Login Register Cart 0
Generic placeholder image

Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Poly (ADP-Ribose) Polymerases (PARPs) and PARP Inhibitor-Targeted Therapeutics

Author(s): Nan Li*, Yifan Wang, Weiye Deng and Steven H. Lin*

Volume 19, Issue 2, 2019

Page: [206 - 212] Pages: 7

DOI: 10.2174/1871520618666181109164645

Price: $65

Abstract

Background: Poly-ADP-ribosylation, that is, adding ADP-ribose moieties to a protein, is a unique type of protein post-translational modification that regulates various cellular processes such as DNA repair, mitosis, transcription, and cell growth. Small-molecule inhibitors of poly-ADP-ribose polymerase 1 (PARP1) have been developed as anticancer agents because inhibition of PARP enzymes may be a synthetic lethal strategy for cancers with or BRCA2 mutations. However, there are still questions surrounding PARP inhibitors.

Methods/Results: Data were collected from Pubmed, Medline, through searching of these keywords: “PARP”, “BRCA”, “Synthetic lethal” and “Tankyrase inhibitors”. We describe the current knowledge of PARP inhibition and its effects on DNA damage; mechanisms of resistance to PARP inhibitors; the evolution of PARP inhibitors; and the potential use of PARP5a/b (tankyrases) inhibitors in cancer treatment.

Conclusion: PARP inhibitors are already showing promise as therapeutic tools, especially in the management of BRCA-mutated breast and ovarian cancers but also in tumors with dysfunctional BRCA genes. Small-molecule tankyrase inhibitors are important for increasing our understanding of tankyrase biology.

Keywords: PARP inhibitors, BRCA mutation, synthetic lethal, Tankyrase inhibitors, poly-ADP-ribose polymerase 1, ovarian cancers.

« Previous Next »
Graphical Abstract

[1]
Okano, S.; Lan, L.; Caldecott, K.W.; Mori, T.; Yasui, A. Spatial and temporal cellular responses to single-strand breaks in human cells. Mol. Cell. Biol., 2003, 23(11), 3974-3981.
[2]
Dantzer, F.; Schreiber, V.; Niedergang, C.; Trucco, C.; Flatter, E.; De-La-Rubia, G.; Oliver, J.; Rolli, V.; Menissier-de Murcia, J.; de-Murcia, G. Involvement of poly(ADP-ribose) polymerase in base excision repair. Biochimie, 1999, 81(1-2), 69-75.
[3]
Ali, A.A.E.; Timinszky, G.; Arribas-Bosacoma, R.; Kozlowski, M.; Hassa, P.O.; Hassler, M.; Ladurner, A.G.; Pearl, L.H.; Oliver, A.W. The zinc-finger domains of PARP1 cooperate to recognize DNA strand breaks. Nat. Struct. Mol. Biol., 2012, 19(7), 685-692.
[4]
Smith, S.; Giriat, I.; Schmitt, A.; de-Lange, T. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science, 1998, 282(5393), 1484-1487.
[5]
Huang, S.M.A.; Mishina, Y.M.; Liu, S.M.; Cheung, A.; Stegmeier, F.; Michaud, G.A.; Charlat, O.; Wiellette, E.; Zhang, Y.; Wiessner, S.; Hild, M. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature, 2009, 461(7264), 614-620.
[6]
Li, N.; Zhang, Y.; Han, X.; Liang, K.; Wang, J.; Feng, L.; Wang, W.; Songyang, Z.; Lin, C.; Yang, L.; Yu, Y. Poly-ADP ribosylation of PTEN by tankyrases promotes PTEN degradation and tumor growth. Genes Dev., 2015, 29(2), 157-170.
[7]
Wang, W.; Li, N.; Li, X.; Tran, M.K.; Han, X.; Chen, J. Tankyrase Inhibitors Target YAP by Stabilizing Angiomotin Family Proteins. Cell Reports, 2015, 13(3), 524-532.
[8]
Altmeyer, M.; Messner, S.; Hassa, P.O.; Fey, M.; Hottiger, M.O. Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res., 2009, 37(11), 3723-3738.
[9]
Gibson, B.A.; Kraus, W.L. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat. Rev. Mol. Cell Biol., 2012, 13(7), 411-424.
[10]
Vyas, S.; Chang, P. New PARP targets for cancer therapy. Nat. Rev. Cancer, 2014, 14(7), 502-509.
[11]
Li, N.; Chen, J.J. ADP-Ribosylation: Activation, Recognition, and Removal. Mol. Cells, 2014, 37(1), 9-16.
[12]
Gupte, R.; Liu, Z.Y.; Kraus, W.L. PARPs and ADP-ribosylation: recent advances linking molecular functions to biological outcomes. Genes Dev., 2017, 31(2), 101-126.
[13]
Vyas, S.; Matic, I.; Uchima, L.; Rood, J.; Zaja, R.; Hay, R.T.; Ahel, I.; Chang, P. Family-wide analysis of poly(ADP-ribose) polymerase activity. Nat. Commun., 2014, 5, 4426.
[14]
Kiehlbauch, C.C.; Aboul-Ela, N.; Jacobson, E.L.; Ringer, D.P.; Jacobson, M.K. High resolution fractionation and characterization of ADP-ribose polymers. Anal. Biochem., 1993, 208(1), 26-34.
[15]
Pleschke, J.M.; Kleczkowska, H.E.; Strohm, M.; Althaus, F.R. Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J. Biol. Chem., 2000, 275(52), 40974-40980.
[16]
Scolnick, D.M.; Halazonetis, T.D. Chfr defines a mitotic stress checkpoint that delays entry into metaphase. Nature, 2000, 406(6794), 430-435.
[17]
Iles, N.; Rulten, S.; El-Khamisy, S.F.; Caldecott, K.W. APLF (C2orf13) is a novel human protein involved in the cellular response to chromosomal DNA strand breaks. Mol. Cell. Biol., 2007, 27(10), 3793-3803.
[18]
Oberoi, J.; Richards, M.W.; Crumpler, S.; Brown, N.; Blagg, J.; Bayliss, R. Structural basis of poly(ADP-ribose) recognition by the multizinc binding domain of checkpoint with forkhead-associated and RING Domains (CHFR). J. Biol. Chem., 2010, 285(50), 39348-39358.
[19]
Liu, C.; Vyas, A.; Kassab, M.A.; Singh, A.K.; Yu, X.C. The role of poly ADP-ribosylation in the first wave of DNA damage response. Nucleic Acids Res., 2017, 45(14), 8129-8141.
[20]
Zhang, Y.; Liu, S.; Mickanin, C.; Feng, Y.; Charlat, O.; Michaud, G.A.; Schirle, M.; Shi, X.; Hild, M.; Bauer, A.; Myer, V.E. RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling. Nat. Cell Biol., 2011, 13(5), 623.
[21]
Li, M.; Lu, L.Y.; Yang, C.Y.; Wang, S.M.; Yu, X.C. The FHA and BRCT domains recognize ADP-ribosylation during DNA damage response. Genes Dev., 2013, 27(16), 1752-1768.
[22]
Li, M.; Yu, X. Function of BRCA1 in the DNA damage response is mediated by ADP-ribosylation. Cancer Cell, 2013, 23(5), 693-704.
[23]
Min, W.; Bruhn, C.; Grigaravicius, P.; Zhou, Z.W.; Li, F.; Kruger, A.; Siddeek, B.; Greulich, K.O.; Popp, O.; Meisezahl, C. Calkhoven, C.F. Poly(ADP-ribose) binding to Chk1 at stalled replication forks is required for S-phase checkpoint activation. Nat. Commun., 2013, 4, 2993.
[24]
Li, N.; Feng, L.; Liu, H.; Wang, J.D.; Kasembeli, M.; Tran, M.K.; Tweardy, D.J.; Lin, S.H.; Chen, J.J. PARP inhibition suppresses growth of EGFR-mutant cancers by targeting nuclear PKM2. Cell Reports, 2016, 15(4), 843-856.
[25]
Ikejima, M.; Gill, D.M. Poly(Adp-Ribose) degradation by glycohydrolase starts with an endonucleolytic incision. J. Biol. Chem., 1988, 263(23), 11037-11040.
[26]
Sharifi, R.; Morra, R.; Appel, C.D.; Tallis, M.; Chioza, B.; Jankevicius, G.; Simpson, M.A.; Matic, I.; Ozkan, E.; Golia, B.; Schellenberg, M.J. Deficiency of terminal ADP-ribose protein glycohydrolase TARG1/C6orf130 in neurodegenerative disease. EMBO J., 2013, 32(9), 1225-1237.
[27]
Oka, S.; Kato, J.; Moss, J. Identification and characterization of a mammalian 39-kDa poly(ADP-ribose) glycohydrolase. J. Biol. Chem., 2006, 281(2), 705-713.
[28]
Palazzo, L.; Thomas, B.; Jemth, A.S.; Colby, T.; Leidecker, O.; Feijs, K.L.; Zaja, R.; Loseva, O.; Puigvert, J.C.; Matic, I.; Helleday, T. Processing of protein ADP-ribosylation by Nudix hydrolases. Biochem. J., 2015, 468(2), 293-301.
[29]
Palazzo, L.; Daniels, C.M.; Nettleship, J.E.; Rahman, N.; McPherson, R.L.; Ong, S.E.; Kato, K.; Nureki, O.; Leung, A.K.; Ahel, I. ENPP1 processes protein ADP-ribosylation in vitro. FEBS J., 2016, 283(18), 3371-3388.
[30]
Ame, J.C.; Spenlehauer, C.; de-Murcia, G. The PARP superfamily. BioEssays, 2004, 26(8), 882-893.
[31]
Dantzer, F.; Ame, J.C.; Schreiber, V.; Nakamura, J.; Menissier-de Murcia, J.; de-Murcia, G. Poly(ADP-ribose) polymerase-1 activation during DNA damage and repair. DNA Repair. Pt B, 2006, 409, 493-510.
[32]
Lindahl, T.; Satoh, M.S.; Poirier, G.G.; Klungland, A. Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem. Sci., 1995, 20(10), 405-411.
[33]
Hoeijmakers, J.H.J. Genome maintenance mechanisms for preventing cancer. Nature, 2001, 411(6835), 366-374.
[34]
Tutt, A.; Ashworth, A. The relationship between the roles of BRCA genes in DNA repair and cancer predisposition. Trends Mol. Med., 2002, 8(12), 571-576.
[35]
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.
[36]
Patel, K.J.; Yu, V.P.C.C.; Lee, H.S.; Corcoran, A.; Thistlethwaite, F.C.; Evans, M.J.; Colledge, W.H.; Friedman, L.; Ponder, B.A.J.; Venkitaraman, A.R. Involvement of Brca2 in DNA repair. Mol. Cell, 1998, 1(3), 347-357.
[37]
Feng, L.; Li, N.; Li, Y.; Wang, J.; Gao, M.; Wang, W.; Chen, J. Cell cycle-dependent inhibition of 53BP1 signaling by BRCA1. Cell Discov., 2015, 1, 15019.
[38]
Wooster, R.; Weber, B.L. Breast and ovarian cancer. N. Engl. J. Med., 2003, 348(23), 2339-2347.
[39]
Schultz, N.; Lopez, E.; Saleh-Gohari, N.; Helleday, T. Poly(ADP-ribose) polymerase (PARP-1) has a controlling role in homologous recombination. Nucleic Acids Res., 2003, 31(17), 4959-4964.
[40]
Bryant, H.E.; Schultz, N.; Thomas, H.D.; Parker, K.M.; Flower, D.; Lopez, E.; Kyle, S.; Meuth, M.; Curtin, N.J.; Helleday, T. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature, 2005, 434(7035), 913-917.
[41]
Farmer, H.; McCabe, N.; Lord, C.J.; Tutt, A.N.J.; Johnson, D.A.; Richardson, T.B.; Santarosa, M.; Dillon, K.J.; Hickson, I.; Knights, C.; Martin, N.M. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature, 2005, 434(7035), 917-921.
[42]
Clark, J.B.; Ferris, G.M.; Pinder, S. Inhibition of nuclear nad nucleosidase and poly ADP-Ribose polymerase activity from rat liver by nicotinamide and 5′-Methyl nicotinamide. Biochim. Biophys. Acta, 1971, 238(1), 82-85.
[43]
Kupper, J.H.; Muller, M.; Jacobson, M.K.; Tatsumi-Miyajima, J.; Coyle, D.L.; Jacobson, E.L.; Burkle, A. Trans-dominant inhibition of poly(ADP-ribosyl)ation sensitizes cells against gamma-irradiation and N-methyl-N'-nitro-N-nitrosoguanidine but does not limit DNA replication of a polyomavirus replicon. Mol. Cell. Biol., 1995, 15(6), 3154-3163.
[44]
Bowman, K.J.; White, A.; Golding, B.T.; Griffin, R.J.; Curtin, N.J. Potentiation of anti-cancer agent cytotoxicity by the potent poly(ADP-ribose) polymerase inhibitors NU1025 and NU1064. Br. J. Cancer, 1998, 78(10), 1269-1277.
[45]
Zaremba, T.; Jane-Curtin, N. PARP inhibitor development for systemic cancer targeting. Anticancer. Agents Med. Chem., 2007, 7(5), 515-523.
[46]
Plummer, R.; Middleton, M.; Wilson, R.; Evans, J.; Jones, C.; Olson, A.; Boddy, A.; Curtin, N.; Kaufman, R.; Harris, A. Final clinical, pharmacokinetic and pharmacodynamic results of the phase I study of the novel Poly(ADP-Ribose) Polymerase (PARP) inhibitor, AG014699, in combination with temozolomide. Clin. Cancer Res., 2005, 11(24), 9099s-9099s.
[47]
Bedikian, A.Y.; Papadopoulos, N.E.; Kim, K.B.; Hwu, W.J.; Homsi, J.; Glass, M.R.; Cain, S.; Rudewicz, P.; Vernillet, L.; Hwu, P. A phase IB trial of intravenous INO-1001 plus oral temozolomide in subjects with unresectable stage-III or IV melanoma. Cancer Invest., 2009, 27(7), 756-763.
[48]
Penson, R.T.; Whalen, C.; Lasonde, B.; Krasner, C.N.; Konstantinopoulos, P.; Stallings, T.E.; Bradley, C.R.; Birrer, M.J.; Matulonis, U. A phase II trial of iniparib (BSI-201) in combination with gemcitabine/carboplatin (GC) in patients with platinum-sensitive recurrent ovarian cancer. J. Clin. Oncol., 2011, 29(15), 5004.
[49]
Huggins-Puhalla, S.L.; Beumer, J.H.; Appleman, L.J.; Tawbi, H.A.H.; Stoller, R.G.; Lin, Y.; Kiesel, B.; Tan, A.R.; Gibbon, D.; Jiang, Y.X. A phase I study of chronically dosed, single-agent veliparib (ABT-888) in patients (pts) with either BRCA 1/2-mutated cancer (BRCA plus), platinum-refractory ovarian cancer, or basal-like breast cancer (BRCA-wt). J. Clin. Oncol., 2012, 30(15), 2855-2864.
[50]
Swisher, E.M.; Lin, K.K.; Oza, A.M.; Scott, C.L.; Giordano, H.; Sun, J.; Konecny, G.E.; Coleman, R.L.; Tinker, A.V.; O’Malley, D.M.; Kristeleit, R.S. 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.
[51]
De-Bono, J.S.; Mina, L.A.; Gonzalez, M.; Curtin, N.J.; Wang, E.; Henshaw, J.W.; Chadha, M.; Sachdev, J.C.; Matei, D.; Jameson, G.S.; Ong, M. First-in-human trial of novel oral PARP inhibitor BMN 673 in patients with solid tumors. J. Clin. Oncol., 2013, 31(15), 2580.
[52]
Campone, M.; Plummer, R.; Stephens, P.; Brakchi, Z.; Aissat-Daudigny, L.; Kasiborski, F.; Cambois, A.; Moachon, G.; Brown, P.D.; Kayitalire, L. Phase I dose-escalation study to evaluate the safety, pharmacokinetics, and pharmacodynamics of CEP-9722 (a PARP1-2 inhibitor) as single-agent and in combination with temozolomide in patients with advanced solid tumors (NCT00920595). J. Clin. Oncol., 2012, 30(15), 3052.
[53]
Fong, P.C.; Boss, D.S.; Yap, T.A.; Tutt, A.; Wu, P.J.; Mergui-Roelvink, M.; Mortimer, P.; Swaisland, H.; Lau, A.; O’Connor, M.J. Inhibition of Poly(ADP-Ribose) Polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med., 2009, 361(2), 123-134.
[54]
Kaye, S.B.; Lubinski, J.; Matulonis, U.; Ang, J.E.; Gourley, C.; Karlan, B.Y.; Amnon, A.; Bell-McGuinn, K.M.; Chen, L.M.; Friedlander, M.; Phase, I.I. Open-label, randomized, multicenter study comparing the efficacy and safety of olaparib, a poly (ADP-Ribose) polymerase inhibitor, and pegylated liposomal doxorubicin in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer. J. Clin. Oncol., 2012, 30(4), 372-379.
[55]
Kaufman, B.; Shapira-Frommer, R.; Schmutzler, R.K.; Audeh, M.W.; Friedlander, M.; Balmana, J.; Mitchell, G.; Fried, G.; Bowen, K.; Fielding, A. Olaparib monotherapy in patients with advanced cancer and a germ-line BRAC1/2 mutation: An open-label phase II study. J. Clin. Oncol., 2013, 31(15), 244.
[56]
Ledermann, J.; Harter, P.; Gourley, C.; Friedlander, M.; Vergote, I.; Rustin, G.; Scott, C.; Meier, W.; Shapira-Frommer, R.; Safra, T. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N. Engl. J. Med., 2012, 366(15), 1382-1392.
[57]
Tutt, A.; Robson, M.; Garber, J.E.; Domchek, S.M.; Audeh, M.W.; Weitzel, J.N.; Friedlander, M.; Arun, B.; Loman, N.; Schmutzler, R.K. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. Lancet, 2010, 376(9737), 235-244.
[58]
Audeh, M.W.; Carmichael, J.; Penson, R.T.; Friedlander, M.; Powell, B.; Bell-McGuinn, K.M.; Scott, C.; Weitzel, J.N.; Oaknin, A.; Loman, N. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet, 2010, 376(9737), 245-251.
[59]
Barber, L.J.; Sandhu, S.; Chen, L.; Campbell, J.; Kozarewa, I.; Fenwick, K.; Assiotis, I.; Rodrigues, D.N.; Reis-Filho, J.S.; Moreno, V.; Mateo, J. Secondary mutations in BRCA2 associated with clinical resistance to a PARP inhibitor. J. Pathol., 2013, 229(3), 422-429.
[60]
Bunting, S.F.; Callen, E.; Wong, N.; Chen, H.T.; Polato, F.; Gunn, A.; Bothmer, A.; Feldhahn, N.; Fernandez-Capetillo, O.; Cao, L. Xu, X. 53BP1 inhibits homologous recombination in brca1-deficient cells by blocking resection of DNA breaks. Cell, 2010, 141(2), 243-254.
[61]
Bouwman, P.; Aly, A.; Escandell, J.M.; Pieterse, M.; Bartkova, J.; van-der-Gulden, H.; Hiddingh, S.; Thanasoula, M.; Kulkarni, A.; Yang, Q.F. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat. Struct. Mol. Biol., 2010, 17(6), 688.
[62]
Rottenberg, S.; Jaspers, J.E.; Kersbergen, A.; van-der-Burg, E.; Nygren, A.O.H.; Zander, S.A.L.; Derksen, P.W.B.; de-Bruin, M.; Zevenhoven, J.; Lau, A. High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proc. Natl. Acad. Sci. USA, 2008, 105(44), 17079-17084.
[63]
Li, X.F.; Delzer, J.; Voorman, R.; de-Morais, S.M.; Lao, Y.B. Disposition and drug-drug interaction potential of veliparib (ABT-888), a novel and potent inhibitor of poly(ADP-ribose) polymerase. Drug Metab. Dispos., 2011, 39(7), 1161-1169.
[64]
Hsiao, S.J.; Smith, S. Tankyrase function at telomeres, spindle poles, and beyond. Biochimie, 2008, 90(1), 83-92.
[65]
Cook, B.D.; Dynek, J.N.; Chang, W.; Shostak, G.; Smith, S. Role for the related poly(ADP-ribose) polymerases tankyrase 1 and 2 at human telomeres. Mol. Cell. Biol., 2002, 22(1), 332-342.
[66]
Dynek, J.N.; Smith, S. Resolution of sister telomere association is required for progression through mitosis. Science, 2004, 304(5667), 97-100.
[67]
Chang, P.; Coughlin, M.; Mitchison, T.J. Tankyrase-1 polymerization of poly (ADP-ribose) is required for spindle structure and function. Nat. Cell Biol., 2005, 7(11), 1133-1139.
[68]
Chiang, Y.J.; Hsiao, S.J.; Yver, D.; Cushman, S.W.; Tessarollo, L.; Smith, S.; Hodes, R.J. Tankyrase 1 and tankyrase 2 are essential but redundant for mouse embryonic development. PLoS One, 2008, 3(7), e2639.
[69]
Yeh, T.Y.J.; Beiswenger, K.K.; Li, P.P.; Bolin, K.E.; Lee, R.M.; Tsao, T.S.; Murphy, A.N.; Hevener, A.L.; Chi, N.W. Hypermetabolism, hyperphagia, and reduced adiposity in tankyrase-deficient mice. Diabetes, 2009, 58(11), 2476-2485.
[70]
Hsiao, S.J.; Poitras, M.F.; Cook, B.D.; Liu, Y.; Smith, S. Tankyrase 2 poly(ADP-ribose) polymerase domain-deleted mice exhibit growth defects but have normal telomere length and capping. Mol. Cell. Biol., 2006, 26(6), 2044-2054.
[71]
Chang, W.; Dynek, J.N.; Smith, S. TRF1 is degraded by ubiquitin-mediated proteolysis after release from telomeres. Genes Dev., 2003, 17(11), 1328-1333.
[72]
Guettler, S.; LaRose, J.; Petsalaki, E.; Gish, G.; Scotter, A.; Pawson, T.; Rottapel, R.; Sicheri, F. Structural Basis and sequence rules for substrate recognition by tankyrase explain the basis for cherubism disease. Cell, 2011, 147(6), 1340-1354.
[73]
Seimiya, H.; Smith, S. The telomeric poly(ADP-ribose) polymerase, tankyrase 1, contains multiple binding sites for telomeric repeat binding factor 1 (TRF1) and a novel acceptor, 182-kDa tankyrase-binding protein (TAB182). J. Biol. Chem., 2002, 277(16), 14116-14126.
[74]
Silk, A.D.; Holland, A.J.; Cleveland, D.W. Requirements for NuMA in maintenance and establishment of mammalian spindle poles. J. Cell Biol., 2009, 184(5), 677-690.
[75]
Chang, W.; Dynek, J.N.; Smith, S. NuMA is a major acceptor of poly(ADP-ribosyl)ation by tankyrase 1 in mitosis. Biochem. J., 2005, 391, 177-184.
[76]
Reichenberger, E.J.; Levine, M.A.; Olsen, B.R.; Papadaki, M.E.; Lietman, S.A. The role of SH3BP2 in the pathophysiology of cherubism. Orphanet J. Rare Dis., 2012, 7(1), 55.
[77]
Levaot, N.; Voytyuk, O.; Dimitriou, I.; Sircoulomb, F.; Chandrakumar, A.; Deckert, M.; Krzyzanowski, P.M.; Scotter, A.; Gu, S.Q.; Janmohamed, S. Loss of tankyrase-mediated destruction of 3BP2 is the underlying pathogenic mechanism of cherubism. Cell, 2011, 147(6), 1324-1339.
[78]
Zhang, Y.; Liu, S.; Mickanin, C.; Feng, Y.; Charlat, O.; Michaud, G.A.; Schirle, M.; Shi, X.; Hild, M.; Bauer, A.; Myer, V.E. RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and wnt signalling. Nat. Cell Biol., 2011, 13(5), 623-629.
[79]
Manning, B.D.; Cantley, L.C. AKT/PKB signaling: Navigating downstream. Cell, 2007, 129(7), 1261-1274.
[80]
Ozaki, Y.; Matsui, H.; Asou, H.; Nagamachi, A.; Aki, D.; Honda, H.; Yasunaga, S.; Takihara, Y.; Yamamoto, T.; Izumi, S.; Ohsugi, M. Poly-ADP ribosylation of Miki by tankyrase-1 promotes centrosome maturation. Mol. Cell, 2012, 47(5), 694-706.
[81]
Li, X.; Han, H.; Zhou, M.T.; Yang, B.; Ta, A.P.; Li, N.; Chen, J.; Wang, W. Proteomic analysis of the human tankyrase protein interaction network reveals its role in pexophagy. Cell Reports, 2017, 20(3), 737-749.
[82]
Riffell, J.L.; Lord, C.J.; Ashworth, A. Tankyrase-targeted therapeutics: Expanding opportunities in the PARP family. Nat. Rev. Drug Discov., 2012, 11(12), 923-936.
[83]
Waaler, J.; Machon, O.; Tumova, L.; Dinh, H.; Korinek, V.; Wilson, S.R.; Paulsen, J.E.; Pedersen, N.M.; Eide, T.J.; Machonova, O. A novel tankyrase inhibitor decreases canonical wnt signaling in colon carcinoma cells and reduces tumor growth in conditional APC mutant mice. Cancer Res., 2012, 72(11), 2822-2832.
[84]
James, R.G.; Davidson, K.C.; Bosch, K.A.; Biechele, T.L.; Robin, N.C.; Taylor, R.J.; Major, M.B.; Camp, N.D.; Fowler, K.; Martins, T.J. WIKI4, a novel inhibitor of tankyrase and Wnt/ss-catenin signaling. PLoS One, 2012, 7(12), e50457.
[85]
Yashiroda, Y.; Okamoto, R.; Hatsugai, K.; Takemoto, Y.; Goshima, N.; Saito, T.; Hamamoto, M.; Sugimoto, Y.; Osada, H.; Seimiya, H.; Yoshida, M. A novel yeast cell-based screen identifies flavone as a tankyrase inhibitor. Biochem. Biophys. Res. Commun., 2010, 394(3), 569-573.
[86]
Voronkov, A.; Holsworth, D.D.; Waaler, J.; Wilson, S.R.; Ekblad, B.; Perdreau-Dahl, H.; Dinh, H.; Drewes, G.; Hopf, C.; Morth, J.P.; Krauss, S. Structural basis and SAR for G007-LK, a lead stage 1,2,4-Triazole based specific tankyrase 1/2 inhibitor. J. Med. Chem., 2013, 56(7), 3012-3023.

Rights & Permissions Print Cite
Article Metrics
98
9
© 2024 Bentham Science Publishers | Privacy Policy