The mre11 nuclease is critical for the sensitivity of cells to chk1 inhibition

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Thompson, Ruth ^a,b   Montano, Ryan ^a,b   Eastman, Alan ^a,b  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b NORRIS COTTON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CDC25A PROTEIN; CHECKPOINT KINASE 1; CYCLIN DEPENDENT KINASE 2; DEOXYRIBONUCLEASE; MRE11 PROTEIN; MUS81 PROTEIN; NIBRIN; PROTEIN TYROSINE PHOSPHATASE; RAD50 PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; PROTEIN FUNCTION;

CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA-BINDING PROTEINS; HUMANS; OSTEOSARCOMA; PHOSPHORYLATION; PROTEIN KINASES; PYRAZOLES; PYRIMIDINES; PYRIMIDINONES; THIONES;

EID: 84866612162     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044021     Document Type: Article

References (47)

1. Gao Q, Huang X, Tang D, Cao Y, Chen G, et al. (2006) Influence of chk1 and plk1 silencing on radiation- or cisplatin-induced cytotoxicity in human malignant cells. Apoptosis 11: 1789-1800.
2. Cho S, Toouli C, Fujii G, Crain C, Parry D, (2005) Chk1 is essential for tumour viability following activation of the replication checkpoint. Cell Cycle 4: 131-139.
3. Flatten K, Dai NT, Vroman BT, Loegering D, Erlichman C, et al. (2005) The role of checkpoint kinase 1 in sensitivity to topoisomerase I poisons. J Biol Chem 280: 14349-14355.
4. Rodriguez R, Meuth M, (2006) Chk1 and p21 cooperate to prevent apoptosis during DNA replication fork stress. Molecular Biology of the Cell 17: 402-412.
5. Beck H, Nahse V, Larsen MS, Groth P, Clancy T, et al. (2010) Regulators of cyclin-dependent kinases are crucial for maintaining genome integrity in S phase. J Cell Biol 188: 629-638.
6. Scorah J, McGowan CH, (2009) Claspin and Chk1 regulate replication fork stability by different mechanisms. Cell Cycle 8: 1036-1043.
7. Syljuasen RG, Sorensen CS, Hansen LT, Fugger K, Lundin C, et al. (2005) Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol Cell Biol 25: 3553-3562.
8. Maya-Mendoza A, Petermann E, Gillespie DA, Caldecott KW, Jackson DA, (2007) Chk1 regulates the density of active replication origins during the vertebrate S phase. EMBO J 26: 2719-2731.
9. Petermann E, Maya-Mendoza A, Zachos G, Gillespie DA, Jackson DA, et al. (2006) Chk1 requirement for high global rates of replication fork progression during normal vertebrate S phase. Mol Cell Biol 26: 3319-3326.
10. Petermann E, Woodcock M, Helleday T, (2010) Chk1 promotes replication fork progression by controlling replication initiation. Proc Natl Acad Sci U S A 107: 16090-16095.
11. Forment JV, Blasius M, Guerini I, Jackson SP, (2011) Structure-specific DNA endonuclease mus81/eme1 generates DNA damage caused by chk1 inactivation. PLoS One 6: e23517.
12. Uziel T, Lerenthal Y, Moyal L, Andegeko Y, Mittelman L, et al. (2003) Requirement of the MRN complex for ATM activation by DNA damage. EMBO J 22: 5612-5621.
13. Adams KE, Medhurst AL, Dart DA, Lakin ND, (2006) Recruitment of ATR to sites of ionising radiation-induced DNA damage requires ATM and components of the MRN protein complex. Oncogene 25: 3894-3904.
14. Bunch RT, Eastman A, (1996) Enhancement of cisplatin-induced cytotoxicity by 7-hydroxystaurosporine (UCN-01), a new G2-checkpoint inhibitor. Clin Cancer Res 2: 791-797.
15. Montano R, Chung I, Garner KM, Parry D, Eastman A, (2012) Preclinical development of the novel Chk1 inhibitor SCH900776 in combination with DNA-damaging agents and antimetabolites. Mol Cancer Ther 11: 427-438.
16. Leung-Pineda V, Ryan CE, Piwnica-Worms H, (2006) Phosphorylation of Chk1 by ATR is antagonized by a Chk1-regulated protein phosphatase 2A circuit. Mol Cell Biol 26: 7529-7538.
17. Sorensen CS, Hansen LT, Dziegielewski J, Syljuasen RG, Lundin C, et al. (2005) The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat Cell Biol 7: 195-201.
18. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, et al. (2006) ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 8: 37-45.
19. Lee JH, Paull TT, (2005) ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308: 551-554.
20. Williams RS, Moncalian G, Williams JS, Yamada Y, Limbo O, et al. (2008) Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell 135: 97-109.
21. Dupre A, Boyer-Chatenet L, Sattler RM, Modi AP, Lee JH, et al. (2008) A forward chemical genetic screen reveals an inhibitor of the Mre11-Rad50-Nbs1 complex. Nat Chem Biol 4: 119-125.
22. Stewart GS, Maser RS, Stankovic T, Bressan DA, Kaplan MI, et al. (1999) The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 99: 577-587.
23. Delia D, Piane M, Buscemi G, Savio C, Palmeri S, et al. (2004) MRE11 mutations and impaired ATM-dependent responses in an Italian family with ataxia-telangiectasia-like disorder. Hum Mol Genet 13: 2155-2163.
24. Stiff T, Reis C, Alderton GK, Woodbine L, O'Driscoll M, et al. (2005) Nbs1 is required for ATR-dependent phosphorylation events. EMBO J 24: 199-208.
25. Zheng L, Kanagaraj R, Mihaljevic B, Schwendener S, Sartori AA, et al. (2009) MRE11 complex links RECQ5 helicase to sites of DNA damage. Nucleic Acids Res 37: 2645-2657.
26. Gagou ME, Zuazua-Villar P, Meuth M, (2010) Enhanced H2AX phosphorylation, DNA replication fork arrest, and cell death in the absence of Chk1. Mol Biol Cell 21: 739-752.
27. Limbo O, Chahwan C, Yamada Y, de Bruin RA, Wittenberg C, et al. (2007) Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol Cell 28: 134-146.
28. Taylor ER, McGowan CH, (2008) Cleavage mechanism of human Mus81-Eme1 acting on Holliday-junction structures. Proc Natl Acad Sci U S A 105: 3757-3762.
29. Ciccia A, Constantinou A, West SC, (2003) Identification and characterization of the human mus81-eme1 endonuclease. J Biol Chem 278: 25172-25178.
30. Xiao Z, Chen Z, Gunasekera AH, Sowin TJ, Rosenberg SH, et al. (2003) Chk1 mediates S and G2 arrests through Cdc25A degradation in response to DNA-damaging agents. J Biol Chem 278: 21767-21773.
31. Zhao H, Watkins JL, Piwnica-Worms H, (2002) Disruption of the checkpoint kinase 1/cell division cycle 25A pathway abrogates ionizing radiation-induced S and G2 checkpoints. Proc Natl Acad Sci U S A 99: 14795-14800.
32. Sorensen CS, Syljuasen RG, Falck J, Schroeder T, Ronnstrand L, et al. (2003) Chk1 regulates the S phase checkpoint by coupling the physiological turnover and ionizing radiation-induced accelerated proteolysis of Cdc25A. Cancer Cell 3: 247-258.
33. Mailand N, Falck J, Lukas C, Syljuasen RG, Welcker M, et al. (2000) Rapid destruction of human Cdc25A in response to DNA damage. Science 288: 1425-1429.
34. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, et al. (2007) Human CtIP promotes DNA end resection. Nature 450: 509-514.
35. Huertas P, Jackson SP, (2009) Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J Biol Chem 284: 9558-9565.
36. Peterson SE, Li Y, Chait BT, Gottesman ME, Baer R, et al. (2011) Cdk1 uncouples CtIP-dependent resection and Rad51 filament formation during M-phase double-strand break repair. J Cell Biol 194: 705-720.
37. Buis J, Stoneham T, Spehalski E, Ferguson DO, (2012) Mre11 regulates CtIP-dependent double-strand DNA break repair by interaction with CDK2. Nat Struct Mol Biol 19: 246-252.
38. Chen X, Niu H, Chung WH, Zhu Z, Papusha A, et al. (2011) Cell cycle regulation of DNA double-strand break end resection by Cdk1-dependent Dna2 phosphorylation. Nat Struct Mol Biol 18: 1015-1019.
39. Cuadrado M, Martinez-Pastor B, Murga M, Toledo LI, Gutierrez-Martinez P, et al. (2006) ATM regulates ATR chromatin loading in response to DNA double-strand breaks. J Exp Med 203: 297-303.
40. Paull TT, Gellert M, (1999) Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev 13: 1276-1288.
41. Schlacher K, Christ N, Siaud N, Egashira A, Wu H, et al. (2011) Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 145: 529-542.
42. Bahassi EM, Ovesen JL, Riesenberg AL, Bernstein WZ, Hasty PE, et al. (2008) The checkpoint kinases Chk1 and Chk2 regulate the functional associations between hBRCA2 and Rad51 in response to DNA damage. Oncogene 27: 3977-3985.
43. Sorensen CS, Syljuasen RG (2011) Safeguarding genome integrity: the checkpoint kinases ATR, CHK1 and WEE1 restrain CDK activity during normal DNA replication. Nucleic Acids Res.
44. Garner KM, Eastman A, (2011) Variations in Mre11/Rad50/Nbs1 status and DNA damage-induced S-phase arrest in the cell lines of the NCI60 panel. BMC Cancer 11 206: 201-213.
45. Guzi TJ, Paruch K, Dwyer MP, Labroli M, Shanahan F, et al. (2011) Targeting the replication checkpoint using SCH 900776, a potent and functionally selective CHK1 inhibitor identified via high content screening. Mol Cancer Ther 10: 591-602.
46. Garner KM, Pletnev AA, Eastman A, (2009) Corrected structure of mirin, a small-molecule inhibitor of the Mre11-Rad50-Nbs1 complex. Nat Chem Biol 5: 129-130.
47. Rao J, Otto WR, (1992) Fluorimetric DNA assay for cell growth estimation. Anal Biochem 207: 186-192.