DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A

Genes and Development

Volumn 20, Issue 10, 2006, Pages 1343-1352

  Bergink, Steven ^a   Salomons, Florian A ^b   Hoogstraten, Deborah ^a,b   Groothuis, Tom A M ^d   De Waard, Harm ^a   Wu, Junxin ^b   Yuan, Li ^b   Citterio, Elisabetta ^c   Houtsmuller, Adriaan B ^a   Neefjes, Jacques ^d   Hoeijmakers, Jan H J ^a   Vermeulen, Wim ^a   Dantuma, Nico P ^b  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b KAROLINSKA INSTITUTE   (Sweden)

^c FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^d NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

ATR; Chromatin; DNA damage response; DNA repair; H2AX; Histone; Ubiquitin proteasome system

Indexed keywords

ATR PROTEIN; HISTONE H2A; PROTEASOME; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; EXCISION REPAIR; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; CELL NUCLEUS; CELLS, CULTURED; DNA; DNA DAMAGE; DNA REPAIR; HISTONES; HUMANS; MOLECULAR SEQUENCE DATA; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN; UBIQUITIN THIOLESTERASE; ULTRAVIOLET RAYS;

ATAXIA TELANGIECTASIA;

EID: 33646584518     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.373706     Document Type: Article

References (41)

1. Araki, M., Masutani, C., Takemura, M., Uchida, A., Sugasawa, K., Kondoh, J., Ohkuma, Y., and Hanaoka, F. 2001. Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair. J. Biol. Chem. 276: 18665-18672.
2. Brummelkamp, T.R., Bernards, R., and Agami, R. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296: 550-553.
3. Celeste, A., Petersen, S., Romanienko, P.J., Fernandez-Capetillo, O., Chen, H.T., Sedelnikova, O.A., Reina-San-Martin, B., Coppola, V., Meffre, E., Difilippantonio, M.J., et al. 2002. Genomic instability in mice lacking histone H2AX. Science 296: 922-927.
4. Citterio, E., Vermeulen, W., and Hoeijmakers, J.H. 2000. Transcriptional healing. Cell 101: 447-450.
5. Cleaver, J.E. 2005. Cancer in xeroderma pigmentosum and related disorders of DNA repair. Nat. Rev. Cancer 5: 564-573.
6. Dantuma, N.P., Groothuis, T.A. Salomons, F.A., and Neefjes, J. 2006. A dynamic ubiquitin equilibrium couples proteasomal activity to chromatin remodeling. J. Cell. Biol. 173: 19-26.
7. de Laat, W.L., Jaspers, N.G., and Hoeijmakers, J.H. 1999. Molecular mechanism of nucleotide excision repair. Genes & Dev. 13: 768-785.
8. de Napoles, M., Mermoud, J.E., Wakao, R., Tang, Y.A., Endoh, M., Appanah, R., Nesterova, T.B., Silva, J., Otte, A.P., Vidal, M., et al. 2004. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell 7: 663-676.
9. Essers, J., Theil, A.F., Baldeyron, C., van Cappellen, W.A., Houtsmuller, A.B., Kanaar, R., and Vermeulen, W. 2005. Nuclear dynamics of PCNA in DNA replication and repair. Mol. Cell. Biol. 25: 9350-9359.
10. Giancotti, V., Berlingieri, M.T., DiFiore, P.P., Fusco, A., Vecchio, G., and Crane-Robinson, C. 1985. Changes in nuclear proteins on transformation of rat epithelial thyroid cells by a murine sarcoma retrovirus. Cancer Res. 45: 6051-6057.
11. Giannattasio, M., Lazzaro, F., Plevani, P., and Muzi-Falconi, M. 2005. The DNA damage checkpoint response requires histone H2B ubiquitination by Rad6-Bre1 and H3 methylation by Dot1. J. Biol. Chem. 280: 9879-9886.
12. Glickman, M.H. and Ciechanover, A. 2002. The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol. Rev. 82: 373-428.
13. Green, C.M. and Almouzni, G. 2002. When repair meets chromatin. First in series on chromatin dynamics. EMBO Rep. 3: 28-33.
14. Hoege, C., Pfander, B., Moldovan, G.L., Pyrowolakis, G., and Jentsch, S. 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419: 135-141.
15. Hoeijmakers, J.H. 2001. Genome maintenance mechanisms for preventing cancer. Nature 411: 366-374.
16. Houtsmuller, A.B. and Vermeulen, W. 2001. Macromolecular dynamics in living cell nuclei revealed by fluorescence redistribution after photobleaching. Histochem. Cell Biol. 115: 13-21.
17. Jenuwein, T. and Allis, C.D. 2001. Translating the histone code. Science 293: 1074-1080.
18. Kannouche, P.L., Wing, J., and Lehmann, A.R. 2004. Interaction of human DNA polymerase eta with monoubiquitinated PCNA: A possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14: 491-500.
19. Kapetanaki, M.G., Guerrero-Santoro, J., Bisi, D.C., Hsieh, C.L., Rapic-Otrin, V., and Levine, A.S. 2006. The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc. Natl. Acad. Sci. 103: 2588-2593.
20. Katsumi, S., Kobayashi, N., Imoto, K., Nakagawa, A., Yamashina, Y., Muramatsu, T., Shirai, T., Miyagawa, S., Sugiura, S., Hanaoka, F., et al. 2001. In situ visualization of ultraviolet-light-induced DNA damage repair in locally irradiated human fibroblasts. J. Invest. Dermatol. 117: 1156-1161.
21. Leonhardt, H., Rahn, H.P., Weinzierl, P., Sporbert, A., Cremer, T., Zink, D., and Cardoso, M.C. 2000. Dynamics of DNA replication factories in living cells. J. Cell Biol. 149: 271-280.
22. Levinger, L. and Varshavsky, A. 1982. Selective arrangement of ubiquitinated and D1 protein-containing nucleosomes within the Drosophila genome. Cell 28: 375-385.
23. Masutani, C., Kusumoto, R., Yamada, A., Dohmae, N., Yokoi, M., Yuasa, M., Araki, M., Iwai, S., Takio, K., and Hanaoka, F. 1999. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature 399: 700-704.
24. Nickel, B.E. and Davie, J.R. 1989. Structure of polyubiquitinated histone H2A. Biochemistry 28: 964-968.
25. O'Driscoll, M., Ruiz-Perez, V.L., Woods, C.G., Jeggo, P.A., and Goodship, J.A. 2003. A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat. Genet. 33: 497-501.
26. Peterson, C.L. and Cote, J. 2004. Cellular machineries for chromosomal DNA repair. Genes & Dev. 18: 602-616.
27. Qian, S.B., Ott, D.E., Schubert, U., Bennink, J.R., and Yewdell, J.W. 2002. Fusion proteins with COOH-terminal ubiquitin are stable and maintain dual functionality in vivo. J. Biol. Chem. 277: 38818-38826.
28. Rademakers, S., Volker, M., Hoogstraten, D., Nigg, A.L., Mone, M.J., Van Zeeland, A.A., Hoeijmakers, J.H., Houtsmuller, A.B., and Vermeulen, W. 2003. Xeroderma pigmentosum group A protein loads as a separate factor onto DNA lesions. Mol. Cell. Biol. 23: 5755-5767.
29. Robzyk, K., Recht, J., and Osley, M.A. 2000. Rad6-dependent ubiquitination of histone H2B in yeast. Science 287: 501-504.
30. Rogakou, E.P., Pilch, D.R., Orr, A.H., Ivanova, V.S., and Bonner, W.M. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273: 5858-5868.
31. Shiloh, Y. 2003. ATM and related protein kinases: Safeguarding genome integrity. Nat. Rev. Cancer 3: 155-168.
32. Shroff, R., Arbel-Eden, A., Pilch, D., Ira, G., Bonner, W.M., Petrini, J.H., Haber, J.E., and Lichten, M. 2004. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14: 1703-1711.
33. Smerdon, M.J. 1991. DNA repair and the role of chromatin structure. Curr. Opin. Cell Biol. 3: 422-428.
34. Sugasawa, K., Ng, J.M., Masutani, C., Iwai, S., van der Spek, P.J., Eker, A.P., Hanaoka, F., Bootsma, D., and Hoeijmakers, J.H. 1998. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol. Cell 2: 223-232.
35. Sugasawa, K., Okuda, Y., Saijo, M., Nishi, R., Matsuda, N., Chu, G., Mori, T., Iwai, S., Tanaka, K., and Hanaoka, F. 2005. UV-induced ubiquitylation of XPC protein mediated by UVDDB-ubiquitin ligase complex. Cell 121: 387-400.
36. Thiriet, C. and Hayes, J.J. 2005. Chromatin in need of a fix: Phosphorylation of H2AX connects chromatin to DNA repair. Mol. Cell 18: 617-622.
37. Thrower, J.S., Hoffman, L., Rechsteiner, M., and Pickart, C.M. 2000. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19: 94-102.
38. Vidanes, G.M., Bonilla, C.Y., and Toczyski, D.P. 2005. Complicated tails: Histone modifications and the DNA damage response. Cell 121: 973-976.
39. Wang, H., Wang, L., Erdjument-Bromage, H., Vidal, M., Tempst, P., Jones, R.S., and Zhang, Y. 2004. Role of histone H2A ubiquitination in Polycomb silencing. Nature 431: 873-878.
40. Wang, Q.E., Wani, M.A., Chen, J., Zhu, Q., Wani, G., El-Mahdy, M.A., and Wani, A.A. 2005. Cellular ubiquitination and proteasomal functions positively modulate mammalian nucleotide excision repair. Mol. Carcinog. 42: 53-64.
41. Zhang, Y. 2003. Transcriptional regulation by histone ubiquitination and deubiquitination. Genes & Dev. 17: 2733-2740.