The novel Chk1 inhibitor MK-8776 sensitizes human leukemia cells to HDAC inhibitors by targeting the intra-S checkpoint and DNA replication and repair

Molecular Cancer Therapeutics

Volumn 12, Issue 6, 2013, Pages 878-889

  Dai, Yun ^a   Chen, Shuang ^a   Kmieciak, Maciej ^a   Zhou, Liang ^a   Lin, Hui ^a   Pei, Xin Yan ^a   Grant, Steven ^a,b,c  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; MK 8776; PROTEIN SERINE THREONINE KINASE INHIBITOR; UNCLASSIFIED DRUG; VORINOSTAT;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; DNA REPAIR; DNA REPLICATION; DOWN REGULATION; HUMAN; HUMAN CELL; LEUKEMIA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; S PHASE CELL CYCLE CHECKPOINT;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BONE MARROW CELLS; CELLS, CULTURED; DNA REPAIR; DNA REPLICATION; GENE EXPRESSION REGULATION, LEUKEMIC; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; LEUKEMIA; PROTEIN KINASES; PYRAZOLES; PYRIMIDINES; S PHASE CELL CYCLE CHECKPOINTS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84879318134     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-12-0902     Document Type: Article

References (49)

1. Khan O, La Thangue NB. HDAC inhibitors in cancer biology: emerging mechanisms and clinical applications. Immunol Cell Biol 2012;90:85-94.
2. Gaymes TJ, Padua RA, Pla M, Orr S, Omidvar N, Chomienne C, et al. Histone deacetylase inhibitors (HDI) cause DNA damage in leukemia cells: a mechanism for leukemia-specific HDI-dependent apoptosis? Mol Cancer Res 2006;4:563-73.
3. Kachhap SK, Rosmus N, Collis SJ, Kortenhorst MS, Wissing MD, Hedayati M, et al. Downregulation of homologous recombination DNA repair genes by HDAC inhibition in prostate cancer is mediated through the E2F1 transcription factor. PLoS ONE 2010;5: e11208.
4. Lee JH, Choy ML, Ngo L, Foster SS, Marks PA. Histone deacetylase inhibitor induces DNA damage, which normal but not transformed cells can repair. Proc Natl Acad Sci U S A 2010;107:14639-44.
5. Dai Y, Grant S. New insights into checkpoint kinase 1 in the DNA damage response signaling network. Clin Cancer Res 2010;16: 376-83.
6. 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;40:477-86.
7. Syljuasen RG, Sorensen CS, Hansen LT, Fugger K, Lundin C, Johansson F, et al. Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol Cell Biol 2005;25:3553-62.
8. 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.
9. Schenk EL, Koh BD, Flatten K, Peterson KL, Karnitz LM, Parry D, et al. Effects of selective checkpoint kinase 1 inhibition on cytarabine cytotoxicity in acute myelogenous leukemia. Clin Cancer Res 2012; 18:5364-73.
10. Conti C, Leo E, Eichler GS, Sordet O, Martin MM, Fan A, et al. Inhibition of histone deacetylase in cancer cells slows down replication forks, activates dormant origins, and induces DNA damage. Cancer Res 2010;70:4470-80.
11. 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;10:591-602.
12. Ma CX, Cai S, Li S, Ryan CE, Guo Z, Schaiff WT, et al. Targeting Chk1 in p53-deficient triple-negative breast cancer is therapeuti-cally beneficial in human-in-mouse tumor models. J Clin Invest 2012;122:1541-52.
13. Sugimoto K, Toyoshima H, Sakai R, Miyagawa K, Hagiwara K, Ishi-kawa F, et al. Frequent mutations in the p53 gene in human myeloid leukemia cell lines. Blood 1992;79:2378-83.
14. Quentmeier H, Reinhardt J, Zaborski M, Drexler HG. FLT3 mutations in acute myeloid leukemia cell lines. Leukemia 2003;17:120-4.
15. Fleckenstein DS, Uphoff CC, Drexler HG, Quentmeier H. Detection of p53 gene mutations by single strand conformational polymorphism (SSCP) in human acute myeloid leukemia-derived cell lines. Leuk Res 2002;26:207-14.
16. Kojima K, Konopleva M, Samudio IJ, Shikami M, Cabreira-Hansen M, McQueen T, et al. MDM2 antagonists induce p53-dependent apopto-sis in AML: implications for leukemia therapy. Blood 2005;106:3150-9.
17. Dai Y, Yu C, Singh V, Tang L, Wang Z, McInistry R, et al. Pharmacological inhibitors of the mitogen-activated protein kinase (MAPK) kinase/MAPK cascade interact synergistically with UCN-01 to induce mitochondrial dysfunction and apoptosis in human leukemia cells. Cancer Res 2001;61:5106-15.
18. Sutcliffe T, Fu L, Abraham J, Vaziri H, Benchimol S. A functional wildtype p53 gene is expressed in human acute myeloid leukemia cell lines. Blood 1998;92:2977-9.
19. Dai Y, Chen S, Wang L, Pei XY, Kramer LB, Dent P, et al. Bortezomib interacts synergistically with belinostat in human acute myeloid leukaemia and acute lymphoblastic leukaemia cells in association with perturbations in NF-kappaB and Bim. Br J Haematol 2011;153: 222-35.
20. Dai Y, Grant S. Methods to study cancer therapeutic drugs that target cell cycle checkpoints. Methods Mol Biol 2011;782:257-304.
21. 1) human multiple myeloma cells are susceptible to simultaneous inhibition of Chk1 and MEK1/2. Blood 2011;118:5189-200.
22. Goudelock DM, Jiang K, Pereira E, Russell B, Sanchez Y. Regulatory interactions between the checkpoint kinase Chk1 and the proteins of the DNA-dependent protein kinase complex. J Biol Chem 2003;278: 29940-7.
23. Mitchell JB, Choudhuri R, Fabre K, Sowers AL, Citrin D, Zabludoff SD, et al. In vitro and in vivo radiation sensitization of human tumor cells by a novel checkpoint kinase inhibitor, AZD7762. Clin Cancer Res 2010;16:2076-84.
24. Brazelle W, Kreahling JM, Gemmer J, Ma Y, Cress WD, Haura E, et al. Histone deacetylase inhibitors downregulate checkpoint kinase 1 expression to induce cell death in non-small cell lung cancer cells. PLoS ONE 2010;5:e14335.
25. Zhang YW, Brognard J, Coughlin C, You Z, Dolled-Filhart M, Aslanian A, et al. The F box protein Fbx6 regulates Chk1 stability and cellular sensitivity to replication stress. Mol Cell 2009;35:442-53.
26. Salic A, Mitchison TJ. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci U S A 2008; 105:2415-20.
27. Hall JR, Lee HO, Bunker BD, Dorn ES, Rogers GC, Duronio RJ, et al. Cdt1 and Cdc6 are destabilized by rereplication-induced DNA damage. J Biol Chem 2008;283:25356-63.
28. Darzynkiewicz Z, Traganos F, Zhao H, Halicka HD, Skommer J, Wlodkowic D. Analysis of individual molecular events of DNA damage response by flow- and image-assisted cytometry. Methods Cell Biol 2011;103:115-47.
29. You Z, Shi LZ, Zhu Q, Wu P, Zhang YW, Basilio A, et al. CtIP links DNA double-strand break sensing to resection. Mol Cell 2009;36:954-69.
30. You Z, Bailis JM. DNA damage and decisions: CtIP coordinates DNA repair and cell cycle checkpoints. Trends Cell Biol 2010;20:402-9.
31. Cortez D, Wang Y, Qin J, Elledge SJ. Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to doublestrand breaks. Science 1999;286:1162-6.
32. Yun MH, Hiom K. CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature 2009; 459:460-3.
33. Shieh SY, Ahn J, Tamai K, Taya Y, Prives C. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev 2000;14:289-300.
34. Tibbetts RS, Brumbaugh KM, Williams JM, Sarkaria JN, Cliby WA, Shieh SY, et al. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev 1999;13:152-7.
35. Kojima K, Shimanuki M, Shikami M, Samudio IJ, Ruvolo V, Corn P, et al. The dual PI3 kinase/mTOR inhibitor PI-103 prevents p53 induction by Mdm2 inhibition but enhances p53-mediated mitochondrial apoptosis in p53 wild-type AML. Leukemia 2008;22:1728-36.
36. Didier C, Demur C, Grimal F, Jullien D, Manenti S, Ducommun B. Evaluation of checkpoint kinase targeting therapy in acute myeloid leukemia with complex karyotype. Cancer Biol Ther 2012;13:307-13.
37. Feijoo C, Hall-Jackson C, Wu R, Jenkins D, Leitch J, Gilbert DM, et al. Activation of mammalian Chk1 during DNA replication arrest: a role for Chk1 in the intra-S phase checkpoint monitoring replication origin firing. J Cell Biol 2001;154:913-23.
38. Naruyama H, Shimada M, Niida H, Zineldeen DH, Hashimoto Y, Kohri K, et al. Essential role of Chk1 in S phase progression through regulation of RNR2 expression. Biochem Biophys Res Commun 2008;374:79-83.
39. Wohlschlegel JA, Dwyer BT, Dhar SK, Cvetic C, Walter JC, Dutta A. Inhibition of eukaryotic DNA replication by geminin binding to Cdt1. Science 2000;290:2309-12.
40. Saleh-Gohari N, Helleday T. Conservative homologous recombination preferentially repairs DNA double-strand breaks in the S phase of the cell cycle in human cells. Nucleic Acids Res 2004;32:3683-8.
41. Robert T, Vanoli F, Chiolo I, Shubassi G, Bernstein KA, Rothstein R, et al. HDACs link the DNA damage response, processing of doublestrand breaks and autophagy. Nature 2011;471:74-9.
42. Pedersen-Bjergaard J, Andersen MK, Andersen MT, Christiansen DH. Genetics of therapy-related myelodysplasia and acute myeloid leukemia. Leukemia 2008;22:240-8.
43. Offer H, Erez N, Zurer I, Tang X, Milyavsky M, Goldfinger N, et al. The onset of p53-dependent DNA repair or apoptosis is determined by the level of accumulated damaged DNA. Carcinogenesis 2002;23: 1025-32.
44. Fan J, Li L, Small D, Rassool F. Cells expressing FLT3/ITD mutations exhibit elevated repair errors generated through alternative NHEJ pathways: implications for genomic instability and therapy. Blood 2010;116:5298-305.
45. Lee JH, Choy ML, Ngo L, Venta-Perez G, Marks PA. Role of checkpoint kinase 1 (Chk1) in the mechanisms of resistance to histone deacetylase inhibitors. Proc Natl Acad Sci U S A 2011;108:19629-34.
46. Boast S, La MG, Lania L, Blasi F. High efficiency of replication and expression of foreign genes in SV40-transformed human fibroblasts. EMBO J 1983;2:2327-31.
47. Bartucci M, Svensson S, Romania P, Dattilo R, Patrizii M, Signore M, et al. Therapeutic targeting of Chk1 in NSCLC stem cells during chemotherapy. Cell Death Differ 2012;19:768-78.
48. Venkatesha VA, Parsels LA, Parsels JD, Zhao L, Zabludoff SD, Simeone DM, et al. Sensitization of pancreatic cancer stem cells to gemcitabine by chk1 inhibition. Neoplasia 2012;14:519-25.
49. Desmarais JA, Hoffmann MJ, Bingham G, Gagou ME, Meuth M, Andrews PW. Human embryonic stem cells fail to activate CHK1 and commit to apoptosis in response to DNA replication stress. Stem Cells 2012;30:1385-93.