Dynamics of the PI3K-like protein kinase members ATM and DNA-PKcs at DNA double strand breaks

Cell Cycle

Volumn 9, Issue 13, 2010, Pages 2529-2536

  Davis, Anthony J ^a   So, Sairei ^a   Chen, David J ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

ATM; Autophosphorylation; DNA double strand breaks; DNA PKcs; Live cell imaging

Indexed keywords

ATM PROTEIN; DNA DEPENDENT PROTEIN KINASE; DNA DEPENDENT PROTEIN KINASE CATALYTIC SUBUNIT; PHOSPHATIDYLINOSITOL 3 KINASE; UNCLASSIFIED DRUG;

DISSOCIATION; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME MECHANISM; FLUORESCENCE IMAGING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; SIGNAL PROCESSING;

EID: 77955434227     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.13.12148     Document Type: Review

References (55)

1. Khanna KK, Jackson SP. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet 2001; 27:247-54.
2. Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature 2001; 411:366-74.
3. Burma S, Chen BP, Chen DJ. Role of non-homologous end joining (NHEJ) in maintaining genomic integrity. DNA Repair (Amst) 2006; 5:1042-8.
4. Weterings E, Chen DJ. The endless tale of non-homologous end-joining. Cell Res 2008; 18:114-24.
5. Meek K, Dang V, Lees-Miller SP. DNA-PK: the means to justify the ends? Adv Immunol 2008; 99:33-58.
6. Mahaney BL, Meek K, Lees-Miller SP. Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous end-joining. Biochem J 2009; 417:639-50.
7. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 2003; 3:155-68.
8. Lavin MF, Kozlov S. ATM activation and DNA damage response. Cell Cycle 2007; 6:931-42.
9. Lavin MF. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat Rev Mol Cell Biol 2008; 9:759-69.
10. Lavin MF, Shiloh Y. The genetic defect in ataxia-telangiectasia. Annu Rev Immunol 1997; 15:177-202.
11. Riballo E, Kuhne M, Rief N, Doherty A, Smith GC, Recio MJ, et al. A pathway of double-strand break rejoining dependent upon ATM, Artemis and proteins locating to gamma-H2AX foci. Mol Cell 2004; 16:715-24.
12. Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y, Lobrich M, et al. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol Cell 2008; 31:167-77.
13. Walker JR, Corpina RA, Goldberg J. Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 2001; 412:607-14.
14. Van der Burg M, Ijspeert H, Verkaik NS, Turul T, Wiegant WW, Morotomi-Yano K, et al. A DNA-PKcs mutation in a radiosensitive T-B- SCID patient inhibits Artemis activation and nonhomologous end-joining. J Clin Invest 2009; 119:91-8.
15. Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan MB, Bartek J, et al. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J Cell Biol 2006; 173:195-206.
16. Lukas C, Bartek J, Lukas J. Imaging of protein movement induced by chromosomal breakage: tiny 'local' lesions pose great 'global' challenges. Chromosoma 2005; 114:146-54.
17. Uematsu N, Weterings E, Yano K, Morotomi-Yano K, Jakob B, Taucher-Scholz G, et al. Autophosphorylation of DNA-PKCS regulates its dynamics at DNA double-strand breaks. J Cell Biol 2007; 177:219-29.
18. Yano K, Morotomi-Yano K, Wang SY, Uematsu N, Lee KJ, Asaithamby A, et al. Ku recruits XLF to DNA double-strand breaks. EMBO Rep 2008; 9:91-6.
19. So S, Davis AJ, Chen DJ. Autophosphorylation at serine 1981 stabilizes ATM at DNA damage sites. J Cell Biol 2009; 187:977-90.
20. Pellegrini M, Celeste A, Difilippantonio S, Guo R, Wang W, Feigenbaum L, et al. Autophosphorylation at serine 1987 is dispensable for murine Atm activation in vivo. Nature 2006; 443:222-5.
21. You Z, Bailis JM, Johnson SA, Dilworth SM, Hunter T. Rapid activation of ATM on DNA flanking double-strand breaks. Nat Cell Biol 2007; 9:1311-8.
22. Smith GC, Cary RB, Lakin ND, Hann BC, Teo SH, Chen DJ, et al. Purification and DNA binding properties of the ataxia-telangiectasia gene product ATM. Proc Natl Acad Sci USA 1999; 96:11134-9.
23. Hammarsten O, Chu G. DNA-dependent protein kinase: DNA binding and activation in the absence of Ku. Proc Natl Acad Sci USA 1998; 95:525-30.
24. Drouet J, Delteil C, Lefrancois J, Concannon P, Salles B, Calsou P. DNA-dependent protein kinase and XRCC4-DNA ligase IV mobilization in the cell in response to DNA double strand breaks. J Biol Chem 2005; 280:7060-9.
25. Hammarsten O, DeFazio LG, Chu G. Activation of DNA-dependent protein kinase by single-stranded DNA ends. J Biol Chem 2000; 275:1541-50.
26. Cary R, Peterson S, Wang J, Bear D, Bradbury E, Chen D. DNA looping by Ku and the DNA-dependent protein kinase. Proc Natl Acad Sci USA 1997; 94:4267-72.
27. Kitagawa R, Bakkenist CJ, McKinnon PJ, Kastan MB. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev 2004; 18:1423-38.
28. Falck J, Coates J, Jackson SP. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 2005; 434:605-11.
29. Uziel T, Lerenthal Y, Moyal L, Andegeko Y, Mittelman L, Shiloh Y. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J 2003; 22:5612-21.
30. Berkovich E, Monnat RJ Jr, Kastan MB. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat Cell Biol 2007; 9:683-90.
31. de Jager M, van Noort J, van Gent DC, Dekker C, Kanaar R, Wyman C. Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol Cell 2001; 8:1129-35.
32. Paull TT, Gellert M. The 3′ to 5′ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol Cell 1998; 1:969-79.
33. Williams RS, Moncalian G, Williams JS, Yamada Y, Limbo O, Shin DS, et al. Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell 2008; 135:97-109.
34. Paull TT, Gellert M. Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev 1999; 13:1276-88.
35. Arthur LM, Gustausson K, Hopfner KP, Carson CT, Stracker TH, Karcher A, et al. Structural and functional analysis of Mre11-3. Nucleic Acids Res 2004; 32:1886-93.
36. Cerosaletti K, Concannon P. Independent roles for nibrin and Mre11-Rad50 in the activation and function of Atm. J Biol Chem 2004; 279:38813-9.
37. Difilippantonio S, Celeste A, Fernandez-Capetillo O, Chen HT, Reina San Martin B, Van Laethem F, et al. Role of Nbs1 in the activation of the Atm kinase revealed in humanized mouse models. Nat Cell Biol 2005; 7:675-85.
38. Weterings E, Verkaik NS, Keijzers G, Florea BI, Wang SY, Ortega LG, et al. The Ku80 carboxy terminus stimulates joining and artemis-mediated processing of DNA ends. Mol Cell Biol 2009; 29:1134-42.
39. Mari PO, Florea BI, Persengiev SP, Verkaik NS, Bruggenwirth HT, Modesti M, et al. Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc Natl Acad Sci USA 2006; 103:18597-602.
40. Kruhlak MJ, Celeste A, Dellaire G, Fernandez-Capetillo O, Muller WG, McNally JG, et al. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J Cell Biol 2006; 172:823-34.
41. Murr R, Loizou JI, Yang YG, Cuenin C, Li H, Wang ZQ, et al. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat Cell Biol 2006; 8:91-9.
42. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499-506.
43. Kozlov SV, Graham ME, Peng C, Chen P, Robinson PJ, Lavin MF. Involvement of novel autophosphorylation sites in ATM activation. EMBO J 2006; 25:3504-14.
44. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER, 3rd, Hurov KE, Luo J, et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007; 316:1160-6.
45. Daniel JA, Pellegrini M, Lee JH, Paull TT, Feigenbaum L, Nussenzweig A. Multiple autophosphorylation sites are dispensable for murine ATM activation in vivo. J Cell Biol 2008; 183:777-83.
46. Chan DW, Chen BP, Prithivirajsingh S, Kurimasa A, Story MD, Qin J, et al. Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev 2002; 16:2333-8.
47. Chen BP, Chan DW, Kobayashi J, Burma S, Asaithamby A, Morotomi-Yano K, et al. Cell cycle dependence of DNA-dependent protein kinase phosphorylation in response to DNA double strand breaks. J Biol Chem 2005; 280:14709-15.
48. Douglas P, Sapkota GP, Morrice N, Yu Y, Goodarzi AA, Merkle D, et al. Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase. Biochem J 2002; 368:243-51.
49. Douglas P, Cui X, Block WD, Yu Y, Gupta S, Ding Q, et al. The DNA-dependent protein kinase catalytic subunit is phosphorylated in vivo on threonine 3950, a highly conserved amino acid in the protein kinase domain. Mol Cell Biol 2007; 27:1581-91.
50. Ding Q, Reddy YV, Wang W, Woods T, Douglas P, Ramsden DA, et al. Autophosphorylation of the catalytic subunit of the DNA-dependent protein kinase is required for efficient end processing during DNA double-strand break repair. Mol Cell Biol 2003; 23:5836-48.
51. Soubeyrand S, Pope L, Pakuts B, Hache RJ. Threonines 2638/2647 in DNA-PK are essential for cellular resistance to ionizing radiation. Cancer Res 2003; 63:1198-201.
52. Li Z, Otevrel T, Gao Y, Cheng HL, Seed B, Stamato TD, et al. The XRCC4 gene encodes a novel protein involved in DNA double-strand break repair and V(D)J recombination. Cell 1995; 83:1079-89.
53. Block WD, Yu Y, Merkle D, Gifford JL, Ding Q, Meek K, et al. Autophosphorylation-dependent remodeling of the DNA-dependent protein kinase catalytic subunit regulates ligation of DNA ends. Nucleic Acids Res 2004; 32:4351-7.
54. Cui X, Yu Y, Gupta S, Cho YM, Lees-Miller SP, Meek K. Autophosphorylation of DNA-dependent protein kinase regulates DNA end processing and may also alter double-strand break repair pathway choice. Mol Cell Biol 2005; 25:10842-52.
55. Hammel M, Yu Y, Mahaney BL, Cai B, Ye R, Phipps BM, et al. Ku and DNA-dependent protein kinase dynamic conformations and assembly regulate DNA binding and the initial non-homologous end joining complex. J Biol Chem 2010; 285:1414-23.