Synthetic lethality of Chk1 inhibition combined with p53 and/or p21 loss during a DNA damage response in normal and tumor cells

Oncogene

Volumn 32, Issue 5, 2013, Pages 577-588

  Origanti, S ^a   Cai, S R ^a   Munir, A Z ^a   White, L S ^a   Piwnica Worms, H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

apoptosis; cancer; cell cycle; checkpoints

Indexed keywords

5 (3 FLUOROPHENYL) N (3 PIPERIDINYL) 3 UREIDO 2 THIOPHENECARBOXAMIDE; 7 HYDROXYSTAUROSPORINE; CHECKPOINT KINASE 1; DNA; IRINOTECAN; PROTEIN P21; PROTEIN P53; PURVALANOL A;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CELL CYCLE CHECKPOINT; CELL FRACTIONATION; CELL TYPE; CHEMOSENSITIVITY; COLORECTAL CANCER; CONTROLLED STUDY; DNA DAMAGE; DRUG BIOAVAILABILITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; TUMOR CELL; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CAMPTOTHECIN; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; MICE; MICE, KNOCKOUT; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84873411856     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.84     Document Type: Article

References (39)

1. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP et al. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 1998; 282: 1497- 1501. (Pubitemid 28538613)
2. Shimuta K, Nakajo N, Uto K, Hayano Y, Okazaki K, Sagata N. Chk1 is activated transiently and targets Cdc25A for degradation at the Xenopus midblastula transition. EMBO J 2002; 21: 3694 - 3703. (Pubitemid 34787043)
3. Sorensen CS, Syluasen RG, Falck J, Schroeder T, Ronnstrand L, Khanna KK et al. Chk1 regulates the S phase checkpoint by coupling the physiological turnover and ionizing radiation-induced accelerated proteolysis of Cdc25A. Cancer Cell 2003; 3: 247 - 258. (Pubitemid 37443880)
4. Zhao H, Watkins JL, Piwnica-Worms H. Disruption of the checkpoint kinase 1/cell division cycle 25A pathway abrogates ionizing radiation-induced S and G2 checkpoints. Proc Natl Acad Sci USA 2002; 99: 14795 - 14800. (Pubitemid 35334563)
5. Falck J, Mailand N, Syljuasen RG, Bartek J, Lukas J. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature 2001; 410: 842 - 847. (Pubitemid 32303786)
6. Goloudina A, Yamaguchi H, Chervyakova DB, Appella E, Fornace Jr AJ, Bulavin DV. Regulation of human Cdc25A stability by serine 75 phosphorylation is not sufficient to activate a S-phase checkpoint. Cell Cycle 2003; 2: 473 - 478.
7. Hassepass I, Voit R, Hoffmann I. Phosphorylation at serine-75 is required for UVmediated degradation of human Cdc25A phosphatase at the S-phase checkpoint. J Biol Chem 2003; 278: 29824 - 29829. (Pubitemid 36962370)
8. Ma CX, Janetka JW, Piwnica-Worms H. Death by releasing the breaks: CHK1 inhibitors as cancer therapeutics. Trends Mol Med 2010; 17: 88-96.
9. Bunch RT, Eastman A. Enhancement of cisplatin-induced cytotoxicity by 7-hydroxystaurosporine (UCN-01), a new G2 checkpoint inhibitor. Clin Cancer Res 1996; 2: 791 - 797. (Pubitemid 26168931)
10. Wang O, Fan S, Eastman A, Worland PJ, Sausville EA, O'Conner PM. UCN-01: a potent abrogator of G2 checkpoint function in cancer cells with disrupted p53. J Natl Cancer Inst 1996; 88: 956 - 965. (Pubitemid 26239383)
11. Levesque AA, Eastman A. p53-based cancer therapies: is defective p53 the Achilles heel of the tumor? Carcinogenesis 2007; 28: 13-20. (Pubitemid 44942622)
12. Levesque AA, Fanous AA, Poh A, Eastman A. Defective p53 signaling in p53 wildtype tumors attenuates p21waf1 induction and cyclin B repression rendering them sensitive to Chk1 inhibitors that abrogate DNA damage-induced S and G2 arrest. Mol Cancer Ther 2008; 7: 252 - 262. (Pubitemid 351302519)
13. 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: 2955 - 2966.
14. Taylor WR, Stark GR. Regulation of the G2/M transition by p53. Oncogene 2001; 20: 1803 - 1815. (Pubitemid 32458690)
15. Abbas T, Dutta A. p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 2009; 9: 400 - 414.
16. Ferguson AT, Evron E, Umbricht CB, Pandita TK, Chan TA, Hermeking H et al. High frequency of hypermethylation at the 14-3-3 sigma locus leads to gene silencing in breast cancer. Proc Natl Acad Sci USA 2000; 97: 6049 - 6054. (Pubitemid 30367521)
17. Fracasso PM, Williams KJ, Chen RC, Picus J, Ma CX, Ellis MJ et al. A phase 1 study of UCN-01 in combination with irinotecan in patients with resistant solid tumor malignancies. Cancer Chemother Pharmacol 2011; 67: 1225 - 1237.
18. Kohn EA, Ruth ND, Brown MK, Livingstone M, Eastman A. Abrogation of the S phase DNA damage checkpoint results in S phase progression or premature mitosis depending on the concentration of 7-hydroxystaurosporine and the kinetics of Cdc25C activation. J Biol Chem 2002; 277: 26553 - 26564. (Pubitemid 34967153)
19. Sedelnikova OA, Pilch DR, Redon C, Bonner WM. Histone H2AX in DNA damage and repair. Cancer Biol Ther 2003; 2: 233 - 235.
20. Lam MH, Liu Q, Elledge SJ, Rosen JM. Chk1 is haploinsufficient for multiple functions critical to tumor suppression. Cancer Cell 2004; 6: 45-59. (Pubitemid 38903161)
21. Perez RP, Lewis LD, Beelen AP, Olszanski AJ, Johnston N, Rhodes CH et al. Modulation of cell cycle progression in human tumors: a pharmacokinetic and tumor molecular pharmacodynamic study of cisplatin plus the Chk1 inhibitor UCN-01 (NSC 638850). Clin Cancer Res 2006; 12: 7079 - 7085. (Pubitemid 44974507)
22. Xu B, Kim S-T, Kastan MB. Involvement of Brca1 in S-phase and G2-phase checkpoints after ionizing radiation. Mol Cell Biol 2001; 21: 3445 - 3450. (Pubitemid 32381780)
23. Tapia C, Kutzner H, Mentzel T, Savic S, Baumhoer D, Glatz K. Two mitosis-specific antibodies, MPM-2 and phospho-histone H3 (Ser28), allow rapid and precise determination of mitotic activity. Am J Surg Pathol 2006; 30: 83 - 89. (Pubitemid 43740213)
24. Parker LL, Piwnica-Worms H. Inactivation of the p34cdc2-cyclin B complex by the human wee1 tyrosine kinase. Science 1992; 257: 1955 - 1957.
25. Goga A, Yang D, Tward AD, Morgan DO, Bishop JM. Inhibition of CDK1 as a potential therapy for tumors over-expressing MYC. Nat Med 2007; 13: 820 - 827. (Pubitemid 47038193)
26. Cespedes MV, Espina C, Garcia-Cabezas MA, Trias M, Boluda A, Gomez del Pulgar MT et al. Orthotopic microinjection of human colon cancer cells in nude mice induces tumor foci in all clinically relevant metastatic sites. Am J Pathol 2007; 170: 1077-1085. (Pubitemid 47339374)
27. Waldman T, Kinzler KW, Vogelstein B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res 1995; 55: 5187- 5190.
28. Eastman A. Cell cycle checkpoints and their impact on anticancer therapeutic strategies. J Cell Biochem 2004; 91: 223 - 231.
29. Rodriguez R, Meuth M. Chk1 and p21 cooperate to prevent apoptosis during DNA replication fork stress. Mol Biol Cell 2006; 17: 402 - 412. (Pubitemid 43049492)
30. Luo Y, Hurwitz J, Massague J. Cell-cycle inhibition by independent CDK and PCNA binding domains in p21Cip1. Nature 1995; 375: 159 - 161.
31. Besson A, Dowdy SF, Roberts JM. CDK inhibitors: cell cycle regulators and beyond. Dev Cell 2008; 14: 159 - 169. (Pubitemid 351189186)
32. Sherr CJ, Roberts JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 1999; 13: 1501 - 1512. (Pubitemid 29297917)
33. Kohn EA, Yoo CJ, Eastman A. The protein kinase C inhibitor Go6976 is a potent inhibitor of DNA damage-induced S and G2 cell cycle checkpoints. Cancer Res 2003; 63: 31 - 35. (Pubitemid 36070415)
34. Tse AN, Rendahl KG, Sheikh T, Cheema H, Aardalen K, Embry M et al. CHIR-124, a novel potent inhibitor of Chk1, potentiates the cytotoxicity of topoisomerase I poisons in vitro and in vivo. Clin Cancer Res 2007; 13(2 Pt 1): 591 - 602. (Pubitemid 46225366)
35. Fikaris AJ, Lewis AE, Abulaiti A, Tsygankova OM, Meinkoth JL. Ras triggers ataxiatelangiectasia- mutated and Rad-3-related activation and apoptosis through sustained mitogenic signaling. J Biol Chem 2006; 281: 34759 - 34767. (Pubitemid 46043245)
36. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N et al. Oncogeneinduced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006; 444: 633 - 637. (Pubitemid 44864442)
37. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006; 444: 638 - 642. (Pubitemid 44864443)
38. Gilad O, Nabet BY, Ragland RL, Schoppy DW, Smith KD, Durham AC et al. Combining ATR suppression with oncogenic Ras synergistically increases genomic instability, causing synthetic lethality or tumorigenesis in a dosagedependent manner. Cancer Res 2010; 70: 9693 - 9702.
39. Raynaud FI, Fischer PM, Nutley BP, Goddard PM, Lane DP, Workman P. Cassette dosing pharmacokinetics of a library of 2,6,9-trisubstituted purine cyclindependent kinase 2 inhibitors prepared by parallel synthesis. Mol Cancer Ther 2004; 3: 353 - 362. (Pubitemid 39193711)