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Emerging PARP inhibitors for treating breast cancer

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Pages 211-221 | Received 28 Feb 2018, Accepted 20 Sep 2018, Published online: 29 Sep 2018

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016 Feb;66(1):7–30.
  • Cancer genome atlas network. Comprehensive molecular portraits of human breast tumours. Nature. 2012 Oct 4;490(7418):61–70.
  • Turner N, Tutt A, Ashworth A. Hallmarks of “BRCAness” in sporadic cancers. Nat Rev Cancer. 2004 Oct;4(10):814–819.
  • Morris GJ, Naidu S, Topham AK, et al. Differences in breast carcinoma characteristics in newly diagnosed African-American and Caucasian patients: a single-institution compilation compared with the National Cancer Institute’s Surveillance, Epidemiology, and end results database. Cancer. 2007 Aug 15;110(4):876–884.
  • Rastelli F, Biancanelli S, Falzetta A, et al. Triple-negative breast cancer: current state of the art. Tumori. 2010 Dec;96(6):875–888.
  • Lehmann BD, Jovanović B, Chen X, et al. Refinement of triple-negative breast cancer molecular subtypes: implications for neoadjuvant chemotherapy selection. PloS One. 2016;11(6):e0157368.
  • Lehmann BD, Bauer JA, Chen X, et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest. 2011 Jul;121(7):2750–2767.
  • Bareche Y, Venet D, Ignatiadis M, et al. Unravelling triple-negative breast cancer molecular heterogeneity using an integrative multiomic analysis. Ann Oncol Off J Eur Soc Med Oncol. 2018 Apr 1;29(4):895–902.
  • Bettaieb A, Paul C, Plenchette S, et al. Precision medicine in breast cancer: reality or utopia? J Transl Med. 2017 Jun 17;15(1):139.
  • Brown SD, Warren RL, Gibb EA, et al. Neo-antigens predicted by tumor genome meta-analysis correlate with increased patient survival. Genome Res. 2014 May;24(5):743–750.
  • Loi S, Sirtaine N, Piette F, et al. Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02-98. J Clin Oncol Off J Am Soc Clin Oncol. 2013 Mar 1;31(7):860–867.
  • Wimberly H, Brown JR, Schalper K, et al. PD-L1 expression correlates with tumor-infiltrating lymphocytes and response to neoadjuvant chemotherapy in breast cancer. Cancer Immunol Res. 2015 Apr;3(4):326–332.
  • Ali HR, Glont S-E, Blows FM, et al. PD-L1 protein expression in breast cancer is rare, enriched in basal-like tumours and associated with infiltrating lymphocytes. Ann Oncol Off J Eur Soc Med Oncol. 2015 Jul;26(7):1488–1493.
  • Denkert C, von Minckwitz G, Darb-Esfahani S, et al. Tumour-infiltrating lymphocytes and prognosis in different subtypes of breast cancer: a pooled analysis of 3771 patients treated with neoadjuvant therapy. Lancet Oncol. 2018 Jan;19(1):40–50.
  • Dawson SJ, Provenzano E, Caldas C. Triple negative breast cancers: clinical and prognostic implications. Eur J Cancer Oxf Engl 1990. 2009 Sep;45(Suppl 1):27–40.
  • Malorni L, Shetty PB, De Angelis C, et al. Clinical and biologic features of triple-negative breast cancers in a large cohort of patients with long-term follow-up. Breast Cancer Res Treat. 2012 Dec;136(3):795–804.
  • Bianchini G, Balko JM, Mayer IA, et al. Triple-negative breast cancer: challenges and opportunities of a heterogeneous disease. Nat Rev Clin Oncol. 2016 Nov;13(11):674–690.
  • Carey LA, Dees EC, Sawyer L, et al. The triple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin Cancer Res Off J Am Assoc Cancer Res. 2007 Apr 15;13(8):2329–2334.
  • Bonotto M, Gerratana L, Poletto E, et al. Measures of outcome in metastatic breast cancer: insights from a real-world scenario. Oncologist. 2014 Jun;19(6):608–615.
  • Dent R, Trudeau M, Pritchard KI, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res Off J Am Assoc Cancer Res. 2007 Aug 1;13(15 Pt 1):4429–4434.
  • Cardoso F, Costa A, Senkus E, et al. 3rd ESO-ESMO International Consensus Guidelines for Advanced Breast Cancer (ABC 3). Ann Oncol Off J Eur Soc Med Oncol. 2017 Dec 1;28(12):3111.
  • Partridge AH, Rumble RB, Carey LA, et al. Chemotherapy and targeted therapy for women with human epidermal growth factor receptor 2-negative (or unknown) advanced breast cancer: American Society of Clinical Oncology Clinical Practice Guideline. J Clin Oncol Off J Am Soc Clin Oncol. 2014 Oct 10;32(29):3307–3329.
  • Miller K, Wang M, Gralow J, et al. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N Engl J Med. 2007 Dec 27;357(26):2666–2676.
  • Mieog JSD, van der Hage JA. van de Velde CJH. Preoperative chemotherapy for women with operable breast cancer. Cochrane Database Syst Rev. 2007 Apr;18(2):CD005002.
  • Symmans WF, Wei C, Gould R, et al. Long-term prognostic risk after neoadjuvant chemotherapy associated with residual cancer burden and breast cancer subtype. J Clin Oncol Off J Am Soc Clin Oncol. 2017 Apr 1;35(10):1049–1060.
  • Chae YK, Anker JF, Carneiro BA, et al. Genomic landscape of DNA repair genes in cancer. Oncotarget. 2016 Mar 19;7(17):23312–23321.
  • Dizdar O, Arslan C, Altundag K. Advances in PARP inhibitors for the treatment of breast cancer. Expert Opin Pharmacother. 2015 Dec 12;16(18):2751–2758.
  • Lord CJ, Ashworth A. PARP inhibitors: synthetic lethality in the clinic. Science (80- ). 2017;355(6330):1152–1158.
  • Farmer H, McCabe N, Lord CJ, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature. 2005 Apr 14;434(7035):917–921.
  • Thompson D, Easton D. The genetic epidemiology of breast cancer genes. J Mammary Gland Biol Neoplasia. 2004 Jul;9(3):221–236.
  • Lord CJ, Ashworth A. BRCAness revisited. Nat Rev Cancer. 2016 Feb;16(2):110–120.
  • Couch FJ, Nathanson KL, Offit K. Two decades after BRCA: setting paradigms in personalized cancer care and prevention. Science (80- ). 2014 Mar 28;343(6178):1466–1470.
  • King M-C. “The race” to clone BRCA1. Science (80- ). 2014 Mar 28;343(6178):1462–1465.
  • Bryant HE, Schultz N, Thomas HD, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature. 2005 Apr 14;434(7035):913–917.
  • Murai J, Huang SN, Das BB, et al. Trapping of PARP1 and PARP2 by clinical PARP inhibitors. Cancer Res. 2012 Nov 1;72(21):5588–5599.
  • Murai J, Zhang Y, Morris J, et al. Rationale for poly(ADP-ribose) polymerase (PARP) inhibitors in combination therapy with camptothecins or temozolomide based on PARP trapping versus catalytic inhibition. J Pharmacol Exp Ther. 2014 Jun;349(3):408–416.
  • Murai J, Huang S-YN, Renaud A, et al. Stereospecific PARP trapping by BMN 673 and comparison with olaparib and rucaparib. Mol Cancer Ther. 2014 Feb;13(2):433–443.
  • O’Shaughnessy J, Schwartzberg L, Danso MA, et al. Phase III study of iniparib plus gemcitabine and carboplatin versus gemcitabine and carboplatin in patients with metastatic triple-negative breast cancer. J Clin Oncol Off J Am Soc Clin Oncol. 2014 Dec 1;32(34):3840–3847.
  • O’Shaughnessy J, Osborne C, Pippen JE, et al. Iniparib plus chemotherapy in metastatic triple-negative breast cancer. N Engl J Med. 2011 Jan 20;364(3):205–214.
  • 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 Jul 9;361(2):123–134.
  • 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 Jun;106(6):dju089.
  • 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 Lond Engl. 2010 Jul 24;376(9737):235–244.
  • Gelmon KA, Tischkowitz M, Mackay H, et al. Olaparib in patients with recurrent high-grade serous or poorly differentiated ovarian carcinoma or triple-negative breast cancer: a phase 2, multicentre, open-label, non-randomised study. Lancet Oncol. 2011 Sep;12(9):852–861.
  • Robson M, Im S-A, Senkus E, et al. Olaparib for metastatic breast cancer in patients with a germline BRCA mutation. N Engl J Med. 2017 10;377(6):523–533.
  • Research C for DE and Approved Drugs. FDA approves olaparib for germline BRCA-mutated metastatic breast cancer [Internet]. [ cited 2018 Jan 25]; Available from: https://www.fda.gov/Drugs/InformationOnDrugs/ApprovedDrugs/ucm592357.htm
  • Isakoff SJ, Overmoyer B, Tung NM, et al. A phase II trial of the PARP inhibitor veliparib (ABT888) and temozolomide for metastatic breast cancer. J Clin Oncol [Internet]. cited 2018 Jan 25 Available from 2016 Sep 22. DOI:10.1200/jco.2010.28.15_suppl.1019
  • Somlo G, Frankel PH, Arun BK, et al. Efficacy of the PARP inhibitor veliparib with carboplatin or as a single agent in patients with germline BRCA1- or BRCA2-associated metastatic breast cancer: California cancer consortium trial NCT01149083. Clin Cancer Res Off J Am Assoc Cancer Res. 2017 Aug 1;23(15):4066–4076.
  • Rodler ET, Kurland BF, Griffin M, et al. Phase I study of veliparib (ABT-888) combined with cisplatin and vinorelbine in advanced triple-negative breast cancer and/or BRCA mutation-associated breast cancer. Clin Cancer Res Off J Am Assoc Cancer Res. 2016 Jun 15;22(12):2855–2864.
  • Kummar S, Wade JL, Oza AM, et al. Randomized phase II trial of cyclophosphamide and the oral poly (ADP-ribose) polymerase inhibitor veliparib in patients with recurrent, advanced triple-negative breast cancer. Invest New Drugs. 2016;34(3):355–363.
  • Mehta MP, Wang D, Wang F, et al. Veliparib in combination with whole brain radiation therapy in patients with brain metastases: results of a phase 1 study. J Neurooncol. 2015 Apr;122(2):409–417.
  • Geyer CE, O’Shaughnessy J, Untch M, et al. Phase 3 study evaluating efficacy and safety of veliparib (V) plus carboplatin (Cb) or Cb in combination with standard neoadjuvant chemotherapy (NAC) in patients (pts) with early stage Triple-Negative Breast Cancer (TNBC). J Clin Oncol. 2017 May 20;35(15_suppl):520.
  • Rugo HS, Olopade OI, DeMichele A, et al. Adaptive randomization of Veliparib-carboplatin treatment in breast cancer. N Engl J Med. 2016 Jul 7;375(1):23–34.
  • Litton J, Rugo H, Ettl J. EMBRACA: a phase 3 trial comparing talazoparib, an oral PARP inhibitor, to physician’s choice of therapy in patients with advanced breast cancer and a germline. BRCA Mutation [Internet]. 2017 cited 2018 Jan 25. Available from: http://www.abstracts2view.com/sabcs/view.php?nu=SABCS17L_1735&terms=
  • Mirza MR, Monk BJ, Herrstedt J, et al. Niraparib maintenance therapy in platinum-sensitive, recurrent ovarian cancer. N Engl J Med. 2016;375(22):2154–2164.
  • Sandhu SK, Schelman WR, Wilding G, et al. The poly(ADP-ribose) polymerase inhibitor niraparib (MK4827) in BRCA mutation carriers and patients with sporadic cancer: a phase 1 dose-escalation trial. Lancet Oncol. 2013 Aug;14(9):882–892.
  • Drew Y, Ledermann J, Hall G, et al. Phase 2 multicentre trial investigating intermittent and continuous dosing schedules of the poly(ADP-ribose) polymerase inhibitor rucaparib in germline BRCA mutation carriers with advanced ovarian and breast cancer. Br J Cancer. 2016 Mar 29;114(7):723–730.
  • McNeish IA, Oza AM, Coleman RL, et al. Results of ARIEL2: A Phase 2 trial to prospectively identify ovarian cancer patients likely to respond to rucaparib using tumor genetic analysis. J Clin Oncol [Internet]. cited 2018 Jan 25 Available from 2017 Jan 31. DOI:10.1200/jco.2015.33.15_suppl.5508
  • Patsouris A, Vicier C, Campion L, et al. An open-label, phase II study of rucaparib, a PARP inhibitor, in HER2- metastatic breast cancer patients with high genomic loss of heterozygosity: RUBY. J Clin Oncol. 2017 May 20;35(15_suppl):TPS1117–TPS1117.
  • 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 Off J Am Soc Clin Oncol. 2010 May 20;28(15):2512–2519.
  • 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 Aug 15;66(16):8109–8115.
  • Robert M, Frenel J-S, Gourmelon C, et al. Olaparib for the treatment of breast cancer. Expert Opin Investig Drugs. 2017 Jun;26(6):751–759.
  • Lim JSJ, Tan DSP. Understanding resistance mechanisms and expanding the therapeutic utility of PARP inhibitors. Cancers (Basel). 2017 Aug 22;9(8).
  • Berger NA. Poly(ADP-ribose) in the cellular response to DNA damage. Radiat Res. 1985 Jan;101(1):4–15.
  • Durkacz BW, Omidiji O, Gray DA, et al. (ADP-ribose)n participates in DNA excision repair. Nature. 1980 Feb 7;283(5747):593–596.
  • Galluzzi L, Senovilla L, Zitvogel L, et al. The secret ally: immunostimulation by anticancer drugs. Nat Rev Drug Discov. 2012 Feb 3;11(3):215–233.
  • 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 Nov;3(11):1257–1268.
  • Jiao S, Xia W, Yamaguchi H, et al. PARP inhibitor upregulates PD-L1 expression and enhances cancer-associated immunosuppression. Clin Cancer Res [Internet]. 2017 Feb 6 [cited 2017 Sep 28]. Available from: http://clincancerres.aacrjournals.org/content/early/2017/05/01/1078-0432.CCR-16-3215
  • Lee J-M, Cimino-Mathews A, Peer CJ, et al. Safety and clinical activity of the programmed death-ligand 1 inhibitor durvalumab in combination with poly (ADP-Ribose) polymerase inhibitor olaparib or vascular endothelial growth factor receptor 1-3 inhibitor cediranib in women’s cancers: a dose-escalation, phase I study. J Clin Oncol Off J Am Soc Clin Oncol. 2017 Jul 1;35(19):2193–2202.
  • Timms KM, Abkevich V, Hughes E, et al. Association of BRCA1/2 defects with genomic scores predictive of DNA damage repair deficiency among breast cancer subtypes. Breast Cancer Res BCR. 2014 Dec 5;16(6):475.
  • Richardson LA, Silver DP, Szallasi Z, et al. Abstract P3-06-11: homologous recombination deficiency (HRD) assay predicts response to cisplatin neoadjuvant chemotherapy in patients with triple negative breast cancer. Cancer Res. 2015 May;1(75):P3–06.
  • Watkins J, Weekes D, Shah V, et al. Genomic complexity profiling reveals that HORMAD1 overexpression contributes to homologous recombination deficiency in triple-negative breast cancers. Cancer Discov. 2015 5;May(5):488–505.
  • 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.
  • Montoni A, Robu M, Pouliot E, et al. Resistance to PARP-inhibitors in cancer therapy. Front Pharmacol. 2013;4:18.
  • Lord CJ, Ashworth A. Mechanisms of resistance to therapies targeting BRCA-mutant cancers. Nat Med. 2013 Nov;19(11):1381–1388.
  • Jaspers JE, Kersbergen A, Boon U, et al. Loss of 53BP1 causes PARP inhibitor resistance in Brca1-mutated mouse mammary tumors. Cancer Discov. 2013 Jan;3(1):68–81.
  • Patel AG, Sarkaria JN, Kaufmann SH. Nonhomologous end joining drives poly(ADP-ribose) polymerase (PARP) inhibitor lethality in homologous recombination-deficient cells. Proc Natl Acad Sci USA. 2011 Feb 22;108(8):3406–3411.
  • Xu G, Chapman JR, Brandsma I, et al. REV7 counteracts DNA double-strand break resection and affects PARP inhibition. Nature. 2015 May 28;521(7553):541–544.
  • Ledermann JA, Harter P, Gourley C, et al. Overall survival in patients with platinum-sensitive recurrent serous ovarian cancer receiving olaparib maintenance monotherapy: an updated analysis from a randomised, placebo-controlled, double-blind, phase 2 trial. Lancet Oncol. 2016 Nov;17(11):1579–1589.
  • Kaufman B, Shapira-Frommer R, Schmutzler RK, et al. Olaparib monotherapy in patients with advanced cancer and a germline BRCA1/2 mutation. J Clin Oncol Off J Am Soc Clin Oncol. 2015 Jan 20;33(3):244–250.
  • Bonner WM, Redon CE, Dickey JS, et al. GammaH2AX and cancer. Nat Rev Cancer. 2008 Dec;8(12):957–967.
  • Rogakou EP, Pilch DR, Orr AH, et al. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem. 1998 Mar 6;273(10):5858–5868.
  • Lowndes NF, Toh GW-L. DNA repair: the importance of phosphorylating histone H2AX. Curr Biol CB. 2005 Feb 8;15(3):R99–102.
  • Sonnenblick A, de Azambuja E, Azim HA, et al. An update on PARP inhibitors–moving to the adjuvant setting. Nat Rev Clin Oncol. 2015 Jan;12(1):27–41.

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