Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response

Journal of Cell Biology

Volumn 186, Issue 6, 2009, Pages 835-847

  Marteijn, Jurgen A ^a   Bekker Jensen, Simon ^b   Mailand, Niels ^b   Lans, Hannes ^a   Schwertman, Petra ^a   Gourdin, Audrey M ^a   Dantuma, Nico P ^c   Lukas, Jiri ^b   Vermeulen, Wim ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; GREEN FLUORESCENT PROTEIN; HISTONE H2A; HISTONE H2AX; PROTEIN MDC1; PROTEIN RNF8; SCAFFOLD PROTEIN; SMALL INTERFERING RNA; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME 13; UNCLASSIFIED DRUG; ATR PROTEIN, HUMAN; BRCA1 PROTEIN; BRCA1 PROTEIN, HUMAN; CELL CYCLE PROTEIN; DNA; DNA BINDING PROTEIN; HISTONE; HYBRID PROTEIN; MDC1 PROTEIN, HUMAN; NUCLEAR PROTEIN; PROTEIN SERINE THREONINE KINASE; RNF8 PROTEIN, HUMAN; SIGNAL PEPTIDE; TP53BP1 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN; UBE2N PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME; XPC PROTEIN, HUMAN;

ARTICLE; CELL SURVIVAL; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; EXCISION REPAIR; FIBROBLAST; FLUORESCENCE ACTIVATED CELL SORTER; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; UBIQUITINATION; ULTRAVIOLET IRRADIATION; WESTERN BLOTTING; GENETIC EPIGENESIS; GENETIC TRANSFECTION; GENETICS; METABOLISM; PROTEIN PROCESSING; RADIATION EXPOSURE; RADIATION RESPONSE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME; ULTRAVIOLET RADIATION;

ATAXIA TELANGIECTASIA;

BRCA1 PROTEIN; CELL CYCLE PROTEINS; DNA; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, RADIATION; EPIGENESIS, GENETIC; HELA CELLS; HISTONES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NUCLEAR PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANS-ACTIVATORS; TRANSFECTION; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION; ULTRAVIOLET RAYS;

EID: 70349944658     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200902150     Document Type: Article

References (60)

1. Abraham, R.T. 2004. PI 3-kinase related kinases: 'big' players in stress-induced signaling pathways. DNA Repair (Amst.). 3:883-887. doi:10.1016/j.dnarep.2004.04.002
2. Baarends, W.M., E. Wassenaar, R. van der Laan, J. Hoogerbrugge, E. Sleddens-Linkels, J.H. Hoeijmakers, P. de Boer, and J.A. Grootegoed. 2005. Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis. Mol. Cell. Biol. 25:1041-1053. doi:10.1128/MCB.25.3.1041-1053. 2005
3. 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. doi:10.1083/jcb.200510130
4. Bennett, E.J., and J.W. Harper. 2008. DNA damage: ubiquitin marks the spot. Nat. Struct. Mol. Biol. 15:20-22. doi:10.1038/nsmb0108-20
5. Bergink, S., F.A. Salomons, D. Hoogstraten, T.A. Groothuis, H. de Waard, J. Wu, L. Yuan, E. Citterio, A.B. Houtsmuller, J. Neefjes, et al. 2006. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev. 20:1343-1352. doi:10.1101/gad.373706
6. Choudhury, A.D., H. Xu, and R. Baer. 2004. Ubiquitination and proteasomal degradation of the BRCA1 tumor suppressor is regulated during cell cycle progression. J. Biol. Chem. 279:33909-33918. doi:10.1074/jbc.M403646200
7. Cortez, D., S. Guntuku, J. Qin, and S.J. Elledge. 2001. ATR and ATRIP: partners in checkpoint signaling. Science. 294:1713-1716. doi:10.1126/science.1065521
8. Dantuma, N.P., T.A. Groothuis, F.A. Salomons, and J. Neefjes. 2006. A dynamic ubiquitin equilibrium couples proteasomal activity to chromatin remodeling. J. Cell Biol. 173:19-26. doi:10.1083/jcb.200510071
9. Dinant, C., M. de Jager, J. Essers, W.A. van Cappellen, R. Kanaar, A.B. Houtsmuller, and W. Vermeulen. 2007. Activation of multiple DNA repair pathways by sub-nuclear damage induction methods. J. Cell Sci. 120:2731-2740. doi:10.1242/jcs.004523
10. Dinant, C., A.B. Houtsmuller, and W. Vermeulen. 2008. Chromatin structure and DNA damage repair. Epigenetics Chromatin. 1:9. doi:10.1186/1756- 8935-1-9
11. 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. doi:10.1038/nature03442
12. Fang, S., and A.M. Weissman. 2004. A field guide to ubiquitylation. Cell. Mol. Life Sci. 61:1546-1561. doi:10.1007/s00018-004-4129-5
13. Giannattasio, M., F. Lazzaro, M.P. Longhese, P. Plevani, and M. Muzi-Falconi. 2004. Physical and functional interactions between nucleotide excision repair and DNA damage checkpoint. EMBO J. 23:429-438. doi:10.1038/sj.emboj.7600051
14. Giannattasio, M., F. Lazzaro, P. Plevani, and M. Muzi-Falconi. 2005. The DNA damage checkpoint response requires histone H2B ubiquitination by Rad6-Bre1 and H3 methylation by Dot1. J. Biol. Chem. 280:9879-9886. doi:10.1074/jbc.M414453200
15. Giglia-Mari, G., C. Miquel, A.F. Theil, P.O. Mari, D. Hoogstraten, J.M. Ng, C. Dinant, J.H. Hoeijmakers, and W. Vermeulen. 2006. Dynamic interaction of TTDA with TFIIH is stabilized by nucleotide excision repair in living cells. PLoS Biol. 4:e156. doi:10.1371/journal.pbio.0040156
16. Gillet, L.C., and O.D. Schärer. 2006. Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem. Rev. 106:253-276. doi:10.1021/cr040483f
17. Groothuis, T.A., N.P. Dantuma, J. Neefjes, and F.A. Salomons. 2006. Ubiquitin crosstalk connecting cellular processes. Cell Div. 1:21. doi:10.1186/1747-1028-1-21
18. Hammet, A., B.L. Pike, C.J. McNees, L.A. Conlan, N. Tenis, and J. Heierhorst. 2003. FHA domains as phospho-threonine binding modules in cell signaling. IUBMB Life. 55:23-27. doi:10.1080/1521654031000070636
19. Hanasoge, S., and M. Ljungman. 2007. H2AX phosphorylation after UV irradiation is triggered by DNA repair intermediates and is mediated by the ATR kinase. Carcinogenesis. 28:2298-2304. doi:10.1093/carcin/bgm157
20. Harper, J.W., and S.J. Elledge. 2007. The DNA damage response: ten years after. Mol. Cell. 28:739-745. doi:10.1016/j.molcel.2007.11.015
21. Hoeijmakers, J.H. 2001. Genome maintenance mechanisms for preventing cancer. Nature. 411:366-374. doi:10.1038/35077232
22. Hoogstraten, D., S. Bergink, J.M. Ng, V.H. Verbiest, M.S. Luijsterburg, B. Geverts, A. Raams, C. Dinant, J.H. Hoeijmakers, W. Vermeulen, and A.B. Houtsmuller. 2008. Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC. J. Cell Sci. 121:2850-2859. doi:10.1242/jcs.031708
23. Houtsmuller, A.B., and W. Vermeulen. 2001. Macromolecular dynamics in living cell nuclei revealed by fluorescence redistribution after photobleaching. Histochem. Cell Biol. 115:13-21.
24. Huen, M.S., R. Grant, I. Manke, K. Minn, X. Yu, M.B. Yaffe, and J. Chen. 2007. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell. 131:901-914. doi:10.1016/j.cell.2007. 09.041
25. Ikura, T., S. Tashiro, A. Kakino, H. Shima, N. Jacob, R. Amunugama, K. Yoder, S. Izumi, I. Kuraoka, K. Tanaka, et al. 2007. DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell. Biol. 27:7028-7040. doi:10.1128/MCB.00579-07
26. Ito, K., S. Adachi, R. Iwakami, H. Yasuda, Y. Muto, N. Seki, and Y. Okano. 2001. N-Terminally extended human ubiquitin-conjugating enzymes (E2s) mediate the ubiquitination of RING-finger proteins, ARA54 and RNF8. Eur. J. Biochem. 268:2725-2732. doi:10.1046/j.1432-1327.2001.02169.x
27. Jans, J., W. Schul, Y.G. Sert, Y. Rijksen, H. Rebel, A.P. Eker, S. Nakajima, H. van Steeg, F.R. de Gruijl, A. Yasui, et al. 2005. Powerful skin cancer protection by a CPD-photolyase transgene. Curr. Biol. 15:105-115. doi:10.1016/j.cub.2005.01.001
28. 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. doi:10.1016/j.dnarep.2007.04.011
29. Kim, H., and J. Chen. 2008. New players in the BRCA1-mediated DNA damage responsive pathway. Mol. Cells. 25:457-461.
30. Kim, H., J. Chen, and X. Yu. 2007. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science. 316:1202-1205. doi:10.1126/science.1139621
31. Kolas, N.K., J.R. Chapman, S. Nakada, J. Ylanko, R. Chahwan, F.D. Sweeney, S. Panier, M. Mendez, J. Wildenhain, T.M. Thomson, et al. 2007. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science. 318:1637-1640. doi:10.1126/science.1150034
32. Luijsterburg, M.S., J. Goedhart, J. Moser, H. Kool, B. Geverts, A.B. Houtsmuller, L.H. Mullenders, W. Vermeulen, and R. van Driel. 2007. Dynamic in vivo interaction of DDB2 E3 ubiquitin ligase with UV-damaged DNA is independent of damage-recognition protein XPC. J. Cell Sci. 120:2706-2716. doi:10.1242/jcs.008367
33. Mailand, N., S. Bekker-Jensen, H. Faustrup, F. Melander, J. Bartek, C. Lukas, and J. Lukas. 2007. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell. 131:887-900. doi:10.1016/j.cell.2007.09.040
34. Marteijn, J.A., L.T. van der Meer, L. van Emst, S. van Reijmersdal, W. Wissink, T. de Witte, J.H. Jansen, and B.A. Van der Reijden. 2007. Gfi1 ubiquitination and proteasomal degradation is inhibited by the ubiquitin ligase Triad1. Blood. 110:3128-3135. doi:10.1182/blood-2006-11-058602
35. Matsumoto, M., K. Yaginuma, A. Igarashi, M. Imura, M. Hasegawa, K. Iwabuchi, T. Date, T. Mori, K. Ishizaki, K. Yamashita, et al. 2007. Perturbed gap-filling synthesis in nucleotide excision repair causes histone H2AX phosphorylation in human quiescent cells. J. Cell Sci. 120:1104-1112. doi:10.1242/jcs.03391
36. Mitchell, D.L., C.A. Haipek, and J.M. Clarkson. 1985. (6-4)Photoproducts are removed from the DNA of UV-irradiated mammalian cells more efficiently than cyclobutane pyrimidine dimers. Mutat. Res. 143:109-112.
37. Moné, M.J., M. Volker, O. Nikaido, L.H. Mullenders, A.A. van Zeeland, P.J. Verschure, E.M. Manders, and R. van Driel. 2001. Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO Rep. 2:1013-1017. doi:10.1093/embo-reports/kve224
38. Nicassio, F., N. Corrado, J.H. Vissers, L.B. Areces, S. Bergink, J.A. Marteijn, B. Geverts, A.B. Houtsmuller, W. Vermeulen, P.P. Di Fiore, and E. Citterio. 2007. Human USP3 is a chromatin modifier required for S phase progression and genome stability. Curr. Biol. 17:1972-1977. doi:10.1016/j.cub.2007.10.034
39. Niida, H., and M. Nakanishi. 2006. DNA damage checkpoints in mammals. Mutagenesis. 21:3-9. doi:10.1093/mutage/gei063
40. O'Driscoll, M., V.L. Ruiz-Perez, C.G. Woods, P.A. Jeggo, and J.A. Goodship. 2003. A splicing mutation affecting expression of ataxia- telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat. Genet. 33:497-501. doi:10.1038/ng1129
41. Pickart, C.M. 2000. Ubiquitin in chains. Trends Biochem. Sci. 25:544-548. doi:10.1016/S0968-0004(00)01681-9
42. Plans, V., J. Scheper, M. Soler, N. Loukili, Y. Okano, and T.M. Thomson. 2006. The RING finger protein RNF8 recruits UBC13 for lysine 63-based self polyubiquitylation. J. Cell. Biochem. 97:572-582. doi:10.1002/jcb.20587
43. Rademakers, S., M. Volker, D. Hoogstraten, A.L. Nigg, M.J. Moné, A.A. Van Zeeland, J.H. Hoeijmakers, A.B. Houtsmuller, and W. Vermeulen. 2003. Xeroderma pigmentosum group A protein loads as a separate factor onto DNA lesions. Mol. Cell. Biol. 23:5755-5767. doi:10.1128/MCB.23.16.5755-5767. 2003
44. Robzyk, K., J. Recht, and M.A. Osley. 2000. Rad6-dependent ubiquitination of histone H2B in yeast. Science. 287:501-504. doi:10.1126/science.287. 5452.501
45. Rogakou, E.P., D.R. Pilch, A.H. Orr, V.S. Ivanova, and W.M. Bonner. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273:5858-5868. doi:10.1074/jbc.273.10.5858
46. Sakasai, R., and R. Tibbetts. 2008. RNF8-dependent and RNF8-independent regulation of 53BP1 in response to DNA damage. J. Biol. Chem. 283:13549-13555. doi:10.1074/jbc.M710197200
47. Salic, A., and T.J. Mitchison. 2008. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl. Acad. Sci. USA. 105:2415-2420. doi:10.1073/pnas.0712168105
48. Shechter, D., V. Costanzo, and J. Gautier. 2004. Regulation of DNA replication by ATR: signaling in response to DNA intermediates. DNA Repair (Amst.). 3:901-908. doi:10.1016/j.dnarep.2004.03.020
49. Sobhian, B., G. Shao, D.R. Lilli, A.C. Culhane, L.A. Moreau, B. Xia, D.M. Livingston, and R.A. Greenberg. 2007. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science. 316:1198-1202. doi:10.1126/science.1139516
50. Stewart, G.S., B. Wang, C.R. Bignell, A.M. Taylor, and S.J. Elledge. 2003. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature. 421:961-966. doi:10.1038/nature01446
51. Stiff, T., S.A. Walker, K. Cerosaletti, A.A. Goodarzi, E. Petermann, P. Concannon, M. O'Driscoll, and P.A. Jeggo. 2006. ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J. 25:5775-5782. doi:10.1038/sj.emboj.7601446
52. Stiff, T., K. Cerosaletti, P. Concannon, M. O'Driscoll, and P.A. Jeggo. 2008. Replication independent ATR signalling leads to G2/M arrest requiring Nbs1, 53BP1 and MDC1. Hum. Mol. Genet. 17:3247-3253. doi:10.1093/hmg/ ddn220
53. 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. doi:10.1016/j.dnarep.2006.01.012
54. 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. doi:10.1016/j.cell.2005.09.038
55. Vermeulen, W., P. Osseweijer, A.J. de Jonge, and J.H. Hoeijmakers. 1986. Transient correction of excision repair defects in fibroblasts of 9 xeroderma pigmentosum complementation groups by microinjection of crude human cell extracts. Mutat. Res. 165:199-206.
56. Wang, H., L. Zhai, J. Xu, H.Y. Joo, S. Jackson, H. Erdjument-Bromage, P. Tempst, Y. Xiong, and Y. Zhang. 2006. Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol. Cell. 22:383-394. doi:10.1016/j.molcel.2006.03.035
57. Wang, B., S. Matsuoka, B.A. Ballif, D. Zhang, A. Smogorzewska, S.P. Gygi, and S.J. Elledge. 2007. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science. 316:1194-1198. doi:10.1126/science.1139476
58. Yan, J., X.P. Yang, Y.S. Kim, and A.M. Jetten. 2008. RAP80 responds to DNA damage induced by both ionizing radiation and UV irradiation and is phosphorylated at Ser 205. Cancer Res. 68:4269-4276. doi:10.1158/0008- 5472.CAN-07-5950
59. Zhu, Q., G. Wani, H.H. Arab, M.A. El-Mahdy, A. Ray, and A.A. Wani. 2009. Chromatin restoration following nucleotide excision repair involves the incorporation of ubiquitinated H2A at damaged genomic sites. DNA Repair (Amst.). 8:262-273. doi:10.1016/j.dnarep.2008.11.007
60. Zou, L., and S.J. Elledge. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science. 300:1542-1548. doi:10.1126/science.1083430