Recruitment of proteins to DNA double-strand breaks: MDC1 directly recruits RAP80

Cell Cycle

Volumn 10, Issue 17, 2011, Pages 2850-2857

  Strauss, Carmit ^a   Goldberg, Michal ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

DNA damage response; DNA double strand break; Focus formation; MDC1; RAP80

Indexed keywords

ARGININE; BRCA1 PROTEIN; CELL PROTEIN; PROTEIN MDC 1; PROTEIN RAP 80; RAP PROTEIN; UNCLASSIFIED DRUG;

DOUBLE STRANDED DNA BREAK; HELA CELL; MUTATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW;

EID: 80052414082     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.17.17341     Document Type: Review

References (52)

1. Riches L.C., Lynch A.M., Gooderham NJ. Early Events in the Mammalian Response to DNA Double- Strand Breaks. Mutagenesis 2008; 23:331-9; PMID:18644834; DOI:10.1093/mutage/gen039.
2. Harper J.W., Elledge SJ. The DNA damage response: ten years after. Mol Cell 2007; 28:739- 45; PMID:18082599; DOI:10.1016/j.molcel. 2007.11.015.
3. Bartek J., Lukas J. DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 2007; 19:238-45; PMID:17303408; DOI:10.1016/j.ceb.2007.02.009.
4. Ayoub N., Jeyasekharan A.D., Bernal J.A., Venkitaraman AR. Paving the way for H2AX phosphorylation: chromatin changes in the DNA damage response. Cell Cycle 2009; 8:1494-500; PMID:19377276; DOI:10.4161/cc.8.10.8501.
5. De Jager M., Van Noort J., Van Gent D.C., Dekker C., Kanaar R., Wyman C. Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol Cell 2001; 8:1129-35; PMID:11741547; DOI:10.1016/ S1097-2765(01)00381-1.
6. 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; PMID:14532133; DOI:10.1093/emboj/cdg541.
7. Lee J.H., Paull TT. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 2004; 304:93-6; PMID:15064416; DOI:10.1126/science.1091496.
8. Fernandez-Capetillo O., Lee A., Nussenzweig M., Nussenzweig A. H2AX: the histone guardian of the genome. DNA Repair 2004; 3:959-67; PMID:15279782; DOI:10.1016/j. dnarep.2004.03.024.
9. Lee M.S., Edwards R.A., Thede GL. Glover JNm. Structure of the BRCT repeat domain of MDC1 and its specificity for the free COOH-terminal end of the gamma-H2AX histone tail. J Biol Chem 2005; 280:32053-6; PMID:16049003; DOI:10.1074/jbc. C500273200.
10. Stucki M., Clapperton J.A., Mohammad D., Yaffe M.B., Smerdon S.J., Jackson SP. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 2005; 123:1213-26; PMID:16377563; DOI:10.1016/j. cell.2005.09.038.
11. Sobhian B., Shao G., Lilli D.R., Culhane A.C., Moreau L.A., Xia B., et al. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 2007; 316:1198-202; PMID:17525341; DOI:10.1126/science.1139516.
12. Kim H., Chen J., Yu X. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 2007; 316:1202-5; PMID:17525342; DOI:10.1126/science.1139621.
13. Wang B., Matsuoka S., Ballif B.A., Zhang D., Smogorzewska A., Gygi S.P., et al. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 2007; 316:1194-8; PMID:17525340; DOI:10.1126/science. 1139476.
14. Coster G., Goldberg M. The cellular response to DNA damage: A focus on MDC1 and its interacting proteins. Nucleus 2010; 1:166-178; PMID:21326949.
15. Stewart GS. Solving the RIDDLE of 53BP1 recruitment to sites of damage. Cell Cycle 2009; 8:1532-8; PMID:19372751; DOI:10.4161/cc.8.10.8351.
16. Panier S., Durocher D. Regulatory ubiquitylation in response to DNA double-strand breaks. DNA Repair 2009; 8:436-43; PMID:19230794; DOI:10.1016/j. dnarep.2009.01.013.
17. Eliezer Y., Argaman L., Rhie A., Doherty A.J., Goldberg M. The direct interaction between 53BP1 and MDC1 is required for the recruitment of 53BP1 to sites of damage. J Biol Chem 2009; 284:426-35; PMID:18986980; DOI:10.1074/jbc.M807375200.
18. Stewart G.S., Wang B., Bignell C.R., Taylor A.M., Elledge SJ. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 2003; 421:961-6; PMID:12607005; DOI:10.1038/nature01446.
19. Xie A., Hartlerode A., Stucki M., Odate S., Puget N., Kwok A., et al. Distinct roles of chromatinassociated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol Cell 2007; 28:1045-57; PMID:18158901; DOI:10.1016/j.molcel. 2007.12.005.
20. Zhang J., Ma Z., Treszezamsky A., Powell SN. MDC1 interacts with Rad51 and facilitates homologous recombination. Nat Struct Mol Biol 2005; 12:902-9; PMID:16186822; DOI:10.1038/nsmb991.
21. Lou Z., Chen B.P., Asaithamby A., Minter-Dykhouse K., Chen D.J., Chen J. MDC1 regulates DNA-PK autophosphorylation in response to DNA damage. J Biol Chem 2004; 279:46359-62; PMID:15377652; DOI:10.1074/jbc.C400375200.
22. Strauss C., Halevy T., Macarov M., Argaman L., Goldberg M. MDC1 is ubiquitylated on its tandem BRCT domain and directly binds RAP80 in a UBC13-dependent manner. DNA Repair 2011; 10:806-14; PMID:21622030; DOI:10.1016/j. dnarep.2011.04.016.
23. Liu Z., Wu J., Yu X. CCDC98 targets BRCA1 to DNA damage sites. Nat Struct Mol Biol 2007; 14:716-20; PMID:17643121; DOI:10.1038/nsmb1279.
24. Xu B., Kim S., Kastan MB. Involvement of Brca1 in S-phase and G(2)-phase checkpoints after ionizing irradiation. Mol Cell Biol 2001; 21:3445-50; PMID:11313470; DOI:10.1128/MCB.21.10.3445- 3450.2001.
25. Venkitaraman AR. Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 2002; 108:171-82; PMID:11832208; DOI:10.1016/S0092- 8674(02)00615-3.
26. Nikkilä J., Coleman K.A., Morrissey D., Pylkas K., Erkko H., Messick T.E., et al. Familial breast cancer screening reveals an alteration in the RAP80 UIM domain that impairs DNA damage response function. Oncogene 2009; 28:1843-52; PMID:19305427; DOI:10.1038/onc.2009.33.
27. Hiom K. Coping with DNA double strand breaks. DNA Repair 2010; 9:1256-63; PMID:21115283; DOI:10.1016/j.dnarep.2010.09.018.
28. Hu Y., Scully R., Sobhian B., Xie A., Shestakova E., Livingston DM. RAP80-directed tuning of BRCA1 homologous recombination function at ionizing radiation-induced nuclear foci. Genes Dev 2011; 25:685- 700; PMID:21406551; DOI:10.1101/gad.2011011.
29. Coleman K.A., Greenberg RA. The BRCA1-RAP80 complex regulates DNA repair mechanism utilization by restricting end resection. J Biol Chem 2011; 286:13669-80; PMID:21335604; DOI:10.1074/jbc. M110.213728.
30. Ohta T., Sato K., Wu W. The BRCA1 ubiquitin ligase and homologous recombination repair. FEBS Lett 2011; In Press; PMID:21570976; DOI:10.1016/j. febslet.2011.05.005.
31. Iwabuchi K., Basu B.P., Kysela B., Kurihara T., Shibata M., Guan D., et al. Potential role for 53BP1 in DNA end-joining repair through direct interaction with DNA. J Biol Chem 2003; 278:36487-95; PMID:12824158; DOI:10.1074/jbc.M304066200.
32. Bothmer A., Robbiani D.F., Di Virgilio M., Bunting S.F., Klein I.A., Feldhahn N., et al. Regulation of DNA end joining, resection and immunoglobulin class switch recombination by 53BP1. Mol Cell 2011; 42:319-29; PMID:21549309; DOI:10.1016/j.molcel. 2011.03.019.
33. 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; PMID:15758953; DOI:10.1038/nature03442.
34. Lou Z., Minter-Dykhouse K., Franco S., Gostissa M., Rivera M.A., Celeste A., et al. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol Cell 2006; 21:187-200; PMID:16427009; DOI:10.1016/j.molcel.2005.11.025.
35. Huen M.S., Grant R., Manke I., Minn K., Yu X., Yaffe M.B., et al. RNF8 Transduces the DNA-Damage Signal via Histone Ubiquitylation and Checkpoint Protein Assembly. Cell 2007; 131:901-14; PMID:18001825; DOI:10.1016/j.cell.2007. 09.041.
36. Kolas N.K., Chapman J.R., Nakada S., Ylanko J., Chahwan R., Sweeney F.D., et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 2007; 318:1637-40; PMID:18006705; DOI:10.1126/science.1150034.
37. Stewart G.S., Panier S., Townsend K., Al-Hakim A.K., Kolas N.K., Miller E.S., et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 2009; 136:420-34; PMID:19203578; DOI:10.1016/j. cell.2008.12.042.
38. Doil C., Mailand N., Bekker-Jensen S., Menard P., Larsen D.H., Pepperkok R., et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 2009; 136:435-46; PMID:19203579; DOI:10.1016/j.cell.2008.12.041.
39. Spycher C., Miller E.S., Townsend K., Pavic L., Morrice N.A., Janscak P., et al. Constitutive phosphorylation of MDC1 physically links the MRE11-RAD50- NBS1 complex to damaged chromatin. J Cell Biol 2008; 181:227-40; PMID:18411308; DOI:10.1083/ jcb.200709008.
40. Chapman J.R., Jackson SP. Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep 2008; 9:795-801; PMID:18583988; DOI:10.1038/embor.2008.103.
41. Luo K., Yuan J., Lou Z. Oligomerization of MDC1 is important for proper DNA damage response. J Biol Chem 2011.
42. Lukas C., Melander F., Stucki M., Falck J, Bekker- Jensen S, Goldberg M, et al. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J 2004; 23:2674-83; PMID:15201865; DOI:10.1038/ sj.emboj.7600269.
43. Melander F., Bekker-Jensen S., Falck J., Bartek J., Mailand N., Lukas J. Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J Cell Biol 2008; 181:213-26; PMID:18411307; DOI:10.1083/ jcb.200708210.
44. Polo S.E., Jackson SP. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 2011; 25:409-33; PMID:21363960; DOI:10.1101/gad.2021311.
45. Bakkenist C.J., Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499-506; PMID:12556884; DOI:10.1038/nature01368.
46. Burma S., Chen B.P., Murphy M., Kurimasa A., Chen DJ. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 2001; 276:42462-7; PMID:11571274; DOI:10.1074/jbc. C100466200.
47. Mailand N., Bekker-Jensen S., Faustrup H., Melander F., Bartek J., Lukas C., et al. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 2007; 131:887-900; PMID:18001824; DOI:10.1016/j.cell.2007.09.040.
48. Nelson G., Buhmann M., Von Zglinicki T. DNA damage foci in mitosis are devoid of 53BP1. Cell Cycle 2009; 8:3379-83; PMID:19806024; DOI:10.4161/cc.8.20. 9857.
49. Giunta S, Belotserkovskaya R, Jackson SP. DNA damage signaling in response to double-strand breaks during mitosis. J Cell Biol 2010; 190:197-207; PMID:20660628; DOI:10.1083/jcb.200911156.
50. Giunta S., Jackson SP. Give me a break, but not in mitosis: the mitotic DNA damage response marks DNA double-strand breaks with early signaling events. Cell Cycle 2011; 10:1215-21; PMID:21412056; DOI:10.4161/cc.10.8.15334.
51. Nakamura A.J., Rao V.A., Pommier Y., Bonner WM. The complexity of phosphorylated H2AX foci formation and DNA repair assembly at DNA double-strand breaks. Cell Cycle 2010; 9:389-97; PMID:20046100; DOI:10.4161/cc.9.2.10475.
52. Iliakis G. The anatomy and cell cycle evolution of DNA damage signaling and repair foci. Cell Cycle 2010; 9:444-5; PMID:20130450; DOI:10.4161/cc.9.3. 10731.