric cancer patients. Oncotarget. 2015;6(38):40953–40958. doi:10.18632/oncotarget.5944.
  • Kim HS, Kim MA, Hodgson D, et al. Concordance of ATM (ataxia telangiectasia mutated) immunohistochemistry between biopsy or metastatic tumor samples and primary tumors in gastric cancer patients. Pathobiology. 2013;80(3):127–137. doi:10.1159/000346034.
  • Bang Y-J, Im S-A, Lee K-W, et al. Randomized, double-blind Phase II trial with prospective classification by ATM protein level to evaluate the efficacy and tolerability of olaparib plus paclitaxel in patients with recurrent or metastatic gastric cancer. J Clin Oncol. 2015 Nov 20;33(33):3858–3865. doi:10.1200/JCO.2014.60.0320.
  • Gao J, Aksoy BA, Dogrusoz U, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013;6(269):pl1. doi:10.1126/scisignal.2004088.
  • Cerami E, Gao J, Dogrusoz U, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2(5):401–404. doi:10.1158/2159-8290.CD-12-0095.
  • Ruscito I, Dimitrova D, Vasconcelos I, et al. BRCA1 gene promoter methylation status in high-grade serous ovarian cancer patients – a study of the tumour Bank ovarian cancer (TOC) and ovarian cancer diagnosis consortium (OVCAD). Eur J Cancer. 2014;50(12):2090–2098. doi:10.1016/j.ejca.2014.05.001.
  • Alexandrov LB, Nik-Zainal S, Siu HC, et al. A mutational signature in gastric cancer suggests therapeutic strategies. Nat Commun. 2015;6:8683. doi:10.1038/ncomms9683.
  • PLATFORM: Planning treatment of oesophago-gastric (OG) cancer – a randomised maintenance therapy trial. Gastrointestinal Cancers Symposium |Abstracts |Meeting Library; 2016 [cited 2016 Mar 29]. Available from: http://meetinglibrary.asco.org/content/160052-173
  • Relationship between PD-L1 expression and clinical outcomes in patients (Pts) with advanced gastric cancer treated with the anti-PD-1 monoclonal antibody pembrolizumab (Pembro; MK-3475) in KEYNOTE-012. Gastrointestinal Cancers Symposium |Abstracts; 2015 [cited 2016 Mar 29]. Available from: http://meetinglibrary.asco.org/content/140536-158
  • 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. doi:10.18632/oncotarget.7277.
  • Le DT, Uram JN, Wang H, et al. PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med. 2015;372(26):2509–2520. doi:10.1056/NEJMoa1500596.
  • Kan C, Zhang J. BRCA1 mutation: a predictive marker for radiation therapy? Int J Radiat Oncol Biol Phys. 2015;93(2):281–293. doi:10.1016/j.ijrobp.2015.05.037.

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