Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage

Nature

Volumn 434, Issue 7033, 2005, Pages 605-611

  Falck, Jacob ^a   Coates, Julia ^a   Jackson, Stephen P ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; CELLS; ENZYMES; SIGNALING;

CARBOXY-TERMINAL MOTIFFS; DNA DAMAGE; DNA REPLICATION FORKS; PHOSPHOINOSITIDE-3-KINASE-RELATED PROTEIN KINASE (PIKK);

DNA;

ATM PROTEIN; ATR PROTEIN; BINDING PROTEIN; DNA DEPENDENT PROTEIN KINASE; DOUBLE STRANDED DNA; NIBRIN; PHOSPHOINOSITIDE 3 KINASE RELATED PROTEIN KINASE; PROTEIN ATRIP; PROTEIN KINASE; PROTEIN KU80; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; ATR PROTEIN, HUMAN; CELL CYCLE PROTEIN; CELL NUCLEUS ANTIGEN; DNA; DNA BINDING PROTEIN; KU ANTIGEN; NBS1 PROTEIN, HUMAN; NUCLEAR PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PRKDC PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; TUMOR SUPPRESSOR PROTEIN;

DNA;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA STRAND BREAKAGE; ENZYME ACTIVATION; ENZYME SUBUNIT; GENETIC CONSERVATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CHEMISTRY; GENETICS; HAMSTER; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, NUCLEAR; BINDING SITES; CELL CYCLE PROTEINS; CONSERVED SEQUENCE; CRICETINAE; DNA; DNA DAMAGE; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 15844394846     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/nature03442     Document Type: Article

References (43)

1. Zhou, B.-B. S. & Elledge, S. J. The DNA damage response: putting checkpoints in perspective. Nature 408, 433-439 (2000).
2. Rouse, I. & Jackson, S. P. Interfaces between the detection, signaling, and repair of DNA damage. Science 297, 547-551 (2002).
3. Melo, I. & Toczyski, D. A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14, 237-245 (2002).
4. Shiloh, Y. ATM and related protein kinases: safeguarding genome integrity. Nature Rev. Cancer 3, 155-168 (2003).
5. Meek, K., Gupta, S., Ramsden, D. A. & Lees-Miller, S. P. The DNA-dependent protein kinase: the director at the end. Immunol. Rev. 200, 132-141 (2004).
6. Hammarsten, O., DeFazio, L. G. & Chu, G. Activation of DNA-dependent protein kinase by single-stranded DNA ends. J. Biol. Chem. 275, 1541-1550 (2000).
7. Smith, G. C. M, et al. Purification and DNA binding properties of the ataxia-telangiectasia gene product ATM. Proc. Natl Acad. Sci. USA 96, 11134-11139 (1999).
8. Ünsal-Kacmaz, K., Makhov, A. M., Griffith, J. D. & Sancar, A. Preferential binding of ATR protein to UV-damaged DNA. Proc. Natl Acad. Sci. USA 99, 6673-6678 (2002).
9. Unsal-Kacmaz, K. & Sancar, A. Quaternary structure of ATR and effects of ATRIP and replication protein A on its DNA binding and kinase activities. Mol. Cell. Biol. 24, 1292-1300 (2004).
10. Zou, L. & Elledge, S. J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300, 1542-1548 (2003).
11. Gottlieb, T. M. & Jackson, S. P. The DNA-dependent protein kinase; requirement for DNA ends and association with Ku antigen. Cell 72, 131-142 (1993).
12. Dvir, A., Peterson, S. R., Knuth, M. W., Lu, H. & Dynan, W. S. Ku autoantigen is the regulatory component of a template-associated protein kinase that phosphorylates RNA polymerase II. Proc. Natl Acad. Sci. USA 89, 11920-11924 (1992).
13. Andegeko, Y. et al. Nuclear retention of ATM at sites of DNA double strand breaks. J. Biol. Chem. 276, 38224-38230 (2001).
14. Carson, C. T. et al. The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22, 6610-6620 (2003).
15. Kitagawa, R., Bakkenist, C. J., McKinnon, P. J. & Kastan, M. B. Phosphorylation of SMCl is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev. 18, 1423-1438 (2004).
16. D'Amours, D. &c Jackson, S. P. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nature Rev. Mol. Cell Biol. 3, 317-327 (2002).
17. Bakkenist, C. J. & Kastan, M. B. DNA damage activates ATM through intermolecular autophosphorylation and dinier dissociation. Nature 421, 499-506 (2003).
18. Lukas, C., Falck, J., Bartkova, J., Bartek, J. & Lukas, J. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nature Cell Biol. 5, 255-260 (2003).
19. Uziel, T. et al. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22, 5612-5621 (2003).
20. 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).
21. Hickson, I. et al. Identification and characterization of a novel and specific inhibitor of the ataxiatelangiectasia mutated kinase ATM. Cancer Res. 64, 9152-9159 (2004).
22. Veuger, S. J., Curtin, N. J., Smith, G. C. & Durkacz, B. W. Effects of novel inhibitors of poly(ADP-ribose) polymerase-1 and the DNA-dependent protein kinase on enzyme activities and DNA repair. Oncogens 23, 7322-7329 (2004).
23. Stiff, T. et al. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 64, 2390-2396 (2004).
24. Geil, D. & Jackson, S. P. Mapping of protein-protein interactions within the DNA-dependent protein kinase complex. Nucleic Acids Res. 27, 3494-3502 (1999).
25. Singleton, B. K., Tacdoli, G. E., Rottinghaus, S. & Jeggo, P. A. Interaction of the C-terminus of Ku80 with the DNA-dependent protein kinase catalytic subunit. Mol. Cell. Biol 19, 3267-3277 (1999).
26. Chan, D. W. et al. Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev. 16, 2333-2338 (2002).
27. Douglas, P. et al. Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase. Biochem. J. 368, 243-251 (2002).
28. Rothkamm, K. & Lobrich, M. Evidence for a lack of DNA double-strand break repair in human cells exposed to very low x-ray doses. Proc. Natl Acad. Sci. USA 100, 5057-5062 (2003).
29. Zou, L., Cortez, D. & Elledge, S. J. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev. 16, 198-208 (2002).
30. Rouse, J. & Jackson, S. P. Lcd1p recruits Mec1p to DNA lesions in vitro and in vivo. Mol. Cell 9, 857-869 (2002).
31. Costanzo, V., Paull, T., Gottesman, M. & Gautier, J. Mre11 assembles linear DNA fragments into DNA damage signaling complexes. PLoS Biol. 2, E110 (2004).
32. Nakada, D., Matsumoto, K. & Sugimoto, K. ATM-related Tell associates with double-strand breaks through an Xrs2-dependent mechanism. Genes Dev. 17, 1957-1962 (2003).
33. Brodsky, M. H., Sekelsky, J. J., Tsang, G., Hawley, R, S. & Rubin, G. M. mus304 encodes a novel DNA damage checkpoint protein required during Drosophila development. Genes Dev. 14, 666-678 (2000).
34. Wakayama, T., Kondo, T., Ando, S., Matsumoto, K. & Sugimoto, K, Piel, a protein interacting with Meet, controls cell growth and checkpoint responses in Saccharomyces cerevisiae. Mol. Cell Biol. 21, 755-764 (2001).
35. Wolkow, T. D. & Enoch, T. Fission yeast Rad26 is a regulatory subunit of the Rad3 checkpoint kinase. Mol. Biol. Cell 13, 480-492 (2002).
36. Lee, J. H. & Paull, T. T. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304, 93-96 (2004).
37. Brewerton, S. C., Dore, A. S., Drake, A. C., Leuther, K. K. & Blundell, T. L. Structural analysis of DNA-PKcs: modelling of the repeat units and insights into the detailed molecular architecture. J. Struct. Biol. 145, 295-306 (2004).
38. Perry, J. & Kleckner, N. The ATRs, ATMs, and TORs are giant HEAT repeat proteins. Cell 112, 151-155 (2003).
39. Singleton, B. K., Torres-Arzayus, M. I., Rottinghaus, S. T., Taccioli, G. E. & Jeggo, P. A. The C terminus of Ku80 activates the DNA-dependent protein kinase catalytic subunit. Mol. Cell Biol. 19, 3267-3277 (1999).
40. Goldberg, M. et al. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 421, 952-956 (2003).
41. Falck, J., Petrini, J. H. J., Williams, B. R., Lukas, J. & Bartek, J. The DNA damage-dependent intra-S phase checkpoint is regulated by parallel pathways. Nature Genet. 30, 290-294 (2002).
42. 2-phase checkpoints after ionizing irradiation. Mol. Cell. Biol. 21, 3445-3450 (2001).
43. 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).