87
Views
83
CrossRef citations to date
0
Altmetric
Review

Current status of poly(ADP-ribose) polymerase inhibitors and future directions

&
Pages 5195-5208 | Published online: 26 Oct 2017

References

  • BryantHESchultzNThomasHDSpecific killing of BRCA2-deficient tumours with inhibitors of poly (ADP-ribose) polymeraseNature2005434703591391715829966
  • FarmerHMcCabeNLordCJTargeting the DNA repair defect in BRCA mutant cells as a therapeutic strategyNature2005434703591792115829967
  • del RiveroJKohnECPARP Inhibitors: the cornerstone of DNA repair-targeted therapiesOncology (Williston Park)201731426527328412778
  • KaufmanBShapira-FrommerRSchmutzlerRKOlaparib monotherapy in patients with advanced cancer and a germline BRCA1/2 mutationJ Clin Oncol201533324425025366685
  • GelmonKATischkowitzMMackayHOlaparib 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 studyLancet Oncol201112985286121862407
  • LedermannJHarterPGourleyCOlaparib maintenance therapy in platinum-sensitive relapsed ovarian cancerN Engl J Med2012366151382139222452356
  • SwisherEMLinKKOzaAMRucaparib in relapsed, platinum-sensitive high-grade ovarian carcinoma (ARIEL2 Part 1): an international, multicentre, open-label, phase 2 trialLancet Oncol2017181758727908594
  • MirzaMRMonkBJHerrstedtJNiraparib maintenance therapy in platinum-sensitive, recurrent ovarian cancerN Engl J Med2016375222154216427717299
  • LinKYKrausWLPARP inhibitors for cancer therapyCell2017169218328388401
  • BoltonKLChenevix-TrenchGGohCAssociation between BRCA1 and BRCA2 mutations and survival in women with invasive epithelial ovarian cancerJAMA2012307438239022274685
  • Gonzalez-AnguloAMTimmsKMLiuSIncidence and outcome of BRCA mutations in unselected patients with triple receptor-negative breast cancerClin Cancer Res20111751082108921233401
  • LordCJAshworthABRCAness revisitedNat Rev Cancer201616211012026775620
  • McCabeNTurnerNCLordCJDeficiency in the repair of DNA damage by homologous recombination and sensitivity to poly (ADP-ribose) polymerase inhibitionCancer Res200666168109811516912188
  • ChambonPWeillJDMandelPNicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizing nuclear enzymeBiochem Biophys Res Commun196311394314019961
  • AshworthAA synthetic lethal therapeutic approach: poly (ADP) ribose polymerase inhibitors for the treatment of cancers deficient in DNA double-strand break repairJ Clin Oncol200826223785379018591545
  • BrownJSO’CarriganBJacksonSPYapTATargeting DNA repair in cancer: beyond PARP inhibitorsCancer Discov20177203728003236
  • AméJCRolliVSchreiberVPARP-2, a novel mammalian DNA damage-dependent poly(ADP-ribose) polymeraseJ Biol Chem199927425178601786810364231
  • McLornanDPListAMuftiGJApplying synthetic lethality for the selective targeting of cancerN Engl J Med20143711725173525354106
  • SchreiberVDantzerFAmeJCde MurciaGPoly (ADP-ribose): novel functions for an old moleculeNat Rev Mol Cell Biol20067751752816829982
  • LordCJAshworthAThe DNA damage response and cancer therapyNature201248128729422258607
  • PapaACarusoDStrudelMTomaoSTomaoFUpdate on Poly-ADP-ribose polymerase inhibition for ovarian cancer treatmentJ Transl Med20161426727634150
  • MuraiJHuangSYDasBBTrapping of PARP1 and PARP2 by clinical PARP inhibitorsCancer Res201272215588559923118055
  • PlummerERCalvertHTargeting poly (ADP-ribose) polymerase: a two-armed strategy for cancer therapyClin Cancer Res200713216252625617975135
  • LordCJAshworthAPARP inhibitors: synthetic lethality in the clinicScience201735563301152115828302823
  • AnnunziataCMO’ShaughnessyJPoly (ADP-ribose) polymerase as a novel therapeutic target in cancerClin Cancer Res201016184517452620823142
  • O’SullivanCCMoonDHKohnECLeeJMBeyond breast and ovarian cancers: PARP inhibitors for BRCA mutation-associated and BRCA-like solid tumorsFront Oncol201444224616882
  • ShrivastavMDe HaroLPNickoloffJARegulation of DNA double-strand break repair pathway choiceCell Res200818113414718157161
  • BenafifSHallMAn update on PARP inhibitors for the treatment of cancerOnco Targets Ther2015851952825750544
  • ByersLAWangJNilssonMBProteomic profiling identifies dysregulated pathways in small cell lung cancer and novel therapeutic targets including PARP1Cancer Discov20122979881122961666
  • RatnamKLowJACurrent development of clinical inhibitors of poly (ADP-ribose) polymerase in oncologyClin Cancer Res20071351383138817332279
  • RouleauMPatelAHendzelMJKaufmannSHPoirierGGPARP inhibition: PARP1 and beyondNat Rev Cancer201010429330120200537
  • Hughes-DaviesLHuntsmanDRuasMEMSY links the BRCA2 pathway to sporadic breast and ovarian cancerCell2003115552353514651845
  • LimDNgeowJEvaluation of the methods to identify patients who may benefit from PARP inhibitor useEndocr Relat Cancer2016236R267R28527226207
  • PenningtonKPWalshTHarrellMIGermline and somatic mutations in homologous recombination genes predict platinum response and survival in ovarian, fallopian tube, and peritoneal carcinomasClin Cancer Res201420376477524240112
  • MateoJCarreiraSSandhuSDNA-repair defects and olaparib in metastatic prostate cancerN Engl J Med20153731697170826510020
  • The Cancer Genome Atlas Research NetworkIntegrated genomic analyses of ovarian carcinomaNature2011474735360961521720365
  • PommierYO’ConnorMJde BonoJLaying a trap to kill cancer cells: PARP inhibitors and their mechanisms of actionSci Transl Med20168362s17
  • Postel-VinaySVanheckeEOlaussenKALordCJAshworthASoriaJCThe potential of exploiting DNA-repair defects for optimizing lung cancer treatmentNat Rev Clin Oncol20129314415522330686
  • MatulonisUAMonkBJPARP inhibitor and chemotherapy combination trials for the treatment of advanced malignancies: does a development pathway forward exist?Ann Oncol20172844344728057663
  • MuraiJZhangYMorrisJRationale for poly (ADP-ribose) polymerase (PARP) inhibitors in combination therapy with camptothecins or temozolomide based on PARP trapping versus catalytic inhibitionJ Pharmacol Exp Ther2014349340841624650937
  • IhnenMzu EulenburgCKolarovaTTherapeutic potential of the poly (ADP-ribose) polymerase inhibitor rucaparib for the treatment of sporadic human ovarian cancerMol Cancer Ther20131261002101523729402
  • DréanALordCJAshworthAPARP inhibitor combination therapyCrit Rev Oncol Hematol2016108738527931843
  • LuYKwintkiewiczJLiuYChemosensitivity of IDH1-mutated gliomas due to an impairment in PARP1-mediated DNA repairCancer Res20177771709171828202508
  • TateishiKHiguchiFMillerJJThe alkylating chemotherapeutic temozolomide induces metabolic stress in IDH1-mutant cancers and potentiates NAD+ depletion-mediated cytotoxicityCancer Res201777154102411528625978
  • FongPCBossDSYapTAInhibition of poly (ADP-ribose) polymerase in tumors from BRCA mutation carriersN Engl J Med2009361212313419553641
  • FongPCYapTABossDSPoly (ADP)-ribose polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free intervalJ Clin Oncol201028152512251920406929
  • AudehMWCarmichaelJPensonRTOral poly (ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trialLancet2010376973724525120609468
  • LedermannJHarterPGourleyCOlaparib 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 trialLancet Oncol20141585286124882434
  • TuttARobsonMGarberJEOral poly (ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trialLancet2010376973723524420609467
  • HopkinsTAShiYRodriguezLEMechanistic dissection of PARP1 trapping and the impact on in vivo tolerability and efficacy of PARP inhibitorsMol Cancer Res201513111465147726217019
  • de BonoJRamanathanRKMinaLPhase I, dose-escalation, two-part trial of the PARP inhibitor talazoparib in patients with advanced germline BRCA1/2 mutations and selected sporadic cancersCancer Discov20177662062928242752
  • KristeleitRSBurrisHALoRussoPPhase 1/2 study of oral rucaparib: final phase 1 resultsJ Clin Oncol201432suppl abstr2573
  • Shapira-FrommerROzaAMDomchekSMA phase II open-label, multicenter study of single-agent rucaparib in the treatment of patients with relapsed ovarian cancer and a deleterious BRCA mutationJ Clin Oncol201533suppl abstr5513
  • PuhallaSBeumerJHPahujaSFinal results of a phase 1 study of single-agent veliparib (V) in patients (pts) with either BRCA1/2-mutated cancer (BRCA+), platinum-refractory ovarian, or basal-like breast cancer (BRCA-wt)J Clin Oncol201432suppl abstr2570
  • ColemanRLSillMWBell-McGuinnKA phase II evaluation of the potent, highly selective PARP inhibitor veliparib in the treatment of persistent or recurrent epithelial ovarian, fallopian tube, or primary peritoneal cancer in patients who carry a germline BRCA1 or BRCA2 mutation – an NRG Oncology/Gynecologic Oncology Group studyGynecol Oncol2015137338639125818403
  • SandhuSKSchelmanWRWildingGThe poly (ADP-ribose) polymerase inhibitor niraparib (MK4827) in BRCA mutation carriers and patients with sporadic cancer: a phase 1 dose-escalation trialLancet Oncol201314988289223810788
  • Bell-McGuinnKMKonnerJATewWPA phase 2, single arm study of iniparib in patients with BRCA1 or BRCA2 associated advanced epithelial ovarian, fallopian tube, or primary peritoneal cancerInt J Gynecol Cancer201626225526026745694
  • WagnerLMProfile of veliparib and its potential in the treatment of solid tumorsOnco Targets Ther201581931193926251615
  • OzaAMCibulaDBenzaquenAOOlaparib combined with chemotherapy for recurrent platinum-sensitive ovarian cancer: a randomised phase 2 trialLancet Oncol201516879725481791
  • BangYJImSALeeKWRandomized, 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 cancerJ Clin Oncol2015333858386526282658
  • O’ShaughnessyJOsborneCPippenJEIniparib plus chemotherapy in metastatic triple-negative breast cancerN Engl J Med2011364320521421208101
  • LichtSCaoHLiZMechanism of action of iniparib: stimulation of reactive oxygen species (ROS) production in an iniparib-sensitive breast cancer cell lineMol Cancer Ther201110supl 11 abstrA226
  • GuhaMPARP inhibitors stumble in breast cancerNat Biotechnol20112937337421552220
  • O’ShaughnessyJSchwartzbergLDansoMAPhase III study of iniparib plus gemcitabine and carboplatin versus gemcitabine and carboplatin in patients with metastatic triple-negative breast cancerJ Clin Oncol201432343840384725349301
  • ChanNBristowRG“Contextual” synthetic lethality and/or loss of heterozygosity: tumor hypoxia and modification of DNA repairClin Cancer Res2010164553456020823145
  • LiuJFBarryWTBirrerMCombination cediranib and olaparib versus olaparib alone for women with recurrent platinum-sensitive ovarian cancer: a randomised phase 2 studyLancet Oncol201415111207121425218906
  • O’Sullivan CoyneGChenAPMeehanRDoroshowJHPARP inhibitors in reproductive system cancers: current use and developmentsDrugs201777211313028078645
  • LYNPARZA™ (olaparib) capsules, for oral use [prescribing information approved by the US FDA] Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2014/206162lbl.pdfAccessed August 22, 2017
  • StoverEHKonstantinopoulosPAMatulonisUASwisherEMBiomarkers of response and resistance to DNA repair targeted therapiesClin Cancer Res201622235651566027678458
  • RUBRACA™ (rucaparib) tablets, for oral use [prescribing information approved by the US FDA] Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2016/209115s000lbl.pdfAccessed August 22, 2017
  • ZEJULATM (niraparib) capsules, for oral use [prescribing information approved by the US FDA] Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2017/208447lbl.pdfAccessed August 22, 2017
  • WiggansAJCassGKBryantAPoly(ADP-ribose) polymerase (PARP) inhibitors for the treatment of ovarian cancerCochrane Database Syst Rev20155CD007929
  • SakaiWSwisherEMKarlanBYSecondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancersNature200845171821116112018264087
  • YachidaSJonesSBozicIDistant metastasis occurs late during the genetic evolution of pancreatic cancerNature201046773191114111720981102
  • TelliMLTimmsKMReidJHomologous recombination deficiency (HRD) score predicts response to platinum-containing neoadjuvant chemotherapy in patients with triple-negative breast cancerClin Cancer Res201622153764377326957554
  • GraeserMMcCarthyALordCJA marker of homologous recombination predicts pathologic complete response to neoadjuvant chemotherapy in primary breast cancerClin Cancer Res201016246159616820802015
  • von MinckwitzGMüllerBMLoiblSCytoplasmic poly(adenosine diphosphate-ribose) polymerase expression is predictive and prognostic in patients with breast cancer treated with neoadjuvant chemotherapyJ Clin Oncol201129162150215721519019
  • BrennerJCFengFYHanSPARP-1 inhibition as a targeted strategy to treat Ewing’s sarcomaCancer Res20127271608161322287547
  • MichelsJVitaleIGalluzziLCisplatin resistance associated with PARP hyperactivationCancer Res20137372271228023554447
  • MontoniARobuMPouliotEShahGMResistance to PARP-inhibitors in cancer therapyFront Pharmacol201341823450678
  • EdwardsSLBroughRLordCJResistance to therapy caused by intragenic deletion in BRCA2Nature200845171821111111518264088
  • BarberLJSandhuSChenLSecondary mutations in BRCA2 associated with clinical resistance to a PARP inhibitorJ Pathol2013229342242923165508
  • SwisherEMSakaiWKarlanBYWurzKUrbanNTaniguchiTSecondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistanceCancer Res20086882581258618413725
  • NorquistBWurzKAPennilCCSecondary somatic mutations restoring BRCA1/2 predict chemotherapy resistance in hereditary ovarian carcinomasJ Clin Oncol201129223008301521709188
  • DhillonKKSwisherEMTaniguchiTSecondary mutations of BRCA1/2 and drug resistanceCancer Sci201110266366921205087
  • BuntingSFCallénEWongN53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaksCell2010141224325420362325
  • BouwmanPAlyAEscandellJM53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancersNat Struct Mol Biol201017668869520453858
  • SourisseauTManiotisDMcCarthyAAurora-A expressing tumour cells are deficient for homology-directed DNA double strand-break repair and sensitive to PARP inhibitionEMBO Mol Med20102413014220373286
  • Mendes-PereiraAMMartinSABroughRSynthetic lethal targeting of PTEN mutant cells with PARP inhibitorsEMBO Mol Med200916–731532220049735
  • LiuXHanEKAndersonMAcquired resistance to combination treatment with temozolomide and ABT-888 is mediated by both base excision repair and homologous recombination DNA repair pathwaysMol Cancer Res20097101686169219825992
  • KondrashovaONguyenMShield-ArtinKSecondary somatic mutations restoring RAD51C and RAD51D associated with acquired resistance to the PARP inhibitor rucaparib in high-grade ovarian carcinomaCancer Discov20177998499828588062
  • RottenbergSJaspersJEKersbergenAHigh sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugsProc Natl Acad Sci U S A200810544170791708418971340
  • KimYKimASharipAReverse the resistance to PARP inhibitorsInt J Biol Sci20171319820828255272
  • Ter BruggePKristelPvan der BurgEMechanisms of therapy resistance in patient-derived xenograft models of BRCA1-deficient breast cancerJ Natl Cancer Inst201610811djw148
  • ChoiYEMeghaniKBraultMEPlatinum and PARP inhibitor resistance due to overexpression of microRNA-622 in BRCA1-mutant ovarian cancerCell Rep201614342943926774475
  • DuYYamaguchiHWeiYBlocking c-Met-mediated PARP1 phosphorylation enhances anti-tumor effects of PARP inhibitorsNat Med20162219420126779812
  • EspositoMTZhaoLFungTKSynthetic lethal targeting of oncogenic transcription factors in acute leukemia by PARP inhibitorsNat Med201521121481149026594843
  • PatchAMChristieELEtemadmoghadamDWhole-genome characterization of chemoresistant ovarian cancerNature2015521755348949426017449
  • BoothCMEisenhauerEAProgression-free survival: meaningful or simply measurable?J Clin Oncol201230101030103322370321
  • SonnenblickAde AzambujaEAzimHAJrPiccartMAn update on PARP inhibitors – moving to the adjuvant settingNat Rev Clin Oncol2015121274125286972