ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks

Nature Cell Biology

Volumn 8, Issue 1, 2006, Pages 37-45

  Jazayeri, Ali ^a,b   Falck, Jacob ^a   Lukas, Claudia ^c   Bartek, Jiri ^c   Smith, Graeme C M ^b   Lukas, Jiri ^c   Jackson, Stephen P ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b KuDOS Pharmaceuticals Ltd   (United Kingdom)

^c DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 1; CYCLIN DEPENDENT KINASE; DOUBLE STRANDED DNA; MRE11 PROTEIN; NUCLEASE; REPLICATION PROTEIN A; SINGLE STRANDED DNA;

ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA STRAND BREAKAGE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL NUCLEUS; CYCLIN-DEPENDENT KINASES; DNA DAMAGE; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; REPLICATION PROTEIN A; TUMOR SUPPRESSOR PROTEINS;

ATAXIA TELANGIECTASIA;

EID: 30344463835     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1337     Document Type: Article

References (45)

1. Shiloh, Y. ATM and related protein kinases: Safeguarding genome integrity. Nature Rev. Cancer 3, 155-168 (2003).
2. Abraham, R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15, 2177-2196 (2001).
3. Falck, J., Coates, J. & Jackson, S.P. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434, 605-611 (2005).
4. Lee, J.H. & Paull, T.T. ATM Activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 Complex. Science 308, 551-554 (2005).
5. Cortez, D., Guntuku, S., Qin, J. & Elledge, S.J. ATR and ATRIP: Partners in checkpoint signaling. Science 294, 1713-1716 (2001).
6. Zou, L. & Elledge, S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300, 1542-1548 (2003).
7. Costanzo, V. et al. An ATR-and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol. Cell 11, 203-213 (2003).
8. Bartek, J. & Lukas, J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 3, 421-429 (2003).
9. Gatei, M. et al. Ataxia-telangiectasia-mutated (ATM) and NBS1-dependent phosphorylation of Chk1 on Ser-317 in response to ionizing radiation. J. Biol. Chem. 278, 14806-14811 (2003).
10. Liu, Q. et al. Chk1 is an essential kinase that is regulated by Atr and required for the G2/M DNA damage checkpoint. Genes Dev. 14, 1448-1459 (2000).
11. Zhao, H. & Piwnica-Worms, H. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol. Cell. Biol. 21, 4129-4139 (2001).
12. Matsuoka, S. et al. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc. Natl Acad. Sci. USA 97, 10389-10394 (2000).
13. Buscemi, G. et al. Chk2 activation dependence on Nbs1 after DNA damage. Mol. Cell. Biol. 15, 5214-5222 (2001).
14. Tibbetts, R.S. et al. A role for ATR in the DNA damage induced phosphorylation of p53. Genes Dev. 13, 152-157 (1999).
15. Brown, E.J. & Baltimore, D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14, 397-402 (2000).
16. O'Driscoll, M. et al. A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nature Genet. 33, 497-501 (2003).
17. Bao, S. et al. ATR/ATM-mediated phosphorylation of human Rad17 is required for genotoxic stress responses. Nature 411, 969-974 (2001).
18. Post, S. et al. Phosphorylation of serines 635 and 645 of human Rad17 is cell cycle regulated and is required for G1/S checkpoint activation in response to DNA damage. Proc. Natl Acad. Sci. USA 98, 13102-13107 (2001).
19. Yazdi, P.T. et al. SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev. 16, 571-582 (2002).
20. Kim, S.-T., Xu, B. & Kastan, M.B. Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev. 16, 560-570 (2002).
21. Hickson, I. et al. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64, 9152-9159 (2004).
22. D'Andrea, A.D. & Haseltine, W.A. Sequence specific cleavage of DNA by the antitumor antibiotics neocarzinostatin and bleomycin. Proc. Natl Acad. Sci. USA 75, 3608-3612 (1978).
23. Lim, D.-S. et al. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404, 613-617 (2000).
24. Zhao, S. et al. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature 405, 473-477 (2000).
25. Tibbetts, R.S. et al. Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev. 14, 2989-3002 (2000).
26. Lukas, C. et al. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nature Cell Biol. 5, 255-260 (2003).
27. Moreau, S., Ferguson, J.R. & Symington, L.S. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19, 556-566 (1999).
28. Paull, T.T. & Gellert, M. The 3′ to 5′ exonuclease activity of Mre11 facilitates repair of DNA double-strand breaks. Mol. Cell 1, 969-979 (1998).
29. Trujillo, K.M., Yuan, S.-S.F., Lee, E.-Y.P. & Sung, P. Nuclease activities in a complex of human recombination and DNA repair factors Rad50, Mre11, and p95. J. Biol. Chem. 273, 21447-21450 (1998).
30. Nakada, D., Hirano, Y. & Sugimoto, K. Requirement of the Mre11 complex and exonuclease 1 for activation of the Mec1 signaling pathway. Mol. Cell. Biol. 24, 10016-10025 (2004).
31. Uziel, T. et al. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22, 5612-5621 (2003).
32. Stracker, T.H., Carson, C.T. & Weitzman, M.D. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418, 348-352 (2002).
33. Ira, G. et al. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431, 1011-1017 (2004).
34. De Azevedo, W.F. et al. Inhibition of cyclin-dependent kinases by purine analogues: Crystal structure of human cdk2 complexed with roscovitine. Eur. J. Biochem. 243, 518-526 (1997).
35. Wu, X. et al. ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature 405, 477-482 (2000).
36. Gatei, M. et al. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nature Genet. 25, 1155-119 (2000).
37. Costanzo, V. et al. Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell 8, 137-147 (2001).
38. Morrison, C. et al. The controlling role of ATM in homologous recombinational repair of DNA damage. EMBO J. 19, 463-471 (2000).
39. -/- cells. Mutat. Res. 525, 85-92 (2003).
40. Rothkamm, K., Kruger, I., Thompson, L.H. & Lobrich, M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol. 23, 5706-5715 (2003).
41. Esashi, F. et al. CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 434, 598-604 (2005).
42. Sorensen, C.S. et al. The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nature Cell. Biol. 7, 195-201 (2005).
43. Falck, J. et al. The DNA damage-dependent intra-S phase checkpoint is regulated by parallel pathways. Nature Genet. 30, 290-294 (2002).
44. Tsao, C.C., Geisen, C. & Abraham, R.T. Interaction between human MCM7 and Rad17 proteins is required for replication checkpoint signaling. EMBO J. 23, 4660-4669 (2004).
45. Lukas, C. et al. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 23, 2674-2683 (2004).