Generation of DNA single-strand displacement by compromised nucleotide excision repair
Nucleotide excision repair (NER) is a precisely coordinated process essential to avoid DNA damage‐induced cellular malfunction and mutagenesis. Here, we investigate the mechanistic details and effects of the NER machinery when it is compromised by a pathologically significant mutation in a subunit o...
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| Published in | The EMBO journal Vol. 31; no. 17; pp. 3550 - 3563 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Chichester, UK
John Wiley & Sons, Ltd
29.08.2012
Nature Publishing Group UK Springer Nature B.V Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0261-4189 1460-2075 1460-2075 |
| DOI | 10.1038/emboj.2012.193 |
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| Abstract | Nucleotide excision repair (NER) is a precisely coordinated process essential to avoid DNA damage‐induced cellular malfunction and mutagenesis. Here, we investigate the mechanistic details and effects of the NER machinery when it is compromised by a pathologically significant mutation in a subunit of the repair/transcription factor TFIIH, namely XPD. In contrast to previous studies, we find that no single‐ or double‐strand DNA breaks are produced at early time points after UV irradiation of cells bearing a specific XPD mutation, despite the presence of a clear histone H2AX phosphorylation (γH2AX) signal in the UV‐exposed areas. We show that the observed γH2AX signal can be explained by the presence of longer single‐strand gaps possibly generated by strand displacement. Our
in vivo
measurements also indicate a strongly reduced TFIIH‐XPG binding that could promote single‐strand displacement at the site of UV lesions. This finding not only highlights the crucial role of XPG's interactions with TFIIH for proper NER, but also sheds new light on how a faulty DNA repair process can induce extreme genomic instability in human patients.
Strong tumorigenic effects of a particular mutation in the key nucleotide excision repair factor XPD may not be due to DNA break generation, but caused by inefficient excision steps resulting in long single‐strand gaps and genomic instability. |
|---|---|
| AbstractList | Nucleotide excision repair (NER) is a precisely coordinated process essential to avoid DNA damage-induced cellular malfunction and mutagenesis. Here, we investigate the mechanistic details and effects of the NER machinery when it is compromised by a pathologically significant mutation in a subunit of the repair/transcription factor TFIIH, namely XPD. In contrast to previous studies, we find that no single- or double-strand DNA breaks are produced at early time points after UV irradiation of cells bearing a specific XPD mutation, despite the presence of a clear histone H2AX phosphorylation (γH2AX) signal in the UV-exposed areas. We show that the observed γH2AX signal can be explained by the presence of longer single-strand gaps possibly generated by strand displacement. Our in vivo measurements also indicate a strongly reduced TFIIH-XPG binding that could promote single-strand displacement at the site of UV lesions. This finding not only highlights the crucial role of XPG's interactions with TFIIH for proper NER, but also sheds new light on how a faulty DNA repair process can induce extreme genomic instability in human patients. Nucleotide excision repair (NER) is a precisely coordinated process essential to avoid DNA damage‐induced cellular malfunction and mutagenesis. Here, we investigate the mechanistic details and effects of the NER machinery when it is compromised by a pathologically significant mutation in a subunit of the repair/transcription factor TFIIH, namely XPD. In contrast to previous studies, we find that no single‐ or double‐strand DNA breaks are produced at early time points after UV irradiation of cells bearing a specific XPD mutation, despite the presence of a clear histone H2AX phosphorylation (γH2AX) signal in the UV‐exposed areas. We show that the observed γH2AX signal can be explained by the presence of longer single‐strand gaps possibly generated by strand displacement. Our in vivo measurements also indicate a strongly reduced TFIIH‐XPG binding that could promote single‐strand displacement at the site of UV lesions. This finding not only highlights the crucial role of XPG's interactions with TFIIH for proper NER, but also sheds new light on how a faulty DNA repair process can induce extreme genomic instability in human patients. Strong tumorigenic effects of a particular mutation in the key nucleotide excision repair factor XPD may not be due to DNA break generation, but caused by inefficient excision steps resulting in long single‐strand gaps and genomic instability. Nucleotide excision repair (NER) is a precisely coordinated process essential to avoid DNA damage-induced cellular malfunction and mutagenesis. Here, we investigate the mechanistic details and effects of the NER machinery when it is compromised by a pathologically significant mutation in a subunit of the repair/transcription factor TFIIH, namely XPD. In contrast to previous studies, we find that no single- or double-strand DNA breaks are produced at early time points after UV irradiation of cells bearing a specific XPD mutation, despite the presence of a clear histone H2AX phosphorylation (γH2AX) signal in the UV-exposed areas. We show that the observed γH2AX signal can be explained by the presence of longer single-strand gaps possibly generated by strand displacement. Our in vivo measurements also indicate a strongly reduced TFIIH-XPG binding that could promote single-strand displacement at the site of UV lesions. This finding not only highlights the crucial role of XPG's interactions with TFIIH for proper NER, but also sheds new light on how a faulty DNA repair process can induce extreme genomic instability in human patients. [PUBLICATION ABSTRACT] Nucleotide excision repair (NER) is a precisely coordinated process essential to avoid DNA damage‐induced cellular malfunction and mutagenesis. Here, we investigate the mechanistic details and effects of the NER machinery when it is compromised by a pathologically significant mutation in a subunit of the repair/transcription factor TFIIH, namely XPD. In contrast to previous studies, we find that no single‐ or double‐strand DNA breaks are produced at early time points after UV irradiation of cells bearing a specific XPD mutation, despite the presence of a clear histone H2AX phosphorylation (γH2AX) signal in the UV‐exposed areas. We show that the observed γH2AX signal can be explained by the presence of longer single‐strand gaps possibly generated by strand displacement. Our in vivo measurements also indicate a strongly reduced TFIIH‐XPG binding that could promote single‐strand displacement at the site of UV lesions. This finding not only highlights the crucial role of XPG's interactions with TFIIH for proper NER, but also sheds new light on how a faulty DNA repair process can induce extreme genomic instability in human patients. Strong tumorigenic effects of a particular mutation in the key nucleotide excision repair factor XPD may not be due to DNA break generation, but caused by inefficient excision steps resulting in long single‐strand gaps and genomic instability. Strong tumorigenic effects of a particular mutation in the key nucleotide excision repair factor XPD may not be due to DNA break generation, but caused by inefficient excision steps resulting in long single-strand gaps and genomic instability. Nucleotide excision repair (NER) is a precisely coordinated process essential to avoid DNA damage-induced cellular malfunction and mutagenesis. Here, we investigate the mechanistic details and effects of the NER machinery when it is compromised by a pathologically significant mutation in a subunit of the repair/transcription factor TFIIH, namely XPD. In contrast to previous studies, we find that no single- or double-strand DNA breaks are produced at early time points after UV irradiation of cells bearing a specific XPD mutation, despite the presence of a clear histone H2AX phosphorylation (γH2AX) signal in the UV-exposed areas. We show that the observed γH2AX signal can be explained by the presence of longer single-strand gaps possibly generated by strand displacement. Our in vivo measurements also indicate a strongly reduced TFIIH-XPG binding that could promote single-strand displacement at the site of UV lesions. This finding not only highlights the crucial role of XPG's interactions with TFIIH for proper NER, but also sheds new light on how a faulty DNA repair process can induce extreme genomic instability in human patients. Nucleotide excision repair (NER) is a precisely coordinated process essential to avoid DNA damage-induced cellular malfunction and mutagenesis. Here, we investigate the mechanistic details and effects of the NER machinery when it is compromised by a pathologically significant mutation in a subunit of the repair/transcription factor TFIIH, namely XPD. In contrast to previous studies, we find that no single- or double-strand DNA breaks are produced at early time points after UV irradiation of cells bearing a specific XPD mutation, despite the presence of a clear histone H2AX phosphorylation (γH2AX) signal in the UV-exposed areas. We show that the observed γH2AX signal can be explained by the presence of longer single-strand gaps possibly generated by strand displacement. Our in vivo measurements also indicate a strongly reduced TFIIH-XPG binding that could promote single-strand displacement at the site of UV lesions. This finding not only highlights the crucial role of XPG's interactions with TFIIH for proper NER, but also sheds new light on how a faulty DNA repair process can induce extreme genomic instability in human patients.Nucleotide excision repair (NER) is a precisely coordinated process essential to avoid DNA damage-induced cellular malfunction and mutagenesis. Here, we investigate the mechanistic details and effects of the NER machinery when it is compromised by a pathologically significant mutation in a subunit of the repair/transcription factor TFIIH, namely XPD. In contrast to previous studies, we find that no single- or double-strand DNA breaks are produced at early time points after UV irradiation of cells bearing a specific XPD mutation, despite the presence of a clear histone H2AX phosphorylation (γH2AX) signal in the UV-exposed areas. We show that the observed γH2AX signal can be explained by the presence of longer single-strand gaps possibly generated by strand displacement. Our in vivo measurements also indicate a strongly reduced TFIIH-XPG binding that could promote single-strand displacement at the site of UV lesions. This finding not only highlights the crucial role of XPG's interactions with TFIIH for proper NER, but also sheds new light on how a faulty DNA repair process can induce extreme genomic instability in human patients. Nucleotide excision repair (NER) is a precisely coordinated process essential to avoid DNA damage-induced cellular malfunction and mutagenesis. Here, we investigate the mechanistic details and effects of the NER machinery when it is compromised by a pathologically significant mutation in a subunit of the repair/transcription factor TFIIH, namely XPD. In contrast to previous studies, we find that no single- or double-strand DNA breaks are produced at early time points after UV irradiation of cells bearing a specific XPD mutation, despite the presence of a clear histone H2AX phosphorylation ( gamma H2AX) signal in the UV-exposed areas. We show that the observed gamma H2AX signal can be explained by the presence of longer single-strand gaps possibly generated by strand displacement. Our in vivo measurements also indicate a strongly reduced TFIIH-XPG binding that could promote single-strand displacement at the site of UV lesions. This finding not only highlights the crucial role of XPG's interactions with TFIIH for proper NER, but also sheds new light on how a faulty DNA repair process can induce extreme genomic instability in human patients. |
| Author | Mourgues, Sophie Giglia‐Mari, Giuseppina Mourcet, Amandine Mari, Pierre‐Olivier Vermeulen, Wim Nonnekens, Julie Godon, Camille Coin, Fréderic |
| Author_xml | – sequence: 1 givenname: Camille surname: Godon fullname: Godon, Camille organization: Department of Cancer Biology, CNRS, IPBS, Toulouse, France – sequence: 2 givenname: Sophie surname: Mourgues fullname: Mourgues, Sophie organization: Department of Cancer Biology, CNRS, IPBS, Toulouse, France – sequence: 3 givenname: Julie surname: Nonnekens fullname: Nonnekens, Julie organization: Department of Cancer Biology, CNRS, IPBS, Toulouse, France – sequence: 4 givenname: Amandine surname: Mourcet fullname: Mourcet, Amandine organization: Department of Cancer Biology, CNRS, IPBS, Toulouse, France – sequence: 5 givenname: Fréderic surname: Coin fullname: Coin, Fréderic organization: Department of Functional Genomics, IGBMC, CNRS/INSERM/ULP, Illkirch Graffenstaden, France – sequence: 6 givenname: Wim surname: Vermeulen fullname: Vermeulen, Wim organization: Department of Genetics, Erasmus MC, GE Rotterdam, The Netherlands – sequence: 7 givenname: Pierre-Olivier surname: Mari fullname: Mari, Pierre-Olivier organization: Department of Cancer Biology, CNRS, IPBS, Toulouse, France – sequence: 8 givenname: Giuseppina surname: Giglia-Mari fullname: Giglia-Mari, Giuseppina email: ambra.mari@ipbs.fr organization: Department of Cancer Biology, CNRS, IPBS, Toulouse, France |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22863773$$D View this record in MEDLINE/PubMed |
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| DOI | 10.1038/emboj.2012.193 |
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| Keywords | Exo1 γH2AX nucleotide excision repair XPD helicase XPG endonuclease |
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Mol Cell 39: 632-640 Andressoo JO, Mitchell JR, de Wit J, Hoogstraten D, Volker M, Toussaint W, Speksnijder E, Beems RB, van Steeg H, Jans J, de Zeeuw CI, Jaspers NG, Raams A, Lehmann AR, Vermeulen W, Hoeijmakers JH, van der Horst GT (2006) An Xpd mouse model for the combined xeroderma pigmentosum/Cockayne syndrome exhibiting both cancer predisposition and segmental progeria. Cancer Cell 10: 121-132 Oksenych V, Coin F (2010) The long unwinding road: XPB and XPD helicases in damaged DNA opening. Cell Cycle 9: 90-96 Berneburg M, Lowe JE, Nardo T, Araujo S, Fousteri MI, Green MH, Krutmann J, Wood RD, Stefanini M, Lehmann AR (2000) UV damage causes uncontrolled DNA breakage in cells from patients with combined features of XP-D and Cockayne syndrome. EMBO J 19: 1157-1166 Giglia-Mari G, Miquel C, Theil AF, Mari PO, Hoogstraten D, Ng JM, Dinant C, Hoeijmakers JH, Vermeulen W (2006) Dynamic interaction of TTDA with TFIIH is stabilized by nucleotide excision repair in living cells. 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Cell Oncol 32: 121-130 Wolski SC, Kuper J, Hanzelmann P, Truglio JJ, Croteau DL, Van Houten B, Kisker C (2008) Crys Matsumoto, Yaginuma, Igarashi, Imura, Hasegawa, Iwabuchi, Date, Mori, Ishizaki, Yamashita, Inobe, Matsunaga (CR31) 2007; 120 Santagati, Botta, Stefanini, Pedrini (CR37) 2001; 29 Zotter, Luijsterburg, Warmerdam, Ibrahim, Nigg, van Cappellen, Hoeijmakers, van Driel, Vermeulen, Houtsmuller (CR50) 2006; 26 Dupuy, Lafforet, Rachman (CR10) 1974; 29 Liu, Rudolf, Johnson, McMahon, Oke, Carter, McRobbie, Brown, Naismith, White (CR30) 2008; 133 Essers, Theil, Baldeyron, van Cappellen, Houtsmuller, Kanaar, Vermeulen (CR11) 2005; 25 Hoogstraten, Nigg, Heath, Mullenders, van Driel, Hoeijmakers, Vermeulen, Houtsmuller (CR22) 2002; 10 Hanawalt (CR20) 1994; 266 van Vuuren, Appeldoorn, Odijk, Yasui, Jaspers, Bootsma, Hoeijmakers (CR45) 1993; 12 Fan, Fuss, Cheng, Arvai, Hammel, Roberts, Cooper, Tainer (CR12) 2008; 133 Staresincic, Fagbemi, Enzlin, Gourdin, Wijgers, Dunand‐Sauthier, Giglia‐Mari, Clarkson, Vermeulen, Scharer (CR39) 2009; 28 Ito, Kuraoka, Chymkowitch, Compe, Takedachi, Ishigami, Coin, Egly, Tanaka (CR24) 2007; 26 Krasikova, Rechkunova, Maltseva, Petruseva, Lavrik (CR28) 2010; 38 Feaver, Svejstrup, Henry, Kornberg (CR13) 1994; 79 Fousteri, Mullenders (CR14) 2008; 18 Giglia‐Mari, Miquel, Theil, Mari, Hoogstraten, Ng, Dinant, Hoeijmakers, Vermeulen (CR16) 2006; 4 van Hoffen, Kalle, de Jong‐Versteeg, Lehmann, van Zeeland, Mullenders (CR44) 1999; 27 Berneburg, Lowe, Nardo, Araujo, Fousteri, Green, Krutmann, Wood, Stefanini, Lehmann (CR2) 2000; 19 Giannattasio, Follonier, Tourriere, Puddu, Lazzaro, Pasero, Lopes, Plevani, Muzi‐Falconi (CR15) 2010; 40 Hammel, Yu, Mahaney, Cai, Ye, Phipps, Rambo, Hura, Pelikan, So, Abolfath, Chen, Lees‐Miller, Tainer (CR19) 2010; 285 Sertic, Pizzi, Cloney, Lehmann, Marini, Plevani, Muzi‐Falconi (CR38) 2011; 108 Coin, Oksenych, Mocquet, Groh, Blattner, Egly (CR7) 2008; 31 Sandrock, Egly (CR36) 2001; 276 Weber, Chung, Springer, Heitzmann, Warth (CR48) 2010; 32 Wolski, Kuper, Hanzelmann, Truglio, Croteau, Van Houten, Kisker (CR49) 2008; 6 Broughton, Berneburg, Fawcett, Taylor, Arlett, Nardo, Stefanini, Menefee, Price, Queille, Sarasin, Bohnert, Krutmann, Davidson, Kraemer, Lehmann (CR4) 2001; 10 Mone, Volker, Nikaido, Mullenders, van Zeeland, Verschure, Manders, van Driel (CR32) 2001; 2 Ito, Tan, Andoh, Narita, Seki, Hirano, Narita, Kuraoka, Hiraoka, Tanaka (CR25) 2010; 39 Godon, Cordelieres, Biard, Giocanti, Megnin‐Chanet, Hall, Favaudon (CR18) 2008; 36 Sugasawa (CR40) 2010; 685 Kraemer, Patronas, Schiffmann, Brooks, Tamura, Digiovanna (CR27) 2007; 145 Moser, Kool, Giakzidis, Caldecott, Mullenders, Fousteri (CR33) 2007; 27 Theron, Fousteri, Volker, Harries, Botta, Stefanini, Fujimoto, Andressoo, Mitchell, Jaspers, McDaniel, Mullenders, Lehmann (CR42) 2005; 25 de Boer, Andressoo, de Wit, Huijmans, Beems, van Steeg, Weeda, van der Horst, van Leeuwen, Themmen, Meradji, Hoeijmakers (CR8) 2002; 296 Oksenych, Coin (CR35) 2010; 9 Douki, Cadet (CR9) 1992; 15 Ogi, Limsirichaikul, Overmeer, Volker, Takenaka, Cloney, Nakazawa, Niimi, Miki, Jaspers, Mullenders, Yamashita, Fousteri, Lehmann (CR34) 2010; 37 Lieber (CR29) 1997; 19 Coin, Bergmann, Tremeau‐Bravard, Egly (CR6) 1999; 18 Hoogstraten, Bergink, Ng, Verbiest, Luijsterburg, Geverts, Raams, Dinant, Hoeijmakers, Vermeulen, Houtsmuller (CR21) 2008; 121 Giglia‐Mari, Theil, Mari, Mourgues, Nonnekens, Andrieux, de Wit, Miquel, Wijgers, Maas, Fousteri, Hoeijmakers, Vermeulen (CR17) 2009; 7 Bootsma, Hoeijmakers (CR3) 1993; 363 Tishkoff, Amin, Viars, Arden, Kolodner (CR43) 1998; 58 Broughton, Thompson, Harcourt, Vermeulen, Hoeijmakers, Botta, Stefanini, King, Weber, Cole (CR5) 1995; 56 Volker, Mone, Karmakar, van Hoffen, Schul, Vermeulen, Hoeijmakers, van Driel, van Zeeland, Mullenders (CR46) 2001; 8 Sugasawa, Ng, Masutani, Iwai, van der Spek, Eker, Hanaoka, Bootsma, Hoeijmakers (CR41) 1998; 2 Keriel, Stary, Sarasin, Rochette‐Egly, Egly (CR26) 2002; 109 Hwang, Moncollin, Vermeulen, Seroz, van Vuuren, Hoeijmakers, Egly (CR23) 1996; 271 Andressoo, Mitchell, de Wit, Hoogstraten, Volker, Toussaint, Speksnijder, Beems, van Steeg, Jans, de Zeeuw, Jaspers, Raams, Lehmann, Vermeulen, Hoeijmakers, van der Horst (CR1) 2006; 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| Snippet | Nucleotide excision repair (NER) is a precisely coordinated process essential to avoid DNA damage‐induced cellular malfunction and mutagenesis. Here, we... Nucleotide excision repair (NER) is a precisely coordinated process essential to avoid DNA damage-induced cellular malfunction and mutagenesis. Here, we... Strong tumorigenic effects of a particular mutation in the key nucleotide excision repair factor XPD may not be due to DNA break generation, but caused by... |
| SourceID | pubmedcentral proquest pubmed wiley springer istex |
| SourceType | Open Access Repository Aggregation Database Index Database Publisher |
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| SubjectTerms | Animals Cell Line Deoxyribonucleic acid DNA DNA Damage DNA Repair DNA, Single-Stranded - genetics DNA-Binding Proteins - genetics EMBO13 EMBO24 Endonucleases - genetics Exo1 Humans Irradiation Lesions Mice Mice, Transgenic Molecular biology Mutagenesis Mutation Nuclear Proteins - genetics nucleotide excision repair Signal transduction Transcription Factors - genetics Ultraviolet radiation Ultraviolet Rays Xeroderma Pigmentosum Group D Protein - genetics XPD helicase XPG endonuclease γH2AX |
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| Title | Generation of DNA single-strand displacement by compromised nucleotide excision repair |
| URI | https://api.istex.fr/ark:/67375/WNG-GNNCSXTF-1/fulltext.pdf https://link.springer.com/article/10.1038/emboj.2012.193 https://onlinelibrary.wiley.com/doi/abs/10.1038%2Femboj.2012.193 https://www.ncbi.nlm.nih.gov/pubmed/22863773 https://www.proquest.com/docview/1038363337 https://www.proquest.com/docview/1037660944 https://www.proquest.com/docview/1093443261 https://pubmed.ncbi.nlm.nih.gov/PMC3433779 |
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