Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage

Molecular and Cellular Biology

Volumn 25, Issue 9, 2005, Pages 3553-3562

  Syljuåsen, Randi G ^a   Sørensen, Claus Storgaard ^a,f   Hansen, Lasse Tengbjerg ^b   Fugger, Kasper ^a   Lundin, Cecilia ^d   Johansson, Fredrik ^d   Helleday, Thomas ^d,e   Sehested, Maxwell ^c   Lukas, Jiri ^a   Bartek, Jiri ^a  

^a DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c Rigshospitalet   (Denmark)

^d STOCKHOLM UNIVERSITY   (Sweden)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

7 HYDROXYSTAUROSPORINE; ATR PROTEIN; CAFFEINE; CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 45; CEP 3891; CHECKPOINT KINASE 1; HISTONE H2A; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN; PROTEIN P53; REPLICATION PROTEIN A; ROSCOVITINE; SINGLE STRANDED DNA; SMALL INTERFERING RNA; SMC1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA REPLICATION; DNA STRAND BREAKAGE; DOWN REGULATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING;

CAFFEINE; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA DAMAGE; DNA REPLICATION; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; HISTONES; HUMANS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PURINES; REPLICATION PROTEIN A; RNA, SMALL INTERFERING; STAUROSPORINE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 20244388673     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.9.3553-3562.2005     Document Type: Article

References (46)

1. Abraham, R. T. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2177-2196.
2. Brown, E. J., and D. Baltimore. 2000. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14:397-402.
3. Brown, E. J., and D. Baltimore. 2003. Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev. 17:615-628.
4. de Klein, A., M. Muijtjens, R. van Os, Y. Verhoeven, B. Smit, A. M. Carr, A. R. Lehmann, and J. H. Hoeijmakers. 2000. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10:479-482.
5. Dixon, H., and C. J. Norbury. 2002. Therapeutic exploitation of checkpoint defects in cancer cells lacking p53 function. Cell Cycle 1:362-368.
6. Ekholm-Reed, S., J. Mendez, D. Tedesco, A. Zetterberg, B. Stillman, and S. I. Reed. 2004. Deregulation of cyclin E in human cells interferes with prereplication complex assembly. J. Cell Biol. 165:789-800.
7. Erixon, K., and G. Ahnstrom. 1979. Single-strand breaks in DNA during repair of UV-induced damage in normal human and xeroderma pigmentosum cells as determined by alkaline DNA unwinding and hydroxylapatite chromatography: effects of hydroxyurea, 5-fluorodeoxyuridine, and 1-β-D-arabinofuranosylcytosine on the kinetics of repair. Mutat. Res. 59:257-271.
8. Feijoo, C., C. Hall-Jackson, R. Wu, D. Jenkins, J. Leitch, D. M. Gilbert, and C. Smythe. 2001. 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. 154:913-923.
9. Furnari, B., N. Rhind, and P. Russell. 1997. Cdc25 mitotic inducer targeted by chk1 DNA damage checkpoint kinase. Science 277:1495-1497.
10. Guo, Z., A. Kumagai, S. X. Wang, and W. G. Dunphy. 2000. Requirement for Atr in phosphorylation of Chk1 and cell cycle regulation in response to DNA replication blocks and UV-damaged DNA in Xenopus egg extracts. Genes Dev. 14:2745-2756.
11. Hartwell, L. H., and T. A. Weinert. 1989. Checkpoints: controls that ensure the order of cell cycle events. Science 246:629-634.
12. Ishimi, Y., Y. Komamura-Kohno, H. J. Kwon, K. Yamada, and M. Nakanishi. 2003. Identification of MCM4 as a target of the DNA replication block checkpoint system. J. Biol. Chem. 278:24644-24650.
13. Kumagai, A., and W. G. Dunphy. 2000. Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol. Cell 6:839-849.
14. Lam, M. H., Q. Liu, S. J. Elledge, and J. M. Rosen. 2004. Chk1 is haploinsufficient for multiple functions critical to tumor suppression. Cancer Cell 6:45-59.
15. 2/M DNA damage checkpoint. Genes Dev. 14:1448-1459.
16. Lundin, C., K. Erixon, C. Arnaudeau, N. Schultz, D. Jenssen, M. Meuth, and T. Helleday. 2002. Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol. Cell. Biol. 22:5869-5878.
17. Mailand, N., J. Falck, C. Lukas, R. G. Syljuasen, M. Welcker, J. Bartek, and J. Lukas. 2000. Rapid destruction of human Cdc25A in response to DNA damage. Science 288:1425-1429.
18. 2/M events by Cdc25A through phosphorylation-dependent modulation of its stability. EMBO J. 21:5911-5920.
19. Marheineke, K., and O. Hyrien. 2004. Control of replication origin density and firing time in Xenopus egg extracts: role of a caffeine-sensitive, ATR-dependent checkpoint. J. Biol. Chem. 279:28071-28081.
20. Masuda, T., S. Mimura, and H. Takisawa. 2003. CDK- and Cdc45-dependent priming of the MCM complex on chromatin during S-phase in Xenopus egg extracts: possible activation of MCM helicase by association with Cdc45. Genes Cells 8:145-161.
21. Mendez, J., and B. Stillman. 2003. Perpetuating the double helix: molecular machines at eukaryotic DNA replication origins. Bioessays 25:1158-1167.
22. Ortega, S., I. Prieto, J. Odajima, A. Martin, P. Dubus, R. Sotillo, J. L. Barbero, M. Malumbres, and M. Barbacid. 2003. Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat. Genet. 35:25-31.
23. Rajagopalan, H., P. V. Jallepalli, C. Rago, V. E. Velculescu, K. W. Kinzler, B. Vogelstein, and C. Lengauer. 2004. Inactivation of hCDC4 can cause chromosomal instability. Nature 428:77-81.
24. Sanchez, Y., C. Wong, R. S. Thoma, R. Richman, Z. Wu, H. Piwnica-Worms, and S. J. Elledge. 1997. Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 277:1497-1501.
25. Sarkaria, J. N., E. C. Busby, R. S. Tibbetts, P. Roos, Y. Taya, L. M. Karnitz, and R. T. Abraham. 1999. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 59:4375-4382.
26. Sehested, M., I. Wessel, L. H. Jensen, B. Holm, R. S. Oliveri, S. Kenwrick, A. M. Creighton, J. L. Nitiss, and P. B. Jensen. 1998. Chinese hamster ovary cells resistant to the topoisomerase II catalytic inhibitor ICRF-159: a Tyr49Phe mutation confers high-level resistance to bisdioxopiperazines. Cancer Res. 58:1460-1468.
27. Shechter, D., V. Costanzo, and J. Gautier. 2004. ATR and ATM regulate the timing of DNA replication origin firing. Nat. Cell Biol. 6:648-655.
28. Sogo, J. M., M. Lopes, and M. Foiani. 2002. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297:599-602.
29. Sorensen, C. S., R. G. Syljuasen, J. Falck, T. Schroeder, L. Ronnstrand, K. K. Khanna, B. B. Zhou, J. Bartek, and J. Lukas. 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.
30. Sorensen, C. S., R. G. Syljuasen, J. Lukas, and J. Bartek. 2004. ATR, Claspin and the Rad9-Rad1-Hus1 complex regulate Chk1 and Cdc25A in the absence of DNA damage. Cell Cycle 3:941-945.
31. Spruck, C. H., K. A. Won, and S. I. Reed. 1999. Deregulated cyclin E induces chromosome instability. Nature 401:297-300.
32. Syljuasen, R. G., C. S. Sorensen, J. Nylandsted, C. Lukas, J. Lukas, and J. Bartek. 2004. Chk1 inhibition by CEP-3891 accelerates mitotic nuclear fragmentation in response to ionizing radiation (IR). Cancer Res. 64:9035-9040.
33. -/- mice. Genes Dev. 14:1439-1447.
34. Tercero, J. A., K. Labib, and J. F. Diffley. 2000. DNA synthesis at individual replication forks requires the essential initiation factor Cdc45p. EMBO J. 19:2082-2093.
35. Tetsu, O., and F. McCormick. 2003. Proliferation of cancer cells despite CDK2 inhibition. Cancer Cell 3:233-245.
36. Tibbetts, R. S., K. M. Brumbaugh, J. M. Williams, J. N. Sarkaria, W. A. Cliby, S. Y. Shieh, Y. Taya, C. Prives, and R. T. Abraham. 1999. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev. 13:152-157.
37. Walter, J., and J. Newport. 2000. Initiation of eukaryotic DNA replication: origin unwinding and sequential chromatin association of Cdc45, RPA, and DNA polymerase alpha. Mol. Cell 5:617-627.
38. Ward, I. M., and J. Chen. 2001. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276:47759-47762.
39. Zachos, G., M. D. Rainey, and D. A. Gillespie. 2003. Chk1-deficient tumour cells are viable but exhibit multiple checkpoint and survival defects. EMBO J. 22:713-723.
40. Zhao, H., and H. Piwnica-Wonns. 2001. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol. Cell. Biol. 21:4129-4139.
41. 2 checkpoints. Proc. Natl. Acad. Sci. USA 99:14795-14800.
42. Zhou, B. B., and J. Bartek. 2004. Targeting the checkpoint kinases: chemosensitization versus chemoprotection. Nat. Rev. Cancer 4:216-225.
43. Zhou, B. B., and S. J. Elledge. 2000. The DNA damage response: putting checkpoints in perspective. Nature 408:433-439.
44. Ziv, Y., A. Bar-Shira, I. Pecker, P. Russell, T. J. Jorgensen, I. Tsarfati, and Y. Shiloh. 1997. Recombinant ATM protein complements the cellular A-T phenotype. Oncogene 15:159-167.
45. Zou, L., and S. J. Elledge. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-1548.
46. Zon, L., and B. Stillman. 1998. Formation of a preinitiation complex by S-phase cyclin CDK-dependent loading of Cdc45p onto chromatin. Science 280:593-596.