Wee1 kinase as a target for cancer therapy

Cell Cycle

Volumn 12, Issue 19, 2013, Pages 3348-3353

  Do, Khanh ^a   Doroshow, James H ^a   Kummar, Shivaani ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Cell cycle; Cyclin dependent kinase; DNA damage; G2 checkpoint; MK 1775

Indexed keywords

ANTINEOPLASTIC AGENT; CAMPTOTHECIN; CAPECITABINE; CARBOPLATIN; CISPLATIN; DOXORUBICIN; FLUOROURACIL; GEMCITABINE; MITOMYCIN; MK 1775; PACLITAXEL; PEMETREXED; PROTEIN KINASE; PROTEIN KINASE INHIBITOR; UNCLASSIFIED DRUG; WEE1 KINASE;

ANTINEOPLASTIC ACTIVITY; CANCER RADIOTHERAPY; CANCER THERAPY; CELL CYCLE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; ESOPHAGUS CANCER; HEAD AND NECK CANCER; HUMAN; IC 50; NEOPLASM; NONHUMAN; OVARY TUMOR; PERITONEUM TUMOR; REVIEW; SOLID TUMOR; STOMACH CANCER; UTERINE TUBE TUMOR;

CELL CYCLE; CYCLIN-DEPENDENT KINASE; DNA DAMAGE; G2 CHECKPOINT; MK 1775;

ANTINEOPLASTIC AGENTS; CELL CYCLE PROTEINS; CLINICAL TRIALS AS TOPIC; DNA DAMAGE; DNA REPAIR; G2 PHASE CELL CYCLE CHECKPOINTS; HUMANS; NEOPLASMS; NUCLEAR PROTEINS; PROTEIN-TYROSINE KINASES; PYRAZOLES; PYRIMIDINES; RNA INTERFERENCE;

EID: 84886644238     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.26062     Document Type: Review

References (47)

1. Russell P, Nurse P. Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homolog. Cell 1987; 49:559-67; PMID:3032459; http://dx.doi.org/10.1016/0092-8674(87)90458-2
2. Parker LL, Piwnica-Worms H. Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science 1992; 257:1955- 7; PMID:1384126; http://dx.doi.org/10.1126/science.1384126
3. Bartek J, Lukas J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 2003; 3:421- 9; PMID:12781359; http://dx.doi.org/10.1016/ S1535-6108(03)00110-7 (Pubitemid 38340288)
4. Matsuoka S, Rotman G, Ogawa A, Shiloh Y, Tamai K, Elledge SJ. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci U S A 2000; 97:10389-94; PMID:10973490; http://dx.doi.org/10.1073/pnas. 190030497
5. Johnson N, Cai D, Kennedy RD, Pathania S, Arora M, Li YC, D'Andrea AD, Parvin JD, Shapiro GI. Cdk1 participates in BRCA1-dependent S phase checkpoint control in response to DNA damage. Mol Cell 2009; 35:327-39; PMID:19683496; http://dx.doi.org/10.1016/j.molcel.2009.06.036
6. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, Lukas J, Jackson SP. ATM- and cell cycledependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 2006; 8:37- 45; PMID:16327781; http://dx.doi.org/10.1038/ ncb1337 (Pubitemid 43064795)
7. 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; PMID:21859861; http://dx.doi.org/10.1083/jcb.201101047
8. Martín Y, Domínguez-Kelly R, Freire R. Novel insights into maintaining genomic integrity: Wee1 regulating Mus81/Eme1. Cell Div 2011; 6:21; PMID:22152133; http://dx.doi.org/10.1186/1747-1028-6-21
9. Masaki T, Shiratori Y, Rengifo W, Igarashi K, Yamagata M, Kurokohchi K, Uchida N, Miyauchi Y, Yoshiji H, Watanabe S, et al. Cyclins and cyclindependent kinases: comparative study of hepatocellular carcinoma versus cirrhosis. Hepatology 2003; 37:534-43; PMID:12601350; http://dx.doi.org/10.1053/jhep.2003. 50112 (Pubitemid 36258774)
10. Iorns E, Lord CJ, Grigoriadis A, McDonald S, Fenwick K, Mackay A, Mein CA, Natrajan R, Savage K, Tamber N, et al. Integrated functional, gene expression and genomic analysis for the identification of cancer targets. PLoS One 2009; 4:e5120; PMID:19357772; http://dx.doi.org/10.1371/journal.pone.0005120
11. Mir SE, De Witt Hamer PC, Krawczyk PM, Balaj L, Claes A, Niers JM, Van Tilborg AA, Zwinderman AH, Geerts D, Kaspers GJ, et al. In silico analysis of kinase expression identifies WEE1 as a gatekeeper against mitotic catastrophe in glioblastoma. Cancer Cell 2010; 18:244-57; PMID:20832752; http://dx.doi.org/10. 1016/j.ccr.2010.08.011
12. Magnussen GI, Holm R, Emilsen E, Rosnes AKR, Slipicevic A, Flørenes VA. High expression of Wee1 is associated with poor disease-free survival in malignant melanoma: potential for targeted therapy. PLoS One 2012; 7:e38254; PMID:22719872; http://dx.doi.org/10.1371/journal.pone.0038254
13. Wang Y, Li J, Booher RN, Kraker A, Lawrence T, Leopold WR, Sun Y. Radiosensitization of p53 mutant cells by PD0166285, a novel G(2) checkpoint abrogator. Cancer Res 2001; 61:8211-7; PMID:11719452 (Pubitemid 33091614)
14. Wang Y, Decker SJ, Sebolt-Leopold J. Knockdown of Chk1, Wee1 and Myt1 by RNA interference abrogates G2 checkpoint and induces apoptosis. Cancer Biol Ther 2004; 3:305-13; PMID:14726685; http://dx.doi.org/10.4161/cbt.3.3.697 (Pubitemid 41350885)
15. PosthumaDeBoer J, Würdinger T, Graat HC, van Beusechem VW, Helder MN, van Royen BJ, Kaspers GJ. WEE1 inhibition sensitizes osteosarcoma to radiotherapy. BMC Cancer 2011; 11:156; PMID:21529352; http://dx.doi.org/10.1186/ 1471-2407-11-156
16. Hirai H, Iwasawa Y, Okada M, Arai T, Nishibata T, Kobayashi M, Kimura T, Kaneko N, Ohtani J, Yamanaka K, et al. Small-molecule inhibition of Wee1 kinase by MK-1775 selectively sensitizes p53-deficient tumor cells to DNA-damaging agents. Mol Cancer Ther 2009; 8:2992-3000; PMID:19887545; http://dx.doi.org/10. 1158/1535-7163.MCT-09-0463
17. Hirai H, Arai T, Okada M, Nishibata T, Kobayashi M, Sakai N, Imagaki K, Ohtani J, Sakai T, Yoshizumi T, et al. MK-1775, a small molecule Wee1 inhibitor, enhances anti-tumor efficacy of various DNAdamaging agents, including 5-fluorouracil. Cancer Biol Ther 2010; 9:514-22; PMID:20107315; http://dx.doi.org/10.4161/cbt.9.7.11115
18. Rajeshkumar NV, De Oliveira E, Ottenhof N, Watters J, Brooks D, Demuth T, et al. MK-1775, a potent Wee1 inihibitor, synergizes with gemcitabine to achieve tumor regressions, selectively in p53-deficient pancreatic cancer xenografts. Clin Cancer Res 2011; 17:1-8; http://dx.doi.org/10.1158/1078-0432. CCR-10-2580
19. Bridges KA, Hirai H, Buser CA, Brooks C, Liu H, Buchholz TA, Molkentine JM, Mason KA, Meyn RE. MK-1775, a novel Wee1 kinase inhibitor, radiosensitizes p53-defective human tumor cells. Clin Cancer Res 2011; 17:5638-48; PMID:21799033; http://dx.doi.org/10.1158/1078-0432.CCR-11-0650
20. Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature 2009; 461:1071- 8; PMID:19847258; http://dx.doi.org/10.1038/ nature08467
21. Murrow LM, Garimella SV, Jones TL, Caplen NJ, Lipkowitz S. Identification of WEE1 as a potential molecular target in cancer cells by RNAi screening of the human tyrosine kinome. Breast Cancer Res Treat 2010; 122:347-57; PMID:19821025; http://dx.doi.org/10.1007/s10549-009-0571-2
22. Beck H, Nähse V, Larsen MS, Groth P, Clancy T, Lees M, Jørgensen M, Helleday T, Syljuåsen RG, Sørensen CS. Regulators of cyclin-dependent kinases are crucial for maintaining genome integrity in S phase. J Cell Biol 2010; 188:629-38; PMID:20194642; http://dx.doi.org/10.1083/jcb.200905059
23. Kreahling JM, Gemmer JY, Reed D, Letson D, Bui M, Altiok SMK. MK1775, a selective Wee1 inhibitor, shows single-agent antitumor activity against sarcoma cells. Mol Cancer Ther 2012; 11:174-82; PMID:22084170; http://dx.doi.org/10. 1158/1535- 7163.MCT-11-0529
24. Guertin AD, Li J, Liu Y, Hurd MS, Schuller AG, Long B, Hirsch HA, Feldman I, Benita Y, Toniatti C, et al. Preclinical Evaluation of the WEE1 Inhibitor MK-1775 as Single-Agent Anticancer Therapy. Mol Cancer Ther 2013; 12:1442-52; PMID:23699655; http://dx.doi.org/10.1158/1535-7163.MCT-13-0025
25. Schellens JH, Leijen S, Shapiro GI, Pavlick AC, Tibes R, O'Day SJ, et al. ASCO Annual Meeting Proceedings. A phase I and pharmacologic study of MK-1775, a Wee1 tyrosine kinase inhibitor, in both monotherapy and in combination with gemcitabine, cisplatin, or carboplatin in patients with advanced solid tumors. J Clin Oncol 2009
26. A Phase I Dose Escalation Study Evaluating MK1775 in Both Monotherapy and in Combination With Either Gemcitabine, Cisplatin, or Carboplatin in Adult Subjects With Advanced Solid Tumors (MK- 1775-001 AM7). Clinical Trials. gov Identifier: NCT00648648
27. A Phase I Dose Escalation Study of MK1775 in Monotherapy, in Combination With 5-Fluorouracil, and in Combination With 5-Fluorouracil and Cisplatin in Patients With Advanced Solid Tumor (1775-005). Clinical Trials. gov Identifier: NCT01047007
28. A Two Part, Phase I-IIa Study Evaluating MK1775 in Combination With Topotecan/Cisplatin in Adult Patients With Cervical Cancer (1775-008). Clinical Trials. gov Identifier: NCT01076400
29. Phase II Pharmacological Study With Wee-1 Inhibitor MK-1775 Combined With Carboplatin in Patients With p53 Mutated Epithelial Ovarian Cancer and Early Relapse (< 3 Months) or Progression During Standard First Line Treatment (M10MKO). Clinical Trials. gov Identifier: NCT01164995
30. A Randomized, Phase II Study Evaluating MK-1775 in Combination With Paclitaxel and Carboplatin Versus Paclitaxel and Carboplatin Alone in Adult Patients With Platinum Sensitive p53 Mutant Ovarian Cancer. Clinical Trials. gov Identifier: NCT01357161
31. A Phase I Study of Single-agent MK-1775, a Wee1 Inhibitor, in Patients With Advanced Refractory Solid Tumors. Clinical Trials. gov Identifier: NCT01748825
32. Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S, Carotenuto W, Liberi G, Bressan D, Wan L, Hollingsworth NM, et al. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 2004; 431:1011- 7; PMID:15496928; http://dx.doi.org/10.1038/nature02964 (Pubitemid 39434425)
33. Esashi F, Christ N, Gannon J, Liu Y, Hunt T, Jasin M, West SC. CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 2005; 434:598- 604; PMID:15800615; http://dx.doi.org/10.1038/nature03404 (Pubitemid 40488546)
34. Johnson N, Li YC, Walton ZE, Cheng KA, Li D, Rodig SJ, Moreau LA, Unitt C, Bronson RT, Thomas HD, et al. Compromised CDK1 activity sensitizes BRCA-proficient cancers to PARP inhibition. Nat Med 2011; 17:875-82; PMID:21706030; http://dx.doi.org/10.1038/nm.2377
35. Krajewska M, Heijink AM, Bisselink YJ, Seinstra RI, Silljé HH, de Vries EG, et al. Forced activation of Cdk1 via wee1 inhibition impairs homologous recombination. Oncogene 2012; PMID:22797065
36. Houtgraaf JH, Versmissen J, van der Giessen WJ. A concise review of DNA damage checkpoints and repair in mammalian cells. Cardiovasc Revasc Med 2006; 7:165-72; PMID:16945824; http://dx.doi.org/10.1016/j.carrev.2006.02.002 (Pubitemid 44292065)
37. El-Khamisy SF, Masutani M, Suzuki H, Caldecott KW. A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res 2003; 31:5526-33; PMID:14500814; http://dx.doi.org/10.1093/nar/gkg761 (Pubitemid 37441922)
38. Haince JF, McDonald D, Rodrigue A, Déry U, Masson JY, Hendzel MJ, Poirier GG. PARP1- dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J Biol Chem 2008; 283:1197-208; PMID:18025084; http://dx.doi.org/10.1074/jbc.M706734200
39. Wang M, Wu W, Wu W, Rosidi B, Zhang L, Wang H, Iliakis G. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res 2006; 34:6170-82; PMID:17088286; http://dx.doi.org/10.1093/ nar/gkl840 (Pubitemid 44942738)
40. Helleday T. The underlying mechanism for the PARP and BRCA synthetic lethality: clearing up the misunderstandings. Mol Oncol 2011; 5:387- 93; PMID:21821475; http://dx.doi.org/10.1016/j.molonc.2011.07.001
41. Davies KD, Cable PL, Garrus JE, Sullivan FX, von Carlowitz I, Huerou YL, Wallace E, Woessner RD, Gross S. Chk1 inhibition and Wee1 inhibition combine synergistically to impede cellular proliferation. Cancer Biol Ther 2011; 12:788-96; PMID:21892012; http://dx.doi.org/10.4161/cbt.12.9.17673
42. Sørensen CS, Hansen LT, Dziegielewski J, Syljuåsen RG, Lundin C, Bartek J, Helleday T. The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat Cell Biol 2005; 7:195-201; PMID:15665856; http://dx.doi.org/10.1038/ncb1212 (Pubitemid 40268135)
43. Aligue R, Akhavan-Niak H, Russell P. A role for Hsp90 in cell cycle control: Wee1 tyrosine kinase activity requires interaction with Hsp90. EMBO J 1994; 13:6099-106; PMID:7813446
44. Mollapour M, Tsutsumi S, Neckers L. Hsp90 phosphorylation, Wee1 and the cell cycle. Cell Cycle 2010; 9:2310-6; PMID:20519952; http://dx.doi.org/10.4161/ cc.9.12.12054
45. Mollapour M, Tsutsumi S, Donnelly AC, Beebe K, Tokita MJ, Lee MJ, Lee S, Morra G, Bourboulia D, Scroggins BT, et al. Swe1Wee1-dependent tyrosine phosphorylation of Hsp90 regulates distinct facets of chaperone function. Mol Cell 2010; 37:333- 43; PMID:20159553; http://dx.doi.org/10.1016/j.molcel.2010. 01.005
46. Iwai A, Bourboulia D, Mollapour M, Jensen- Taubman S, Lee S, Donnelly AC, Yoshida S, Miyajima N, Tsutsumi S, Smith AK, et al. Combined inhibition of Wee1 and Hsp90 activates intrinsic apoptosis in cancer cells. Cell Cycle 2012; 11:3649- 55; PMID:22935698; http://dx.doi.org/10.4161/cc.21926
47. Garimella SV, Rocca A, Lipkowitz S. WEE1 inhibition sensitizes basal breast cancer cells to TRAILinduced apoptosis. Mol Cancer Res 2012; 10:75-85; PMID:22112940; http://dx.doi.org/10.1158/1541- 7786.MCR-11-0500