CHK1 and WEE1 inhibition combine synergistically to enhance therapeutic efficacy in acute myeloid leukemia ex vivo

Haematologica

Volumn 99, Issue 4, 2014, Pages 688-696

  Chaudhuri, Leena ^a   Vincelette, Nicole D ^b   Koh, Brian D ^c   Naylor, Ryan M ^c   Flatten, Karen S ^c   Peterson, Kevin L ^c   McNally, Amanda ^a   Gojo, Ivana ^d   Karp, Judith E ^d   Mesa, Ruben A ^a   Sproat, Lisa O ^a   Bogenberger, James M ^a   Kaufmann, Scott H ^b,c   Tibes, Raoul ^a  

^a MAYO CLINIC   (United States)

^b Department of Molecular Pharmacology and Experimental Therapeutics ^*  (United States)

^c Division of Oncology Research and Mayo Clinic   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; CYCLIN DEPENDENT KINASE 2; MK 1775; MK 8776; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; 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; ATM PROTEIN; CELL CYCLE PROTEIN; MK-8776; NUCLEAR PROTEIN; PROTEIN KINASE INHIBITOR; PROTEIN TYROSINE KINASE; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE; WEE1 PROTEIN, HUMAN;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; CELL CULTURE; CELL CYCLE; CELL CYCLE CHECKPOINT; CFU COUNTING; CONTROLLED STUDY; DOSE RESPONSE; DRUG POTENTIATION; ENZYME INHIBITION; EX VIVO STUDY; GENE; GENE SILENCING; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; RNA INTERFERENCE; ANTAGONISTS AND INHIBITORS; APOPTOSIS; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION PROFILING; GENETICS; LEUKEMIA, MYELOID, ACUTE; METABOLISM; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

APOPTOSIS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; GENE EXPRESSION PROFILING; GENE SILENCING; HUMANS; LEUKEMIA, MYELOID, ACUTE; NUCLEAR PROTEINS; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; PROTEIN-TYROSINE KINASES; PYRAZOLES; PYRIMIDINES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR STEM CELL ASSAY;

EID: 84897429295     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2013.093187     Document Type: Article

References (40)

1. Burnett A, Wetzler M, Lowenberg B. Therapeutic advances in acute myeloid leukemia. J Clin Oncol. 2011;29(5):487-94.
2. Bartek J, Lukas J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell. 2003;3(5):421-9.
3. Cavelier C, Didier C, Prade N, Mansat-De Mas V, Manenti S, Recher C, et al. Constitutive activation of the DNA damage signaling pathway in acute myeloid leukemia with complex karyotype: potential importance for checkpoint targeting therapy. Cancer Res. 2009;69(22):8652-61.
4. Bowen D, Groves MJ, Burnett AK, Patel Y, Allen C, Green C, et al. TP53 gene mutation is frequent in patients with acute myeloid leukemia and complex karyotype, and is associated with very poor prognosis. Leukemia. 2009;23(1):203-6.
5. Seifert H, Mohr B, Thiede C, Oelschlagel U, Schakel U, Illmer T, et al. The prognostic impact of 17p (p53) deletion in 2272 adults with acute myeloid leukemia. Leukemia. 2009;23(4):656-63.
6. Haferlach C, Dicker F, Herholz H, Schnittger S, Kern W, Haferlach T. Mutations of the TP53 gene in acute myeloid leukemia are strongly associated with a complex aberrant karyotype. Leukemia. 2008;22(8):1539-41.
7. Tibes R, Bogenberger JM, Chaudhuri L, Hagelstrom RT, Chow D, Buechel ME, et al. RNAi screening of the kinome with cytarabine in leukemias. Blood. 2012;119(12): 2863-72.
8. Watanabe N, Broome M, Hunter T. Regulation of the human WEE1Hu CDK tyrosine 15-kinase during the cell cycle. Embo J. 1995;14(9):1878-91.
9. Sorensen CS, Syljuasen RG. Safeguarding genome integrity: the checkpoint kinases ATR, CHK1 and WEE1 restrain CDK activity during normal DNA replication. Nucleic Acids Res. 2012;40(2):477-86.
10. Dominguez-Kelly R, Martin Y, Koundrioukoff S, Tanenbaum ME, Smits VA, Medema RH, et al. Wee1 controls genomic stability during replication by regulating the Mus81-Eme1 endonuclease. J Cell Biol. 2011;194(4):567-79.
11. Hirai H, Iwasawa Y, Okada M, Arai T, Nishibata T, Kobayashi M, 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(11):2992-3000.
12. Rajeshkumar NV, De Oliveira E, Ottenhof N, Watters J, Brooks D, Demuth T, 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(9):2799-806.
13. Nurse P. Universal control mechanism regulating onset of M-phase. Nature. 1990;344 (6266):503-8.
14. Dunphy WG. The decision to enter mitosis. Trends Cell Biol. 1994;4(6):202-7.
15. 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(3): 545-54.
16. Elledge SJ. Cell cycle checkpoints: preventing an identity crisis. Science. 1996;274 (5293):1664-72.
17. Wilsker D, Petermann E, Helleday T, Bunz F. Essential function of Chk1 can be uncoupled from DNA damage checkpoint and replication control. Proc Natl Acad Sci USA. 2008;105(52):20752-7.
18. Kasahara K, Goto H, Enomoto M, Tomono Y, Kiyono T, Inagaki M. 14-3-3gamma mediates Cdc25A proteolysis to block premature mitotic entry after DNA damage. Embo J. 2010;29(16):2802-12.
19. 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 (2):427-38.
20. Zabludoff SD, Deng C, Grondine MR, Sheehy AM, Ashwell S, Caleb BL, et al. AZD7762, a novel checkpoint kinase inhibitor, drives checkpoint abrogation and potentiates DNA-targeted therapies. Mol Cancer Ther. 2008;7(9):2955-66.
21. Guzi TJ, Paruch K, Dwyer MP, Labroli M, Shanahan F, Davis N, et al. Targeting the replication checkpoint using SCH 900776, a potent and functionally selective CHK1 inhibitor identified via high content screening. Mol Cancer Ther. 2011;10(4):591-602.
22. Karp JE, Thomas BM, Greer JM, Sorge C, Gore SD, Pratz KW, et al. 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):6723-31.
23. Thomas BM, Kaufmann SH, Greer JM, Gore SD, Pratz KW, Smith BD, et al. Phase I doseescalation study of SCH 900776 in combination with cytarabine (Ara-C) in patients with acute leukemia. Blood. 2011;118(21): 665-65.
24. Schenk EL, Koh BD, Flatten KS, Peterson KL, Parry D, Hess AD, et al. Effects of selective checkpoint kinase 1 inhibition on cytarabine cytotoxicity in acute myelogenous leukemia cells in vitro. Clin Cancer Res. 2012;18(19): 5364-73.
25. Pike BL, Robinson WA. Human bone marrow colony growth in agar-gel. J Cell Physiol. 1970;76(1):77-84.
26. Eaves C, Lambie K. Atlas of Human Hematopoietic Colonies. In: StemCell Technologies, Inc. Vancouver, 1995.
27. Melixetian M, Klein DK, Sorensen CS, Helin K. NEK11 regulates CDC25A degradation and the IR-induced G2/M checkpoint. Nat Cell Biol. 2009;11(10):1247-53.
28. Liu S, Song N, Zou L. The conserved C terminus of Claspin interacts with Rad9 and promotes rapid activation of Chk1. Cell Cycle. 2012;11(14):2711-6.
29. Yang XH, Shiotani B, Classon M, Zou L. Chk1 and Claspin potentiate PCNA ubiquitination. Gene Dev. 2008;22(9):1147-52.
30. Leijen S, Schellens JH, Shapiro G, Pavlick AC, Tibes R, Demuth T, et al. A phase I pharmacological and pharmacodynamic study of MK-1775, a Wee1 tyrosine kinase inhibitor, in monotherapy and combination with gemcitabine, cisplatin, or carboplatin in patients with advanced solid tumors. 2010 ASCO Annual Meeting 2010. J Clin Oncol 2010.
31. 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.
32. Weiss WA, Taylor SS, Shokat KM. Recognizing and exploiting differences between RNAi and small-molecule inhibitors. Nat Chem Biol. 2007;3(12):739-44.
33. Ye XS, Xu G, Pu RT, Fincher RR, McGuire SL, Osmani AH, et al. The NIMA protein kinase is hyperphosphorylated and activated downstream of p34cdc2/cyclin B: coordination of two mitosis promoting kinases. Embo J. 1995;14(5):986-94.
34. Berry LD, Gould KL. Regulation of Cdc2 activity by phosphorylation at T14/Y15. Prog Cell Cycle Res. 1996;2:99-105.
35. Leijen S, Beijnen JH, Schellens JH. Abrogation of the G2 checkpoint by inhibition of Wee-1 kinase results in sensitization of p53-deficient tumor cells to DNA-damaging agents. Curr Clin Pharmacol. 2010;5(3): 186-91.
36. Huntoon CJ, Flatten KS, Wahner Hendrickson AE, Huehls AM, Sutor SL, Kaufmann SH, et al. ATR inhibition broadly sensitizes ovarian cancer cells to chemotherapy independent of BRCA status. Cancer Res. 2013;73(12):3683-91.
37. Russell MR, Levin K, Rader J, Belcastro L, Li Y, Martinez D, et al. Combination therapy targeting the Chk1 and Wee1 kinases shows therapeutic efficacy in neuroblastoma. Cancer Res. 2013;73(2):776-84.
38. Davies KD, Cable PL, Garrus JE, Sullivan FX, von Carlowitz I, Huerou YL, et al. Chk1 inhibition and Wee1 inhibition combine synergistically to impede cellular proliferation. Cancer Biol Ther. 2011;12(9):788-96.
39. Carrassa L, Chila R, Lupi M, Ricci F, Celenza C, Mazzoletti M, et al. Combined inhibition of Chk1 and Wee1: in vitro synergistic effect translates to tumor growth inhibition in vivo. Cell Cycle. 2012;11(13):2507-17.
40. Guertin AD, Martin MM, Roberts B, Hurd M, Qu X, Miselis NR, et al. Unique functions of CHK1 and WEE1 underlie synergistic anti-tumor activity upon pharmacologic inhibition. Cancer Cell Int. 2012;12(1):45.