Abrogating G2/M checkpoint through WEE1 inhibition in combination with chemotherapy as a promising therapeutic approach for mesothelioma

Cancer Biology and Therapy

Volumn 15, Issue 4, 2014, Pages 380-388

  Indovina, Paola ^a,b   Marcelli, Eleonora ^a   Di Marzo, Domenico ^c   Casini, Nadia ^a   Forte, Iris Maria ^c   Giorgi, Francesca ^a   Alfano, Luigi ^c   Pentimalli, Francesca ^c   Giordano, Antonio ^a,b,c  

^a UNIVERSITY OF SIENA   (Italy)

^b Temple University   (United States)

^c NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Apoptosis; CDK1; Cisplatin; G2 M checkpoint; Mesothelioma; MK 1775; WEE1

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE 3; CISPLATIN; CYCLIN DEPENDENT KINASE 1; HISTONE H2AX; HISTONE H3; MK 1775; PROTEIN P53; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE INHIBITOR; UNCLASSIFIED DRUG; WEE1 KINASE; 2 ALLYL 1 [6 (1 HYDROXY 1 METHYLETHYL) 2 PYRIDINYL] 6 [4 (4 METHYL 1 PIPERAZINYL)ANILINO] 1H PYRAZOLO[3,4 D]PYRIMIDIN 3(2H) ONE; CELL CYCLE PROTEIN; NUCLEAR PROTEIN; PROTEIN TYROSINE KINASE; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE; WEE1 PROTEIN, HUMAN;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CELL VIABILITY; CHEMOSENSITIZATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DNA DAMAGE CHECKPOINT; DRUG POTENTIATION; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; EPITHELIOID CELL; FIBROBLAST; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; GENE MUTATION; HUMAN; HUMAN CELL; IC 50; MALIGNANT MESOTHELIOMA; MITOSIS; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; LUNG NEOPLASMS; MESOTHELIOMA; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CISPLATIN; DRUG SYNERGISM; G2 PHASE CELL CYCLE CHECKPOINTS; HUMANS; LUNG NEOPLASMS; MESOTHELIOMA; NUCLEAR PROTEINS; PROTEIN-TYROSINE KINASES; PYRAZOLES; PYRIMIDINES;

EID: 84897499154     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.27623     Document Type: Article

References (40)

1. Bridda A, Padoan I, Mencarelli R, Frego M. Peritoneal mesothelioma: a review. MedGenMed 2007; 9:32; PMID:17955087
2. Robinson BW, Musk AW, Lake RA. Malignant mesothelioma. Lancet 2005; 366:397-408; PMID:16054941; http://dx.doi.org/10.1016/S0140-6736(05)67025-0
3. Tsao AS, Wistuba I, Roth JA, Kindler HL. Malignant pleural mesothelioma. J Clin Oncol 2009; 27:2081-90; PMID:19255316; http://dx.doi.org/10.1200/JCO. 2008.19.8523
4. Zhou BB, Bartek J. Targeting the checkpoint kinases: chemosensitization versus chemoprotection. Nat Rev Cancer 2004; 4:216-25; PMID:14993903; http://dx.doi.org/10.1038/nrc1296
5. Kawabe T. G 2 checkpoint abrogators as anticancer drugs. Mol Cancer Ther 2004; 3:513-9; PMID:15078995
6. Levesque AA, Eastman A. p53-based cancer therapies: Is defective p53 the Achilles heel of the tumor? Carcinogenesis 2007; 28:13-20; PMID:17088261; http://dx.doi.org/10.1093/carcin/bgl214
7. Lee AY, Raz DJ, He B, Jablons DM. Update on the molecular biology of malignant mesothelioma. Cancer 2007; 109:1454-61; PMID:17348013; http://dx.doi.org/10.1002/cncr.22552
8. Prins JB, Williamson KA, Kamp MM, Van Hezik EJ, Van der Kwast TH, Hagemeijer A, Versnel MA. The gene for the cyclin-dependent-kinase-4 inhibitor, CDKN2A, is preferentially deleted in malignant mesothelioma. Int J Cancer 1998; 75:649-53; PMID:9466670; http://dx.doi.org/10.1002/(SICI)1097-0215(19980209)75: 4〈649::AIDIJC25〉3.0.CO;2-2
9. Sharpless NE, DePinho RA. The INK4A/ARF locus and its two gene products. Curr Opin Genet Dev 1999; 9:22-30; PMID:10072356; http://dx.doi.org/10.1016/ S0959-437X(99)80004-5
10. Wong L, Zhou J, Anderson D, Kratzke RA. Inactivation of p16INK4a expression in malignant mesothelioma by methylation. Lung Cancer 2002; 38:131-6; PMID:12399123; http://dx.doi.org/10.1016/S0169-5002(02)00178-2
11. Gazdar AF, Butel JS, Carbone M. SV40 and human tumours: myth, association or causality? Nat Rev Cancer 2002; 2:957-64; PMID:12459734; http://dx.doi.org/10.1038/nrc947
12. Testa JR, Giordano A. SV40 and cell cycle perturbations in malignant mesothelioma. Semin Cancer Biol 2001; 11:31-8; PMID:11243897; http://dx.doi.org/10.1006/scbi.2000.0344
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
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
15. 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
16. 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 DNA-damaging agents, including 5-fluorouracil. Cancer Biol Ther 2010; 9:514-22; PMID:20107315; http://dx.doi.org/10.4161/cbt.9.7.11115
17. Indovina P, Giordano A. Targeting the checkpoint kinase WEE1: selective sensitization of cancer cells to DNA-damaging drugs. Cancer Biol Ther 2010; 9:523-5; PMID:20150761; http://dx.doi.org/10.4161/cbt.9.7.11276
18. 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
19. Rajeshkumar NV, De Oliveira E, Ottenhof N, Watters J, Brooks D, Demuth T, Shumway SD, Mizuarai S, Hirai H, Maitra A, et al. MK-1775, a potent Wee1 inhibitor, synergizes with gemcitabine to achieve tumor regressions, selectively in p53-deficient pancreatic cancer xenografts. Clin Cancer Res 2011; 17:2799-806; PMID:21389100; http://dx.doi.org/10.1158/1078-0432.CCR-10-2580
20. Sarcar B, Kahali S, Prabhu AH, Shumway SD, Xu Y, Demuth T, Chinnaiyan P. Targeting radiation-induced G(2) checkpoint activation with the Wee-1 inhibitor MK-1775 in glioblastoma cell lines. Mol Cancer Ther 2011; 10:2405-14; PMID:21992793; http://dx.doi.org/10.1158/1535-7163.MCT-11-0469
21. 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
22. 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
23. Cozzi M, Giorgi F, Marcelli E, Pentimalli F, Forte IM, Schenone S, D'Urso V, De Falco G, Botta M, Giordano A, et al. Antitumor activity of new pyrazolo[3,4-d]pyrimidine SRC kinase inhibitors in Burkitt lymphoma cell lines and its enhancement by WEE1 inhibition. Cell Cycle 2012; 11:1029-39; PMID:22333592; http://dx.doi.org/10.4161/cc.11.5.19519
24. O'Connell MJ, Raleigh JM, Verkade HM, Nurse P. Chk1 is a wee1 kinase in the G2 DNA damage checkpoint inhibiting cdc2 by Y15 phosphorylation. EMBO J 1997; 16:545-54; PMID:9034337; http://dx.doi.org/10.1093/emboj/16.3.545
25. Leijen S, Schellens JH, Shapiro G, Pavlick R, Tibes T, Demuth J, Viscusi J, Cheng JD, Xu Y, Oza AM. A phase I pharmacological and pharmacodynamics study of MK-1775, a Wee1 tyrosine kinase inhibitor, in monotherapy and combination with gemcitabine, cisplatin, or carboplatin in patients with advanced solid tumors. J Clin Oncol 2010; 28:15s
26. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984; 22:27-55; PMID:6382953; http://dx.doi.org/10.1016/0065-2571(84)90007-4
27. Manfredi JJ, Dong J, Liu WJ, Resnick-Silverman L, Qiao R, Chahinian P, Saric M, Gibbs AR, Phillips JI, Murray J, et al. Evidence against a role for SV40 in human mesothelioma. Cancer Res 2005; 65:2602-9; PMID:15805256; http://dx.doi.org/10.1158/0008-5472.CAN-04-2461
28. Pietruska JR, Kane AB. SV40 oncoproteins enhance asbestos-induced DNA double-strand breaks and abrogate senescence in murine mesothelial cells. Cancer Res 2007; 67:3637-45; PMID:17440075; http://dx.doi.org/10.1158/0008-5472.CAN- 05-3727
29. Di Marzo D, Forte IM, Indovina P, Di Gennaro E, Rizzo V, Giorgi F, Mattioli E, Iannuzzi CA, Budillon A, Giordano A, et al. Pharmacological targeting of p53 through RITA is an effective antitumoral strategy for malignant pleural mesothelioma. Cell Cycle 2014; 13:652-65; PMID:24345738; http://dx.doi.org/10.4161/cc.27546
30. Brooks CL, Gu W. p53 ubiquitination: Mdm2 and beyond. Mol Cell 2006; 21:307-15; PMID:16455486; http://dx.doi.org/10.1016/j.molcel.2006.01.020
31. Villanova F, Procopio A, Rippo MR. Malignant mesothelioma resistance to apoptosis: recent discoveries and their implication for effective therapeutic strategies. Curr Med Chem 2008; 15:631-41; PMID:18336278; http://dx.doi.org/10. 2174/092986708783885273
32. Nilsonne G, Sun X, Nyström C, Rundlöf AK, Potamitou Fernandes A, Björnstedt M, Dobra K. Selenite induces apoptosis in sarcomatoid malignant mesothelioma cells through oxidative stress. Free Radic Biol Med 2006; 41:874-85; PMID:16934670; http://dx.doi.org/10.1016/j.freeradbiomed.2006.04.031
33. Aung W, Hasegawa S, Furukawa T, Saga T. Potential role of ferritin heavy chain in oxidative stress and apoptosis in human mesothelial and mesothelioma cells: implications for asbestos-induced oncogenesis. Carcinogenesis 2007; 28:2047-52; PMID:17434931; http://dx.doi.org/10.1093/carcin/bgm090
34. Hashimoto O, Shinkawa M, Torimura T, Nakamura T, Selvendiran K, Sakamoto M, Koga H, Ueno T, Sata M. Cell cycle regulation by the Wee1 inhibitor PD0166285, pyrido [2,3-d] pyimidine, in the B16 mouse melanoma cell line. BMC Cancer 2006; 6:292; PMID:17177986; http://dx.doi.org/10.1186/1471-2407-6-292
35. 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
36. Kreahling JM, Gemmer JY, Reed D, Letson D, Bui M, Altiok S. 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
37. 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
38. Romagnoli S, Fasoli E, Vaira V, Falleni M, Pellegrini C, Catania A, Roncalli M, Marchetti A, Santambrogio L, Coggi G, et al. Identification of potential therapeutic targets in malignant mesothelioma using cell-cycle gene expression analysis. Am J Pathol 2009; 174:762-70; PMID:19218339; http://dx.doi.org/10.2353/ajpath.2009.080721
39. Pianigiani E, Ierardi F, Mazzanti B, Saccardi R, Cuciti C, Fimiani M. Human de-epidermized dermis as a stem cell carrier. Transplant Proc 2010; 42:2244-6; PMID:20692454; http://dx.doi.org/10.1016/j.transproceed.2010.05.040
40. Indovina P, Giorgi F, Rizzo V, Khadang B, Schenone S, Di Marzo D, Forte IM, Tomei V, Mattioli E, D'Urso V, et al. New pyrazolo[3,4-d]pyrimidine SRC inhibitors induce apoptosis in mesothelioma cell lines through p27 nuclear stabilization. Oncogene 2012; 31:929-38; PMID:21785466; http://dx.doi.org/10. 1038/onc.2011.286