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

Recent Advances in Therapeutic Application of DNA Damage Response Inhibitors against Cancer

Author(s): Stina George Fernandes, Prachi Shah and Ekta Khattar*

Volume 22, Issue 3, 2022

Published on: 08 June, 2021

Page: [469 - 484] Pages: 16

DOI: 10.2174/1871520621666210608105735

Price: $65

Abstract

DNA’s integrity is continuously challenged by intrinsic cellular processes and environmental agents. To overcome this genomic damage, cells have developed multiple signalling pathways collectively named as DNA Damage Response (DDR) and composed of three components: (i) sensor proteins, which detect DNA damage, (ii) mediators that relay the signal downstream and recruit the repair machinery and (iii) the repair proteins, which restore the damaged DNA. A flawed DDR and failure to repair the damage lead to the accumulation of genetic lesions and increased genomic instability, which is recognized as a hallmark of cancer. Cancer cells tend to harbor increased mutations in DDR genes and often have fewer DDR pathways than normal cells. This makes cancer cells more dependent on particular DDR pathways and thus become more susceptible to compounds inhibiting those pathways compared to normal cells, which have all the DDR pathways intact. Understanding the roles of different DDR proteins in the DNA damage response and repair pathways and the identification of their structures have paved the way for development of their inhibitors as targeted cancer therapy. In this review, we describe the major participants of various DDR pathways, their significance in carcinogenesis and focus on the inhibitors developed against several key DDR proteins.

Keywords: DNA damage response, double strand breaks, checkpoint inhibitors, synthetic lethality, targeted cancer therapy, response inhibitors.

« Previous Next »
Graphical Abstract

[1]
Blackford, A.N.; Jackson, S.P. ATM, ATR, and DNA-PK: the trinity at the heart of the dna damage response. Mol. Cell, 2017, 66(6), 801-817.
[http://dx.doi.org/10.1016/j.molcel.2017.05.015] [PMID: 28622525]
[2]
Bassing, C.H.; Alt, F.W. The cellular response to general and programmed DNA double strand breaks. DNA Repair (Amst.), 2004, 3(8-9), 781-796.
[http://dx.doi.org/10.1016/j.dnarep.2004.06.001] [PMID: 15279764]
[3]
Caron, P.; van der Linden, J.; van Attikum, H. Bon voyage: a transcriptional journey around DNA breaks. DNA Repair (Amst.), 2019, 82102686
[http://dx.doi.org/10.1016/j.dnarep.2019.102686] [PMID: 31476573]
[4]
Ron, E. Ionizing radiation and cancer risk: evidence from epidemiology. Pediatr. Radiol., 2002, 32(4), 232-237.
[http://dx.doi.org/10.1007/s00247-002-0672-0] [PMID: 11956701]
[5]
Kirtonia, A.; Sethi, G.; Garg, M. The multifaceted role of reactive oxygen species in tumorigenesis. Cell. Mol. Life Sci., 2020, 77(22), 4459-4483.
[http://dx.doi.org/10.1007/s00018-020-03536-5] [PMID: 32358622]
[6]
Brandsma, I.; Gent, D.C. Pathway choice in DNA double strand break repair: observations of a balancing act. Genome Integr., 2012, 3(1), 9.
[http://dx.doi.org/10.1186/2041-9414-3-9] [PMID: 23181949]
[7]
Lee, J.H.; Paull, T.T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science, 2005, 308(5721), 551-554.
[http://dx.doi.org/10.1126/science.1108297] [PMID: 15790808]
[8]
Bakkenist, C.J.; Kastan, M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature, 2003, 421(6922), 499-506.
[http://dx.doi.org/10.1038/nature01368] [PMID: 12556884]
[9]
Burma, S.; Chen, B.P.; Murphy, M.; Kurimasa, A.; Chen, D.J. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem., 2001, 276(45), 42462-42467.
[http://dx.doi.org/10.1074/jbc.C100466200] [PMID: 11571274]
[10]
Falck, J.; Mailand, N.; Syljuåsen, R.G.; Bartek, J.; Lukas, J. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature, 2001, 410(6830), 842-847.
[http://dx.doi.org/10.1038/35071124] [PMID: 11298456]
[11]
Isono, M.; Niimi, A.; Oike, T.; Hagiwara, Y.; Sato, H.; Sekine, R.; Yoshida, Y.; Isobe, S.Y.; Obuse, C.; Nishi, R.; Petricci, E.; Nakada, S.; Nakano, T.; Shibata, A. BRCA1 directs the repair pathway to homologous recombination by promoting 53bp1 dephosphorylation. Cell Rep., 2017, 18(2), 520-532.
[http://dx.doi.org/10.1016/j.celrep.2016.12.042] [PMID: 28076794]
[12]
Daley, J.M.; Niu, H.; Miller, A.S.; Sung, P. Biochemical mechanism of DSB end resection and its regulation. DNA Repair (Amst.), 2015, 32, 66-74.
[http://dx.doi.org/10.1016/j.dnarep.2015.04.015] [PMID: 25956866]
[13]
Zou, L.; Elledge, S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science, 2003, 300(5625), 1542-1548.
[http://dx.doi.org/10.1126/science.1083430] [PMID: 12791985]
[14]
Li, X.; Heyer, W.D. Homologous recombination in DNA repair and DNA damage tolerance. Cell Res., 2008, 18(1), 99-113.
[http://dx.doi.org/10.1038/cr.2008.1] [PMID: 18166982]
[15]
Maréchal, A.; Zou, L. DNA damage sensing by the ATM and ATR kinases. Cold Spring Harb. Perspect. Biol., 2013, 5(9)a012716
[http://dx.doi.org/10.1101/cshperspect.a012716] [PMID: 24003211]
[16]
Sonoda, E.; Hochegger, H.; Saberi, A.; Taniguchi, Y.; Takeda, S. Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair (Amst.), 2006, 5(9-10), 1021-1029.
[http://dx.doi.org/10.1016/j.dnarep.2006.05.022] [PMID: 16807135]
[17]
Davis, A.J.; Chen, B.P.; Chen, D.J. DNA-PK: a dynamic enzyme in a versatile DSB repair pathway. DNA Repair (Amst.), 2014, 17, 21-29.
[http://dx.doi.org/10.1016/j.dnarep.2014.02.020] [PMID: 24680878]
[18]
Davis, A.J.; Chen, D.J. DNA double strand break repair via non-homologous end-joining. Transl. Cancer Res., 2013, 2(3), 130-143.
[PMID: 24000320]
[19]
Audebert, M.; Salles, B.; Calsou, P. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J. Biol. Chem., 2004, 279(53), 55117-55126.
[http://dx.doi.org/10.1074/jbc.M404524200] [PMID: 15498778]
[20]
Chatterjee, N.; Walker, G.C. Mechanisms of DNA damage, repair, and mutagenesis. Environ. Mol. Mutagen., 2017, 58(5), 235-263.
[http://dx.doi.org/10.1002/em.22087] [PMID: 28485537]
[21]
Jacobs, A.L.; Schär, P. DNA glycosylases: in DNA repair and beyond. Chromosoma, 2012, 121(1), 1-20.
[http://dx.doi.org/10.1007/s00412-011-0347-4] [PMID: 22048164]
[22]
Abbotts, R.; Wilson, D.M., III Coordination of DNA single strand break repair. Free Radic. Biol. Med., 2017, 107, 228-244.
[http://dx.doi.org/10.1016/j.freeradbiomed.2016.11.039] [PMID: 27890643]
[23]
Caldecott, K.W. DNA single-strand break repair. Exp. Cell Res., 2014, 329(1), 2-8.
[http://dx.doi.org/10.1016/j.yexcr.2014.08.027] [PMID: 25176342]
[24]
Schärer, O.D. Nucleotide excision repair in eukaryotes. Cold Spring Harb. Perspect. Biol., 2013, 5(10)a012609
[http://dx.doi.org/10.1101/cshperspect.a012609] [PMID: 24086042]
[25]
Liu, D.; Keijzers, G.; Rasmussen, L.J. DNA mismatch repair and its many roles in eukaryotic cells. Mutat. Res., 2017, 773, 174-187.
[http://dx.doi.org/10.1016/j.mrrev.2017.07.001] [PMID: 28927527]
[26]
Lord, C.J.; Ashworth, A. The DNA damage response and cancer therapy. Nature, 2012, 481(7381), 287-294.
[http://dx.doi.org/10.1038/nature10760] [PMID: 22258607]
[27]
Lord, C.J.; Ashworth, A. BRCAness revisited. Nat. Rev. Cancer, 2016, 16(2), 110-120.
[http://dx.doi.org/10.1038/nrc.2015.21] [PMID: 26775620]
[28]
Birgisdottir, V.; Stefansson, O.A.; Bodvarsdottir, S.K.; Hilmarsdottir, H.; Jonasson, J.G.; Eyfjord, J.E. Epigenetic silencing and deletion of the BRCA1 gene in sporadic breast cancer. Breast Cancer Res., 2006, 8(4), R38.
[http://dx.doi.org/10.1186/bcr1522] [PMID: 16846527]
[29]
Ruscito, I.; Dimitrova, D.; Vasconcelos, I.; Gellhaus, K.; Schwachula, T.; Bellati, F.; Zeillinger, R.; Benedetti-Panici, P.; Vergote, I.; Mahner, S.; Cacsire-Tong, D.; Concin, N.; Darb-Esfahani, S.; Lambrechts, S.; Sehouli, J.; Olek, S.; Braicu, E.I. 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.
[http://dx.doi.org/10.1016/j.ejca.2014.05.001] [PMID: 24889916]
[30]
Esteller, M.; Silva, J.M.; Dominguez, G.; Bonilla, F.; Matias-Guiu, X.; Lerma, E.; Bussaglia, E.; Prat, J.; Harkes, I.C.; Repasky, E.A.; Gabrielson, E.; Schutte, M.; Baylin, S.B.; Herman, J.G. Promoter hypermethylation and BRCA1 inactivation in sporadic breast and ovarian tumors. J. Natl. Cancer Inst., 2000, 92(7), 564-569.
[http://dx.doi.org/10.1093/jnci/92.7.564] [PMID: 10749912]
[31]
McCabe, N.; Turner, N.C.; Lord, C.J.; Kluzek, K.; Bialkowska, A.; Swift, S.; Giavara, S.; O’Connor, M.J.; Tutt, A.N.; Zdzienicka, M.Z.; Smith, G.C.; Ashworth, A. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res., 2006, 66(16), 8109-8115.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-0140] [PMID: 16912188]
[32]
Richman, S. Deficient mismatch repair: read all about it. Review Int. J. Oncol., 2015, 47(4), 1189-1202.
[http://dx.doi.org/10.3892/ijo.2015.3119] [PMID: 26315971]
[33]
Jackson, S.P.; Bartek, J. The DNA-damage response in human biology and disease. Nature, 2009, 461(7267), 1071-1078.
[http://dx.doi.org/10.1038/nature08467] [PMID: 19847258]
[34]
Hosoya, N.; Miyagawa, K. Targeting DNA damage response in cancer therapy. Cancer Sci., 2014, 105(4), 370-388.
[http://dx.doi.org/10.1111/cas.12366] [PMID: 24484288]
[35]
Sun, M.; Guo, X.; Qian, X.; Wang, H.; Yang, C.; Brinkman, K.L.; Serrano-Gonzalez, M.; Jope, R.S.; Zhou, B.; Engler, D.A.; Zhan, M.; Wong, S.T.; Fu, L.; Xu, B. Activation of the ATM-Snail pathway promotes breast cancer metastasis. J. Mol. Cell Biol., 2012, 4(5), 304-315.
[http://dx.doi.org/10.1093/jmcb/mjs048] [PMID: 22923499]
[36]
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.
[http://dx.doi.org/10.1200/JCO.2008.16.0812] [PMID: 18591545]
[37]
Curtin, N.J. DNA repair dysregulation from cancer driver to therapeutic target. Nat. Rev. Cancer, 2012, 12(12), 801-817.
[http://dx.doi.org/10.1038/nrc3399] [PMID: 23175119]
[38]
Lavin, M.F.; Shiloh, Y. The genetic defect in ataxia-telangiectasia. Annu. Rev. Immunol., 1997, 15(1), 177-202.
[http://dx.doi.org/10.1146/annurev.immunol.15.1.177] [PMID: 9143686]
[39]
Hickson, I.; Zhao, Y.; Richardson, C.J.; Green, S.J.; Martin, N.M.; Orr, A.I.; Reaper, P.M.; Jackson, S.P.; Curtin, N.J.; Smith, G.C. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res., 2004, 64(24), 9152-9159.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-2727] [PMID: 15604286]
[40]
Golding, S.E.; Rosenberg, E.; Valerie, N.; Hussaini, I.; Frigerio, M.; Cockcroft, X.F.; Chong, W.Y.; Hummersone, M.; Rigoreau, L.; Menear, K.A.; O’Connor, M.J.; Povirk, L.F.; van Meter, T.; Valerie, K. Improved ATM kinase inhibitor KU-60019 radiosensitizes glioma cells, compromises insulin, AKT and ERK prosurvival signaling, and inhibits migration and invasion. Mol. Cancer Ther., 2009, 8(10), 2894-2902.
[http://dx.doi.org/10.1158/1535-7163.MCT-09-0519] [PMID: 19808981]
[41]
Biddlestone-Thorpe, L.; Sajjad, M.; Rosenberg, E.; Beckta, J.M.; Valerie, N.C.; Tokarz, M.; Adams, B.R.; Wagner, A.F.; Khalil, A.; Gilfor, D.; Golding, S.E.; Deb, S.; Temesi, D.G.; Lau, A.; O’Connor, M.J.; Choe, K.S.; Parada, L.F.; Lim, S.K.; Mukhopadhyay, N.D.; Valerie, K. ATM kinase inhibition preferentially sensitizes p53-mutant glioma to ionizing radiation. Clin. Cancer Res., 2013, 19(12), 3189-3200.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-3408] [PMID: 23620409]
[42]
Rainey, M.D.; Charlton, M.E.; Stanton, R.V.; Kastan, M.B. Transient inhibition of ATM kinase is sufficient to enhance cellular sensitivity to ionizing radiation. Cancer Res., 2008, 68(18), 7466-7474.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-0763] [PMID: 18794134]
[43]
Batey, M.A.; Zhao, Y.; Kyle, S.; Richardson, C.; Slade, A.; Martin, N.M.; Lau, A.; Newell, D.R.; Curtin, N.J. Preclinical evaluation of a novel ATM inhibitor, KU59403, in vitro and >in vivo in p53 functional and dysfunctional models of human cancer. Mol. Cancer Ther., 2013, 12(6), 959-967.
[http://dx.doi.org/10.1158/1535-7163.MCT-12-0707] [PMID: 23512991]
[44]
Pike, K.G.; Barlaam, B.; Cadogan, E.; Campbell, A.; Chen, Y.; Colclough, N. The identification of potent, selective, and orally available inhibitors of ataxia telangiectasia mutated (ATM) kinase: the discovery of azd0156 (8-{6-[3-(dimethylamino)propoxy]pyridin-3-yl}-3-meth yl-1-(tetrahydro-2 h-pyran-4-yl)-1,3-dihydro-2 h-imidazo[4,5-c]quin olin-2-one). J. Med. Chem., 2018, 61(9), 3823-3841.
[http://dx.doi.org/10.1021/acs.jmedchem.7b01896] [PMID: 29683659]
[45]
Durant, S.T.; Zheng, L.; Wang, Y.; Chen, K.; Zhang, L.; Zhang, T. The brain-penetrant clinical ATM inhibitor AZD1390 radiosensitizes and improves survival of preclinical brain tumor models.Sci. Adv., 2018, 4(6), eaat1719.,
[http://dx.doi.org/10.1126/sciadv.aat1719]
[46]
Zeman, M.K.; Cimprich, K.A. Causes and consequences of replication stress. Nat. Cell Biol., 2014, 16(1), 2-9.
[http://dx.doi.org/10.1038/ncb2897] [PMID: 24366029]
[47]
Karnitz, L.M.; Zou, L. Molecular pathways: targeting ATR in cancer therapy. Clin. Cancer Res., 2015, 21(21), 4780-4785.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-0479] [PMID: 26362996]
[48]
Sarkaria, J.N.; Busby, E.C.; Tibbetts, R.S.; Roos, P.; Taya, Y.; Karnitz, L.M.; Abraham, R.T. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res., 1999, 59(17), 4375-4382.
[PMID: 10485486]
[49]
Sarkaria, J.N.; Tibbetts, R.S.; Busby, E.C.; Kennedy, A.P.; Hill, D.E.; Abraham, R.T. Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res., 1998, 58(19), 4375-4382.
[PMID: 9766667]
[50]
Nishida, H.; Tatewaki, N.; Nakajima, Y.; Magara, T.; Ko, K.M.; Hamamori, Y.; Konishi, T. Inhibition of ATR protein kinase activity by schisandrin B in DNA damage response. Nucleic Acids Res., 2009, 37(17), 5678-5689.
[http://dx.doi.org/10.1093/nar/gkp593] [PMID: 19625493]
[51]
Peasland, A.; Wang, L.Z.; Rowling, E.; Kyle, S.; Chen, T.; Hopkins, A.; Cliby, W.A.; Sarkaria, J.; Beale, G.; Edmondson, R.J.; Curtin, N.J. Identification and evaluation of a potent novel ATR inhibitor, NU6027, in breast and ovarian cancer cell lines. Br. J. Cancer, 2011, 105(3), 372-381.
[http://dx.doi.org/10.1038/bjc.2011.243] [PMID: 21730979]
[52]
Toledo, L.I.; Murga, M.; Zur, R.; Soria, R.; Rodriguez, A.; Martinez, S.; Oyarzabal, J.; Pastor, J.; Bischoff, J.R.; Fernandez-Capetillo, O. A cell-based screen identifies ATR inhibitors with synthetic lethal properties for cancer-associated mutations. Nat. Struct. Mol. Biol., 2011, 18(6), 721-727.
[http://dx.doi.org/10.1038/nsmb.2076] [PMID: 21552262]
[53]
Charrier, J.D.; Durrant, S.J.; Golec, J.M.; Kay, D.P.; Knegtel, R.M.; MacCormick, S.; Mortimore, M.; O’Donnell, M.E.; Pinder, J.L.; Reaper, P.M.; Rutherford, A.P.; Wang, P.S.; Young, S.C.; Pollard, J.R. Discovery of potent and selective inhibitors of ataxia telangiectasia mutated and Rad3 related (ATR) protein kinase as potential anticancer agents. J. Med. Chem., 2011, 54(7), 2320-2330.
[http://dx.doi.org/10.1021/jm101488z] [PMID: 21413798]
[54]
Reaper, P.M.; Griffiths, M.R.; Long, J.M.; Charrier, J.D.; Maccormick, S.; Charlton, P.A.; Golec, J.M.; Pollard, J.R. Selective killing of ATM- or p53-deficient cancer cells through inhibition of ATR. Nat. Chem. Biol., 2011, 7(7), 428-430.
[http://dx.doi.org/10.1038/nchembio.573] [PMID: 21490603]
[55]
Sangster-Guity, N.; Conrad, B.H.; Papadopoulos, N.; Bunz, F. ATR mediates cisplatin resistance in a p53 genotype-specific manner. Oncogene, 2011, 30(22), 2526-2533.
[http://dx.doi.org/10.1038/onc.2010.624] [PMID: 21258400]
[56]
Pires, I.M.; Olcina, M.M.; Anbalagan, S.; Pollard, J.R.; Reaper, P.M.; Charlton, P.A.; McKenna, W.G.; Hammond, E.M. Targeting radiation-resistant hypoxic tumour cells through ATR inhibition. Br. J. Cancer, 2012, 107(2), 291-299.
[http://dx.doi.org/10.1038/bjc.2012.265] [PMID: 22713662]
[57]
Horsman, M.R.; Overgaard, J. The impact of hypoxia and its modification of the outcome of radiotherapy. J. Radiat. Res. (Tokyo), 2016, 57(Suppl. 1), i90-i98.
[http://dx.doi.org/10.1093/jrr/rrw007] [PMID: 26983987]
[58]
Fokas, E.; Prevo, R.; Pollard, J.R.; Reaper, P.M.; Charlton, P.A.; Cornelissen, B.; Vallis, K.A.; Hammond, E.M.; Olcina, M.M.; Gillies McKenna, W.; Muschel, R.J.; Brunner, T.B. Targeting ATR in vivo using the novel inhibitor VE-822 results in selective sensitization of pancreatic tumors to radiation. Cell Death Dis., 2012, 3e441
[http://dx.doi.org/10.1038/cddis.2012.181] [PMID: 23222511]
[59]
Hall, A.B.; Newsome, D.; Wang, Y.; Boucher, D.M.; Eustace, B.; Gu, Y.; Hare, B.; Johnson, M.A.; Milton, S.; Murphy, C.E.; Takemoto, D.; Tolman, C.; Wood, M.; Charlton, P.; Charrier, J.D.; Furey, B.; Golec, J.; Reaper, P.M.; Pollard, J.R. Potentiation of tumor responses to DNA damaging therapy by the selective ATR inhibitor VX-970. Oncotarget, 2014, 5(14), 5674-5685.
[http://dx.doi.org/10.18632/oncotarget.2158] [PMID: 25010037]
[60]
Gorecki, L.; Andrs, M.; Rezacova, M.; Korabecny, J. Discovery of ATR kinase inhibitor berzosertib (VX-970, M6620): clinical candidate for cancer therapy. Pharmacol. Ther., 2020, 210107518
[http://dx.doi.org/10.1016/j.pharmthera.2020.107518] [PMID: 32109490]
[61]
Foote, K.M.; Blades, K.; Cronin, A.; Fillery, S.; Guichard, S.S.; Hassall, L. Discovery of 4-{4-[(3R)-3-Methylmorpholin-4-yl]-6-[1-(methylsulfonyl)cyclopropyl]pyrimidin-2-y l}-1H-indole (AZ20): a potent and selective inhibitor of ATR protein kinase with monotherapy in vivo antitumor activity. J. Med. Chem., 2013, 56(5), 2125-2138.
[http://dx.doi.org/10.1021/jm301859s] [PMID: 23394205]
[62]
Foote, K.M.; Nissink, J.W.M.; McGuire, T.; Turner, P.; Guichard, S.; Yates, J.W.T.; Lau, A.; Blades, K.; Heathcote, D.; Odedra, R.; Wilkinson, G.; Wilson, Z.; Wood, C.M.; Jewsbury, P.J. Discovery and characterization of azd6738, a potent inhibitor of ataxia telangiectasia mutated and rad3 related (ATR) kinase with application as an anticancer agent. J. Med. Chem., 2018, 61(22), 9889-9907.
[http://dx.doi.org/10.1021/acs.jmedchem.8b01187] [PMID: 30346772]
[63]
Mohni, K.N.; Thompson, P.S.; Luzwick, J.W.; Glick, G.G.; Pendleton, C.S.; Lehmann, B.D.; Pietenpol, J.A.; Cortez, D. A synthetic lethal screen identifies DNA repair pathways that sensitize cancer cells to combined atr inhibition and cisplatin treatments. PLoS One, 2015, 10(5)e0125482
[http://dx.doi.org/10.1371/journal.pone.0125482] [PMID: 25965342]
[64]
Kwok, M.; Davies, N.; Agathanggelou, A.; Smith, E.; Oldreive, C.; Petermann, E.; Stewart, G.; Brown, J.; Lau, A.; Pratt, G.; Parry, H.; Taylor, M.; Moss, P.; Hillmen, P.; Stankovic, T. ATR inhibition induces synthetic lethality and overcomes chemoresistance in TP53- or ATM-defective chronic lymphocytic leukemia cells. Blood, 2016, 127(5), 582-595.
[http://dx.doi.org/10.1182/blood-2015-05-644872] [PMID: 26563132]
[65]
Vendetti, F.P.; Lau, A.; Schamus, S.; Conrads, T.P.; O’Connor, M.J.; Bakkenist, C.J. The orally active and bioavailable ATR kinase inhibitor AZD6738 potentiates the anti-tumor effects of cisplatin to resolve ATM-deficient non-small cell lung cancer in vivo. Oncotarget, 2015, 6(42), 44289-44305.
[http://dx.doi.org/10.18632/oncotarget.6247] [PMID: 26517239]
[66]
Bartek, J.; Lukas, J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell, 2003, 3(5), 421-429.
[http://dx.doi.org/10.1016/S1535-6108(03)00110-7] [PMID: 12781359]
[67]
Garrett, M.D.; Collins, I. Anticancer therapy with checkpoint inhibitors: what, where and when? Trends Pharmacol. Sci., 2011, 32(5), 308-316.
[http://dx.doi.org/10.1016/j.tips.2011.02.014] [PMID: 21458083]
[68]
Fuse, E.; Tanii, H.; Kurata, N.; Kobayashi, H.; Shimada, Y.; Tamura, T.; Sasaki, Y.; Tanigawara, Y.; Lush, R.D.; Headlee, D.; Figg, W.D.; Arbuck, S.G.; Senderowicz, A.M.; Sausville, E.A.; Akinaga, S.; Kuwabara, T.; Kobayashi, S. Unpredicted clinical pharmacology of UCN-01 caused by specific binding to human α1-acid glycoprotein. Cancer Res., 1998, 58(15), 3248-3253.
[PMID: 9699650]
[69]
Dwyer, M.P.; Paruch, K.; Labroli, M.; Alvarez, C.; Keertikar, K.M.; Poker, C.; Rossman, R.; Fischmann, T.O.; Duca, J.S.; Madison, V.; Parry, D.; Davis, N.; Seghezzi, W.; Wiswell, D.; Guzi, T.J. Discovery of pyrazolo[1,5-a]pyrimidine-based CHK1 inhibitors: a template-based approach-part 1. Bioorg. Med. Chem. Lett., 2011, 21(1), 467-470.
[http://dx.doi.org/10.1016/j.bmcl.2010.10.113] [PMID: 21094608]
[70]
Labroli, M.; Paruch, K.; Dwyer, M.P.; Alvarez, C.; Keertikar, K.; Poker, C.; Rossman, R.; Duca, J.S.; Fischmann, T.O.; Madison, V.; Parry, D.; Davis, N.; Seghezzi, W.; Wiswell, D.; Guzi, T.J. Discovery of pyrazolo[1,5-a]pyrimidine-based CHK1 inhibitors: a template-based approach-part 2. Bioorg. Med. Chem. Lett., 2011, 21(1), 471-474.
[http://dx.doi.org/10.1016/j.bmcl.2010.10.114] [PMID: 21094607]
[71]
Montano, R.; Thompson, R.; Chung, I.; Hou, H.; Khan, N.; Eastman, A. Sensitization of human cancer cells to gemcitabine by the Chk1 inhibitor MK-8776: cell cycle perturbation and impact of administration schedule in vitro and in vivo. BMC Cancer, 2013, 13(1), 604.
[http://dx.doi.org/10.1186/1471-2407-13-604] [PMID: 24359526]
[72]
Dai, Y.; Chen, S.; Kmieciak, M.; Zhou, L.; Lin, H.; Pei, X.Y.; Grant, S. The novel Chk1 inhibitor MK-8776 sensitizes human leukemia cells to HDAC inhibitors by targeting the intra-S checkpoint and DNA replication and repair. Mol. Cancer Ther., 2013, 12(6), 878-889.
[http://dx.doi.org/10.1158/1535-7163.MCT-12-0902] [PMID: 23536721]
[73]
Zhou, Z.R.; Yang, Z.Z.; Wang, S.J.; Zhang, L.; Luo, J.R.; Feng, Y.; Yu, X.L.; Chen, X.X.; Guo, X.M. The Chk1 inhibitor MK-8776 increases the radiosensitivity of human triple-negative breast cancer by inhibiting autophagy. Acta Pharmacol. Sin., 2017, 38(4), 513-523.
[http://dx.doi.org/10.1038/aps.2016.136] [PMID: 28042876]
[74]
Bridges, K.A.; Chen, X.; Liu, H.; Rock, C.; Buchholz, T.A.; Shumway, S.D.; Skinner, H.D.; Meyn, R.E. MK-8776, a novel chk1 kinase inhibitor, radiosensitizes p53-defective human tumor cells. Oncotarget, 2016, 7(44), 71660-71672.
[http://dx.doi.org/10.18632/oncotarget.12311] [PMID: 27690219]
[75]
Daud, A.I.; Ashworth, M.T.; Strosberg, J.; Goldman, J.W.; Mendelson, D.; Springett, G.; Venook, A.P.; Loechner, S.; Rosen, L.S.; Shanahan, F.; Parry, D.; Shumway, S.; Grabowsky, J.A.; Freshwater, T.; Sorge, C.; Kang, S.P.; Isaacs, R.; Munster, P.N. Phase I dose-escalation trial of checkpoint kinase 1 inhibitor MK-8776 as monotherapy and in combination with gemcitabine in patients with advanced solid tumors. J. Clin. Oncol., 2015, 33(9), 1060-1066.
[http://dx.doi.org/10.1200/JCO.2014.57.5027] [PMID: 25605849]
[76]
Karp, J.E.; Thomas, B.M.; Greer, J.M.; Sorge, C.; Gore, S.D.; Pratz, K.W.; Smith, B.D.; Flatten, K.S.; Peterson, K.; Schneider, P.; Mackey, K.; Freshwater, T.; Levis, M.J.; McDevitt, M.A.; Carraway, H.E.; Gladstone, D.E.; Showel, M.M.; Loechner, S.; Parry, D.A.; Horowitz, J.A.; Isaacs, R.; Kaufmann, S.H. Phase I and pharmacologic trial of cytosine arabinoside with the selective checkpoint 1 inhibitor Sch 900776 in refractory acute leukemias. Clin. Cancer Res., 2012, 18(24), 6723-6731.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-2442] [PMID: 23092873]
[77]
Webster, J.A.; Tibes, R.; Morris, L.; Blackford, A.L.; Litzow, M.; Patnaik, M.; Rosner, G.L.; Gojo, I.; Kinders, R.; Wang, L.; Doyle, L.A.; Huntoon, C.J.; Karnitz, L.M.; Kaufmann, S.H.; Karp, J.E.; Smith, B.D. Randomized phase II trial of cytosine arabinoside with and without the CHK1 inhibitor MK-8776 in relapsed and refractory acute myeloid leukemia. Leuk. Res., 2017, 61, 108-116.
[http://dx.doi.org/10.1016/j.leukres.2017.09.005] [PMID: 28957699]
[78]
Zabludoff, S.D.; Deng, C.; Grondine, M.R.; Sheehy, A.M.; Ashwell, S.; Caleb, B.L.; Green, S.; Haye, H.R.; Horn, C.L.; Janetka, J.W.; Liu, D.; Mouchet, E.; Ready, S.; Rosenthal, J.L.; Queva, C.; Schwartz, G.K.; Taylor, K.J.; Tse, A.N.; Walker, G.E.; White, A.M. AZD7762, a novel checkpoint kinase inhibitor, drives checkpoint abrogation and potentiates DNA-targeted therapies. Mol. Cancer Ther., 2008, 7(9), 2955-2966.
[http://dx.doi.org/10.1158/1535-7163.MCT-08-0492] [PMID: 18790776]
[79]
Xu, H.; Cheung, I.Y.; Wei, X.X.; Tran, H.; Gao, X.; Cheung, N.K. Checkpoint kinase inhibitor synergizes with DNA-damaging agents in G1 checkpoint-defective neuroblastoma. Int. J. Cancer, 2011, 129(8), 1953-1962.
[http://dx.doi.org/10.1002/ijc.25842] [PMID: 21154747]
[80]
Isono, M.; Hoffmann, M.J.; Pinkerneil, M.; Sato, A.; Michaelis, M.; Cinatl, J., Jr; Niegisch, G.; Schulz, W.A. Checkpoint kinase inhibitor AZD7762 strongly sensitises urothelial carcinoma cells to gemcitabine. J. Exp. Clin. Cancer Res., 2017, 36(1), 1.
[http://dx.doi.org/10.1186/s13046-016-0473-1] [PMID: 28049532]
[81]
Morgan, M.A.; Parsels, L.A.; Zhao, L.; Parsels, J.D.; Davis, M.A.; Hassan, M.C.; Arumugarajah, S.; Hylander-Gans, L.; Morosini, D.; Simeone, D.M.; Canman, C.E.; Normolle, D.P.; Zabludoff, S.D.; Maybaum, J.; Lawrence, T.S. Mechanism of radiosensitization by the Chk1/2 inhibitor AZD7762 involves abrogation of the G2 checkpoint and inhibition of homologous recombinational DNA repair. Cancer Res., 2010, 70(12), 4972-4981.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-3573] [PMID: 20501833]
[82]
Ho, A.; Bendell, J.; Cleary, J.; Schwartz, G.; Burris, H.; Oakes, P. Phase I, open-label, dose-escalation study of AZD7762 in combination with irinotecan (irino) in patients (Pts) with advanced solid tumors. J. Clin. Oncol., 2011, 29(15-suppl), 3033.,
[83]
Sausville, E.; Lorusso, P.; Carducci, M.; Carter, J.; Quinn, M.F.; Malburg, L.; Azad, N.; Cosgrove, D.; Knight, R.; Barker, P.; Zabludoff, S.; Agbo, F.; Oakes, P.; Senderowicz, A. Phase I dose-escalation study of AZD7762, a checkpoint kinase inhibitor, in combination with gemcitabine in US patients with advanced solid tumors. Cancer Chemother. Pharmacol., 2014, 73(3), 539-549.
[http://dx.doi.org/10.1007/s00280-014-2380-5] [PMID: 24448638]
[84]
Wang, F.Z.; Fei, H.R.; Cui, Y.J.; Sun, Y.K.; Li, Z.M.; Wang, X.Y.; Yang, X.Y.; Zhang, J.G.; Sun, B.L. The checkpoint 1 kinase inhibitor LY2603618 induces cell cycle arrest, DNA damage response and autophagy in cancer cells. Apoptosis, 2014, 19(9), 1389-1398.
[http://dx.doi.org/10.1007/s10495-014-1010-3] [PMID: 24928205]
[85]
Zhang, Y.; Lai, J.; Du, Z.; Gao, J.; Yang, S.; Gorityala, S.; Xiong, X.; Deng, O.; Ma, Z.; Yan, C.; Susana, G.; Xu, Y.; Zhang, J. Targeting radioresistant breast cancer cells by single agent CHK1 inhibitor via enhancing replication stress. Oncotarget, 2016, 7(23), 34688-34702.
[http://dx.doi.org/10.18632/oncotarget.9156] [PMID: 27167194]
[86]
King, C.; Diaz, H.; Barnard, D.; Barda, D.; Clawson, D.; Blosser, W.; Cox, K.; Guo, S.; Marshall, M. Characterization and preclinical development of LY2603618: a selective and potent Chk1 inhibitor. Invest. New Drugs, 2014, 32(2), 213-226.
[http://dx.doi.org/10.1007/s10637-013-0036-7] [PMID: 24114124]
[87]
Barnard, D.; Diaz, H.B.; Burke, T.; Donoho, G.; Beckmann, R.; Jones, B.; Barda, D.; King, C.; Marshall, M. LY2603618, a selective CHK1 inhibitor, enhances the anti-tumor effect of gemcitabine in xenograft tumor models. Invest. New Drugs, 2016, 34(1), 49-60.
[http://dx.doi.org/10.1007/s10637-015-0310-y] [PMID: 26612134]
[88]
Doi, T.; Yoshino, T.; Shitara, K.; Matsubara, N.; Fuse, N.; Naito, Y.; Uenaka, K.; Nakamura, T.; Hynes, S.M.; Lin, A.B. Phase I study of LY2603618, a CHK1 inhibitor, in combination with gemcitabine in Japanese patients with solid tumors. Anticancer Drugs, 2015, 26(10), 1043-1053.
[http://dx.doi.org/10.1097/CAD.0000000000000278] [PMID: 26288133]
[89]
Angius, G.; Tomao, S.; Stati, V.; Vici, P.; Bianco, V.; Tomao, F. Prexasertib, a checkpoint kinase inhibitor: from preclinical data to clinical development. Cancer Chemother. Pharmacol., 2020, 85(1), 9-20.
[http://dx.doi.org/10.1007/s00280-019-03950-y] [PMID: 31512029]
[90]
Infante, J.R.; Hollebecque, A.; Postel-Vinay, S.; Bauer, T.M.; Blackwood, E.M.; Evangelista, M.; Mahrus, S.; Peale, F.V.; Lu, X.; Sahasranaman, S.; Zhu, R.; Chen, Y.; Ding, X.; Murray, E.R.; Schutzman, J.L.; Lauchle, J.O.; Soria, J.C.; LoRusso, P.M. Phase I study of GDC-0425, a checkpoint kinase 1 inhibitor, in combination with gemcitabine in patients with refractory solid tumors. Clin. Cancer Res., 2017, 23(10), 2423-2432.
[http://dx.doi.org/10.1158/1078-0432.CCR-16-1782] [PMID: 27815358]
[91]
Italiano, A.; Infante, J.R.; Shapiro, G.I.; Moore, K.N.; LoRusso, P.M.; Hamilton, E.; Cousin, S.; Toulmonde, M.; Postel-Vinay, S.; Tolaney, S.; Blackwood, E.M.; Mahrus, S.; Peale, F.V.; Lu, X.; Moein, A.; Epler, J.; DuPree, K.; Tagen, M.; Murray, E.R.; Schutzman, J.L.; Lauchle, J.O.; Hollebecque, A.; Soria, J.C. Phase I study of the checkpoint kinase 1 inhibitor GDC-0575 in combination with gemcitabine in patients with refractory solid tumors. Ann. Oncol., 2018, 29(5), 1304-1311.
[http://dx.doi.org/10.1093/annonc/mdy076] [PMID: 29788155]
[92]
Laroche-Clary, A.; Lucchesi, C.; Rey, C.; Verbeke, S.; Bourdon, A.; Chaire, V.; Algéo, M.P.; Cousin, S.; Toulmonde, M.; Vélasco, V.; Shutzman, J.; Savina, A.; Le Loarer, F.; Italiano, A. CHK1 inhibition in soft-tissue sarcomas: biological and clinical implications. Ann. Oncol., 2018, 29(4), 1023-1029.
[http://dx.doi.org/10.1093/annonc/mdy039] [PMID: 29409053]
[93]
Hauge, S.; Naucke, C.; Hasvold, G.; Joel, M.; Rødland, G.E.; Juzenas, P.; Stokke, T.; Syljuåsen, R.G. Combined inhibition of Wee1 and Chk1 gives synergistic DNA damage in S-phase due to distinct regulation of CDK activity and CDC45 loading. Oncotarget, 2017, 8(7), 10966-10979.
[http://dx.doi.org/10.18632/oncotarget.14089] [PMID: 28030798]
[94]
Ghelli Luserna Di Rorà, A.; Bocconcelli, M.; Ferrari, A.; Terragna, C.; Bruno, S.; Imbrogno, E.; Beeharry, N.; Robustelli, V.; Ghetti, M.; Napolitano, R.; Chirumbolo, G.; Marconi, G.; Papayannidis, C.; Paolini, S.; Sartor, C.; Simonetti, G.; Yen, T.J.; Martinelli, G. Synergism through wee1 and chk1 inhibition in acute lymphoblastic leukemia. Cancers (Basel), 2019, 11(11)E1654
[http://dx.doi.org/10.3390/cancers11111654] [PMID: 31717700]
[95]
Magnussen, G.I.; Emilsen, E.; Giller Fleten, K.; Engesæter, B.; Nähse-Kumpf, V.; Fjær, R.; Slipicevic, A.; Flørenes, V.A. Combined inhibition of the cell cycle related proteins Wee1 and Chk1/2 induces synergistic anti-cancer effect in melanoma. BMC Cancer, 2015, 15, 462.
[http://dx.doi.org/10.1186/s12885-015-1474-8] [PMID: 26054341]
[96]
Guertin, A.D.; Martin, M.M.; Roberts, B.; Hurd, M.; Qu, X.; Miselis, N.R.; Liu, Y.; Li, J.; Feldman, I.; Benita, Y.; Bloecher, A.; Toniatti, C.; Shumway, S.D. Unique functions of CHK1 and WEE1 underlie synergistic anti-tumor activity upon pharmacologic inhibition. Cancer Cell Int., 2012, 12(1), 45.
[http://dx.doi.org/10.1186/1475-2867-12-45] [PMID: 23148684]
[97]
Matthews, T.P.; Jones, A.M.; Collins, I. Structure-based design, discovery and development of checkpoint kinase inhibitors as potential anticancer therapies. Expert Opin. Drug Discov., 2013, 8(6), 621-640.
[http://dx.doi.org/10.1517/17460441.2013.788496] [PMID: 23594139]
[98]
Jobson, A.G.; Lountos, G.T.; Lorenzi, P.L.; Llamas, J.; Connelly, J.; Cerna, D.; Tropea, J.E.; Onda, A.; Zoppoli, G.; Kondapaka, S.; Zhang, G.; Caplen, N.J.; Cardellina, J.H., II; Yoo, S.S.; Monks, A.; Self, C.; Waugh, D.S.; Shoemaker, R.H.; Pommier, Y. Cellular inhibition of checkpoint kinase 2 (Chk2) and potentiation of camptothecins and radiation by the novel Chk2 inhibitor PV1019 [7-nitro-1H-indole-2-carboxylic acid 4-[1-(guanidinohydrazone)-ethyl]-phenyl-amide J. Pharmacol. Exp. Ther., 2009, 331(3), 816-826.
[http://dx.doi.org/10.1124/jpet.109.154997] [PMID: 19741151]
[99]
Anderson, V.E.; Walton, M.I.; Eve, P.D.; Boxall, K.J.; Antoni, L.; Caldwell, J.J.; Aherne, W.; Pearl, L.H.; Oliver, A.W.; Collins, I.; Garrett, M.D. CCT241533 is a potent and selective inhibitor of CHK2 that potentiates the cytotoxicity of PARP inhibitors. Cancer Res., 2011, 71(2), 463-472.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-1252] [PMID: 21239475]
[100]
Lavecchia, A.; Di Giovanni, C.; Novellino, E. Inhibitors of Cdc25 phosphatases as anticancer agents: a patent review. Expert Opin. Ther. Pat., 2010, 20(3), 405-425.
[http://dx.doi.org/10.1517/13543771003623232] [PMID: 20166845]
[101]
Lavecchia, A.; Di Giovanni, C.; Novellino, E. CDC25 phosphatase inhibitors: an update. Mini Rev. Med. Chem., 2012, 12(1), 62-73.
[http://dx.doi.org/10.2174/138955712798868940] [PMID: 22070688]
[102]
Squire, C.J.; Dickson, J.M.; Ivanovic, I.; Baker, E.N. Structure and inhibition of the human cell cycle checkpoint kinase, Wee1A kinase: an atypical tyrosine kinase with a key role in CDK1 regulation. Structure, 2005, 13(4), 541-550.
[http://dx.doi.org/10.1016/j.str.2004.12.017] [PMID: 15837193]
[103]
Lee, J.; Kumagai, A.; Dunphy, W.G. Positive regulation of Wee1 by Chk1 and 14-3-3 proteins. Mol. Biol. Cell, 2001, 12(3), 551-563.
[http://dx.doi.org/10.1091/mbc.12.3.551] [PMID: 11251070]
[104]
Parker, L.L.; Piwnica-Worms, H. Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science, 1992, 257(5078), 1955-1957.
[http://dx.doi.org/10.1126/science.1384126] [PMID: 1384126]
[105]
Aarts, M.; Sharpe, R.; Garcia-Murillas, I.; Gevensleben, H.; Hurd, M.S.; Shumway, S.D.; Toniatti, C.; Ashworth, A.; Turner, N.C. Forced mitotic entry of S-phase cells as a therapeutic strategy induced by inhibition of WEE1. Cancer Discov., 2012, 2(6), 524-539.
[http://dx.doi.org/10.1158/2159-8290.CD-11-0320] [PMID: 22628408]
[106]
Beck, H.; Nähse, V.; Larsen, M.S.; Groth, P.; Clancy, T.; Lees, M.; Jørgensen, M.; Helleday, T.; Syljuåsen, R.G.; Sørensen, C.S. Regulators of cyclin-dependent kinases are crucial for maintaining genome integrity in S phase. J. Cell Biol., 2010, 188(5), 629-638.
[http://dx.doi.org/10.1083/jcb.200905059] [PMID: 20194642]
[107]
Hirai, H.; Iwasawa, Y.; Okada, M.; Arai, T.; Nishibata, T.; Kobayashi, M.; Kimura, T.; Kaneko, N.; Ohtani, J.; Yamanaka, K.; Itadani, H.; Takahashi-Suzuki, I.; Fukasawa, K.; Oki, H.; Nambu, T.; Jiang, J.; Sakai, T.; Arakawa, H.; Sakamoto, T.; Sagara, T.; Yoshizumi, T.; Mizuarai, S.; Kotani, H. Small-molecule inhibition of Wee1 kinase by MK-1775 selectively sensitizes p53-deficient tumor cells to DNA-damaging agents. Mol. Cancer Ther., 2009, 8(11), 2992-3000.
[http://dx.doi.org/10.1158/1535-7163.MCT-09-0463] [PMID: 19887545]
[108]
Geenen, J.J.J.; Schellens, J.H.M. Molecular pathways: targeting the protein kinase wee1 in cancer. Clin. Cancer Res., 2017, 23(16), 4540-4544.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-0520] [PMID: 28442503]
[109]
Diab, A.; Kao, M.; Kehrli, K.; Kim, H.Y.; Sidorova, J.; Mendez, E. Multiple defects sensitize p53-deficient head and neck cancer cells to the wee1 kinase inhibition. Mol. Cancer Res., 2019, 17(5), 1115-1128.
[http://dx.doi.org/10.1158/1541-7786.MCR-18-0860] [PMID: 30679201]
[110]
Bridges, K.A.; Hirai, H.; Buser, C.A.; Brooks, C.; Liu, H.; Buchholz, T.A.; Molkentine, J.M.; Mason, K.A.; Meyn, R.E. MK-1775, a novel Wee1 kinase inhibitor, radiosensitizes p53-defective human tumor cells. Clin. Cancer Res., 2011, 17(17), 5638-5648.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-0650] [PMID: 21799033]
[111]
Hirai, H.; Arai, T.; Okada, M.; Nishibata, T.; Kobayashi, M.; Sakai, N.; Imagaki, K.; Ohtani, J.; Sakai, T.; Yoshizumi, T.; Mizuarai, S.; Iwasawa, Y.; Kotani, H. MK-1775, a small molecule Wee1 inhibitor, enhances anti-tumor efficacy of various DNA-damaging agents, including 5-fluorouracil. Cancer Biol. Ther., 2010, 9(7), 514-522.
[http://dx.doi.org/10.4161/cbt.9.7.11115] [PMID: 20107315]
[112]
Parsels, L.A.; Karnak, D.; Parsels, J.D.; Zhang, Q.; Vélez-Padilla, J.; Reichert, Z.R.; Wahl, D.R.; Maybaum, J.; O’Connor, M.J.; Lawrence, T.S.; Morgan, M.A. PARP1 trapping and dna replication stress enhance radiosensitization with combined wee1 and parp inhibitors. Mol. Cancer Res., 2018, 16(2), 222-232.
[http://dx.doi.org/10.1158/1541-7786.MCR-17-0455] [PMID: 29133592]
[113]
Pfister, S.X.; Markkanen, E.; Jiang, Y.; Sarkar, S.; Woodcock, M.; Orlando, G.; Mavrommati, I.; Pai, C.C.; Zalmas, L.P.; Drobnitzky, N.; Dianov, G.L.; Verrill, C.; Macaulay, V.M.; Ying, S.; La Thangue, N.B.; D’Angiolella, V.; Ryan, A.J.; Humphrey, T.C. Inhibiting wee1 selectively kills histone h3k36me3-deficient cancers by dntp starvation. Cancer Cell, 2015, 28(5), 557-568.
[http://dx.doi.org/10.1016/j.ccell.2015.09.015] [PMID: 26602815]
[114]
Kausar, T.; Schreiber, J.S.; Karnak, D.; Parsels, L.A.; Parsels, J.D.; Davis, M.A.; Zhao, L.; Maybaum, J.; Lawrence, T.S.; Morgan, M.A. Sensitization of pancreatic cancers to gemcitabine chemoradiation by wee1 kinase inhibition depends on homologous recombination repair. Neoplasia, 2015, 17(10), 757-766.
[http://dx.doi.org/10.1016/j.neo.2015.09.006] [PMID: 26585231]
[115]
Do, K.; Wilsker, D.; Ji, J.; Zlott, J.; Freshwater, T.; Kinders, R.J.; Collins, J.; Chen, A.P.; Doroshow, J.H.; Kummar, S. Phase I study of single-agent azd1775 (mk-1775), a wee1 kinase inhibitor, in patients with refractory solid tumors. J. Clin. Oncol., 2015, 33(30), 3409-3415.
[http://dx.doi.org/10.1200/JCO.2014.60.4009] [PMID: 25964244]
[116]
Leijen, S.; van Geel, R.M.; Pavlick, A.C.; Tibes, R.; Rosen, L.; Razak, A.R.; Lam, R.; Demuth, T.; Rose, S.; Lee, M.A.; Freshwater, T.; Shumway, S.; Liang, L.W.; Oza, A.M.; Schellens, J.H.; Shapiro, G.I. Phase I study evaluating wee1 inhibitor azd1775 as monotherapy and in combination with gemcitabine, cisplatin, or carboplatin in patients with advanced solid tumors. J. Clin. Oncol., 2016, 34(36), 4371-4380.
[http://dx.doi.org/10.1200/JCO.2016.67.5991] [PMID: 27601554]
[117]
Cuneo, K.C.; Morgan, M.A.; Sahai, V.; Schipper, M.J.; Parsels, L.A.; Parsels, J.D.; Devasia, T.; Al-Hawaray, M.; Cho, C.S.; Nathan, H.; Maybaum, J.; Zalupski, M.M.; Lawrence, T.S. Dose escalation trial of the Wee1 inhibitor Adavosertib (AZD1775) in combination with gemcitabine and radiation for patients with locally advanced pancreatic cancer. J. Clin. Oncol., 2019, 37(29), 2643-2650.
[http://dx.doi.org/10.1200/JCO.19.00730] [PMID: 31398082]
[118]
Leijen, S.; van Geel, R.M.; Sonke, G.S.; de Jong, D.; Rosenberg, E.H.; Marchetti, S.; Pluim, D.; van Werkhoven, E.; Rose, S.; Lee, M.A.; Freshwater, T.; Beijnen, J.H.; Schellens, J.H. Phase II study of wee1 inhibitor AZD1775 plus carboplatin in patients with tp53-mutated ovarian cancer refractory or resistant to first-line therapy within 3 months. J. Clin. Oncol., 2016, 34(36), 4354-4361.
[http://dx.doi.org/10.1200/JCO.2016.67.5942] [PMID: 27998224]
[119]
Oza, A.M.; Estevez-Diz, M.; Grischke, E.M.; Hall, M.; Marmé, F.; Provencher, D.; Uyar, D.; Weberpals, J.I.; Wenham, R.M.; Laing, N.; Tracy, M.; Freshwater, T.; Lee, M.A.; Liu, J.; Qiu, J.; Rose, S.; Rubin, E.H.; Moore, K. A biomarker-enriched, randomized phase ii trial of adavosertib (AZD1775) plus paclitaxel and carboplatin for women with platinum-sensitive tp53-mutant ovarian cancer. Clin. Cancer Res., 2020, 26(18), 4767-4776.
[http://dx.doi.org/10.1158/1078-0432.CCR-20-0219] [PMID: 32611648]
[120]
Lieber, M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem., 2010, 79, 181-211.
[http://dx.doi.org/10.1146/annurev.biochem.052308.093131] [PMID: 20192759]
[121]
Mahaney, B.L.; Meek, K.; Lees-Miller, S.P. Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous end-joining. Biochem. J., 2009, 417(3), 639-650.
[http://dx.doi.org/10.1042/BJ20080413] [PMID: 19133841]
[122]
Collis, S.J.; DeWeese, T.L.; Jeggo, P.A.; Parker, A.R. The life and death of DNA-PK. Oncogene, 2005, 24(6), 949-961.
[http://dx.doi.org/10.1038/sj.onc.1208332] [PMID: 15592499]
[123]
Vlahos, C.J.M.W.; Matter, W.F.; Hui, K.Y.; Brown, R.F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem., 1994, 269(7), 5241-5248.
[http://dx.doi.org/10.1016/S0021-9258(17)37680-9] [PMID: 8106507]
[124]
Clapham, K.M.; Bardos, J.; Finlay, M.R.; Golding, B.T.; Griffen, E.J.; Griffin, R.J.; Hardcastle, I.R.; Menear, K.A.; Ting, A.; Turner, P.; Young, G.L.; Cano, C. DNA-dependent protein kinase (DNA-PK) inhibitors: structure-activity relationships for O-alkoxyphenylchromen-4-one probes of the ATP-binding domain. Bioorg. Med. Chem. Lett., 2011, 21(3), 966-970.
[http://dx.doi.org/10.1016/j.bmcl.2010.12.047] [PMID: 21216595]
[125]
Ihmaid, S.; Al-Rawi, J.; Bradley, C.; Angove, M.J.; Robertson, M.N.; Clark, R.L. Synthesis, structural elucidation, DNA-PK inhibition, homology modelling and anti-platelet activity of morpholino-substituted-1,3-naphth-oxazines. Bioorg. Med. Chem., 2011, 19(13), 3983-3994.
[http://dx.doi.org/10.1016/j.bmc.2011.05.032] [PMID: 21664823]
[126]
Hardcastle, I.R.; Cockcroft, X.; Curtin, N.J.; El-Murr, M.D.; Leahy, J.J.; Stockley, M.; Golding, B.T.; Rigoreau, L.; Richardson, C.; Smith, G.C.; Griffin, R.J. Discovery of potent chromen-4-one inhibitors of the DNA-dependent Protein Kinase (DNA-PK) using a small-molecule library approach. J. Med. Chem., 2005, 48(24), 7829-7846.
[http://dx.doi.org/10.1021/jm050444b] [PMID: 16302822]
[127]
Elliott, S.L.; Crawford, C.; Mulligan, E.; Summerfield, G.; Newton, P.; Wallis, J.; Mainou-Fowler, T.; Evans, P.; Bedwell, C.; Durkacz, B.W.; Willmore, E. Mitoxantrone in combination with an inhibitor of DNA-dependent protein kinase: a potential therapy for high risk B-cell chronic lymphocytic leukaemia. Br. J. Haematol., 2011, 152(1), 61-71.
[http://dx.doi.org/10.1111/j.1365-2141.2010.08425.x] [PMID: 21083655]
[128]
Ciszewski, W.M.; Tavecchio, M.; Dastych, J.; Curtin, N.J. DNA-PK inhibition by NU7441 sensitizes breast cancer cells to ionizing radiation and doxorubicin. Breast Cancer Res. Treat., 2014, 143(1), 47-55.
[http://dx.doi.org/10.1007/s10549-013-2785-6] [PMID: 24292814]
[129]
Yanai, M.; Makino, H.; Ping, B.; Takeda, K.; Tanaka, N.; Sakamoto, T.; Yamaguchi, K.; Kodani, M.; Yamasaki, A.; Igishi, T.; Shimizu, E. DNA-PK inhibition by NU7441 enhances chemosensitivity to topoisomerase inhibitor in non-small cell lung carcinoma cells by blocking DNA damage repair. Yonago Acta Med., 2017, 60(1), 9-15.
[PMID: 28331416]
[130]
Zhao, Y.; Thomas, H.D.; Batey, M.A.; Cowell, I.G.; Richardson, C.J.; Griffin, R.J.; Calvert, A.H.; Newell, D.R.; Smith, G.C.; Curtin, N.J. Preclinical evaluation of a potent novel DNA-dependent protein kinase inhibitor NU7441. Cancer Res., 2006, 66(10), 5354-5362.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-4275] [PMID: 16707462]
[131]
Veuger, S.J.; Curtin, N.J.; Richardson, C.J.; Smith, G.C.; Durkacz, B.W. Radiosensitization and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly(ADP-ribose) polymerase-1. Cancer Res., 2003, 63(18), 6008-6015.
[PMID: 14522929]
[132]
Willmore, E.; de Caux, S.; Sunter, N.J.; Tilby, M.J.; Jackson, G.H.; Austin, C.A.; Durkacz, B.W. A novel DNA-dependent protein kinase inhibitor, NU7026, potentiates the cytotoxicity of topoisomerase II poisons used in the treatment of leukemia. Blood, 2004, 103(12), 4659-4665.
[http://dx.doi.org/10.1182/blood-2003-07-2527] [PMID: 15010369]
[133]
Amrein, L.; Loignon, M.; Goulet, A.C.; Dunn, M.; Jean-Claude, B.; Aloyz, R.; Panasci, L. Chlorambucil cytotoxicity in malignant B lymphocytes is synergistically increased by 2-(morpholin-4-yl)-benzo[h]chomen-4-one (NU7026)-mediated inhibition of DNA double-strand break repair via inhibition of DNA-dependent protein kinase. J. Pharmacol. Exp. Ther., 2007, 321(3), 848-855.
[http://dx.doi.org/10.1124/jpet.106.118356] [PMID: 17351105]
[134]
Niazi, M.T.; Mok, G.; Heravi, M.; Lee, L.; Vuong, T.; Aloyz, R.; Panasci, L.; Muanza, T. Effects of dna-dependent protein kinase inhibition by NU7026 on dna repair and cell survival in irradiated gastric cancer cell line N87. Curr. Oncol., 2014, 21(2), 91-96.
[http://dx.doi.org/10.3747/co.21.1509] [PMID: 24764698]
[135]
Dolman, M.E.; van der Ploeg, I.; Koster, J.; Bate-Eya, L.T.; Versteeg, R.; Caron, H.N.; Molenaar, J.J. DNA-dependent protein kinase as molecular target for radiosensitization of neuroblastoma cells. PLoS One, 2015, 10(12)e0145744
[http://dx.doi.org/10.1371/journal.pone.0145744] [PMID: 26716839]
[136]
Yang, L.; Yang, X.; Tang, Y.; Zhang, D.; Zhu, L.; Wang, S.; Wang, B.; Ma, T. Inhibition of DNA PK activity sensitizes A549 cells to X ray irradiation by inducing the ATM dependent DNA damage response. Mol. Med. Rep., 2018, 17(6), 7545-7552.
[http://dx.doi.org/10.3892/mmr.2018.8828] [PMID: 29620203]
[137]
Yang, L.; Liu, Y.; Sun, C.; Yang, X.; Yang, Z.; Ran, J.; Zhang, Q.; Zhang, H.; Wang, X.; Wang, X. Inhibition of DNA-PKcs enhances radiosensitivity and increases the levels of ATM and ATR in NSCLC cells exposed to carbon ion irradiation. Oncol. Lett., 2015, 10(5), 2856-2864.
[http://dx.doi.org/10.3892/ol.2015.3730] [PMID: 26722253]
[138]
Tichý, A.; Novotná, E.; Durisová, K.; Salovská, B.; Sedlaríková, R.; Pejchal, J.; Zárybnická, L.; Vávrová, J.; Sinkorová, Z.; Rezácová, M. Radio-sensitization of human leukaemic molt-4 cells by DNA-dependent protein kinase inhibitor, NU7026. Acta Med. (Hradec Kralove), 2012, 55(2), 66-73.
[http://dx.doi.org/10.14712/18059694.2015.57] [PMID: 23101268]
[139]
Nutley, B.P.; Smith, N.F.; Hayes, A.; Kelland, L.R.; Brunton, L.; Golding, B.T.; Smith, G.C.; Martin, N.M.; Workman, P.; Raynaud, F.I. Preclinical pharmacokinetics and metabolism of a novel prototype DNA-PK inhibitor NU7026. Br. J. Cancer, 2005, 93(9), 1011-1018.
[http://dx.doi.org/10.1038/sj.bjc.6602823] [PMID: 16249792]
[140]
Kashishian, A.; Douangpanya, H.; Clark, D.; Schlachter, S.T.; Eary, C.T.; Schiro, J.G.; Huang, H.; Burgess, L.E.; Kesicki, E.A.; Halbrook, J. DNA-dependent protein kinase inhibitors as drug candidates for the treatment of cancer. Mol. Cancer Ther., 2003, 2(12), 1257-1264.
[PMID: 14707266]
[141]
Take, Y.; Kumano, M.; Hamano, Y.; Fukatsu, H.; Teraoka, H.; Nishimura, S.; Okuyama, A. OK-1035, a selective inhibitor of DNA-dependent protein kinase. Biochem. Biophys. Res. Commun., 1995, 215(1), 41-47.
[http://dx.doi.org/10.1006/bbrc.1995.2431] [PMID: 7575620]
[142]
Shinohara, E.T.; Geng, L.; Tan, J.; Chen, H.; Shir, Y.; Edwards, E.; Halbrook, J.; Kesicki, E.A.; Kashishian, A.; Hallahan, D.E. DNA-dependent protein kinase is a molecular target for the development of noncytotoxic radiation-sensitizing drugs. Cancer Res., 2005, 65(12), 4987-4992.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-4250] [PMID: 15958537]
[143]
Ismail, I.H.; Mårtensson, S.; Moshinsky, D.; Rice, A.; Tang, C.; Howlett, A.; McMahon, G.; Hammarsten, O. SU11752 inhibits the DNA-dependent protein kinase and DNA double-strand break repair resulting in ionizing radiation sensitization. Oncogene, 2004, 23(4), 873-882.
[http://dx.doi.org/10.1038/sj.onc.1207303] [PMID: 14661061]
[144]
Hisatomi, T.; Sueoka-Aragane, N.; Sato, A.; Tomimasu, R.; Ide, M.; Kurimasa, A.; Okamoto, K.; Kimura, S.; Sueoka, E. NK314 potentiates antitumor activity with adult T-cell leukemia-lymphoma cells by inhibition of dual targets on topoisomerase IIalpha and DNA-dependent protein kinase. Blood, 2011, 117(13), 3575-3584.
[http://dx.doi.org/10.1182/blood-2010-02-270439] [PMID: 21245486]
[145]
Cano, C.; Saravanan, K.; Bailey, C.; Bardos, J.; Curtin, N.J.; Frigerio, M.; Golding, B.T.; Hardcastle, I.R.; Hummersone, M.G.; Menear, K.A.; Newell, D.R.; Richardson, C.J.; Shea, K.; Smith, G.C.; Thommes, P.; Ting, A.; Griffin, R.J. 1-substituted (Dibenzo[b,d]thiophen-4-yl)-2-morpholino-4H-chromen-4-ones endowed with dual DNA-PK/PI3-K inhibitory activity. J. Med. Chem., 2013, 56(16), 6386-6401.
[http://dx.doi.org/10.1021/jm400915j] [PMID: 23855836]
[146]
Munck, J.M.; Batey, M.A.; Zhao, Y.; Jenkins, H.; Richardson, C.J.; Cano, C.; Tavecchio, M.; Barbeau, J.; Bardos, J.; Cornell, L.; Griffin, R.J.; Menear, K.; Slade, A.; Thommes, P.; Martin, N.M.; Newell, D.R.; Smith, G.C.; Curtin, N.J. Chemosensitization of cancer cells by KU-0060648, a dual inhibitor of DNA-PK and PI-3K. Mol. Cancer Ther., 2012, 11(8), 1789-1798.
[http://dx.doi.org/10.1158/1535-7163.MCT-11-0535] [PMID: 22576130]
[147]
Fok, J.H.L.; Ramos-Montoya, A.; Vazquez-Chantada, M.; Wijnhoven, P.W.G.; Follia, V.; James, N.; Farrington, P.M.; Karmokar, A.; Willis, S.E.; Cairns, J.; Nikkilä, J.; Beattie, D.; Lamont, G.M.; Finlay, M.R.V.; Wilson, J.; Smith, A.; O’Connor, L.O.; Ling, S.; Fawell, S.E.; O’Connor, M.J.; Hollingsworth, S.J.; Dean, E.; Goldberg, F.W.; Davies, B.R.; Cadogan, E.B. AZD7648 is a potent and selective DNA-PK inhibitor that enhances radiation, chemotherapy and olaparib activity. Nat. Commun., 2019, 10(1), 5065.
[http://dx.doi.org/10.1038/s41467-019-12836-9] [PMID: 31699977]
[148]
Wong, W.W.; Jackson, R.K.; Liew, L.P.; Dickson, B.D.; Cheng, G.J.; Lipert, B.; Gu, Y.; Hunter, F.W.; Wilson, W.R.; Hay, M.P. Hypoxia-selective radiosensitisation by SN38023, a bioreductive prodrug of DNA-dependent protein kinase inhibitor IC87361. Biochem. Pharmacol., 2019, 169113641
[http://dx.doi.org/10.1016/j.bcp.2019.113641] [PMID: 31541630]
[149]
Willoughby, C.E.; Jiang, Y.; Thomas, H.D.; Willmore, E.; Kyle, S.; Wittner, A.; Phillips, N.; Zhao, Y.; Tudhope, S.J.; Prendergast, L.; Junge, G.; Lourenco, L.M.; Finlay, M.R.V.; Turner, P.; Munck, J.M.; Griffin, R.J.; Rennison, T.; Pickles, J.; Cano, C.; Newell, D.R.; Reeves, H.L.; Ryan, A.J.; Wedge, S.R. Selective DNA-PKcs inhibition extends the therapeutic index of localized radiotherapy and chemotherapy. J. Clin. Invest., 2020, 130(1), 258-271.
[http://dx.doi.org/10.1172/JCI127483] [PMID: 31581151]
[150]
Baumann, P.; West, S.C. Role of the human RAD51 protein in homologous recombination and double-stranded-break repair. Trends Biochem. Sci., 1998, 23(7), 247-251.
[http://dx.doi.org/10.1016/S0968-0004(98)01232-8] [PMID: 9697414]
[151]
Klein, H.L. The consequences of Rad51 overexpression for normal and tumor cells. DNA Repair (Amst.), 2008, 7(5), 686-693.
[http://dx.doi.org/10.1016/j.dnarep.2007.12.008] [PMID: 18243065]
[152]
Huang, F.; Motlekar, N.A.; Burgwin, C.M.; Napper, A.D.; Diamond, S.L.; Mazin, A.V. Identification of specific inhibitors of human RAD51 recombinase using high-throughput screening. ACS Chem. Biol., 2011, 6(6), 628-635.
[http://dx.doi.org/10.1021/cb100428c] [PMID: 21428443]
[153]
Huang, F.; Mazina, O.M.; Zentner, I.J.; Cocklin, S.; Mazin, A.V. Inhibition of homologous recombination in human cells by targeting RAD51 recombinase. J. Med. Chem., 2012, 55(7), 3011-3020.
[http://dx.doi.org/10.1021/jm201173g] [PMID: 22380680]
[154]
Huang, F.; Mazin, A.V. A small molecule inhibitor of human RAD51 potentiates breast cancer cell killing by therapeutic agents in mouse xenografts. PLoS One, 2014, 9(6)e100993
[http://dx.doi.org/10.1371/journal.pone.0100993] [PMID: 24971740]
[155]
Budke, B.; Logan, H.L.; Kalin, J.H.; Zelivianskaia, A.S.; Cameron McGuire, W.; Miller, L.L.; Stark, J.M.; Kozikowski, A.P.; Bishop, D.K.; Connell, P.P. RI-1: a chemical inhibitor of RAD51 that disrupts homologous recombination in human cells. Nucleic Acids Res., 2012, 40(15), 7347-7357.
[http://dx.doi.org/10.1093/nar/gks353] [PMID: 22573178]
[156]
Budke, B.; Kalin, J.H.; Pawlowski, M.; Zelivianskaia, A.S.; Wu, M.; Kozikowski, A.P.; Connell, P.P. An optimized RAD51 inhibitor that disrupts homologous recombination without requiring Michael acceptor reactivity. J. Med. Chem., 2013, 56(1), 254-263.
[http://dx.doi.org/10.1021/jm301565b] [PMID: 23231413]
[157]
Ward, A.; Khanna, K.K.; Wiegmans, A.P. Targeting homologous recombination, new pre-clinical and clinical therapeutic combinations inhibiting RAD51. Cancer Treat. Rev., 2015, 41(1), 35-45.
[http://dx.doi.org/10.1016/j.ctrv.2014.10.006] [PMID: 25467108]
[158]
Dupré, A.; Boyer-Chatenet, L.; Sattler, R.M.; Modi, A.P.; Lee, J.H.; Nicolette, M.L.; Kopelovich, L.; Jasin, M.; Baer, R.; Paull, T.T.; Gautier, J. A forward chemical genetic screen reveals an inhibitor of the Mre11-Rad50-Nbs1 complex. Nat. Chem. Biol., 2008, 4(2), 119-125.
[http://dx.doi.org/10.1038/nchembio.63] [PMID: 18176557]
[159]
Schreiber, V.; Amé, J.C.; Dollé, P.; Schultz, I.; Rinaldi, B.; Fraulob, V.; Ménissier-de Murcia, J.; de Murcia, G. Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J. Biol. Chem., 2002, 277(25), 23028-23036.
[http://dx.doi.org/10.1074/jbc.M202390200] [PMID: 11948190]
[160]
Ray Chaudhuri, A.; Nussenzweig, A. The multifaceted roles of PARP1 in DNA repair and chromatin remodelling. Nat. Rev. Mol. Cell Biol., 2017, 18(10), 610-621.
[http://dx.doi.org/10.1038/nrm.2017.53] [PMID: 28676700]
[161]
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.
[http://dx.doi.org/10.1016/0005-2787(71)90012-8] [PMID: 4325158]
[162]
Purnell, M.R.; Whish, W.J. Novel inhibitors of poly(ADP-ribose) synthetase. Biochem. J., 1980, 185(3), 775-777.
[http://dx.doi.org/10.1042/bj1850775] [PMID: 6248035]
[163]
Mateo, J.; Lord, C.J.; Serra, V.; Tutt, A.; Balmaña, J.; Castroviejo-Bermejo, M.; Cruz, C.; Oaknin, A.; Kaye, S.B.; de Bono, J.S. A decade of clinical development of PARP inhibitors in perspective. Ann. Oncol., 2019, 30(9), 1437-1447.
[http://dx.doi.org/10.1093/annonc/mdz192] [PMID: 31218365]
[164]
Farmer, H.; McCabe, N.; Lord, C.J.; Tutt, A.N.; Johnson, D.A.; Richardson, T.B.; Santarosa, M.; Dillon, K.J.; Hickson, I.; Knights, C.; Martin, N.M.; Jackson, S.P.; Smith, G.C.; Ashworth, A. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature, 2005, 434(7035), 917-921.
[http://dx.doi.org/10.1038/nature03445] [PMID: 15829967]
[165]
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.
[http://dx.doi.org/10.1038/nature03443] [PMID: 15829966]
[166]
Prakash, R.; Zhang, Y.; Feng, W.; Jasin, M. Homologous recombination and human health: the roles of BRCA1, BRCA2, and associated proteins. Cold Spring Harb. Perspect. Biol., 2015, 7(4)a016600
[http://dx.doi.org/10.1101/cshperspect.a016600] [PMID: 25833843]
[167]
Menear, K.A.; Adcock, C.; Boulter, R.; Cockcroft, X.L.; Copsey, L.; Cranston, A.; Dillon, K.J.; Drzewiecki, J.; Garman, S.; Gomez, S.; Javaid, H.; Kerrigan, F.; Knights, C.; Lau, A.; Loh, V.M., Jr; Matthews, I.T.; Moore, S.; O’Connor, M.J.; Smith, G.C.; Martin, N.M. 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), 6581-6591.
[http://dx.doi.org/10.1021/jm8001263] [PMID: 18800822]
[168]
Fong, P.C.; Boss, D.S.; Yap, T.A.; Tutt, A.; Wu, P.; Mergui-Roelvink, M.; Mortimer, P.; Swaisland, H.; Lau, A.; O’Connor, M.J.; Ashworth, A.; Carmichael, J.; Kaye, S.B.; Schellens, J.H.; de Bono, J.S. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med., 2009, 361(2), 123-134.
[http://dx.doi.org/10.1056/NEJMoa0900212] [PMID: 19553641]
[169]
Plummer, R.; Jones, C.; Middleton, M.; Wilson, R.; Evans, J.; Olsen, A.; Curtin, N.; Boddy, A.; McHugh, P.; Newell, D.; Harris, A.; Johnson, P.; Steinfeldt, H.; Dewji, R.; Wang, D.; Robson, L.; Calvert, H. Phase I study of the poly(ADP-ribose) polymerase inhibitor, AG014699, in combination with temozolomide in patients with advanced solid tumors. Clin. Cancer Res., 2008, 14(23), 7917-7923.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-1223] [PMID: 19047122]
[170]
Thorsell, A-G.; Ekblad, T.; Karlberg, T.; Löw, M.; Pinto, A.F.; Trésaugues, L.; Moche, M.; Cohen, M.S.; Schüler, H. Structural basis for potency and promiscuity in poly (ADP-ribose) polymerase (PARP) and tankyrase inhibitors. J. Med. Chem., 2017, 60(4), 1262-1271.
[http://dx.doi.org/10.1021/acs.jmedchem.6b00990] [PMID: 28001384]
[171]
Murai, J.; Huang, S.Y.; Das, B.B.; Renaud, A.; Zhang, Y.; Doroshow, J.H.; Ji, J.; Takeda, S.; Pommier, Y. Trapping of PARP1 and PARP2 by clinical PARP inhibitors. Cancer Res., 2012, 72(21), 5588-5599.
[http://dx.doi.org/10.1158/0008-5472.CAN-12-2753] [PMID: 23118055]
[172]
Plummer, R.; Dua, D.; Cresti, N.; Drew, Y.; Stephens, P.; Foegh, M.; Knudsen, S.; Sachdev, P.; Mistry, B.M.; Dixit, V.; McGonigle, S.; Hall, N.; Matijevic, M.; McGrath, S.; Sarker, D. First-in-human study of the PARP/tankyrase inhibitor E7449 in patients with advanced solid tumours and evaluation of a novel drug-response predictor. Br. J. Cancer, 2020, 123(4), 525-533.
[http://dx.doi.org/10.1038/s41416-020-0916-5] [PMID: 32523090]
[173]
Ledermann, J.; Harter, P.; Gourley, C.; Friedlander, M.; Vergote, I.; Rustin, G.; Scott, C.; Meier, W.; Shapira-Frommer, R.; Safra, T.; Matei, D.; Macpherson, E.; Watkins, C.; Carmichael, J.; Matulonis, U. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N. Engl. J. Med., 2012, 366(15), 1382-1392.
[http://dx.doi.org/10.1056/NEJMoa1105535] [PMID: 22452356]
[174]
Mirza, M.R.; Monk, B.J.; Herrstedt, J.; Oza, A.M.; Mahner, S.; Redondo, A.; Fabbro, M.; Ledermann, J.A.; Lorusso, D.; Vergote, I.; Ben-Baruch, N.E.; Marth, C.; Mądry, R.; Christensen, R.D.; Berek, J.S.; Dørum, A.; Tinker, A.V.; du Bois, A.; González-Martín, A.; Follana, P.; Benigno, B.; Rosenberg, P.; Gilbert, L.; Rimel, B.J.; Buscema, J.; Balser, J.P.; Agarwal, S.; Matulonis, U.A. Niraparib maintenance therapy in platinum-sensitive, recurrent ovarian cancer. N. Engl. J. Med., 2016, 375(22), 2154-2164.
[http://dx.doi.org/10.1056/NEJMoa1611310] [PMID: 27717299]
[175]
Coleman, R.L.; Oza, A.M.; Lorusso, D.; Aghajanian, C.; Oaknin, A.; Dean, A.; Colombo, N.; Weberpals, J.I.; Clamp, A.; Scambia, G.; Leary, A.; Holloway, R.W.; Gancedo, M.A.; Fong, P.C.; Goh, J.C.; O’Malley, D.M.; Armstrong, D.K.; Garcia-Donas, J.; Swisher, E.M.; Floquet, A.; Konecny, G.E.; McNeish, I.A.; Scott, C.L.; Cameron, T.; Maloney, L.; Isaacson, J.; Goble, S.; Grace, C.; Harding, T.C.; Raponi, M.; Sun, J.; Lin, K.K.; Giordano, H.; Ledermann, J.A. 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), 1949-1961.
[http://dx.doi.org/10.1016/S0140-6736(17)32440-6] [PMID: 28916367]
[176]
Barret, J-M.; Cadou, M.; Hill, B.T. Inhibition of nucleotide excision repair and sensitisation of cells to DNA cross-linking anticancer drugs by F 11782, a novel fluorinated epipodophylloid. Biochem. Pharmacol., 2002, 63(2), 251-258.
[http://dx.doi.org/10.1016/S0006-2952(01)00835-8] [PMID: 11841800]
[177]
Jordheim, L.P.; Barakat, K.H.; Heinrich-Balard, L.; Matera, E.L.; Cros-Perrial, E.; Bouledrak, K.; El Sabeh, R.; Perez-Pineiro, R.; Wishart, D.S.; Cohen, R.; Tuszynski, J.; Dumontet, C. Small molecule inhibitors of ERCC1-XPF protein-protein interaction synergize alkylating agents in cancer cells. Mol. Pharmacol., 2013, 84(1), 12-24.
[http://dx.doi.org/10.1124/mol.112.082347] [PMID: 23580445]
[178]
Chapman, T.M.; Gillen, K.J.; Wallace, C.; Lee, M.T.; Bakrania, P.; Khurana, P.; Coombs, P.J.; Stennett, L.; Fox, S.; Bureau, E.A.; Brownlees, J.; Melton, D.W.; Saxty, B. Catechols and 3-hydroxypyridones as inhibitors of the DNA repair complex ERCC1-XPF. Bioorg. Med. Chem. Lett., 2015, 25(19), 4097-4103.
[http://dx.doi.org/10.1016/j.bmcl.2015.08.031] [PMID: 26318993]
[179]
McNeil, E.M.; Astell, K.R.; Ritchie, A.M.; Shave, S.; Houston, D.R.; Bakrania, P.; Jones, H.M.; Khurana, P.; Wallace, C.; Chapman, T.; Wear, M.A.; Walkinshaw, M.D.; Saxty, B.; Melton, D.W. Inhibition of the ERCC1-XPF structure-specific endonuclease to overcome cancer chemoresistance. DNA Repair (Amst.), 2015, 31, 19-28.
[http://dx.doi.org/10.1016/j.dnarep.2015.04.002] [PMID: 25956741]
[180]
Barakat, K.H.; Jordheim, L.P.; Perez-Pineiro, R.; Wishart, D.; Dumontet, C.; Tuszynski, J.A. Virtual screening and biological evaluation of inhibitors targeting the XPA-ERCC1 interaction. PLoS One, 2012, 7(12)e51329
[http://dx.doi.org/10.1371/journal.pone.0051329] [PMID: 23272099]
[181]
Martin, S.A.; McCarthy, A.; Barber, L.J.; Burgess, D.J.; Parry, S.; Lord, C.J.; Ashworth, A. Methotrexate induces oxidative DNA damage and is selectively lethal to tumour cells with defects in the DNA mismatch repair gene MSH2. EMBO Mol. Med., 2009, 1(6-7), 323-337.
[http://dx.doi.org/10.1002/emmm.200900040] [PMID: 20049736]
[182]
Wu, Q.; Vasquez, K.M. Human MLH1 protein participates in genomic damage checkpoint signaling in response to DNA interstrand crosslinks, while MSH2 functions in DNA repair. PLoS Genet., 2008, 4(9)e1000189
[http://dx.doi.org/10.1371/journal.pgen.1000189] [PMID: 18787700]
[183]
Martin, S.A.; McCabe, N.; Mullarkey, M.; Cummins, R.; Burgess, D.J.; Nakabeppu, Y.; Oka, S.; Kay, E.; Lord, C.J.; Ashworth, A. DNA polymerases as potential therapeutic targets for cancers deficient in the DNA mismatch repair proteins MSH2 or MLH1. Cancer Cell, 2010, 17(3), 235-248.
[http://dx.doi.org/10.1016/j.ccr.2009.12.046] [PMID: 20227038]
[184]
Begum, R.; Martin, S.A. Targeting mismatch repair defects: a novel strategy for personalized cancer treatment. DNA Repair (Amst.), 2016, 38, 135-139.
[http://dx.doi.org/10.1016/j.dnarep.2015.11.026] [PMID: 26698647]
[185]
Eso, Y.; Shimizu, T.; Takeda, H.; Takai, A.; Marusawa, H. Microsatellite instability and immune checkpoint inhibitors: toward precision medicine against gastrointestinal and hepatobiliary cancers. J. Gastroenterol., 2020, 55(1), 15-26.
[http://dx.doi.org/10.1007/s00535-019-01620-7] [PMID: 31494725]
[186]
Sahin, I.H. Fine-tuning immunotherapy in MMR-D/MSI-H colorectal cancer. Colorect. Cancer, 2020, 8(4).,
[187]
Nakad, R.; Schumacher, B. DNA damage response and immune defense: links and mechanisms. Front. Genet., 2016, 7, 147.
[http://dx.doi.org/10.3389/fgene.2016.00147] [PMID: 27555866]
[188]
Higuchi, T.; Flies, D.B.; Marjon, N.A.; Mantia-Smaldone, G.; Ronner, L.; Gimotty, P.A.; Adams, S.F. CTLA-4 blockade synergizes therapeutically with parp inhibition in brca1-deficient ovarian cancer. Cancer Immunol. Res., 2015, 3(11), 1257-1268.
[http://dx.doi.org/10.1158/2326-6066.CIR-15-0044] [PMID: 26138335]
[189]
Wang, H.; Sun, W. CRISPR-mediated targeting of HER2 inhibits cell proliferation through a dominant negative mutation. Cancer Lett., 2017, 385, 137-143.
[http://dx.doi.org/10.1016/j.canlet.2016.10.033] [PMID: 27815036]
[190]
Bothmer, A.; Phadke, T.; Barrera, L.A.; Margulies, C.M.; Lee, C.S.; Buquicchio, F.; Moss, S.; Abdulkerim, H.S.; Selleck, W.; Jayaram, H.; Myer, V.E.; Cotta-Ramusino, C. Characterization of the interplay between DNA repair and CRISPR/Cas9-induced DNA lesions at an endogenous locus. Nat. Commun., 2017, 8, 13905.
[http://dx.doi.org/10.1038/ncomms13905] [PMID: 28067217]

Rights & Permissions Print Cite
Article Metrics
35
4
© 2024 Bentham Science Publishers | Privacy Policy