Constitutive phosphorylation of MDC1 physically links the MRE11-RAD50-NBS1 complex to damaged chromatin

Journal of Cell Biology

Volumn 181, Issue 2, 2008, Pages 227-240

  Spycher, Christoph ^a   Miller, Edward S ^b   Townsend, Kelly ^b   Pavic, Lucijana ^a   Morrice, Nicholas A ^c   Janscak, Pavel ^a   Stewart, Grant S ^b   Stucki, Manuel ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; CASEIN KINASE II; HYBRID PROTEIN; MRE11 PROTEIN; NIBRIN; PROTEOME; RAD50 PROTEIN; SMALL INTERFERING RNA; ABC TRANSPORTER; CELL CYCLE PROTEIN; COMPLEMENTARY DNA; DNA BINDING PROTEIN; MDC1 PROTEIN, MOUSE; MRE11A PROTEIN, MOUSE; NBN PROTEIN, HUMAN; NIJMEGEN BREAKAGE SYNDROME 1 PROTEIN, MOUSE; NUCLEAR PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; RAD50 PROTEIN, MOUSE; SIGNAL PEPTIDE;

ARTICLE; DNA DAMAGE; FIBROBLAST; HUMAN; MASS SPECTROMETRY; NIJMEGEN BREAKAGE SYNDROME; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ANIMAL; CHROMATIN; GENE VECTOR; GENETIC TRANSFECTION; GENETICS; HELA CELL; METABOLISM; MOUSE; PHOSPHORYLATION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CASEIN KINASE II; CELL CYCLE PROTEINS; CHROMATIN; DNA DAMAGE; DNA REPAIR ENZYMES; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; GENETIC VECTORS; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; NUCLEAR PROTEINS; PHOSPHORYLATION; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 42449115711     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200709008     Document Type: Article

References (43)

1. Beausoleil, S.A., M. Jedrychowski, D. Schwartz, J.E. Elias, J. Villen, J. Li, M.A. Cohn, L.C. Cantley, and S.P. Gygi. 2004. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl. Acad. Sci. USA. 101:12130-12135.
2. Bekker-Jensen, S., C. Lukas, R. Kitagawa, F. Melander, M.B. Kastan, J. Bartek, and J. Lukas. 2006. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173:195-206.
3. Bekker-Jensen, S., K. Fugger, J.R. Danielsen, I. Gromova, M. Sehested, J. Celis, J. Bartek, J. Lukas, and N. Mailand. 2007. Human Xip1 (C2orf13) is a novel regulator of cellular responses to DNA strand breaks. J. Biol. Chem. 282:19638-19643.
4. Bhaskara, V., A. Dupre, B. Lengsfeld, B.B. Hopkins, A. Chan, J.H. Lee, X. Zhang, J. Gautier, V. Zakian, and T.T. Paull. 2007. Rad50 adenylate kinase activity regulates DNA tethering by Mre11/Rad50 complexes. Mol. Cell. 25:647-661.
5. Burma, S., B.P. Chen, M. Murphy, A. Kurimasa, and D.J. Chen. 2001. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276:42462-42467.
6. Celeste, A., O. Fernandez-Capetillo, M.J. Kruhlak, D.R. Pilch, D.W. Staudt, A. Lee, R.F. Bonner, W.M. Bonner, and A. Nussenzweig. 2003. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5:675-679.
7. Cerosaletti, K.M., and P. Concannon. 2003. Nibrin forkhead-associated domain and breast cancer C-terminal domain are both required for nuclear focus formation and phosphorylation. J. Biol. Chem. 278:21944-21951.
8. Costanzo, V., T. Paull, M. Gottesman, and J. Gautier. 2004. Mre11 assembles linear DNA fragments into DNA damage signaling complexes. PLoS Biol. 2: E110.
9. D' Amours, D., and S.P. Jackson. 2002. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3:317-327.
10. Difilippantonio, S., A. Celeste, O. Fernandez-Capetillo, H.T. Chen, B. Reina San Martin, F. Van Laethem, Y.P. Yang, G.V. Petukhova, M. Eckhaus, L. Feigenbaum, et al. 2005. Role of Nbs1 in the activation of the Atm kinase revealed in humanized mouse models. Nat. Cell Biol. 7:675-685.
11. Difilippantonio, S., A. Celeste, M.J. Kruhlak, Y. Lee, M.J. Difilippantonio, L. Feigenbaum, S.P. Jackson, P.J. McKinnon, and A. Nussenzweig. 2007. Distinct domains in Nbs1 regulate irradiation-induced checkpoints and apoptosis. J. Exp. Med. 204:1003-1011.
12. Durocher, D., and S.P. Jackson. 2002. The FHA domain. FEBS Lett. 513:58-66.
13. Falck, J., J. Coates, and S.P. Jackson. 2005. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature. 434:605-611.
14. Fernandez-Capetillo, O., A. Lee, M. Nussenzweig, and A. Nussenzweig. 2004. H2AX: the histone guardian of the genome. DNA Repair (Amst.). 3:959-967.
15. Glover, J.N., R.S. Williams, and M.S. Lee. 2004. Interactions between BRCT repeats and phosphoproteins: tangled up in two. Trends Biochem. Sci. 29:579-585.
16. Goldberg, M., M. Stucki, J. Falck, D. D' Amours, D. Rahman, D. Pappin, J. Bartek, and S.P. Jackson. 2003. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature. 421:952-956.
17. Horejsi, Z., J. Falck, C.J. Bakkenist, M.B. Kastan, J. Lukas, and J. Bartek. 2004. Distinct functional domains of Nbs1 modulate the timing and magnitude of ATM activation after low doses of ionizing radiation. Oncogene. 23:3122-3127.
18. Jazayeri, A., J. Falck, C. Lukas, J. Bartek, G.C. Smith, J. Lukas, and S.P. Jackson. 2006. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8:37-45.
19. Jowsey, P., N.A. Morrice, C.J. Hastie, H. McLauchlan, R. Toth, and J. Rouse. 2007. Characterisation of the sites of DNA damage-induced 53BP1 phosphorylation catalysed by ATM and ATR. DNA Repair (Amst.). 6:1536-1544.
20. Kobayashi, J., H. Tauchi, S. Sakamoto, A. Nakamura, K. Morishima, S. Matsuura, T. Kobayashi, K. Tamai, K. Tanimoto, and K. Komatsu. 2002. NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr. Biol. 12:1846-1851.
21. Koch, C.A., R. Agyei, S. Galicia, P. Metalnikov, P. O' Donnell, A. Starostine, M. Weinfeld, and D. Durocher. 2004. Xrcc4 physically links DNA end processing by polynucleotide kinase to DNA ligation by DNA ligase IV. EMBO J. 23:3874-3885.
22. Lee, J.H., and T.T. Paull. 2005. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science. 308:551-554.
23. Lee, J.H., B. Xu, C.H. Lee, J.Y. Ahn, M.S. Song, H. Lee, C.E. Canman, J.S. Lee, M.B. Kastan, and D.S. Lim. 2003. Distinct functions of Nijmegen breakage syndrome in ataxia telangiectasia mutated-dependent responses to DNA damage. Mol. Cancer Res. 1:674-681.
24. Loizou, J.I., S.F. El-Khamisy, A. Zlatanou, D.J. Moore, D.W. Chan, J. Qin, S. Sarno, F. Meggio, L.A. Pinna, and K.W. Caldecott. 2004. The protein kinase CK2 facilitates repair of chromosomal DNA single-strand breaks. Cell. 117:17-28.
25. Lou, Z., K. Minter-Dykhouse, S. Franco, M. Gostissa, M.A. Rivera, A. Celeste, J.P. Manis, J. van Deursen, A. Nussenzweig, T.T. Paull, et al. 2006. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell. 21:187-200.
26. Lukas, C., F. Melander, M. Stucki, J. Falck, S. Bekker-Jensen, M. Goldberg, Y. Lerenthal, S.P. Jackson, J. Bartek, and J. Lukas. 2004. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 23:2674-2683.
27. Luo, H., D.W. Chan, T. Yang, M. Rodriguez, B.P. Chen, M. Leng, J.J. Mu, D. Chen, Z. Songyang, Y. Wang, and J. Qin. 2004. A new XRCC1-containing complex and its role in cellular survival of methyl methanesulfonate treatment. Mol. Cell. Biol. 24:8356-8365.
28. Maser, R.S., K.J. Monsen, B.E. Nelms, and J.H. Petrini. 1997. hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks. Mol. Cell. Biol. 17:6087-6096.
29. Matsuoka, S., B.A. Ballif, A. Smogorzewska, E.R. McDonald III, K.E. Hurov, J. Luo, C.E. Bakalarski, Z. Zhao, N. Solimini, Y. Lerenthal, et al. 2007. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science. 316:1160-1166.
30. Melander, F., S. Bekker-Jensen, J. Falck, J. Bartek, N. Mailand, and J. Lukas. 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.
31. Olsen, J.V., B. Blagoev, F. Gnad, B. Macek, C. Kumar, P. Mortensen, and M. Mann. 2006. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell. 127:635-648.
32. Stewart, G.S., B. Wang, C.R. Bignell, A.M.R. Taylor, and S.J. Elledge. 2003. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature. 421:961-966.
33. Stracker, T.H., J.W. Theunissen, M. Morales, and J.H. Petrini. 2004. The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA Repair (Amst.). 3:845-854.
34. Stracker, T.H., M. Morales, S.S. Couto, H. Hussein, and J.H. Petrini. 2007. The carboxy terminus of NBS1 is required for induction of apoptosis by the MRE11 complex. Nature. 447:218-221.
35. Stucki, M., and S.P. Jackson. 2004. MDC1/NFBD1: a key regulator of the DNA damage response in higher eukaryotes. DNA Repair (Amst.). 3:953-957.
36. Stucki, M., and S.P. Jackson. 2006. gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amst.). 5:534-543.
37. Stucki, M., J.A. Clapperton, D. Mohammad, M.B. Yaffe, S.J. Smerdon, and S.P. Jackson. 2005. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell. 123:1213-1226.
38. Villen, J., S.A. Beausoleil, S.A. Gerber, and S.P. Gygi. 2007. Large-scale phosphorylation analysis of mouse liver. Proc. Natl. Acad. Sci. USA. 104:1488-1493.
39. Williams, R.S., J.S. Williams, and J.A. Tainer. 2007. Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chromatin template. Biochem. Cell Biol. 85:509-520.
40. Williamson, B.L., J. Marchese, and N. Morrice. 2006. Automated identification and quantification of protein phosphorylation sites by LC/MS on a hybrid triple quadrupole linear ion trap mass spectrometer. Mol. Cell. Proteomics. 5:337-346.
41. Yaffe, M.B., G.G. Leparc, J. Lai, T. Obata, S. Volinia, and L.C. Cantley. 2001. A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat. Biotechnol. 19:348-353.
42. Zhao, S., W. Renthal, and E.Y. Lee. 2002. Functional analysis of FHA and BRCT domains of NBS1 in chromatin association and DNA damage responses. Nucleic Acids Res. 30:4815-4822.
43. Zhou, B.B., and S.J. Elledge. 2000. The DNA damage response: putting checkpoints in perspective. Nature. 408:433-439.