Cisplatin-induced DNA damage activates replication checkpoint signaling components that differentially affect tumor cell survival

Molecular Pharmacology

Volumn 76, Issue 1, 2009, Pages 208-214

  Wagner, Jill M ^a   Karnitz, Larry M ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE; ATR PROTEIN; BRCA1 PROTEIN; BRCA2 PROTEIN; CARBOPLATIN; CHECKPOINT KINASE 1; CISPLATIN; FANCONI ANEMIA GROUP D2 PROTEIN; GEMCITABINE; OXALIPLATIN; PROTEIN RAD9; RAD18 PROTEIN; RAD51 PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL CYCLE ARREST; CELL CYCLE S PHASE; CELL SURVIVAL; CHEMOSENSITIZATION; CONTROLLED STUDY; DNA DAMAGE; EMBRYO; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR RESISTANCE;

ANTINEOPLASTIC AGENTS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL SURVIVAL; CISPLATIN; DNA DAMAGE; DNA REPAIR; HUMANS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; S PHASE;

EID: 67649842315     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.109.055178     Document Type: Article

References (40)

1. Ashwell S and Zabludoff S (2008) DNA damage detection and repair pathways- recent advances with inhibitors of checkpoint kinases in cancer therapy. Clin Cancer Res 14:4032-4037.
2. Bartz SR, Zhang Z, Burchard J, Imakura M, Martin M, Palmieri A, Needham R, Guo J, Gordon M, Chung N, et al. (2006) Small interfering RNA screens reveal enhanced cisplatin cytotoxicity in tumor cells having both BRCA network and TP53 disruptions. Mol Cell Biol 26:9377-9386. (Pubitemid 44904431)
3. Blasina A, Hallin J, Chen E, Arango ME, Kraynov E, Register J, Grant S, Ninkovic S, Chen P, Nichols T, et al. (2008) Breaching the DNA damage checkpoint via PF-00477736, a novel small-molecule inhibitor of checkpoint kinase 1. Mol Cancer Ther 7:2394-2404.
4. Burrows AE and Elledge SJ (2008) How ATR turns on: TopBP1 goes on ATRIP with ATR. Genes Dev 22:1416-1421. (Pubitemid 351793075)
5. Casper AM, Nghiem P, Arlt MF, and Glover TW (2002) ATR regulates fragile site stability. Cell 111:779-789. (Pubitemid 36106400)
6. Cho SH, Toouli CD, Fujii GH, Crain C, and Parry D (2005) Chk1 is essential for tumor cell viability following activation of the replication checkpoint. Cell Cycle 4:131-139. (Pubitemid 41038942)
7. Cimprich KA and Cortez D (2008) ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 9:616-627. (Pubitemid 352032926)
8. Donaldson KL, Goolsby GL, and Wahl AF (1994) Cytotoxicity of the anticancer agents cisplatin and Taxol during cell proliferation and the cell cycle. Int J Cancer 57:847-855. (Pubitemid 24216822)
9. Dronkert ML and Kanaar R (2001) Repair of DNA interstrand cross-links. Mutat Res 486:217-247.
10. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, and Tuschl T (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498. (Pubitemid 32494397)
11. Enders GH (2008) Expanded roles for Chk1 in genome maintenance. J Biol Chem 283:17749-17752.
12. Foulkes WD (2006) BRCA1 and BRCA2: chemosensitivity, treatment outcomes and prognosis. Fam Cancer 5:135-142. (Pubitemid 43824469)
13. Ganzinelli M, Carrassa L, Crippa F, Tavecchio M, Broggini M, and Damia G (2008) Checkpoint kinase 1 down-regulation by an inducible small interfering RNA expression system sensitized in vivo tumors to treatment with 5-fluorouracil. Clin Cancer Res 14:5131-5141.
14. Gao Q, Huang X, Tang D, Cao Y, Chen G, Lu Y, Zhuang L, Wang S, Xu G, Zhou J, et al. (2006) Influence of chk1 and plk1 silencing on radiation- or cisplatin-induced cytotoxicity in human malignant cells. Apoptosis 11:1789-1800. (Pubitemid 44371052)
15. García MJ and Benítez J (2008) The Fanconi anaemia/BRCA pathway and cancer susceptibility. Searching for new therapeutic targets. Clin Transl Oncol 10:78-84.
16. Gossage L and Madhusudan S (2007) Current status of excision repair cross complementing- group 1 (ERCC1) in cancer. Cancer Treat Rev 33:565-577. (Pubitemid 47355341)
17. Gudmundsdottir K and Ashworth A (2006) The roles of BRCA1 and BRCA2 and associated proteins in the maintenance of genomic stability. Oncogene 25:5864-5874. (Pubitemid 44453442)
18. Hopkins KM, Auerbach W, Wang XY, Hande MP, Hang H, Wolgemuth DJ, Joyner AL, and Lieberman HB (2004) Deletion of mouse rad9 causes abnormal cellular responses to DNA damage, genomic instability, and embryonic lethality. Mol Cell Biol 24:7235-7248. (Pubitemid 39014449)
19. Huang M, Miao ZH, Zhu H, Cai YJ, Lu W, and Ding J (2008) Chk1 and Chk2 are differentially involved in homologous recombination repair and cell cycle arrest in response to DNA double-strand breaks induced by camptothecins. Mol Cancer Ther 7:1440-1449.
20. Karnitz LM, Flatten KS, Wagner JM, Loegering D, Hackbarth JS, Arlander SJ, Vroman BT, Thomas MB, Baek YU, Hopkins KM, et al. (2005) Gemcitabineinduced activation of checkpoint signaling pathways that affect tumor cell survival. Mol Pharmacol 68:1636-1644. (Pubitemid 41654347)
21. Kelland L (2007) The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer 7:573-584.
22. Lehmann AR (2006) Translesion synthesis in mammalian cells. Exp Cell Res 312: 2673-2676.
23. Lio YC, Schild D, Brenneman MA, Redpath JL, and Chen DJ (2004) Human Rad51C deficiency destabilizes XRCC3, impairs recombination, and radiosensitizes S/G2- phase cells. J Biol Chem 279:42313-42320. (Pubitemid 39313680)
24. 2/M DNA damage checkpoint. Genes Dev 14:1448-1459.
25. Lyakhovich A and Surralles J (2006) Disruption of the Fanconi anemia/BRCA pathway in sporadic cancer. Cancer Lett 232:99-106. (Pubitemid 43053937)
26. Matthews DJ, Yakes FM, Chen J, Tadano M, Bornheim L, Clary DO, Tai A, Wagner JM, Miller N, Kim YD, et al. (2007) Pharmacological abrogation of S-phase checkpoint enhances the anti-tumor activity of gemcitabine in vivo. Cell Cycle 6:104-110. (Pubitemid 46173886)
27. Miyagawa K (2008) Clinical relevance of the homologous recombination machinery in cancer therapy. Cancer Sci 99:187-194. (Pubitemid 351228469)
28. Morgan MA, Parsels LA, Parsels JD, Lawrence TS, and Maybaum J (2006) The relationship of premature mitosis to cytotoxicity in response to checkpoint abrogation and antimetabolite treatment. Cell Cycle 5:1983-1988. (Pubitemid 44435305)
29. Powell SN and Kachnic LA (2008) Therapeutic exploitation of tumor cell defects in homologous recombination. Anticancer Agents Med Chem 8:448-460. (Pubitemid 351761429)
30. Räschle M, Knipsheer P, Enoiu M, Angelov T, Sun J, Griffith JD, Ellenberger TE, Schärer OD, and Walter JC (2008) Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134:969-980.
31. Robinson HM, Jones R, Walker M, Zachos G, Brown R, Cassidy J, and Gillespie DA (2006) Chk1-dependent slowing of S-phase progression protects DT40 Blymphoma cells against killing by the nucleoside analogue 5-fluorouracil. Oncogene 25:5359-5369. (Pubitemid 44330279)
32. Roos-Mattjus P, Hopkins KM, Oestreich AJ, Vroman BT, Johnson KL, Naylor S, Lieberman HB, and Karnitz LM (2003) Phosphorylation of human Rad9 is required for genotoxin-activated checkpoint signaling. J Biol Chem 278:24428-24437. (Pubitemid 37548594)
33. Sakai W, Swisher EM, Karlan BY, Agarwal MK, Higgins J, Friedman C, Villegas E, Jacquemont C, Farrugia DJ, Couch FJ, et al. (2008) Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature 451:1116-1120. (Pubitemid 351317449)
34. Soørensen CS, Hansen LT, Dziegielewski J, Syljuåsen RG, Lundin C, Bartek J, and Helleday T (2005) The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat Cell Biol 7:195-201. (Pubitemid 40268135)
35. Volkmer E and Karnitz LM (1999) Human homologs of Schizosaccharomyces pombe Rad1, Hus1, and Rad9 form a DNA damage-responsive protein complex. J Biol Chem 274:567-570. (Pubitemid 129535209)
36. Wang W (2007) Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat Rev Genet 8:735-748. (Pubitemid 47429206)
37. Wang X, Kennedy RD, Ray K, Stuckert P, Ellenberger T, and D'Andrea AD (2007) Chk1-mediated phosphorylation of FANCE is required for the Fanconi anemia/ BRCA pathway. Mol Cell Biol 27:3098-3108. (Pubitemid 46581321)
38. Wang Y and Qin J (2003) MSH2 and ATR form a signaling module and regulate two branches of the damage response to DNA methylation. Proc Natl Acad Sci U S A 100:15387-15392. (Pubitemid 38020999)
39. Zabludoff SD, Deng C, Grondine MR, Sheehy AM, Ashwell S, Caleb BL, Green S, Haye HR, Horn CL, Janetka JW, et al. (2008) AZD7762, a novel checkpoint kinase inhibitor, drives checkpoint abrogation and potentiates DNA-targeted therapies. Mol Cancer Ther 7:2955-2966.
40. 2 checkpoints. Proc Natl Acad Sci U S A 99:14795-14800.