Ubiquitin-Specific Protease 5 Is Required for the Efficient Repair of DNA Double-Strand Breaks
Identifieur interne : 000152 ( Pmc/Checkpoint ); précédent : 000151; suivant : 000153Ubiquitin-Specific Protease 5 Is Required for the Efficient Repair of DNA Double-Strand Breaks
Auteurs : Satoshi Nakajima [États-Unis] ; Li Lan [États-Unis] ; Leizhen Wei [États-Unis] ; Ching-Lung Hsieh [États-Unis] ; Vesna Rapi Otrin [États-Unis] ; Akira Yasui [Japon] ; Arthur S. Levine [États-Unis]Source :
- PLoS ONE [ 1932-6203 ] ; 2014.
Abstract
During the DNA damage response (DDR), ubiquitination plays an important role in the recruitment and regulation of repair proteins. However, little is known about elimination of the ubiquitination signal after repair is completed. Here we show that the ubiquitin-specific protease 5 (USP5), a deubiquitinating enzyme, is involved in the elimination of the ubiquitin signal from damaged sites and is required for efficient DNA double-strand break (DSB) repair. Depletion of USP5 sensitizes cells to DNA damaging agents, produces DSBs, causes delayed disappearance of γH2AX foci after Bleocin treatment, and influences DSB repair efficiency in the homologous recombination pathway but not in the non-homologous end joining pathway. USP5 co-localizes to DSBs induced by laser micro-irradiation in a RAD18-dependent manner. Importantly, polyubiquitin chains at sites of DNA damage remained for longer periods in USP5-depleted cells. Our results show that disassembly of polyubiquitin chains by USP5 at sites of damage is important for efficient DSB repair.
Url:
DOI: 10.1371/journal.pone.0084899
PubMed: 24454762
PubMed Central: 3891734
Affiliations:
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xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Molecular Genetics and University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Lan, Li" sort="Lan, Li" uniqKey="Lan L" first="Li" last="Lan">Li Lan</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Molecular Genetics and University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Molecular Genetics and University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Wei, Leizhen" sort="Wei, Leizhen" uniqKey="Wei L" first="Leizhen" last="Wei">Leizhen Wei</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Molecular Genetics and University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Molecular Genetics and University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Hsieh, Ching Lung" sort="Hsieh, Ching Lung" uniqKey="Hsieh C" first="Ching-Lung" last="Hsieh">Ching-Lung Hsieh</name><affiliation wicri:level="2"><nlm:aff 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xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Molecular Genetics and University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Yasui, Akira" sort="Yasui, Akira" uniqKey="Yasui A" first="Akira" last="Yasui">Akira Yasui</name><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Division of the Dynamic Proteome, Institute of Development, Aging, and Cancer, Tohoku University, Sendai, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Division of the Dynamic Proteome, Institute of Development, Aging, and Cancer, Tohoku University, Sendai</wicri:regionArea><orgName type="university">Université du Tōhoku</orgName><placeName><settlement type="city">Sendai</settlement><region type="province">Région de Tōhoku</region></placeName></affiliation></author><author><name sortKey="Levine, Arthur S" sort="Levine, Arthur S" uniqKey="Levine A" first="Arthur S." last="Levine">Arthur S. Levine</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Molecular Genetics and University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Molecular Genetics and University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>During the DNA damage response (DDR), ubiquitination plays an important role in the recruitment and regulation of repair proteins. However, little is known about elimination of the ubiquitination signal after repair is completed. Here we show that the ubiquitin-specific protease 5 (USP5), a deubiquitinating enzyme, is involved in the elimination of the ubiquitin signal from damaged sites and is required for efficient DNA double-strand break (DSB) repair. Depletion of USP5 sensitizes cells to DNA damaging agents, produces DSBs, causes delayed disappearance of γH2AX foci after Bleocin treatment, and influences DSB repair efficiency in the homologous recombination pathway but not in the non-homologous end joining pathway. USP5 co-localizes to DSBs induced by laser micro-irradiation in a RAD18-dependent manner. Importantly, polyubiquitin chains at sites of DNA damage remained for longer periods in USP5-depleted cells. Our results show that disassembly of polyubiquitin chains by USP5 at sites of damage is important for efficient DSB repair.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Ciccia, A" uniqKey="Ciccia A">A Ciccia</name></author><author><name sortKey="Elledge, Sj" uniqKey="Elledge S">SJ Elledge</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jackson, Sp" uniqKey="Jackson S">SP Jackson</name></author><author><name sortKey="Bartek, J" uniqKey="Bartek J">J Bartek</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Polo, Se" uniqKey="Polo S">SE Polo</name></author><author><name sortKey="Jackson, Sp" uniqKey="Jackson S">SP Jackson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Van Attikum, H" uniqKey="Van Attikum H">H van Attikum</name></author><author><name sortKey="Gasser, Sm" uniqKey="Gasser S">SM Gasser</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rossetto, D" uniqKey="Rossetto D">D Rossetto</name></author><author><name sortKey="Truman, Aw" uniqKey="Truman A">AW Truman</name></author><author><name sortKey="Kron, Sj" uniqKey="Kron S">SJ Kron</name></author><author><name sortKey="Cote, J" uniqKey="Cote J">J Cote</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bekker Jensen, S" uniqKey="Bekker Jensen S">S Bekker-Jensen</name></author><author><name sortKey="Mailand, N" uniqKey="Mailand N">N Mailand</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Galanty, Y" uniqKey="Galanty Y">Y Galanty</name></author><author><name sortKey="Belotserkovskaya, R" uniqKey="Belotserkovskaya R">R Belotserkovskaya</name></author><author><name sortKey="Coates, J" uniqKey="Coates J">J Coates</name></author><author><name sortKey="Polo, S" uniqKey="Polo S">S Polo</name></author><author><name sortKey="Miller, Km" uniqKey="Miller K">KM Miller</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Morris, Jr" uniqKey="Morris J">JR Morris</name></author><author><name sortKey="Boutell, C" uniqKey="Boutell C">C Boutell</name></author><author><name sortKey="Keppler, M" uniqKey="Keppler M">M Keppler</name></author><author><name sortKey="Densham, R" uniqKey="Densham R">R Densham</name></author><author><name sortKey="Weekes, D" uniqKey="Weekes D">D Weekes</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shroff, R" uniqKey="Shroff R">R Shroff</name></author><author><name sortKey="Arbel Eden, A" uniqKey="Arbel Eden A">A Arbel-Eden</name></author><author><name sortKey="Pilch, D" uniqKey="Pilch D">D Pilch</name></author><author><name sortKey="Ira, G" uniqKey="Ira G">G Ira</name></author><author><name sortKey="Bonner, Wm" uniqKey="Bonner W">WM Bonner</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mattiroli, F" uniqKey="Mattiroli F">F Mattiroli</name></author><author><name sortKey="Vissers, Jh" uniqKey="Vissers J">JH Vissers</name></author><author><name sortKey="Van Dijk, Wj" uniqKey="Van Dijk W">WJ van Dijk</name></author><author><name sortKey="Ikpa, P" uniqKey="Ikpa P">P Ikpa</name></author><author><name sortKey="Citterio, E" uniqKey="Citterio E">E Citterio</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Huen, Ms" uniqKey="Huen M">MS Huen</name></author><author><name sortKey="Chen, J" uniqKey="Chen J">J Chen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Reyes Turcu, Fe" uniqKey="Reyes Turcu F">FE Reyes-Turcu</name></author><author><name sortKey="Ventii, Kh" uniqKey="Ventii K">KH Ventii</name></author><author><name sortKey="Wilkinson, Kd" uniqKey="Wilkinson K">KD Wilkinson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lam, Ya" uniqKey="Lam Y">YA Lam</name></author><author><name sortKey="Xu, W" uniqKey="Xu W">W Xu</name></author><author><name sortKey="Demartino, Gn" uniqKey="Demartino G">GN DeMartino</name></author><author><name sortKey="Cohen, Re" uniqKey="Cohen R">RE Cohen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lee, Bh" uniqKey="Lee B">BH Lee</name></author><author><name sortKey="Lee, Mj" uniqKey="Lee M">MJ Lee</name></author><author><name sortKey="Park, S" uniqKey="Park S">S Park</name></author><author><name sortKey="Oh, Dc" uniqKey="Oh D">DC Oh</name></author><author><name sortKey="Elsasser, S" uniqKey="Elsasser S">S Elsasser</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nijman, Sm" uniqKey="Nijman S">SM Nijman</name></author><author><name sortKey="Huang, Tt" uniqKey="Huang T">TT Huang</name></author><author><name sortKey="Dirac, Am" uniqKey="Dirac A">AM Dirac</name></author><author><name sortKey="Brummelkamp, Tr" uniqKey="Brummelkamp T">TR Brummelkamp</name></author><author><name sortKey="Kerkhoven, Rm" uniqKey="Kerkhoven R">RM Kerkhoven</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Huang, Tt" uniqKey="Huang T">TT Huang</name></author><author><name sortKey="Nijman, Sm" uniqKey="Nijman S">SM Nijman</name></author><author><name sortKey="Mirchandani, Kd" uniqKey="Mirchandani K">KD Mirchandani</name></author><author><name sortKey="Galardy, Pj" uniqKey="Galardy P">PJ Galardy</name></author><author><name sortKey="Cohn, Ma" uniqKey="Cohn M">MA Cohn</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nakajima, S" uniqKey="Nakajima S">S Nakajima</name></author><author><name sortKey="Lan, L" uniqKey="Lan L">L Lan</name></author><author><name sortKey="Kanno, S" uniqKey="Kanno S">S Kanno</name></author><author><name sortKey="Usami, N" uniqKey="Usami N">N Usami</name></author><author><name sortKey="Kobayashi, K" uniqKey="Kobayashi K">K Kobayashi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shiomi, N" uniqKey="Shiomi N">N Shiomi</name></author><author><name sortKey="Mori, M" uniqKey="Mori M">M Mori</name></author><author><name sortKey="Tsuji, H" uniqKey="Tsuji H">H Tsuji</name></author><author><name sortKey="Imai, T" uniqKey="Imai T">T Imai</name></author><author><name sortKey="Inoue, H" uniqKey="Inoue H">H Inoue</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lan, L" uniqKey="Lan L">L Lan</name></author><author><name sortKey="Ui, A" uniqKey="Ui A">A Ui</name></author><author><name sortKey="Nakajima, S" uniqKey="Nakajima S">S Nakajima</name></author><author><name sortKey="Hatakeyama, K" uniqKey="Hatakeyama K">K Hatakeyama</name></author><author><name sortKey="Hoshi, M" uniqKey="Hoshi M">M Hoshi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gabriel, Jm" uniqKey="Gabriel J">JM Gabriel</name></author><author><name sortKey="Lacombe, T" uniqKey="Lacombe T">T Lacombe</name></author><author><name sortKey="Carobbio, S" uniqKey="Carobbio S">S Carobbio</name></author><author><name sortKey="Paquet, N" uniqKey="Paquet N">N Paquet</name></author><author><name sortKey="Bisig, R" uniqKey="Bisig R">R Bisig</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Inagaki, A" uniqKey="Inagaki A">A Inagaki</name></author><author><name sortKey="Sleddens Linkels, E" uniqKey="Sleddens Linkels E">E Sleddens-Linkels</name></author><author><name sortKey="Van Cappellen, Wa" uniqKey="Van Cappellen W">WA van Cappellen</name></author><author><name sortKey="Hibbert, Rg" uniqKey="Hibbert R">RG Hibbert</name></author><author><name sortKey="Sixma, Tk" uniqKey="Sixma T">TK Sixma</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dayal, S" uniqKey="Dayal S">S Dayal</name></author><author><name sortKey="Sparks, A" uniqKey="Sparks A">A Sparks</name></author><author><name sortKey="Jacob, J" uniqKey="Jacob J">J Jacob</name></author><author><name sortKey="Allende Vega, N" uniqKey="Allende Vega N">N Allende-Vega</name></author><author><name sortKey="Lane, Dp" uniqKey="Lane D">DP Lane</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lan, L" uniqKey="Lan L">L Lan</name></author><author><name sortKey="Nakajima, S" uniqKey="Nakajima S">S Nakajima</name></author><author><name sortKey="Komatsu, K" uniqKey="Komatsu K">K Komatsu</name></author><author><name sortKey="Nussenzweig, A" uniqKey="Nussenzweig A">A Nussenzweig</name></author><author><name sortKey="Shimamoto, A" uniqKey="Shimamoto A">A Shimamoto</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Prasad, R" uniqKey="Prasad R">R Prasad</name></author><author><name sortKey="Liu, Y" uniqKey="Liu Y">Y Liu</name></author><author><name sortKey="Deterding, Lj" uniqKey="Deterding L">LJ Deterding</name></author><author><name sortKey="Poltoratsky, Vp" uniqKey="Poltoratsky V">VP Poltoratsky</name></author><author><name sortKey="Kedar, Ps" uniqKey="Kedar P">PS Kedar</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ogiwara, H" uniqKey="Ogiwara H">H Ogiwara</name></author><author><name sortKey="Ui, A" uniqKey="Ui A">A Ui</name></author><author><name sortKey="Otsuka, A" uniqKey="Otsuka A">A Otsuka</name></author><author><name sortKey="Satoh, H" uniqKey="Satoh H">H Satoh</name></author><author><name sortKey="Yokomi, I" uniqKey="Yokomi I">I Yokomi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pierce, Aj" uniqKey="Pierce A">AJ Pierce</name></author><author><name sortKey="Johnson, Rd" uniqKey="Johnson R">RD Johnson</name></author><author><name sortKey="Thompson, Lh" uniqKey="Thompson L">LH Thompson</name></author><author><name sortKey="Jasin, M" uniqKey="Jasin M">M Jasin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wilkinson, Kd" uniqKey="Wilkinson K">KD Wilkinson</name></author><author><name sortKey="Tashayev, Vl" uniqKey="Tashayev V">VL Tashayev</name></author><author><name sortKey="O Connor, Lb" uniqKey="O Connor L">LB O'Connor</name></author><author><name sortKey="Larsen, Cn" uniqKey="Larsen C">CN Larsen</name></author><author><name sortKey="Kasperek, E" uniqKey="Kasperek E">E Kasperek</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lan, L" uniqKey="Lan L">L Lan</name></author><author><name sortKey="Nakajima, S" uniqKey="Nakajima S">S Nakajima</name></author><author><name sortKey="Oohata, Y" uniqKey="Oohata Y">Y Oohata</name></author><author><name sortKey="Takao, M" uniqKey="Takao M">M Takao</name></author><author><name sortKey="Okano, S" uniqKey="Okano S">S Okano</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Volker, M" uniqKey="Volker M">M Volker</name></author><author><name sortKey="Mone, Mj" uniqKey="Mone M">MJ Mone</name></author><author><name sortKey="Karmakar, P" uniqKey="Karmakar P">P Karmakar</name></author><author><name sortKey="Van Hoffen, A" uniqKey="Van Hoffen A">A van Hoffen</name></author><author><name sortKey="Schul, W" uniqKey="Schul W">W Schul</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Katsumi, S" uniqKey="Katsumi S">S Katsumi</name></author><author><name sortKey="Kobayashi, N" uniqKey="Kobayashi N">N Kobayashi</name></author><author><name sortKey="Imoto, K" uniqKey="Imoto K">K Imoto</name></author><author><name sortKey="Nakagawa, A" uniqKey="Nakagawa A">A Nakagawa</name></author><author><name sortKey="Yamashina, Y" uniqKey="Yamashina Y">Y Yamashina</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Okano, S" uniqKey="Okano S">S Okano</name></author><author><name sortKey="Lan, L" uniqKey="Lan L">L Lan</name></author><author><name sortKey="Caldecott, Kw" uniqKey="Caldecott K">KW Caldecott</name></author><author><name sortKey="Mori, T" uniqKey="Mori T">T Mori</name></author><author><name sortKey="Yasui, A" uniqKey="Yasui A">A Yasui</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Adamson, B" uniqKey="Adamson B">B Adamson</name></author><author><name sortKey="Smogorzewska, A" uniqKey="Smogorzewska A">A Smogorzewska</name></author><author><name sortKey="Sigoillot, Fd" uniqKey="Sigoillot F">FD Sigoillot</name></author><author><name sortKey="King, Rw" uniqKey="King R">RW King</name></author><author><name sortKey="Elledge, Sj" uniqKey="Elledge S">SJ Elledge</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hadari, T" uniqKey="Hadari T">T Hadari</name></author><author><name sortKey="Warms, Jv" uniqKey="Warms J">JV Warms</name></author><author><name sortKey="Rose, Ia" uniqKey="Rose I">IA Rose</name></author><author><name sortKey="Hershko, A" uniqKey="Hershko A">A Hershko</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Reyes Turcu, Fe" uniqKey="Reyes Turcu F">FE Reyes-Turcu</name></author><author><name sortKey="Horton, Jr" uniqKey="Horton J">JR Horton</name></author><author><name sortKey="Mullally, Je" uniqKey="Mullally J">JE Mullally</name></author><author><name sortKey="Heroux, A" uniqKey="Heroux A">A Heroux</name></author><author><name sortKey="Cheng, X" uniqKey="Cheng X">X Cheng</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Nijman, Sm" uniqKey="Nijman S">SM Nijman</name></author><author><name sortKey="Luna Vargas, Mp" uniqKey="Luna Vargas M">MP Luna-Vargas</name></author><author><name sortKey="Velds, A" uniqKey="Velds A">A Velds</name></author><author><name sortKey="Brummelkamp, Tr" uniqKey="Brummelkamp T">TR Brummelkamp</name></author><author><name sortKey="Dirac, Am" uniqKey="Dirac A">AM Dirac</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ventii, Kh" uniqKey="Ventii K">KH Ventii</name></author><author><name sortKey="Wilkinson, Kd" uniqKey="Wilkinson K">KD Wilkinson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Watanabe, K" uniqKey="Watanabe K">K Watanabe</name></author><author><name sortKey="Tateishi, S" uniqKey="Tateishi S">S Tateishi</name></author><author><name sortKey="Kawasuji, M" uniqKey="Kawasuji M">M Kawasuji</name></author><author><name sortKey="Tsurimoto, T" uniqKey="Tsurimoto T">T Tsurimoto</name></author><author><name sortKey="Inoue, H" uniqKey="Inoue H">H Inoue</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kannouche, Pl" uniqKey="Kannouche P">PL Kannouche</name></author><author><name sortKey="Wing, J" uniqKey="Wing J">J Wing</name></author><author><name sortKey="Lehmann, Ar" uniqKey="Lehmann A">AR Lehmann</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ting, L" uniqKey="Ting L">L Ting</name></author><author><name sortKey="Jun, H" uniqKey="Jun H">H Jun</name></author><author><name sortKey="Junjie, C" uniqKey="Junjie C">C Junjie</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Huang, J" uniqKey="Huang J">J Huang</name></author><author><name sortKey="Huen, Ms" uniqKey="Huen M">MS Huen</name></author><author><name sortKey="Kim, H" uniqKey="Kim H">H Kim</name></author><author><name sortKey="Leung, Cc" uniqKey="Leung C">CC Leung</name></author><author><name sortKey="Glover, Jn" uniqKey="Glover J">JN Glover</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bish, Ra" uniqKey="Bish R">RA Bish</name></author><author><name sortKey="Myers, Mp" uniqKey="Myers M">MP Myers</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tsuji, Y" uniqKey="Tsuji Y">Y Tsuji</name></author><author><name sortKey="Watanabe, K" uniqKey="Watanabe K">K Watanabe</name></author><author><name sortKey="Araki, K" uniqKey="Araki K">K Araki</name></author><author><name sortKey="Shinohara, M" uniqKey="Shinohara M">M Shinohara</name></author><author><name sortKey="Yamagata, Y" uniqKey="Yamagata Y">Y Yamagata</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Galanty, Y" uniqKey="Galanty Y">Y Galanty</name></author><author><name sortKey="Belotserkovskaya, R" uniqKey="Belotserkovskaya R">R Belotserkovskaya</name></author><author><name sortKey="Coates, J" uniqKey="Coates J">J Coates</name></author><author><name sortKey="Jackson, Sp" uniqKey="Jackson S">SP Jackson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mallette, Fa" uniqKey="Mallette F">FA Mallette</name></author><author><name sortKey="Mattiroli, F" uniqKey="Mattiroli F">F Mattiroli</name></author><author><name sortKey="Cui, G" uniqKey="Cui G">G Cui</name></author><author><name sortKey="Young, Lc" uniqKey="Young L">LC Young</name></author><author><name sortKey="Hendzel, Mj" uniqKey="Hendzel M">MJ Hendzel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Levy Barda, A" uniqKey="Levy Barda A">A Levy-Barda</name></author><author><name sortKey="Lerenthal, Y" uniqKey="Lerenthal Y">Y Lerenthal</name></author><author><name sortKey="Davis, Aj" uniqKey="Davis A">AJ Davis</name></author><author><name sortKey="Chung, Ym" uniqKey="Chung Y">YM Chung</name></author><author><name sortKey="Essers, J" uniqKey="Essers J">J Essers</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bekker Jensen, S" uniqKey="Bekker Jensen S">S Bekker-Jensen</name></author><author><name sortKey="Mailand, N" uniqKey="Mailand N">N Mailand</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hong, Z" uniqKey="Hong Z">Z Hong</name></author><author><name sortKey="Jiang, J" uniqKey="Jiang J">J Jiang</name></author><author><name sortKey="Lan, L" uniqKey="Lan L">L Lan</name></author><author><name sortKey="Nakajima, S" uniqKey="Nakajima S">S Nakajima</name></author><author><name sortKey="Kanno, S" uniqKey="Kanno S">S Kanno</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Uematsu, N" uniqKey="Uematsu N">N Uematsu</name></author><author><name sortKey="Weterings, E" uniqKey="Weterings E">E Weterings</name></author><author><name sortKey="Yano, K" uniqKey="Yano K">K Yano</name></author><author><name sortKey="Morotomi Yano, K" uniqKey="Morotomi Yano K">K Morotomi-Yano</name></author><author><name sortKey="Jakob, B" uniqKey="Jakob B">B Jakob</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hanna, J" uniqKey="Hanna J">J Hanna</name></author><author><name sortKey="Leggett, Ds" uniqKey="Leggett D">DS Leggett</name></author><author><name sortKey="Finley, D" uniqKey="Finley D">D Finley</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Butler, Lr" uniqKey="Butler L">LR Butler</name></author><author><name sortKey="Densham, Rm" uniqKey="Densham R">RM Densham</name></author><author><name sortKey="Jia, J" uniqKey="Jia J">J Jia</name></author><author><name sortKey="Garvin, Aj" uniqKey="Garvin A">AJ Garvin</name></author><author><name sortKey="Stone, Hr" uniqKey="Stone H">HR Stone</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shao, G" uniqKey="Shao G">G Shao</name></author><author><name sortKey="Lilli, Dr" uniqKey="Lilli D">DR Lilli</name></author><author><name sortKey="Patterson Fortin, J" uniqKey="Patterson Fortin J">J Patterson-Fortin</name></author><author><name sortKey="Coleman, Ka" uniqKey="Coleman K">KA Coleman</name></author><author><name sortKey="Morrissey, De" uniqKey="Morrissey D">DE Morrissey</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nicassio, F" uniqKey="Nicassio F">F Nicassio</name></author><author><name sortKey="Corrado, N" uniqKey="Corrado N">N Corrado</name></author><author><name sortKey="Vissers, Jh" uniqKey="Vissers J">JH Vissers</name></author><author><name sortKey="Areces, Lb" uniqKey="Areces L">LB Areces</name></author><author><name sortKey="Bergink, S" uniqKey="Bergink S">S Bergink</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dong, Y" uniqKey="Dong Y">Y Dong</name></author><author><name sortKey="Hakimi, Ma" uniqKey="Hakimi M">MA Hakimi</name></author><author><name sortKey="Chen, X" uniqKey="Chen X">X Chen</name></author><author><name sortKey="Kumaraswamy, E" uniqKey="Kumaraswamy E">E Kumaraswamy</name></author><author><name sortKey="Cooch, Ns" uniqKey="Cooch N">NS Cooch</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Murai, J" uniqKey="Murai J">J Murai</name></author><author><name sortKey="Yang, K" uniqKey="Yang K">K Yang</name></author><author><name sortKey="Dejsuphong, D" uniqKey="Dejsuphong D">D Dejsuphong</name></author><author><name sortKey="Hirota, K" uniqKey="Hirota K">K Hirota</name></author><author><name sortKey="Takeda, S" uniqKey="Takeda S">S Takeda</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Amerik, A" uniqKey="Amerik A">A Amerik</name></author><author><name sortKey="Swaminathan, S" uniqKey="Swaminathan S">S Swaminathan</name></author><author><name sortKey="Krantz, Ba" uniqKey="Krantz B">BA Krantz</name></author><author><name sortKey="Wilkinson, Kd" uniqKey="Wilkinson K">KD Wilkinson</name></author><author><name sortKey="Hochstrasser, M" uniqKey="Hochstrasser M">M Hochstrasser</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Li, W" uniqKey="Li W">W Li</name></author><author><name sortKey="Bengtson, Mh" uniqKey="Bengtson M">MH Bengtson</name></author><author><name sortKey="Ulbrich, A" uniqKey="Ulbrich A">A Ulbrich</name></author><author><name sortKey="Matsuda, A" uniqKey="Matsuda A">A Matsuda</name></author><author><name sortKey="Reddy, Va" uniqKey="Reddy V">VA Reddy</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24454762</article-id><article-id pub-id-type="pmc">3891734</article-id><article-id pub-id-type="publisher-id">PONE-D-13-35160</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0084899</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Nucleic Acids</subject><subj-group><subject>DNA</subject><subj-group><subject>DNA recombination</subject><subject>DNA repair</subject></subj-group></subj-group></subj-group><subj-group><subject>Proteins</subject><subj-group><subject>DNA-binding proteins</subject></subj-group></subj-group></subj-group><subj-group><subject>Molecular Cell Biology</subject><subj-group><subject>Gene Expression</subject><subj-group><subject>DNA modification</subject></subj-group></subj-group><subj-group><subject>Nucleic Acids</subject><subj-group><subject>DNA</subject><subj-group><subject>DNA repair</subject><subject>DNA replication</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Physics</subject><subj-group><subject>Biophysics</subject><subj-group><subject>Nucleic Acids</subject><subj-group><subject>DNA</subject><subj-group><subject>DNA recombination</subject><subject>DNA repair</subject></subj-group></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Ubiquitin-Specific Protease 5 Is Required for the Efficient Repair of DNA Double-Strand Breaks</article-title><alt-title alt-title-type="running-head">USP5 Is Required for Efficient DSB Repair</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Nakajima</surname><given-names>Satoshi</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lan</surname><given-names>Li</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wei</surname><given-names>Leizhen</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Hsieh</surname><given-names>Ching-Lung</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Rapić-Otrin</surname><given-names>Vesna</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Yasui</surname><given-names>Akira</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Levine</surname><given-names>Arthur S.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Department of Microbiology and Molecular Genetics and University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, United States of America</addr-line></aff><aff id="aff2"><label>2</label><addr-line>Division of the Dynamic Proteome, Institute of Development, Aging, and Cancer, Tohoku University, Sendai, Japan</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Lustig</surname><given-names>Arthur J.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Tulane University Health Sciences Center, United States of America</addr-line></aff><author-notes><corresp id="cor1">* E-mail: <email>san48@pitt.edu</email> (SN); <email>lil64@pitt.edu</email> (LL)</corresp><fn fn-type="conflict"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p>Conceived and designed the experiments: SN. Performed the experiments: SN LL LW AY. Analyzed the data: SN LL LW AY. Contributed reagents/materials/analysis tools: CLH VRO AY. Wrote the paper: SN LL ASL.</p></fn></author-notes><pub-date pub-type="collection"><year>2014</year></pub-date><pub-date pub-type="epub"><day>14</day><month>1</month><year>2014</year></pub-date><volume>9</volume><issue>1</issue><elocation-id>e84899</elocation-id><history><date date-type="received"><day>26</day><month>8</month><year>2013</year></date><date date-type="accepted"><day>27</day><month>11</month><year>2013</year></date></history><permissions><copyright-year>2014</copyright-year><copyright-holder>Nakajima et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><abstract><p>During the DNA damage response (DDR), ubiquitination plays an important role in the recruitment and regulation of repair proteins. However, little is known about elimination of the ubiquitination signal after repair is completed. Here we show that the ubiquitin-specific protease 5 (USP5), a deubiquitinating enzyme, is involved in the elimination of the ubiquitin signal from damaged sites and is required for efficient DNA double-strand break (DSB) repair. Depletion of USP5 sensitizes cells to DNA damaging agents, produces DSBs, causes delayed disappearance of γH2AX foci after Bleocin treatment, and influences DSB repair efficiency in the homologous recombination pathway but not in the non-homologous end joining pathway. USP5 co-localizes to DSBs induced by laser micro-irradiation in a RAD18-dependent manner. Importantly, polyubiquitin chains at sites of DNA damage remained for longer periods in USP5-depleted cells. Our results show that disassembly of polyubiquitin chains by USP5 at sites of damage is important for efficient DSB repair.</p></abstract><funding-group><funding-statement>UPCI shared resources that are supported in part by award P30CA047904 were used for this project. The project described was supported by the National Institutes of Health through Grant Numbers UL1 RR024153 and UL1TR000005. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><page-count count="11"></page-count></counts></article-meta></front></pmc><affiliations><list><country><li>Japon</li><li>États-Unis</li></country><region><li>Pennsylvanie</li><li>Région de Tōhoku</li></region><settlement><li>Sendai</li></settlement><orgName><li>Université du Tōhoku</li></orgName></list><tree><country name="États-Unis"><region name="Pennsylvanie"><name sortKey="Nakajima, Satoshi" sort="Nakajima, Satoshi" uniqKey="Nakajima S" first="Satoshi" last="Nakajima">Satoshi Nakajima</name></region><name sortKey="Hsieh, Ching Lung" sort="Hsieh, Ching Lung" uniqKey="Hsieh C" first="Ching-Lung" last="Hsieh">Ching-Lung Hsieh</name><name sortKey="Lan, Li" sort="Lan, Li" uniqKey="Lan L" first="Li" last="Lan">Li Lan</name><name sortKey="Levine, Arthur S" sort="Levine, Arthur S" uniqKey="Levine A" first="Arthur S." last="Levine">Arthur S. Levine</name><name sortKey="Rapi Otrin, Vesna" sort="Rapi Otrin, Vesna" uniqKey="Rapi Otrin V" first="Vesna" last="Rapi Otrin">Vesna Rapi Otrin</name><name sortKey="Wei, Leizhen" sort="Wei, Leizhen" uniqKey="Wei L" first="Leizhen" last="Wei">Leizhen Wei</name></country><country name="Japon"><region name="Région de Tōhoku"><name sortKey="Yasui, Akira" sort="Yasui, Akira" uniqKey="Yasui A" first="Akira" last="Yasui">Akira Yasui</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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