nature.com

Understanding nucleotide excision repair and its roles in cancer and ageing - Nature Reviews Molecular Cell Biology

  • ️Hoeijmakers, Jan H. J.
  • ️Mon Jun 23 2014
  • Gates, K. S. An overview of chemical processes that damage cellular DNA: spontaneous hydrolysis, alkylation, and reactions with radicals. Chem. Res. Toxicol. 22, 1747–1760 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swenberg, J. A. et al. Endogenous versus exogenous DNA adducts: their role in carcinogenesis, epidemiology, and risk assessment. Toxicol. Sci. 120, S130–145 (2011).

    Article  CAS  PubMed  Google Scholar 

  • Sale, J. E., Lehmann, A. R. & Woodgate, R. Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nature Rev. Mol. Cell Biol. 13, 141–152 (2012).

    Article  CAS  Google Scholar 

  • Jackson, S. P. & Bartek, J. The DNA-damage response in human biology and disease. Nature 461, 1071–1078 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoeijmakers, J. H. Genome maintenance mechanisms for preventing cancer. Nature 411, 366–374 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Masutani, C. et al. Purification and cloning of a nucleotide excision repair complex involving the xeroderma pigmentosum group C protein and a human homologue of yeast RAD23. EMBO J. 13, 1831–1843 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishi, R. et al. Centrin 2 stimulates nucleotide excision repair by interacting with xeroderma pigmentosum group C protein. Mol. Cell. Biol. 25, 5664–5674 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugasawa, K. et al. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol. Cell 2, 223–232 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Sugasawa, K. et al. A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 15, 507–521 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maillard, O., Camenisch, U., Clement, F. C., Blagoev, K. B. & Naegeli, H. DNA repair triggered by sensors of helical dynamics. Trends Biochem. Sci. 32, 494–499 (2007).

    Article  CAS  PubMed  Google Scholar 

  • Min, J. H. & Pavletich, N. P. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature 449, 570–575 (2007). Shows the crystal structure of Rad4, the yeast orthologue of XPC, bound to a DNA substrate that contains a small unpaired region. Rad4 recognizes the local destabilization of the DNA duplex, which is common to many structurally unrelated DNA lesions, and thus explains the ability of Rad4 and XPC to detect a myriad of lesions.

    Article  CAS  PubMed  Google Scholar 

  • Hoogstraten, D. et al. Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC. J. Cell Sci. 121, 2850–2859 (2008).

    Article  CAS  PubMed  Google Scholar 

  • Reardon, J. T. & Sancar, A. Recognition and repair of the cyclobutane thymine dimer, a major cause of skin cancers, by the human excision nuclease. Genes Dev. 17, 2539–2551 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chu, G. & Chang, E. Xeroderma pigmentosum group E cells lack a nuclear factor that binds to damaged DNA. Science 242, 564–567 (1988).

    Article  CAS  PubMed  Google Scholar 

  • Wakasugi, M. et al. DDB accumulates at DNA damage sites immediately after UV irradiation and directly stimulates nucleotide excision repair. J. Biol. Chem. 277, 1637–1640 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Scrima, A. et al. Structural basis of UV DNA-damage recognition by the DDB1 DDB2 complex. Cell 135, 1213–1223 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groisman, R. et al. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113, 357–367 (2003).

    Article  CAS  PubMed  Google Scholar 

  • Volker, M. et al. Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell 8, 213–224 (2001). Demonstrates, in response to localized UV damage, the sequential assembly of NER proteins and identifies XPC as the main initiator of GG-NER.

    Article  CAS  PubMed  Google Scholar 

  • Yokoi, M. et al. The xeroderma pigmentosum group C protein complex XPC HR23B plays an important role in the recruitment of transcription factor IIH to damaged DNA. J. Biol. Chem. 275, 9870–9875 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Riedl, T., Hanaoka, F. & Egly, J. M. The comings and goings of nucleotide excision repair factors on damaged DNA. EMBO J. 22, 5293–5303 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tapias, A. et al. Ordered conformational changes in damaged DNA induced by nucleotide excision repair factors. J. Biol. Chem. 279, 19074–19083 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Compe, E. & Egly, J. M. TFIIH: when transcription met DNA repair. Nature Rev. Mol. Cell Biol. 13, 343–354 (2012).

    Article  CAS  Google Scholar 

  • Coin, F., Oksenych, V. & Egly, J. M. Distinct roles for the XPB/p52 and XPD/p44 subcomplexes of TFIIH in damaged DNA opening during nucleotide excision repair. Mol. Cell 26, 245–256 (2007).

    Article  CAS  PubMed  Google Scholar 

  • Oksenych, V., Bernardes de Jesus, B., Zhovmer, A., Egly, J. M. & Coin, F. Molecular insights into the recruitment of TFIIH to sites of DNA damage. EMBO J. 28, 2971–2980 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winkler, G. S. et al. TFIIH with inactive XPD helicase functions in transcription initiation but is defective in DNA repair. J. Biol. Chem. 275, 4258–4266 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Sugasawa, K., Akagi, J., Nishi, R., Iwai, S. & Hanaoka, F. Two-step recognition of DNA damage for mammalian nucleotide excision repair: Directional binding of the XPC complex and DNA strand scanning. Mol. Cell 36, 642–653 (2009). Shows that upon DNA binding in vitro , TFIIH scans the DNA in a 5′–3′ direction, which suggests that it verifies the presence of a lesion after being recruited by XPC.

    Article  CAS  PubMed  Google Scholar 

  • Fan, L. et al. XPD helicase structures and activities: insights into the cancer and aging phenotypes from XPD mutations. Cell 133, 789–800 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolski, S. C. et al. Crystal structure of the FeS cluster-containing nucleotide excision repair helicase XPD. PLoS Biol. 6, e149 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pugh, R. A., Wu, C. G. & Spies, M. Regulation of translocation polarity by helicase domain 1 in SF2B helicases. EMBO J. 31, 503–514 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Mathieu, N., Kaczmarek, N., Ruthemann, P., Luch, A. & Naegeli, H. DNA quality control by a lesion sensor pocket of the xeroderma pigmentosum group D helicase subunit of TFIIH. Curr. Biol. 23, 204–212 (2013).

    Article  CAS  PubMed  Google Scholar 

  • Liu, H. et al. Structure of the DNA repair helicase XPD. Cell 133, 801–812 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Camenisch, U., Dip, R., Schumacher, S. B., Schuler, B. & Naegeli, H. Recognition of helical kinks by xeroderma pigmentosum group A protein triggers DNA excision repair. Nature Struct. Mol. Biol. 13, 278–284 (2006).

    Article  CAS  Google Scholar 

  • Hoogstraten, D. et al. Rapid switching of TFIIH between RNA polymerase I and II transcription and DNA repair in vivo. Mol. Cell 10, 1163–1174 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Coin, F. et al. Nucleotide excision repair driven by the dissociation of CAK from TFIIH. Mol. Cell 31, 9–20 (2008).

    Article  CAS  PubMed  Google Scholar 

  • Giglia-Mari, G. et al. A new, tenth subunit of TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A. Nature Genet. 36, 714–719 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Theil, A. F. et al. Disruption of TTDA results in complete nucleotide excision repair deficiency and embryonic lethality. PLoS Genet. 9, e1003431 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luijsterburg, M. S. et al. Stochastic and reversible assembly of a multiprotein DNA repair complex ensures accurate target site recognition and efficient repair. J. Cell Biol. 189, 445–463 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vermeulen, W. Dynamics of mammalian NER proteins. DNA Repair 10, 760–771 (2011).

    Article  CAS  PubMed  Google Scholar 

  • Fagbemi, A. F., Orelli, B. & Scharer, O. D. Regulation of endonuclease activity in human nucleotide excision repair. DNA Repair 10, 722–729 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godon, C. et al. Generation of DNA single-strand displacement by compromised nucleotide excision repair. EMBO J. 31, 3550–3563 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scharer, O. D. Nucleotide excision repair in eukaryotes. Cold Spring Harb. Perspect. Biol. 5, a012609 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • de Laat, W. L. et al. DNA-binding polarity of human replication protein A positions nucleases in nucleotide excision repair. Genes Dev. 12, 2598–2609 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dunand-Sauthier, I. et al. The spacer region of XPG mediates recruitment to nucleotide excision repair complexes and determines substrate specificity. J. Biol. Chem. 280, 7030–7037 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Zotter, A. et al. Recruitment of the nucleotide excision repair endonuclease XPG to sites of UV induced DNA damage depends on functional TFIIH. Mol. Cell. Biol. 26, 8868–8879 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito, S. et al. XPG stabilizes TFIIH, allowing transactivation of nuclear receptors: implications for Cockayne syndrome in XP G/CS patients. Mol. Cell 26, 231–243 (2007).

    Article  CAS  PubMed  Google Scholar 

  • Staresincic, L. et al. Coordination of dual incision and repair synthesis in human nucleotide excision repair. EMBO J. 28, 1111–1120 (2009). Shows that during NER, the 5′ incision made by XPF–ERCC1 precedes the 3′ incision made by XPG and that it is sufficient to initiate gap-filling DNA synthesis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsodikov, O. V. et al. Structural basis for the recruitment of ERCC1 XPF to nucleotide excision repair complexes by XPA. EMBO J. 26, 4768–4776 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orelli, B. et al. The XPA-binding domain of ERCC1 is required for nucleotide excision repair but not other DNA repair pathways. J. Biol. Chem. 285, 3705–3712 (2010).

    Article  CAS  PubMed  Google Scholar 

  • Mocquet, V. et al. Sequential recruitment of the repair factors during NER: the role of XPG in initiating the resynthesis step. EMBO J. 27, 155–167 (2008).

    Article  CAS  PubMed  Google Scholar 

  • Overmeer, R. M. et al. Replication protein A safeguards genome integrity by controlling NER incision events. J. Cell Biol. 192, 401–415 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogi, T. et al. Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol. Cell 37, 714–727 (2010).

    Article  CAS  PubMed  Google Scholar 

  • Moser, J. et al. Sealing of chromosomal DNA nicks during nucleotide excision repair requires XRCC1 and DNA ligase III α in a cell-cycle-specific manner. Mol. Cell 27, 311–323 (2007). Identifies, together with reference 51, cell-cycle-dependent use of different ligases and DNA polymerases for NER gap-filling DNA synthesis and ligation.

    Article  CAS  PubMed  Google Scholar 

  • Ljungman, M. & Zhang, F. Blockage of RNA polymerase as a possible trigger for U.V. light-induced apoptosis. Oncogene 13, 823–831 (1996).

    CAS  PubMed  Google Scholar 

  • Marietta, C. & Brooks, P. J. Transcriptional bypass of bulky DNA lesions causes new mutant RNA transcripts in human cells. EMBO Rep. 8, 388–393 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hendriks, G. et al. Transcription-dependent cytosine deamination is a novel mechanism in ultraviolet light-induced mutagenesis. Curr. Biol. 20, 170–175 (2010).

    Article  CAS  PubMed  Google Scholar 

  • Hanawalt, P. C. & Spivak, G. Transcription-coupled DNA repair: two decades of progress and surprises. Nature Rev. Mol. Cell Biol. 9, 958–970 (2008).

    Article  CAS  Google Scholar 

  • Vermeulen, W. & Fousteri, M. Mammalian transcription-coupled excision repair. Cold Spring Harb. Perspect. Biol. 5, a012625 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fousteri, M., Vermeulen, W., van Zeeland, A. A. & Mullenders, L. H. Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol. Cell 23, 471–482 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Schwertman, P. et al. UV sensitive syndrome protein UVSSA recruits USP7 to regulate transcription-coupled repair. Nature Genet. 44, 598–602 (2012).

    Article  CAS  PubMed  Google Scholar 

  • de Waard, H. et al. Different effects of CSA and CSB deficiency on sensitivity to oxidative DNA damage. Mol. Cell. Biol. 24, 7941–7948 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevnsner, T., Muftuoglu, M., Aamann, M. D. & Bohr, V. A. The role of Cockayne Syndrome group B (CSB) protein in base excision repair and aging. Mech. Ageing Dev. 129, 441–448 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuraoka, I. et al. Effects of endogenous DNA base lesions on transcription elongation by mammalian RNA polymerase II. Implications for transcription-coupled DNA repair and transcriptional mutagenesis. J. Biol. Chem. 278, 7294–7299 (2003).

    Article  CAS  PubMed  Google Scholar 

  • Kathe, S. D., Shen, G. P. & Wallace, S. S. Single-stranded breaks in DNA but not oxidative DNA base damages block transcriptional elongation by RNA polymerase II in HeLa cell nuclear extracts. J. Biol. Chem. 279, 18511–18520 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Larsen, E., Kwon, K., Coin, F., Egly, J. M. & Klungland, A. Transcription activities at 8 oxoG lesions in DNA. DNA Repair 3, 1457–1468 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Menoni, H., Hoeijmakers, J. H. & Vermeulen, W. Nucleotide excision repair-initiating proteins bind to oxidative DNA lesions in vivo. J. Cell Biol. 199, 1037–1046 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nardo, T. et al. A UV sensitive syndrome patient with a specific CSA mutation reveals separable roles for CSA in response to UV and oxidative DNA damage. Proc. Natl Acad. Sci. USA 106, 6209–6214 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tornaletti, S., Reines, D. & Hanawalt, P. C. Structural characterization of RNA polymerase II complexes arrested by a cyclobutane pyrimidine dimer in the transcribed strand of template DNA. J. Biol. Chem. 274, 24124–24130 (1999).

    Article  CAS  PubMed  Google Scholar 

  • Wilson, M. D., Harreman, M. & Svejstrup, J. Q. Ubiquitylation and degradation of elongating RNA polymerase II: the last resort. Biochim. Biophys. Acta 1829, 151–157 (2013).

    Article  CAS  PubMed  Google Scholar 

  • Sigurdsson, S., Dirac-Svejstrup, A. B. & Svejstrup, J. Q. Evidence that transcript cleavage is essential for RNA polymerase II transcription and cell viability. Mol. Cell 38, 202–210 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Citterio, E. et al. ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair–transcription-coupling factor. Mol. Cell. Biol. 20, 7643–7653 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beerens, N., Hoeijmakers, J. H., Kanaar, R., Vermeulen, W. & Wyman, C. The CSB protein actively wraps DNA. J. Biol. Chem. 280, 4722–4729 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Bensimon, A., Aebersold, R. & Shiloh, Y. Beyond ATM: the protein kinase landscape of the DNA damage response. FEBS Lett. 585, 1625–1639 (2011).

    Article  CAS  PubMed  Google Scholar 

  • Sousa, F. G. et al. PARPs and the DNA damage response. Carcinogenesis 33, 1433–1440 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Pines, A. et al. PARP1 promotes nucleotide excision repair through DDB2 stabilization and recruitment of ALC1. J. Cell Biol. 199, 235–249 (2012). Shows that PARylation facilitates GG-NER through stabilization of DDB2 and recruitment of the chromatin remodeller ALC1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson, S. P. & Durocher, D. Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 49, 795–807 (2013).

    Article  CAS  PubMed  Google Scholar 

  • Povlsen, L. K. et al. Systems-wide analysis of ubiquitylation dynamics reveals a key role for PAF15 ubiquitylation in DNA-damage bypass. Nature Cell Biol. 14, 1089–1098 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Bergink, S. & Jentsch, S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 458, 461–467 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Komander, D. & Rape, M. The ubiquitin code. Annu. Rev. Biochem. 81, 203–229 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Husnjak, K. & Dikic, I. Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 81, 291–322 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Jacq, X., Kemp, M., Martin, N. M. & Jackson, S. P. Deubiquitylating enzymes & DNA damage response pathways. Cell Biochem. Biophys. (2013).

  • Vertegaal, A. C. Uncovering ubiquitin and ubiquitin-like signaling networks. Chem. Rev. 111, 7923–7940 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Q. E. et al. DNA repair factor XPC is modified by SUMO 1 and ubiquitin following UV irradiation. Nucleic Acids Res. 33, 4023–4034 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poulsen, S. L. et al. RNF111/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response. J. Cell Biol. 201, 797–807 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugasawa, K. et al. UV induced ubiquitylation of XPC protein mediated by UV DDB-ubiquitin ligase complex. Cell 121, 387–400 (2005). Reports that ubiquitylation of XPC by the UV–DDB complex regulates its DNA damage affinity.

    Article  CAS  PubMed  Google Scholar 

  • Hannah, J. & Zhou, P. Regulation of DNA damage response pathways by the cullin–RING ubiquitin ligases. DNA Repair 8, 536–543 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapetanaki, M. G. et al. 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. USA 103, 2588–2593 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Scrima, A. et al. Detecting UV lesions in the genome: The modular CRL4 ubiquitin ligase does it best! FEBS Lett. 585, 2818–2825 (2011).

    Article  CAS  PubMed  Google Scholar 

  • Moser, J. et al. The UV damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV induced photo lesions. DNA Repair 4, 571–582 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Liu, L. et al. CUL4A abrogation augments DNA damage response and protection against skin carcinogenesis. Mol. Cell 34, 451–460 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okuda, Y. et al. Relative levels of the two mammalian Rad23 homologs determine composition and stability of the xeroderma pigmentosum group C protein complex. DNA Repair 3, 1285–1295 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Ng, J. M. et al. A novel regulation mechanism of DNA repair by damage-induced and RAD23 dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev. 17, 1630–1645 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergink, S. et al. Recognition of DNA damage by XPC coincides with disruption of the XPC RAD23 complex. J. Cell Biol. 196, 681–688 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groisman, R. et al. CSA-dependent degradation of CSB by the ubiquitin-proteasome pathway establishes a link between complementation factors of the Cockayne syndrome. Genes Dev. 20, 1429–1434 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakazawa, Y. et al. Mutations in UVSSA cause UV sensitive syndrome and impair RNA polymerase IIo processing in transcription-coupled nucleotide-excision repair. Nature Genet. 44, 586–592 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Zhang, X. et al. Mutations in UVSSA cause UV sensitive syndrome and destabilize ERCC6 in transcription-coupled DNA repair. Nature Genet. 44, 593–597 (2012). Shows, together with references 59 and 94, the cloning and functional analysis of UVSSA in TC-NER, the causative gene of UVSS (the last unresolved NER-deficient disorder).

    Article  CAS  PubMed  Google Scholar 

  • Fei, J. & Chen, J. KIAA1530 protein is recruited by Cockayne syndrome complementation group protein A (CSA) to participate in transcription-coupled repair (TCR). J. Biol. Chem. 287, 35118–35126 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anindya, R. et al. A ubiquitin-binding domain in Cockayne syndrome B required for transcription-coupled nucleotide excision repair. Mol. Cell 38, 637–648 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woudstra, E. C. et al. A Rad26 Def1 complex coordinates repair and RNA pol II proteolysis in response to DNA damage. Nature 415, 929–933 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Green, C. M. & Almouzni, G. When repair meets chromatin. First in series on chromatin dynamics. EMBO Rep. 3, 28–33 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smerdon, M. J. DNA repair and the role of chromatin structure. Curr. Opin. Cell Biol. 3, 422–428 (1991).

    Article  CAS  PubMed  Google Scholar 

  • Gong, F., Kwon, Y. & Smerdon, M. J. Nucleotide excision repair in chromatin and the right of entry. DNA Repair 4, 884–896 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Soria, G., Polo, S. E. & Almouzni, G. Prime, repair, restore: the active role of chromatin in the DNA damage response. Mol. Cell 46, 722–734 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Guerrero-Santoro, J. et al. The cullin 4B based UV damaged DNA-binding protein ligase binds to UV damaged chromatin and ubiquitinates histone H2A. Cancer Res. 68, 5014–5022 (2008).

    Article  CAS  PubMed  Google Scholar 

  • Wang, H. et al. Histone H3 and H4 ubiquitylation by the CUL4 DDB ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol. Cell 22, 383–394 (2006).

    Article  PubMed  CAS  Google Scholar 

  • Luijsterburg, M. S. et al. DDB2 promotes chromatin decondensation at UV induced DNA damage. J. Cell Biol. 197, 267–281 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lans, H., Marteijn, J. A. & Vermeulen, W. ATP-dependent chromatin remodeling in the DNA-damage response. Epigenetics Chromatin 5, 4 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hara, R. & Sancar, A. The SWI/SNF chromatin-remodeling factor stimulates repair by human excision nuclease in the mononucleosome core particle. Mol. Cell. Biol. 22, 6779–6787 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, L., Zhang, Q., Jones, K., Patel, M. & Gong, F. The chromatin remodeling factor BRG1 stimulates nucleotide excision repair by facilitating recruitment of XPC to sites of DNA damage. Cell Cycle 8, 3953–3959 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Zhao, Q. et al. Modulation of nucleotide excision repair by mammalian SWI/SNF chromatin-remodeling complex. J. Biol. Chem. 284, 30424–30432 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang, Y. et al. INO80 chromatin remodeling complex promotes the removal of UV lesions by the nucleotide excision repair pathway. Proc. Natl Acad. Sci. USA 107, 17274–17279 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Datta, A. et al. The p48 subunit of the damaged-DNA binding protein DDB associates with the CBP/p300 family of histone acetyltransferase. Mutat. Res. 486, 89–97 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Rapic-Otrin, V., McLenigan, M. P., Bisi, D. C., Gonzalez, M. & Levine, A. S. Sequential binding of UV DNA damage binding factor and degradation of the p48 subunit as early events after UV irradiation. Nucleic Acids Res. 30, 2588–2598 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Martinez, E. et al. Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors in vivo. Mol. Cell. Biol. 21, 6782–6795 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, S., Teng, Y., Waters, R. & Reed, S. H. How chromatin is remodelled during DNA repair of UV induced DNA damage in Saccharomyces cerevisiae. PLoS Genet. 7, e1002124 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo, R., Chen, J., Mitchell, D. L. & Johnson, D. G. GCN5 and E2F1 stimulate nucleotide excision repair by promoting H3K9 acetylation at sites of damage. Nucleic Acids Res. 39, 1390–1397 (2011).

    Article  CAS  PubMed  Google Scholar 

  • Rubbi, C. P. & Milner, J. p53 is a chromatin accessibility factor for nucleotide excision repair of DNA damage. EMBO J. 22, 975–986 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muftuoglu, M., Selzer, R., Tuo, J., Brosh, R. M. Jr & Bohr, V. A. Phenotypic consequences of mutations in the conserved motifs of the putative helicase domain of the human Cockayne syndrome group B gene. Gene 283, 27–40 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Citterio, E. et al. Biochemical and biological characterization of wild-type and ATPase-deficient Cockayne syndrome B repair protein. J. Biol. Chem. 273, 11844–11851 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Selzer, R. R. et al. Differential requirement for the ATPase domain of the Cockayne syndrome group B gene in the processing of UV induced DNA damage and 8 oxoguanine lesions in human cells. Nucleic Acids Res. 30, 782–793 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lake, R. J., Geyko, A., Hemashettar, G., Zhao, Y. & Fan, H. Y. UV induced association of the CSB remodeling protein with chromatin requires ATP-dependent relief of N terminal autorepression. Mol. Cell 37, 235–246 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho, I., Tsai, P. F., Lake, R. J., Basheer, A. & Fan, H. Y. ATP-dependent chromatin remodeling by Cockayne syndrome protein B and NAP1 like histone chaperones is required for efficient transcription-coupled DNA repair. PLoS Genet. 9, e1003407 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dinant, C. et al. Enhanced chromatin dynamics by FACT promotes transcriptional restart after UV induced DNA damage. Mol. Cell 51, 469–479 (2013).

    Article  CAS  PubMed  Google Scholar 

  • Oksenych, V. et al. Histone methyltransferase DOT1L drives recovery of gene expression after a genotoxic attack. PLoS Genet. 9, e1003611 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adam, S., Polo, S. E. & Almouzni, G. Transcription Recovery after DNA Damage Requires Chromatin Priming by the H3.3 Histone Chaperone HIRA. Cell 155, 94–106 (2013). Provides evidence, together with reference 122, for extensive chromatin remodelling during TC-NER, which implicates accelerated H2A–H2B exchange by the histone chaperone complex FACT (facilitates chromatin transcription) and incorporation of H3.3 by HIRA in this process.

    Article  CAS  PubMed  Google Scholar 

  • Gaillard, P. H. et al. Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell 86, 887–896 (1996).

    Article  CAS  PubMed  Google Scholar 

  • Green, C. M. & Almouzni, G. Local action of the chromatin assembly factor CAF 1 at sites of nucleotide excision repair in vivo. EMBO J. 22, 5163–5174 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polo, S. E., Roche, D. & Almouzni, G. New histone incorporation marks sites of UV repair in human cells. Cell 127, 481–493 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Giglia-Mari, G. et al. Differentiation driven changes in the dynamic organization of basal transcription initiation. PLoS Biol. 7, e1000220 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu, S. C., Parsons, S. & Hanawalt, P. C. DNA repair in cultured keratinocytes. J. Invest. Dermatol. 81, 179s–183s (1983).

    Article  CAS  PubMed  Google Scholar 

  • Li, G., Ho, V. C., Mitchell, D. L., Trotter, M. J. & Tron, V. A. Differentiation-dependent p53 regulation of nucleotide excision repair in keratinocytes. Am. J. Pathol. 150, 1457–1464 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nouspikel, T. & Hanawalt, P. C. Terminally differentiated human neurons repair transcribed genes but display attenuated global DNA repair and modulation of repair gene expression. Mol. Cell. Biol. 20, 1562–1570 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nouspikel, T. & Hanawalt, P. C. Impaired nucleotide excision repair upon macrophage differentiation is corrected by E1 ubiquitin-activating enzyme. Proc. Natl Acad. Sci. USA 103, 16188–16193 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nouspikel, T. & Hanawalt, P. C. DNA repair in terminally differentiated cells. DNA Repair 1, 59–75 (2002).

    Article  CAS  PubMed  Google Scholar 

  • van der Wees, C. et al. Nucleotide excision repair in differentiated cells. Mutat. Res. 614, 16–23 (2007).

    Article  CAS  PubMed  Google Scholar 

  • Nouspikel, T. P., Hyka-Nouspikel, N. & Hanawalt, P. C. Transcription domain-associated repair in human cells. Mol. Cell. Biol. 26, 8722–8730 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lans, H. et al. Involvement of global genome repair, transcription coupled repair, and chromatin remodeling in UV DNA damage response changes during development. PLoS Genet. 6, e1000941 (2010). Reports that in C. elegans germ cells, GG-NER is active and maintains the entire genome, whereas in later stage somatic cells TC-NER rather than GG-NER is important.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jansen, J. et al. Nucleotide excision repair in rat male germ cells: low level of repair in intact cells contrasts with high dual incision activity in vitro. Nucleic Acids Res. 29, 1791–1800 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu, G. et al. Nucleotide excision repair activity varies among murine spermatogenic cell types. Biol. Reprod. 73, 123–130 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Roerink, S. F., Koole, W., Stapel, L. C., Romeijn, R. J. & Tijsterman, M. A broad requirement for TLS polymerases η and κ, and interacting sumoylation and nuclear pore proteins, in lesion bypass during C. elegans embryogenesis. PLoS Genet. 8, e1002800 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Waard, H. et al. Cell-type-specific consequences of nucleotide excision repair deficiencies: Embryonic stem cells versus fibroblasts. DNA Repair 7, 1659–1669 (2008).

    Article  CAS  PubMed  Google Scholar 

  • DiGiovanna, J. J. & Kraemer, K. H. Shining a light on xeroderma pigmentosum. J. Invest. Dermatol. 132, 785–796 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barnes, D. E. & Lindahl, T. Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu. Rev. Genet. 38, 445–476 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Brooks, P. J. The 8,5′ cyclopurine-2′ deoxynucleosides: candidate neurodegenerative DNA lesions in xeroderma pigmentosum, and unique probes of transcription and nucleotide excision repair. DNA Repair 7, 1168–1179 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kraemer, K. H. et al. Xeroderma pigmentosum, trichothiodystrophy and Cockayne syndrome: a complex genotype-phenotype relationship. Neuroscience 145, 1388–1396 (2007).

    Article  CAS  PubMed  Google Scholar 

  • Niedernhofer, L. J., Bohr, V. A., Sander, M. & Kraemer, K. H. Xeroderma pigmentosum and other diseases of human premature aging and DNA repair: molecules to patients. Mech. Ageing Dev. 132, 340–347 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaspers, N. G. et al. Anti-tumour compounds illudin S and Irofulven induce DNA lesions ignored by global repair and exclusively processed by transcription- and replication-coupled repair pathways. DNA Repair 1, 1027–1038 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Ljungman, M. & Lane, D. P. Transcription — guarding the genome by sensing DNA damage. Nature Rev. Cancer 4, 727–737 (2004).

    Article  CAS  Google Scholar 

  • Hoeijmakers, J. H. DNA damage, aging, and cancer. New Engl. J. Med. 361, 1475–1485 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Laugel, V. Cockayne syndrome: the expanding clinical and mutational spectrum. Mech. Ageing Dev. 134, 161–170 (2013).

    Article  CAS  PubMed  Google Scholar 

  • Dolle, M. E. et al. Increased genomic instability is not a prerequisite for shortened lifespan in DNA repair deficient mice. Mutat. Res. 596, 22–35 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Niedernhofer, L. J. et al. A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis. Nature 444, 1038–1043 (2006). Describes the identification of the first patient found to carry a mutation in the gene encoding XPF, which causes prominent symptoms of premature ageing; a corresponding mouse Ercc1 mutant exhibits a very similar progeroid phenotype. Expression profiling of mouse tissues reveals that Ercc1 mutant mice also have suppressed growth and upregulated cellular defences resembling the response to caloric restriction, which promotes longevity. These features are presumably an attempt to counteract the accelerated ageing.

    Article  CAS  PubMed  Google Scholar 

  • Garinis, G. A., van der Horst, G. T., Vijg, J. & Hoeijmakers, J. H. DNA damage and ageing: new-age ideas for an age-old problem. Nature Cell Biol. 10, 1241–1247 (2008).

    Article  CAS  PubMed  Google Scholar 

  • Andressoo, J. O. et al.An Xpb mouse model for combined xeroderma pigmentosum and Cockayne syndrome reveals progeroid features upon further attenuation of DNA repair. Mol. Cell. Biol. 29, 1276–1290 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Niedernhofer, L. J. Nucleotide excision repair deficient mouse models and neurological disease. DNA Repair 7, 1180–1189 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Boer, J. et al. Premature aging in mice deficient in DNA repair and transcription. Science 296, 1276–1279 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Vermeulen, W. et al. A temperature-sensitive disorder in basal transcription and DNA repair in humans. Nature Genet. 27, 299–303 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Scharer, O. D. XPG: its products and biological roles. Adv. Exp. Med. Biol. 637, 83–92 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trego, K. S. et al. The DNA repair endonuclease XPG interacts directly and functionally with the WRN helicase defective in Werner syndrome. Cell Cycle 10, 1998–2007 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregg, S. Q., Robinson, A. R. & Niedernhofer, L. J. Physiological consequences of defects in ERCC1 XPF DNA repair endonuclease. DNA Repair 10, 781–791 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaspers, N. G. et al. First reported patient with human ERCC1 deficiency has cerebro-oculo-facio-skeletal syndrome with a mild defect in nucleotide excision repair and severe developmental failure. Am. J. Hum. Genet. 80, 457–466 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bogliolo, M. et al. Mutations in ERCC4, encoding the DNA-repair endonuclease XPF, cause Fanconi anemia. Am. J. Hum. Genet. 92, 800–806 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kashiyama, K. et al. Malfunction of nuclease ERCC1 XPF results in diverse clinical manifestations and causes Cockayne syndrome, xeroderma pigmentosum, and Fanconi anemia. Am. J. Hum. Genet. 92, 807–819 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dolle, M. E. et al. Broad segmental progeroid changes in short-lived Ercc1−/Δ7 mice. Pathobiol. Aging Age Relat. Dis. 1, 7219 (2011).

    Article  CAS  Google Scholar 

  • Schumacher, B. et al. Delayed and accelerated aging share common longevity assurance mechanisms. PLoS Genet. 4, e1000161 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Spivak, G. UV sensitive syndrome. Mutat. Res. 577, 162–169 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Horibata, K. et al. Complete absence of Cockayne syndrome group B gene product gives rise to UV sensitive syndrome but not Cockayne syndrome. Proc. Natl Acad. Sci. USA 101, 15410–15415 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lukas, J., Lukas, C. & Bartek, J. More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance. Nature Cell Biol. 13, 1161–1169 (2011).

    Article  CAS  PubMed  Google Scholar 

  • Bartek, J. & Lukas, J. DNA damage checkpoints: from initiation to recovery or adaptation. Curr. Opin. Cell Biol. 19, 238–245 (2007).

    Article  CAS  PubMed  Google Scholar 

  • Nam, E. A. & Cortez, D. ATR signalling: more than meeting at the fork. Biochem. J. 436, 527–536 (2011).

    Article  CAS  PubMed  Google Scholar 

  • Marini, F. et al. DNA nucleotide excision repair-dependent signaling to checkpoint activation. Proc. Natl Acad. Sci. USA 103, 17325–17330 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marteijn, J. A. et al. Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response. J. Cell Biol. 186, 835–847 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanasoge, S. & Ljungman, M. H2AX phosphorylation after UV irradiation is triggered by DNA repair intermediates and is mediated by the ATR kinase. Carcinogenesis 28, 2298–2304 (2007).

    Article  CAS  PubMed  Google Scholar 

  • MacDougall, C. A., Byun, T. S., Van, C., Yee, M. C. & Cimprich, K. A. The structural determinants of checkpoint activation. Genes Dev. 21, 898–903 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giannattasio, M. et al. Exo1 competes with repair synthesis, converts NER intermediates to long ssDNA gaps, and promotes checkpoint activation. Mol. Cell 40, 50–62 (2010).

    Article  CAS  PubMed  Google Scholar 

  • Sertic, S. et al. Human exonuclease 1 connects nucleotide excision repair (NER) processing with checkpoint activation in response to UV irradiation. Proc. Natl Acad. Sci. USA 108, 13647–13652 (2011). Shows, together with reference 174, that exonuclease 1 (EXO1)-mediated processing of NER intermediates generates large ssDNA gaps. Demonstrates further that intermediates produced during processing of NER lesions, rather than the lesions themselves, stimulate checkpoint signalling.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergink, S. et al. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev. 20, 1343–1352 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mattiroli, F. et al. RNF168 ubiquitinates K13 15 on H2A/H2AX to drive DNA damage signaling. Cell 150, 1182–1195 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Sy, S. M. et al. Critical roles of ring finger protein RNF8 in replication stress responses. J. Biol. Chem. 286, 22355–22361 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar