Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint

Genes and Development

Volumn 19, Issue 9, 2005, Pages 1040-1052

  Byun, Tony S ^a   Pacek, Marcin ^b   Yee, Muh Ching ^a   Walter, Johannes C ^b   Cimprich, Karlene A ^a  

^a STANFORD UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

ATR; Checkpoint; DNA damage; Xenopus

Indexed keywords

APHIDICOLIN; ATR PROTEIN; CELL CYCLE PROTEIN; CHECKPOINT KINASE 1; CISPLATIN; DNA DIRECTED DNA POLYMERASE ALPHA; DNA POLYMERASE; HELICASE; PROTEIN CDC45; PROTEIN MCM HELICASE; PROTEIN MCM7; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA SYNTHESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ULTRAVIOLET IRRADIATION; XENOPUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APHIDICOLIN; CELL CYCLE PROTEINS; CELL-FREE SYSTEM; CHROMATIN; DNA DAMAGE; DNA HELICASES; DNA PRIMERS; DNA REPLICATION; DNA, SINGLE-STRANDED; DNA-DIRECTED DNA POLYMERASE; PHOSPHORYLATION; PLASMIDS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; XENOPUS; XENOPUS PROTEINS;

EID: 18244371925     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1301205     Document Type: Article

References (59)

1. Arias, E.E. and Walter, J.C. 2005. Replication-dependent destruction of Cdt1 limits DNA replication to a single round per cell cycle in Xenopus egg extracts. Genes & Dev. 19: 114-126.
2. Bhaumik, D. and Wang, T.S. 1998. Mutational effect of fission yeast pol α on cell cycle events. Mol. Biol. Cell 9: 2107-2123.
3. Cimprich, K.A. 2003. Fragile sites: Breaking up over a slow-down. Curr. Biol. 18: R231-R233.
4. Cliby, W.A., Roberts, C.J., Cimprich, K.A., Stringer, C.M., Lamb, J.R., Schreiber, S.L., and Friend, S.H. 1998. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 17: 159-169.
5. Cortez, D., Guntuku, S., Qin, J., and Elledge, S.J. 2001. ATR and ATRIP: Partners in checkpoint signaling. Science 294: 1713-1716.
6. Cortez, D., Glick, G., and Elledge, S.J. 2004. Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc. Natl. Acad. Sci. 101: 10078-10083.
7. Costanzo, V., Shechter, D., Lupardus, P.J., Cimprich, K.A., Gottesman, M., and Gautier, J. 2003. An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol. Cell 11: 203-213.
8. Edwards, M.C., Tutter, A.V., Cvetic, C., Gilbert, C.H., Prokhorova, T.A., and Walter, J.C. 2002. MCM2-7 complexes bind chroma tin in a distributed pattern surrounding the origin recognition complex in Xenopus egg extracts. J. Biol. Chem. 277: 33049-33057.
9. Ellison, V. and Stillman, B. 2003. Biochemical characterization of DNA damage checkpoint complexes: Clamp loader and clamp complexes with specificity for 5′ recessed DNA. PLoS Biol. 1: 231-243.
10. Guo, Z., Kumagai, A., Wang, S.X., and Dunphy, W.G. 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. Hekmat-Nejad, M., You, Z., Yee, M.-C., Newport, J., and Cimprich, K.A. 2000. Xenopus ATR is a replication-dependent chromatin binding protein required for the DNA replication checkpoint. Curr. Biol. 10: 1565-1573.
12. Kartalou, M. and Essigmann, J.M. 2001. Recognition of cisplatin adducts by cellular proteins. Mutat. Res. 478: 1-21.
13. Katou, Y., Kanoh, Y., Bando, M., Noguchi, H., Tanaka, H., Ashikari, T., Sugimoto, K., and Shirahige, K. 2003. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424: 1078-1083.
14. Kondo, T., Wakayama, T., Naiki, T., Matsumoto, K., and Sugimoto, K. 2001. Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science 294: 867-870.
15. Kumagai, A. and Dunphy, W.G. 2000. Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol. Cell 6: 836-849.
16. Labib, K. and Diffley, J.F. 2001. Is the MCM2-7 complex the eukaryotic DNA replication fork helicase? Curr. Opin. Genet. Dev. 11: 64-70.
17. Lee, T., Kumagai, A., and Dunphy, W.G. 2003. Claspin, a Chk1-regulatory protein, monitors DNA replication on chromatin independently of RPA, ATR, and Rad17. Mol. Cell 11: 329-340.
18. Liu, Q., Guntuku, S., Cui, X.S., Matsuoka, S., Cortez, D., Tamai, K., Luo, G., Carattini-Rivera, S., DeMayo, F., Bradley, A., et al. 2000. Chk1 is an essential kinase that is regulated by ATR and required for the G(2)/M DNA damage checkpoint. Genes & Dev. 14: 1448-1459.
19. Longhese, M.P., Neecke, H., Paciotti, V., Lucchini, G., and Plevani, P. 1996. The 70 kDa subunit of replication protein A is required for the G1/S and intra-S DNA damage checkpoints in budding yeast. Nucleic Acids Res. 24: 3533-3537.
20. Lonn, U. and Lonn, S. 1988. Extensive regions of single-stranded DNA in aphidicolin-treated melanoma cells. Biochemistry 27: 566-570.
21. Lucas, I., Chevrier-Miller, M., Sogo, J.M., and Hyrien, O. 2000. Mechanisms ensuring rapid and complete DNA replication despite random initiation in Xenopus early embryos. J. Mol. Biol. 296: 769-786.
22. Lupardus, P.J., Byun, T., Yee, M.C., Hekmat-Nejad, M., and Cimprich, K.A. 2002. A requirement for replication in activation of the ATR-dependent DNA damage checkpoint. Genes & Dev. 16: 2327-2332.
23. Marheineke, K. and Hyrien, O. 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.
24. Masuda, T., Mimura, S., and Takisawa, H. 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.
25. McGarry, T.J. and Kirschner, M.W. 1998. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93: 1043-1053.
26. Melo, J. and Toczyski, D. 2002. A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14: 237-245.
27. Melo, J.A., Cohen, J., and Toczyski, D.P. 2001. Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes & Dev. 15: 2809-2821.
28. Michael, W.M., Ott, R., Fanning, E., and Newport, J. 2000. Activation of the DNA replication checkpoint through RNA synthesis by primase. Science 289: 2133-2137.
29. Mimura, S., Masuda, T., Matsui, T., and Takisawa, H. 2000. Central role for cdc45 in establishing an initiation complex of DNA replication in Xenopus egg extracts. Genes Cells 5: 439-452.
30. Moore, P.D., Bose, K.K., Rabkin, S.D., and Strauss, B.S. 1981. Sites of termination of in vitro DNA synthesis on ultraviolet- and N-acetylaminofluorene- treated φ X174 templates by prokaryotic and eukaryotic DNA polymerases. Proc. Natl. Acad. Sci. 78: 110-114.
31. Pacek, M. and Walter, J.C. 2004. A requirement for MCM7 and Cdc45 in chromosome unwinding during eukaryotic DNA replication. EMBO J. 23: 3667-3676.
32. Pape, T., Meka, H., Chen, S., Vicentini, G., van Heel, M., and Onesti, S. 2003. Hexameric ring structure of the full-length archaeal MCM protein complex. EMBO Rep. 4: 1079-1083.
33. Pellicioli, A., Lucca, C., Liberi, G., Marini, F., Lopes, M., Plevani, P., Romano, A., DiFiore, P.P., and Foiani, M. 1999. Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J. 18: 6561-6572.
34. Prokhorova, T.A., Mowrer, K., Gilbert, C.H., and Walter, J.C. 2003. DNA replication of mitotic chromatin in Xenopus egg extracts. Proc. Natl. Acad. Sci. 100: 13241-13246.
35. Scudiero, D. and Strauss, B. 1974. Accumulation of single-stranded regions in DNA and the block to replication in a human cell line alkylated with methyl methane sulfonate. J. Mol. Biol. 83: 17-34.
36. Sheaff, R., Ilsley, D., and Kuchta, R. 1991. Mechanism of DNA polymerase α inhibition by aphidicolin. Biochemistry 30: 8590-8597.
37. Shechter, D., Costanzo, V., and Gautier, J. 2004a. ATR and ATM regulate the timing of DNA replication origin firing. Nat. Cell Biol. 6: 648-655.
38. Shechter, D., Ying, C.Y., and Gautier, J. 2004b. DNA unwinding is an MCM complex-dependent and ATP hydrolysis-dependent process. J. Biol. Chem. 279: 45586-45593.
39. Sherr, C.J. 2004. Principles of tumor suppression. Cell 116: 235-246.
40. Shimada, K., Pasero, P., and Gasser, S.M. 2002. ORC and the intra-S-phase checkpoint: A threshold regulates Rad53p activation in S phase. Genes & Dev. 16: 3236-3252.
41. Sogo, J.M., Lopes, M., and Foiani, M. 2002. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602.
42. Sterner, J.M., Dew-Knight, S., Musahl, C., Kornbluth, S., and Horowitz, J.M. 1998. Negative regulation of DNA replication by the retinoblastoma protein is mediated by its association with MCM7. Mol. Cell. Biol. 18: 2748-2757.
43. Stewart, B.W. and Hristoforidis, C. 1987. Persistent structural change in replicating hepatic DNA isolated from diethylnitrosamine-treated rats. Cancer Lett. 35: 263-269.
44. Stokes, M.P., Van Hatten, R., Lindsay, H.D., and Michael, W.M. 2002. DNA replication is required for the checkpoint response to damaged DNA in Xenopus egg extracts. J. Cell Biol. 158: 863-872.
45. Tanaka, S., Hu, S.Z., Wang, T.S., and Korn, D. 1982. Preparation and preliminary characterization of monoclonal antibodies against human DNA polymerase α. J. Biol. Chem. 257: 8386-8390.
46. Tercero, J.A., Longhese, M.P., and Diffley, J.F. 2003. A central role for DNA replication forks in checkpoint activation and response. Mol. Cell 11: 1323-1336.
47. Tsao, C.C., Geisen, C., and Abraham, R.T. 2004. Interaction between human MCM7 and Rad17 proteins is required for replication checkpoint signaling. EMBO J. 23: 4660-4669.
48. Veaute, X., Mari-Giglia, G., Lawrence, C.W., and Sarasin, A. 2000. UV lesions located on the leading strand inhibit DNA replication but do not inhibit SV40 T-antigen helicase activity. Mutat. Res. 459: 19-28.
49. Walter, J.C. 2000. Evidence for sequential action of cdc7 and cdk2 protein kinases during initiation of DNA replication in Xenopus egg extracts. J. Biol. Chem. 275: 39773-39778.
50. Walter, J. and Newport, J. 2000. Initiation of eukaryotic DNA replication: Origin unwinding and sequential chromatin association of Cdc45, RPA, and DNA polymerase α. Mol. Cell 5: 617-627.
51. Walter, J., Sun, L., and Newport, J. 1998. Regulated chromosomal DNA replication in the absence of a nucleus. Mol. Cell 1: 519-529.
52. Ward, I.M., Minn, K., and Chen, J. 2004. UV-induced ataxia- telangiectasia-mutated and Rad3-related (ATR) activation requires replication stress. J. Biol. Chem. 279: 9677-9680.
53. Yagura, T., Tanaka, S., Kozu, T., Seno, T., and Korn, D. 1983. Tight association of DNA primase with a subspecies of mouse DNA polymerase α. J. Biol. Chem. 258: 6698-6700.
54. You, Z., Kong, L., and Newport, J. 2002. The role of single-stranded DNA and polymerase α in establishing the ATR, Hus1 DNA replication checkpoint. J. Biol. Chem. 277: 27088-27093.
55. Zhao, H. and Piwnica-Worms, H. 2001. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chkl. Mol. Cell. Biol. 21: 4129-4139.
56. Zhou, B.B. and Elledge, S.J. 2000. The DNA damage response: Putting checkpoints in perspective. Nature 408: 433-439.
57. Zou, L. and Elledge, S.J. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.
58. Zou, L., Cortez, D., and Elledge, S.J. 2002. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes & Dev. 16: 198-208.
59. Zou, L., Liu, D., and Elledge, S.J. 2003. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc. Natl. Acad. Sci. 100: 13827-13832.