Polyubiquitinated PCNA Recruits the ZRANB3 Translocase to Maintain Genomic Integrity after Replication Stress

被引:229
作者
Ciccia, Alberto [1 ,2 ]
Nimonkar, Amitabh V. [3 ,4 ]
Hu, Yiduo [1 ,5 ]
Hajdu, Ildiko [1 ,2 ]
Achar, Yathish Jagadheesh [6 ]
Izhar, Lior [1 ,2 ]
Petit, Sarah A. [1 ,5 ]
Adamson, Britt [1 ,2 ]
Yoon, John C. [1 ,2 ]
Kowalczykowski, Stephen C. [3 ,4 ]
Livingston, David M. [1 ,5 ]
Haracska, Lajos [6 ]
Elledge, Stephen J. [1 ,2 ]
机构
[1] Harvard Univ, Brigham & Womens Hosp, Sch Med, Dept Genet, Boston, MA 02115 USA
[2] Harvard Univ, Brigham & Womens Hosp, Sch Med, Howard Hughes Med Inst,Div Genet, Boston, MA 02115 USA
[3] Univ Calif Davis, Dept Microbiol, Davis, CA 95616 USA
[4] Univ Calif Davis, Dept Mol & Cellular Biol, Davis, CA 95616 USA
[5] Dana Farber Canc Inst, Dept Canc Biol, Boston, MA 02115 USA
[6] Hungarian Acad Sci, Biol Res Ctr, Inst Genet, H-6726 Szeged, Hungary
关键词
DNA-REPLICATION; HOMOLOGOUS RECOMBINATION; POSTREPLICATION REPAIR; FORK REVERSAL; UBIQUITIN; HELICASE; BINDING; PROTEIN; WRNIP1; IDENTIFICATION;
D O I
10.1016/j.molcel.2012.05.024
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Completion of DNA replication after replication stress depends on PCNA, which undergoes monoubiquitination to stimulate direct bypass of DNA lesions by specialized DNA polymerases or is polyubiquitinated to promote recombination-dependent DNA synthesis across DNA lesions by template switching mechanisms. Here we report that the ZRANB3 translocase, a SNF2 family member related to the SIOD disorder SMARCAL1 protein, is recruited by polyubiquitinated PCNA to promote fork restart following replication arrest. ZRANB3 depletion in mammalian cells results in an increased frequency of sister chromatid exchange and DNA damage sensitivity after treatment with agents that cause replication stress. Using in vitro biochemical assays, we show that recombinant ZRANB3 remodels DNA structures mimicking stalled replication forks and disassembles recombination intermediates. We therefore propose that ZRANB3 maintains genomic stability at stalled or collapsed replication forks by facilitating fork restart and limiting inappropriate recombination that could occur during template switching events.
引用
收藏
页码:396 / 409
页数:14
相关论文
共 52 条
[1]   Ubiquitin interactions of NZF zinc fingers [J].
Alam, SL ;
Sun, J ;
Payne, M ;
Welch, BD ;
Blake, BK ;
Davis, DR ;
Meyer, HH ;
Emr, SD ;
Sundquist, WI .
EMBO JOURNAL, 2004, 23 (07) :1411-1421
[2]   Replication fork reversal and the maintenance of genome stability [J].
Atkinson, John ;
McGlynn, Peter .
NUCLEIC ACIDS RESEARCH, 2009, 37 (11) :3475-3492
[3]   RecQ helicases: guardian angels of the DNA replication fork [J].
Bachrati, Csanad Z. ;
Hickson, Ian D. .
CHROMOSOMA, 2008, 117 (03) :219-233
[4]   The annealing helicase SMARCAL1 maintains genome integrity at stalled replication forks [J].
Bansbach, Carol E. ;
Betous, Remy ;
Lovejoy, Courtney A. ;
Glick, Gloria G. ;
Cortez, David .
GENES & DEVELOPMENT, 2009, 23 (20) :2405-2414
[5]   RTEL1 Maintains Genomic Stability by Suppressing Homologous Recombination [J].
Barber, Louise J. ;
Youds, Jillian L. ;
Ward, Jordan D. ;
McIlwraith, Michael J. ;
O'Neil, Nigel J. ;
Petalcorin, Mark I. R. ;
Martin, Julie S. ;
Collis, Spencer J. ;
Cantor, Sharon B. ;
Auclair, Melissa ;
Tissenbaum, Heidi ;
West, Stephen C. ;
Rose, Ann M. ;
Boulton, Simon J. .
CELL, 2008, 135 (02) :261-271
[6]   Principles of ubiquitin and SUMO modifications in DNA repair [J].
Bergink, Steven ;
Jentsch, Stefan .
NATURE, 2009, 458 (7237) :461-467
[7]   SMARCAL1 catalyzes fork regression and Holliday junction migration to maintain genome stability during DNA replication [J].
Betous, Remy ;
Mason, Aaron C. ;
Rambo, Robert P. ;
Bansbach, Carol E. ;
Badu-Nkansah, Akosua ;
Sirbu, Bianca M. ;
Eichman, Brandt F. ;
Cortez, David .
GENES & DEVELOPMENT, 2012, 26 (02) :151-162
[8]   Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis [J].
Bienko, M ;
Green, CM ;
Crosetto, N ;
Rudolf, F ;
Zapart, G ;
Coull, B ;
Kannouche, P ;
Wider, G ;
Peter, M ;
Lehmann, AR ;
Hofmann, K ;
Dikic, I .
SCIENCE, 2005, 310 (5755) :1821-1824
[9]   Werner helicase-interacting protein 1 binds polyubiquitin via its zinc finger domain [J].
Bish, Rebecca A. ;
Myers, Michael P. .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2007, 282 (32) :23184-23193
[10]   Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression [J].
Blastyák, Andras ;
Pintér, Lajos ;
Unk, Ildiko ;
Prakash, Louise ;
Prakash, Satya ;
Haracska, Lajos .
MOLECULAR CELL, 2007, 28 (01) :167-175