Two-step activation of ATM by DNA and the Mre11-Rad50-Nbs1 complex

Nature Structural and Molecular Biology

Volumn 13, Issue 5, 2006, Pages 451-457

  Dupré, Aude ^a   Boyer Chatenet, Louise ^a   Gautier, Jean ^a  

^a HHSC1602 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; DNA; DOUBLE STRANDED DNA; MRE11 PROTEIN; NIBRIN; RAD50 PROTEIN; SERINE;

ARTICLE; ATAXIA TELANGIECTASIA; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; ENZYME ACTIVATION; ENZYME ACTIVITY; GENETIC DISORDER; NIJIMEGEN BREAKAGE SYNDROME; NONHUMAN; PHENOTYPE; PHOSPHORYLATION; PRIORITY JOURNAL;

ANIMALS; CELL CYCLE PROTEINS; DNA; DNA REPAIR ENZYMES; DNA REPLICATION; DNA-BINDING PROTEINS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS; XENOPUS LAEVIS; XENOPUS PROTEINS;

ATAXIA TELANGIECTASIA;

EID: 33745058037     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb1090     Document Type: Article

References (37)

1. Sancar, A., Lindsey-Boltz, L.A., Unsal-Kacmaz, K. & Linn, S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73, 39-85 (2004).
2. Bakkenist, C.J. & Kastan, M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421, 499-506 (2003).
3. D'Amours, D. & Jackson, S.P. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3, 317-327 (2002).
4. Lim, D.S. et al. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404, 613-617 (2000).
5. Gatei, M. et al. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nat. Genet. 25, 115-119 (2000).
6. Falck, J., Petrini, J.H., Williams, B.R., Lukas, J. & Bartek, J. The DNA damage-dependent intra-S phase checkpoint is regulated by parallel pathways. Nat. Genet. 30, 290-294 (2002).
7. 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).
8. Girard, P.M., Riballo, E., Begg, A.C., Waugh, A. & Jeggo, P.A. Nbs1 promotes ATM dependent phosphorylation events including those required for G1/S arrest. Oncogene 21, 4191-4199 (2002).
9. Lee, J.H. et al. Distinct functions of Nijmegen breakage syndrome in ataxia telangiectasia mutated-dependent responses to DNA damage. Mol. Cancer Res. 1, 674-681 (2003).
10. Uziel, T. et al. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22, 5612-5621 (2003).
11. Carson, C.T. et al. The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22, 6610-6620 (2003).
12. Difilippantonio, S. et al. Role of Nbs1 in the activation of the Atm kinase revealed in humanized mouse models. Nat. Cell Biol. 7, 675-685 (2005).
13. Costanzo, V., Paull, T., Gottesman, M. & Gautier, J. Mre11 assembles linear DNA fragments into DNA damage signaling complexes. PLoS Biol. 2, E110 (2004).
14. You, Z., Chahwan, C., Bailis, J., Hunter, T. & Russell, P. ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol. Cell. Biol. 25, 5363-5379 (2005).
15. Mochan, T.A., Venere, M., DiTullio, R.A., Jr. & Halazonetis, T.D. 53BP1 and NFBD1/MDC1-Nbs1 function in parallel interacting pathways activating ataxia-telangiectasia mutated (ATM) in response to DNA damage. Cancer Res. 63, 8586-8591 (2003).
16. Lee, J.H. & Paull, T.T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308, 551-554 (2005).
17. Kim, J.S., Krasieva, T.B., LaMorte, V., Taylor, A.M. & Yokomori, K. Specific recruitment of human cohesin to laser-induced DNA damage. J. Biol. Chem. 277, 45149-45153 (2002).
18. Buscemi, G. et al. Activation of ATM and Chk2 kinases in relation to the amount of DNA strand breaks. Oncogene 23, 7691-7700 (2004).
19. Shiloh, Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3, 155-168 (2003).
20. Kitagawa, R., Bakkenist, C.J., McKinnon, P.J. & Kastan, M.B. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev. 18, 1423-1438 (2004).
21. Cerosaletti, K. & Concannon, P. Independent roles for nibrin and Mre11-Rad50 in the activation and function of Atm. J. Biol. Chem. 279, 38813-38819 (2004).
22. Horejsi, Z. et al. Distinct functional domains of Nbs1 modulate the timing and magnitude of ATM activation after low doses of ionizing radiation. Oncogene 23, 3122-3127 (2004).
23. 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).
24. Cerosaletti, K., Wright, J. & Concannon, P. Active role for nibrin in the kinetics of atm activation. Mol. Cell. Biol. 26, 1691-1699 (2006).
25. Lee, J.H. & Paull, T.T. Direct activation of the ATM protein kinasebythe Mre11/Rad50/Nbs1 complex. Science 304, 93-96 (2004).
26. Costanzo, V. et al. Reconstitution of an ATM-dependent checkpoint that inhibits chromosomal DNA replication following DNA damage. Mol. Cell 6, 649-659 (2000).
27. Yoo, H.Y., Shevchenko, A., Shevchenko, A. & Dunphy, W.G. Mcm2 is a direct substrate of ATM and ATR during DNA damage and DNA replication checkpoint responses. J. Biol. Chem. 279, 53353-53364 (2004).
28. Van den Bosch, M., Bree, R.T. & Lowndes, N.F. The MRN complex: coordinating and mediating the response to broken chromosomes. EMBO Rep. 4, 844-849 (2003).
29. Moncalian, G. et al. The rad50 signature motif: essential to ATP binding and biological function. J. Mol. Biol. 335, 937-951 (2004).
30. Aten, J.A. et al. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303, 92-95 (2004).
31. Lisby, M. & Rothstein, R. DNA damage checkpoint and repair centers. Curr. Opin. Cell Biol. 16, 328-334 (2004).
32. Perry, J. & Kleckner, N. The ATRs, ATMs, and TORs are giant HEAT repeat proteins. Cell 112, 151-155 (2003).
33. De Lange, T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19, 2100-2110 (2005).
34. Lin, X.H. et al. Protein phosphatase 2A is required for the initiation of chromosomal DNA replication. Proc. Natl Acad. Sci. USA 95, 14693-14698 (1998).
35. Robertson, K., Hensey, C. & Gautier, J. Isolation and characterization of Xenopus ATM (X-ATM): expression, localization, and complex formation during oogenesis and early development. Oncogene 18, 7070-7079 (1999).
36. Friedland, W., Jacob, P., Paretzke, H.G., Merzagora, M. & Ottolenghi, A. Simulation of DNA fragment distributions after irradiation with photons. Radiat. Environ. Biophys. 38, 39-47 (1999).
37. Paull, T.T. & Gellert, M. The 3′ to 5′ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1, 969-979 (1998).