MDC1 regulates intra-S-phase checkpoint by targeting NBS1 to DNA double-strand breaks

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 32, 2008, Pages 11200-11205

  Wu, Liming ^a   Luo, Kuntian ^b   Lou, Zhenkun ^b   Chen, Junjie ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAYO CLINIC   (United States)

Author keywords

53BP1; BRCA1; Casein kinase 2; MRE11

Indexed keywords

BRCA1 PROTEIN; CASEIN KINASE II; FORKHEAD TRANSCRIPTION FACTOR; NIBRIN; NUCLEAR PROTEIN; PHOSPHOPEPTIDE; PROTEIN MDC1;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE S PHASE; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

ANIMALS; CASEIN KINASE II; CELL CYCLE PROTEINS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; S PHASE; TRANS-ACTIVATORS;

EID: 49649089537     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0802885105     Document Type: Article

References (37)

1. Varon R, et al. (1998) Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell 93:467-476.
2. Carney JP, et al. (1998) The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: Linkage of double-strand break repair to the cellular DNA damage response. Cell 93:477-486.
3. Stewart GS, et al. (1999) The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 99:577-587.
4. Falck J, Coates J, Jackson SP (2005) Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:605-611.
5. Uziel T, et al. (2003) Requirement of the MRN complex for ATM activation by DNA damage. EMBO J 22:5612-5621.
6. Carson CT, et al. (2003) The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J 22:6610-6620.
7. Horejsi Z, et al. (2004) Distinct functional domains of Nbs1 modulate the timing and magnitude of ATM activation after low doses of ionizing radiation. Oncogene 23:3122-3127.
8. Lee JH, Paull TT (2005) ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308:551-554.
9. Wu X, et al. (2000) ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature 405:477-482.
10. Zhao S, et al. (2000) Functional link between ataxia- telangiectasia and Nijmegen breakage syndrome gene products. Nature 405:473-477.
11. Lim DS, et al. (2000) ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404:613-617.
12. Yazdi PT, et al. (2002) SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev 16:571-582.
13. Kim ST, Xu B, Kastan MB (2002) Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev 16:560-570.
14. Becker E, Meyer V, Madaoui H, Guerois R (2006) Detection of a tandem BRCT in Nbs1 and Xrs2 with functional implications in the DNA damage response. Bioinformatics 22:1289-1292.
15. Lou Z, et al. (2006) MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol Cell 21:187-200.
16. Goldberg M, et al. (2003) MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 421:952-956.
17. Stewart GS, Wang B, Bignell CR, Taylor AM, Elledge SJ (2003) MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421:961-966.
18. Lukas C, et al. (2004) Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J 23:2674-2683.
19. Xu X, Stern DF (2003) NFBD1/MDC1 regulates ionizing radiation-induced focus formation by DNA checkpoint signaling and repair factors. FASEB J 17:1842-1848.
20. Tauchi H, et al. (2001) The forkhead-associated domain of NBS1 is essential for nuclear foci formation after irradiation but not essential for hRAD50·hMRE11·NBS1 complex DNA repair activity. J Biol Chem 276:12-15.
21. Zhao S, Renthal W, Lee EY (2002) Functional analysis of FHA and BRCT domains of NBS1 in chromatin association and DNA damage responses. Nucleic Acids Res 30:4815-4822.
22. Kobayashi J, et al. (2002) NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr Biol 12:1846-1851.
23. Lu R, Niida H, Nakanishi M (2004) Human SAD1 kinase is involved in UV-induced DNA damage checkpoint function. J Biol Chem 279:31164-31170.
24. Stucki M, et al. (2005) MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123:1213-1226.
25. Meggio F, Pinna LA (2003) One-thousand-and-one substrates of protein kinase CK2? FASEB J 17:349-368.
26. Pagano MA, et al. (2004) 2-Dimethylamino-4,5,6,7-tetrabromo-1H- benzimidazole: A novel powerful and selective inhibitor of protein kinase CK2. Biochem Biophys Res Commun 321:1040-1044.
27. Beausoleil SA, et al. (2004) Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci USA 101:12130-12135.
28. Olsen JV, et al. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127:635-648.
29. Huen MS, et al. (2007) RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131:901-914.
30. Kolas NK, et al. (2007) Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318:1637-1640.
31. Mailand N, et al. (2007) RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131:887-900.
32. Wang B, Elledge SJ (2007) Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc Natl Acad Sci USA 104:20759-20763.
33. Lou Z, Minter-Dykhouse K, Wu X, Chen J (2003) MDC1 is coupled to activated CHK2 in mammalian DNA damage response pathways. Nature 421:957-961.
34. Celeste A, et al. (2002) Genomic instability in mice lacking histone H2AX. Science 296:922-927.
35. Melander F, et al. (2008) Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J Cell Biol 181:213-226.
36. Spycher C, et al. (2008) Constitutive phosphorylation of MDC1 physically links the MRE11-RAD50-NBS1 complex to damaged chromatin. J Cell Biol 181:227-240.
37. Chapman JR, Jackson SP (2008) Phospho-dependent interactions between NSB1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep. Epub ahead of print.