Re-purposing clinical kinase inhibitors to enhance chemosensitivity by overriding checkpoints

References

• Vogel C, Hager C, Bastians H. Mechanisms of mitotic cell death induced by chemotherapy-mediated G2 checkpoint abrogation. Cancer Res 2007; 67:339 - 45; http://dx.doi.org/10.1158/0008-5472.CAN-06-2548; PMID: 17210716
   PubMed Web of Science ®Google Scholar
• Zhao H, Piwnica-Worms H. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol Cell Biol 2001; 21:4129 - 39; http://dx.doi.org/10.1128/MCB.21.13.4129-4139.2001; PMID: 11390642
   PubMed Web of Science ®Google Scholar
• Tse AN, Schwartz GK. Potentiation of cytotoxicity of topoisomerase i poison by concurrent and sequential treatment with the checkpoint inhibitor UCN-01 involves disparate mechanisms resulting in either p53-independent clonogenic suppression or p53-dependent mitotic catastrophe. Cancer Res 2004; 64:6635 - 44; http://dx.doi.org/10.1158/0008-5472.CAN-04-0841; PMID: 15374978
   PubMed Web of Science ®Google Scholar
• Morgan MA, Parsels LA, Parsels JD, Mesiwala AK, Maybaum J, Lawrence TS. Role of checkpoint kinase 1 in preventing premature mitosis in response to gemcitabine. Cancer Res 2005; 65:6835 - 42; http://dx.doi.org/10.1158/0008-5472.CAN-04-2246; PMID: 16061666
   PubMed Web of Science ®Google Scholar
• Beeharry N, Rattner JB, Bellacosa A, Smith MR, Yen TJ. Dose dependent effects on cell cycle checkpoints and DNA repair by bendamustine. PLoS One 2012; 7:e40342; http://dx.doi.org/10.1371/journal.pone.0040342; PMID: 22768280
   PubMed Web of Science ®Google Scholar
• Ma CX, Janetka JW, Piwnica-Worms H. Death by releasing the breaks: CHK1 inhibitors as cancer therapeutics. Trends Mol Med 2011; 17:88 - 96; http://dx.doi.org/10.1016/j.molmed.2010.10.009; PMID: 21087899
   PubMed Web of Science ®Google Scholar
• Blasina A, Hallin J, Chen E, Arango ME, Kraynov E, Register J, Grant S, Ninkovic S, Chen P, Nichols T, et al. Breaching the DNA damage checkpoint via PF-00477736, a novel small-molecule inhibitor of checkpoint kinase 1. Mol Cancer Ther 2008; 7:2394 - 404; http://dx.doi.org/10.1158/1535-7163.MCT-07-2391; PMID: 18723486
   PubMed Web of Science ®Google Scholar
• Aarts M, Sharpe R, Garcia-Murillas I, Gevensleben H, Hurd MS, Shumway SD, Toniatti C, Ashworth A, Turner NC. Forced mitotic entry of S-phase cells as a therapeutic strategy induced by inhibition of WEE1. Cancer Discov 2012; 2:524 - 39; http://dx.doi.org/10.1158/2159-8290.CD-11-0320; PMID: 22628408
   PubMed Web of Science ®Google Scholar
• Montano R, Chung I, Garner KM, Parry D, Eastman A. Preclinical development of the novel Chk1 inhibitor SCH900776 in combination with DNA-damaging agents and antimetabolites. Mol Cancer Ther 2012; 11:427 - 38; http://dx.doi.org/10.1158/1535-7163.MCT-11-0406; PMID: 22203733
   PubMed Web of Science ®Google Scholar
• Carrassa L, Damia G. Unleashing Chk1 in cancer therapy. Cell Cycle 2011; 10:2121 - 8; http://dx.doi.org/10.4161/cc.10.13.16398; PMID: 21610326
   PubMed Web of Science ®Google Scholar
• Prevo R, Fokas E, Reaper PM, Charlton PA, Pollard JR, McKenna WG, Muschel RJ, Brunner TB. The novel ATR inhibitor VE-821 increases sensitivity of pancreatic cancer cells to radiation and chemotherapy. Cancer Biol Ther 2012; 13:1072 - 81; http://dx.doi.org/10.4161/cbt.21093; PMID: 22825331
   PubMed Web of Science ®Google Scholar
• Fabian MA, Biggs WH 3rd, Treiber DK, Atteridge CE, Azimioara MD, Benedetti MG, Carter TA, Ciceri P, Edeen PT, Floyd M, et al. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat Biotechnol 2005; 23:329 - 36; http://dx.doi.org/10.1038/nbt1068; PMID: 15711537
   PubMed Web of Science ®Google Scholar
• Anastassiadis T, Deacon SW, Devarajan K, Ma H, Peterson JR. Comprehensive assay of kinase catalytic activity reveals features of kinase inhibitor selectivity. Nat Biotechnol 2011; 29:1039 - 45; http://dx.doi.org/10.1038/nbt.2017; PMID: 22037377
   PubMed Web of Science ®Google Scholar
• Isham CR, Bossou AR, Negron V, Fisher KE, Kumar R, Marlow L, Lingle WL, Smallridge RC, Sherman EJ, Suman VJ, et al. Pazopanib enhances paclitaxel-induced mitotic catastrophe in anaplastic thyroid cancer. Sci Transl Med 2013; 5:ra3; http://dx.doi.org/10.1126/scitranslmed.3004358; PMID: 23283368
   PubMed Web of Science ®Google Scholar
• Blay JY. A decade of tyrosine kinase inhibitor therapy: Historical and current perspectives on targeted therapy for GIST. Cancer Treat Rev 2011; 37:373 - 84; http://dx.doi.org/10.1016/j.ctrv.2010.11.003; PMID: 21195552
   PubMed Web of Science ®Google Scholar
• Blagosklonny MV. A new science-business paradigm in anticancer drug development. Trends Biotechnol 2003; 21:103 - 6; http://dx.doi.org/10.1016/S0167-7799(03)00004-0; PMID: 12628364
   PubMed Web of Science ®Google Scholar
• Shi Z, Azuma A, Sampath D, Li YX, Huang P, Plunkett W. S-Phase arrest by nucleoside analogues and abrogation of survival without cell cycle progression by 7-hydroxystaurosporine. Cancer Res 2001; 61:1065 - 72; PMID: 11221834
   PubMed Web of Science ®Google Scholar
• Toledo LI, Murga M, Zur R, Soria R, Rodriguez A, Martinez S, Oyarzabal J, Pastor J, Bischoff JR, Fernandez-Capetillo O. A cell-based screen identifies ATR inhibitors with synthetic lethal properties for cancer-associated mutations. Nat Struct Mol Biol 2011; 18:721 - 7; http://dx.doi.org/10.1038/nsmb.2076; PMID: 21552262
   PubMed Web of Science ®Google Scholar
• Mukherjee B, Tomimatsu N, Amancherla K, Camacho CV, Pichamoorthy N, Burma S. The dual PI3K/mTOR inhibitor NVP-BEZ235 is a potent inhibitor of ATM- and DNA-PKCs-mediated DNA damage responses. Neoplasia 2012; 14:34 - 43; PMID: 22355272
   PubMed Web of Science ®Google Scholar
• Levinson NM, Boxer SG. Structural and spectroscopic analysis of the kinase inhibitor bosutinib and an isomer of bosutinib binding to the Abl tyrosine kinase domain. PLoS One 2012; 7:e29828; http://dx.doi.org/10.1371/journal.pone.0029828; PMID: 22493660
   PubMedGoogle Scholar
• Guertin AD, Martin MM, Roberts B, Hurd M, Qu X, Miselis NR, Liu Y, Li J, Feldman I, Benita Y, et al. Unique functions of CHK1 and WEE1 underlie synergistic anti-tumor activity upon pharmacologic inhibition. Cancer Cell Int 2012; 12:45; http://dx.doi.org/10.1186/1475-2867-12-45; PMID: 23148684
   PubMed Web of Science ®Google Scholar
• Beeharry N, Rattner JB, Caviston JP, Yen T. Centromere fragmentation is a common mitotic defect of S and G2 checkpoint override. Cell Cycle 2013; 12:1588 - 97; http://dx.doi.org/10.4161/cc.24740; PMID: 23624842
   PubMed Web of Science ®Google Scholar
• Brinkley BR, Zinkowski RP, Mollon WL, Davis FM, Pisegna MA, Pershouse M, Rao PN. Movement and segregation of kinetochores experimentally detached from mammalian chromosomes. Nature 1988; 336:251 - 4; http://dx.doi.org/10.1038/336251a0; PMID: 3057382
   PubMed Web of Science ®Google Scholar
• McNeely S, Conti C, Sheikh T, Patel H, Zabludoff S, Pommier Y, Schwartz G, Tse A. Chk1 inhibition after replicative stress activates a double strand break response mediated by ATM and DNA-dependent protein kinase. Cell Cycle 2010; 9:995 - 1004; http://dx.doi.org/10.4161/cc.9.5.10935; PMID: 20160494
   PubMed Web of Science ®Google Scholar
• Domínguez-Kelly R, Martín Y, Koundrioukoff S, Tanenbaum ME, Smits VA, Medema RH, Debatisse M, Freire R. Wee1 controls genomic stability during replication by regulating the Mus81-Eme1 endonuclease. J Cell Biol 2011; 194:567 - 79; http://dx.doi.org/10.1083/jcb.201101047; PMID: 21859861
   PubMed Web of Science ®Google Scholar
• Krejci L, Altmannova V, Spirek M, Zhao X. Homologous recombination and its regulation. Nucleic Acids Res 2012; 40:5795 - 818; http://dx.doi.org/10.1093/nar/gks270; PMID: 22467216
   PubMed Web of Science ®Google Scholar
• Parsels LA, Morgan MA, Tanska DM, Parsels JD, Palmer BD, Booth RJ, Denny WA, Canman CE, Kraker AJ, Lawrence TS, et al. Gemcitabine sensitization by checkpoint kinase 1 inhibition correlates with inhibition of a Rad51 DNA damage response in pancreatic cancer cells. Mol Cancer Ther 2009; 8:45 - 54; http://dx.doi.org/10.1158/1535-7163.MCT-08-0662; PMID: 19139112
   PubMed Web of Science ®Google Scholar
• Blencke S, Zech B, Engkvist O, Greff Z, Orfi L, Horváth Z, Kéri G, Ullrich A, Daub H. Characterization of a conserved structural determinant controlling protein kinase sensitivity to selective inhibitors. Chem Biol 2004; 11:691 - 701; http://dx.doi.org/10.1016/j.chembiol.2004.02.029; PMID: 15157880
   PubMed Web of Science ®Google Scholar
• Davis MI, Hunt JP, Herrgard S, Ciceri P, Wodicka LM, Pallares G, Hocker M, Treiber DK, Zarrinkar PP. Comprehensive analysis of kinase inhibitor selectivity. Nat Biotechnol 2011; 29:1046 - 51; http://dx.doi.org/10.1038/nbt.1990; PMID: 22037378
   PubMed Web of Science ®Google Scholar
• Blagosklonny MV. Sequential activation and inactivation of G2 checkpoints for selective killing of p53-deficient cells by microtubule-active drugs. Oncogene 2002; 21:6249 - 54; http://dx.doi.org/10.1038/sj.onc.1205793; PMID: 12214265
   PubMed Web of Science ®Google Scholar
• Levinson NM, Boxer SG. A conserved water-mediated hydrogen bond network defines bosutinib’s kinase selectivity. Nat Chem Biol 2014; 10:127 - 32; http://dx.doi.org/10.1038/nchembio.1404; PMID: 24292070
   PubMed Web of Science ®Google Scholar
• Russell MR, Levin K, Rader J, Belcastro L, Li Y, Martinez D, Pawel B, Shumway SD, Maris JM, Cole KA. Combination therapy targeting the Chk1 and Wee1 kinases shows therapeutic efficacy in neuroblastoma. Cancer Res 2013; 73:776 - 84; http://dx.doi.org/10.1158/0008-5472.CAN-12-2669; PMID: 23135916
   PubMed Web of Science ®Google Scholar
• Kim WG, Guigon CJ, Fozzatti L, Park JW, Lu C, Willingham MC, Cheng SY. SKI-606, an Src inhibitor, reduces tumor growth, invasion, and distant metastasis in a mouse model of thyroid cancer. Clin Cancer Res 2012; 18:1281 - 90; http://dx.doi.org/10.1158/1078-0432.CCR-11-2892; PMID: 22271876
   PubMed Web of Science ®Google Scholar
• Cole KA, Huggins J, Laquaglia M, Hulderman CE, Russell MR, Bosse K, Diskin SJ, Attiyeh EF, Sennett R, Norris G, et al. RNAi screen of the protein kinome identifies checkpoint kinase 1 (CHK1) as a therapeutic target in neuroblastoma. Proc Natl Acad Sci U S A 2011; 108:3336 - 41; http://dx.doi.org/10.1073/pnas.1012351108; PMID: 21289283
   PubMed Web of Science ®Google Scholar
• Blackwood E, Epler J, Yen I, Flagella M, O’Brien T, Evangelista M, Schmidt S, Xiao Y, Choi J, Kowanetz K, et al. Combination drug scheduling defines a “window of opportunity” for chemopotentiation of gemcitabine by an orally bioavailable, selective ChK1 inhibitor, GNE-900. Mol Cancer Ther 2013; 12:1968 - 80; http://dx.doi.org/10.1158/1535-7163.MCT-12-1218; PMID: 23873850
   PubMed Web of Science ®Google Scholar
• Xiao Y, Ramiscal J, Kowanetz K, Del Nagro C, Malek S, Evangelista M, Blackwood E, Jackson PK, O’Brien T. Identification of preferred chemotherapeutics for combining with a CHK1 inhibitor. Mol Cancer Ther 2013; 12:2285 - 95; http://dx.doi.org/10.1158/1535-7163.MCT-13-0404; PMID: 24038068
   PubMed Web of Science ®Google Scholar
• Li C, Andrake M, Dunbrack R, Enders GH. A bifunctional regulatory element in human somatic Wee1 mediates cyclin A/Cdk2 binding and Crm1-dependent nuclear export. Mol Cell Biol 2010; 30:116 - 30; http://dx.doi.org/10.1128/MCB.01876-08; PMID: 19858290
   PubMed Web of Science ®Google Scholar
• Blagosklonny MV. The power of chemotherapeutic engineering: arresting cell cycle and suppressing senescence to protect from mitotic inhibitors. Cell Cycle 2011; 10:2295 - 8; http://dx.doi.org/10.4161/cc.10.14.16819; PMID: 21715978
   PubMed Web of Science ®Google Scholar
• Krieger E, Koraimann G, Vriend G. Increasing the precision of comparative models with YASARA NOVA--a self-parameterizing force field. Proteins 2002; 47:393 - 402; http://dx.doi.org/10.1002/prot.10104; PMID: 11948792
   PubMed Web of Science ®Google Scholar
• Meagher KL, Redman LT, Carlson HA. Development of polyphosphate parameters for use with the AMBER force field. J Comput Chem 2003; 24:1016 - 25; http://dx.doi.org/10.1002/jcc.10262; PMID: 12759902
   PubMed Web of Science ®Google Scholar
• Huang D, Zhou T, Lafleur K, Nevado C, Caflisch A. Kinase selectivity potential for inhibitors targeting the ATP binding site: a network analysis. Bioinformatics 2010; 26:198 - 204; http://dx.doi.org/10.1093/bioinformatics/btp650; PMID: 19942586
   PubMed Web of Science ®Google Scholar
• Rattner JB, Rao A, Fritzler MJ, Valencia DW, Yen TJ. CENP-F is a. ca 400 kDa kinetochore protein that exhibits a cell-cycle dependent localization. Cell Motil Cytoskeleton 1993; 26:214 - 26; http://dx.doi.org/10.1002/cm.970260305; PMID: 7904902
   PubMed Web of Science ®Google Scholar
• Yang DH, McKee KK, Chen ZL, Mernaugh G, Strickland S, Zent R, Yurchenco PD. Renal collecting system growth and function depend upon embryonic γ1 laminin expression. Development 2011; 138:4535 - 44; http://dx.doi.org/10.1242/dev.071266; PMID: 21903675
   PubMed Web of Science ®Google Scholar
• Yang DH, Smith ER, Roland IH, Sheng Z, He J, Martin WD, Hamilton TC, Lambeth JD, Xu XX. Disabled-2 is essential for endodermal cell positioning and structure formation during mouse embryogenesis. Dev Biol 2002; 251:27 - 44; http://dx.doi.org/10.1006/dbio.2002.0810; PMID: 12413896
   PubMed Web of Science ®Google Scholar
• Shults A, Ratcliffe SJ, Leonard M. Improved generalized estimating equation analysis via xtqls for implementation of quasi-least squares in Stata. Stata J 2007; 7:147 - 66
   Web of Science ®Google Scholar