RADX Promotes Genome Stability and Modulates Chemosensitivity by Regulating RAD51 at Replication Forks

Molecular Cell - Tập 67 - Trang 374-386.e5 - 2017
Huzefa Dungrawala1, Kamakoti P. Bhat1, Rémy Le Meur1,2, Walter J. Chazin1,2, Xia Ding3, Shyam K. Sharan3, Sarah R. Wessel1, Aditya A. Sathe1, Runxiang Zhao1, David Cortez1
1Department of Biochemistry, Vanderbilt University School of Medicine, Nashville, TN USA
2Center for Structural Biology, Vanderbilt University, Nashville, TN, USA
3Mouse Cancer Genetics Program, Center For Cancer Research, National Cancer Institute, Frederick, MD, USA

Tài liệu tham khảo

Ball, 2005, ATRIP binding to replication protein A-single-stranded DNA promotes ATR-ATRIP localization but is dispensable for Chk1 phosphorylation, Mol. Biol. Cell, 16, 2372, 10.1091/mbc.e04-11-1006 Bansbach, 2009, The annealing helicase SMARCAL1 maintains genome integrity at stalled replication forks, Genes Dev., 23, 2405, 10.1101/gad.1839909 Bass, 2016, ETAA1 acts at stalled replication forks to maintain genome integrity, Nat. Cell Biol., 18, 1185, 10.1038/ncb3415 Bétous, 2012, SMARCAL1 catalyzes fork regression and Holliday junction migration to maintain genome stability during DNA replication, Genes Dev., 26, 151, 10.1101/gad.178459.111 Bétous, 2013, Substrate-selective repair and restart of replication forks by DNA translocases, Cell Rep., 3, 1958, 10.1016/j.celrep.2013.05.002 Bhat, 2015, High-affinity DNA-binding domains of replication protein A (RPA) direct SMARCAL1-dependent replication fork remodeling, J. Biol. Chem., 290, 4110, 10.1074/jbc.M114.627083 Budke, 2016, Recent Developments Using Small Molecules to Target RAD51: How to Best Modulate RAD51 for Anticancer Therapy?, ChemMedChem, 11, 2468, 10.1002/cmdc.201600426 Chow, 2004, RecO acts with RecF and RecR to protect and maintain replication forks blocked by UV-induced DNA damage in Escherichia coli, J. Biol. Chem., 279, 3492, 10.1074/jbc.M311012200 Ciccia, 2009, The SIOD disorder protein SMARCAL1 is an RPA-interacting protein involved in replication fork restart, Genes Dev., 23, 2415, 10.1101/gad.1832309 Ciccia, 2012, Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress, Mol. Cell, 47, 396, 10.1016/j.molcel.2012.05.024 Couch, 2014, Fork reversal, too much of a good thing, Cell Cycle, 13, 1049, 10.4161/cc.28212 Couch, 2013, ATR phosphorylates SMARCAL1 to prevent replication fork collapse, Genes Dev., 27, 1610, 10.1101/gad.214080.113 Courcelle, 1997, recF and recR are required for the resumption of replication at DNA replication forks in Escherichia coli, Proc. Natl. Acad. Sci. USA, 94, 3714, 10.1073/pnas.94.8.3714 Cox, 2007, Regulation of bacterial RecA protein function, Crit. Rev. Biochem. Mol. Biol., 42, 41, 10.1080/10409230701260258 Davies, 2007, Interaction with the BRCA2 C terminus protects RAD51-DNA filaments from disassembly by BRC repeats, Nat. Struct. Mol. Biol., 14, 475, 10.1038/nsmb1251 De Lano, W.L. (2002). The PyMOL Molecular Graphics System. Version 0.99rc6 Schrödinger, LLC, De Lano Scientific, San Carlos. Ding, 2016, Synthetic viability by BRCA2 and PARP1/ARTD1 deficiencies, Nat. Commun., 7, 12425, 10.1038/ncomms12425 Drees, 2004, A RecA filament capping mechanism for RecX protein, Mol. Cell, 15, 789, 10.1016/j.molcel.2004.08.026 Dungrawala, 2015, The replication checkpoint prevents two types of fork collapse without regulating replisome stability, Mol. Cell, 59, 998, 10.1016/j.molcel.2015.07.030 Duursma, 2013, A role for the MRN complex in ATR activation via TOPBP1 recruitment, Mol. Cell, 50, 116, 10.1016/j.molcel.2013.03.006 Edwards, 2008, Resistance to therapy caused by intragenic deletion in BRCA2, Nature, 451, 1111, 10.1038/nature06548 Esashi, 2005, CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair, Nature, 434, 598, 10.1038/nature03404 Eswar, 2007, Comparative protein structure modeling using Modeller, Curr. Protoc. Protein Sci., Chapter 2 Flynn, 2010, Oligonucleotide/oligosaccharide-binding fold proteins: a growing family of genome guardians, Crit. Rev. Biochem. Mol. Biol., 45, 266, 10.3109/10409238.2010.488216 German, 2001, Analysis of sister-chromatid exchanges, Curr. Protoc. Hum. Genet., Chapter 8, 10.1002/0471142905.hg0806s02 Guillemette, 2015, Resistance to therapy in BRCA2 mutant cells due to loss of the nucleosome remodeling factor CHD4, Genes Dev., 29, 489, 10.1101/gad.256214.114 Gunn, 2012, I-SceI-based assays to examine distinct repair outcomes of mammalian chromosomal double strand breaks, Methods Mol. Biol., 920, 379, 10.1007/978-1-61779-998-3_27 Haahr, 2016, Activation of the ATR kinase by the RPA-binding protein ETAA1, Nat. Cell Biol., 18, 1196, 10.1038/ncb3422 Hartlerode, 2009, Mechanisms of double-strand break repair in somatic mammalian cells, Biochem. J., 423, 157, 10.1042/BJ20090942 Hashimoto, 2010, Rad51 protects nascent DNA from Mre11-dependent degradation and promotes continuous DNA synthesis, Nat. Struct. Mol. Biol., 17, 1305, 10.1038/nsmb.1927 Horii, 1968, Degradation of the DNA of Escherichia coli K12 rec- (jc1569b) after irradiation with ultraviolet light, Photochem. Photobiol., 8, 93, 10.1111/j.1751-1097.1968.tb05850.x Källberg, 2012, Template-based protein structure modeling using the RaptorX web server, Nat. Protoc., 7, 1511, 10.1038/nprot.2012.085 Kass, 2016, When genome maintenance goes badly awry, Mol. Cell, 62, 777, 10.1016/j.molcel.2016.05.021 Klein, 2008, The consequences of Rad51 overexpression for normal and tumor cells, DNA Repair (Amst.), 7, 686, 10.1016/j.dnarep.2007.12.008 Kolinjivadi, 2017, Moonlighting at replication forks—a new life for homologous recombination proteins BRCA1, BRCA2 and RAD51, FEBS Lett., 591, 1083, 10.1002/1873-3468.12556 Kowalczykowski, 2015, An overview of the molecular mechanisms of recombinational DNA repair, Cold Spring Harb. Perspect. Biol., 7, 7, 10.1101/cshperspect.a016410 Kuznetsov, 2008, Mouse embryonic stem cell-based functional assay to evaluate mutations in BRCA2, Nat. Med., 14, 875, 10.1038/nm.1719 Larsen, 2013, RecQ helicases: conserved guardians of genomic integrity, Adv. Exp. Med. Biol., 767, 161, 10.1007/978-1-4614-5037-5_8 Lee, 2013, ATAD5 regulates the lifespan of DNA replication factories by modulating PCNA level on the chromatin, J. Cell Biol., 200, 31, 10.1083/jcb.201206084 Lord, 2012, The DNA damage response and cancer therapy, Nature, 481, 287, 10.1038/nature10760 Lord, 2015, Synthetic lethality and cancer therapy: lessons learned from the development of PARP inhibitors, Annu. Rev. Med., 66, 455, 10.1146/annurev-med-050913-022545 Mason, 2014, The RAD51-stimulatory compound RS-1 can exploit the RAD51 overexpression that exists in cancer cells and tumors, Cancer Res., 74, 3546, 10.1158/0008-5472.CAN-13-3220 Norquist, 2011, Secondary somatic mutations restoring BRCA1/2 predict chemotherapy resistance in hereditary ovarian carcinomas, J. Clin. Oncol., 29, 3008, 10.1200/JCO.2010.34.2980 O’Connor, 2015, Targeting the DNA damage response in cancer, Mol. Cell, 60, 547, 10.1016/j.molcel.2015.10.040 Oakley, 2010, Replication protein A: directing traffic at the intersection of replication and repair, Front. Biosci. (Landmark Ed.), 15, 883, 10.2741/3652 Pagès, 2003, recX, a new SOS gene that is co-transcribed with the recA gene in Escherichia coli, DNA Repair (Amst.), 2, 273, 10.1016/S1568-7864(02)00217-3 Pierce, 1999, XRCC3 promotes homology-directed repair of DNA damage in mammalian cells, Genes Dev., 13, 2633, 10.1101/gad.13.20.2633 Quiros, 2011, Rad51 and BRCA2—new molecular targets for sensitizing glioma cells to alkylating anticancer drugs, PLoS ONE, 6, e27183, 10.1371/journal.pone.0027183 Ran, 2013, Genome engineering using the CRISPR-Cas9 system, Nat. Protoc., 8, 2281, 10.1038/nprot.2013.143 Ray Chaudhuri, 2012, Topoisomerase I poisoning results in PARP-mediated replication fork reversal, Nat. Struct. Mol. Biol., 19, 417, 10.1038/nsmb.2258 Ray Chaudhuri, 2016, Replication fork stability confers chemoresistance in BRCA-deficient cells, Nature, 535, 382, 10.1038/nature18325 Richard, 2009, Multiple human single-stranded DNA binding proteins function in genome maintenance: structural, biochemical and functional analysis, Crit. Rev. Biochem. Mol. Biol., 44, 98, 10.1080/10409230902849180 Richardson, 1998, Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations, Genes Dev., 12, 3831, 10.1101/gad.12.24.3831 Richardson, 2004, Rad51 overexpression promotes alternative double-strand break repair pathways and genome instability, Oncogene, 23, 546, 10.1038/sj.onc.1207098 Robu, 2001, RecA protein promotes the regression of stalled replication forks in vitro, Proc. Natl. Acad. Sci. USA, 98, 8211, 10.1073/pnas.131022698 Sakai, 2008, Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers, Nature, 451, 1116, 10.1038/nature06633 Sarbajna, 2014, Holliday junction processing enzymes as guardians of genome stability, Trends Biochem. Sci., 39, 409, 10.1016/j.tibs.2014.07.003 Satta, 1979, Degradation of Escherichia coli DNA: evidence for limitation in vivo by protein X, the recA gene product, Mol. Gen. Genet., 168, 69, 10.1007/BF00267935 Schlacher, 2011, Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11, Cell, 145, 529, 10.1016/j.cell.2011.03.041 Schlacher, 2012, A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2, Cancer Cell, 22, 106, 10.1016/j.ccr.2012.05.015 Sogo, 2002, Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects, Science, 297, 599, 10.1126/science.1074023 Stark, 2004, Genetic steps of mammalian homologous repair with distinct mutagenic consequences, Mol. Cell. Biol., 24, 9305, 10.1128/MCB.24.21.9305-9316.2004 Stohl, 2003, Escherichia coli RecX inhibits RecA recombinase and coprotease activities in vitro and in vivo, J. Biol. Chem., 278, 2278, 10.1074/jbc.M210496200 Symington, 2014, End resection at double-strand breaks: mechanism and regulation, Cold Spring Harb. Perspect. Biol., 1, 6 Tarsounas, 2003, BRCA2-dependent and independent formation of RAD51 nuclear foci, Oncogene, 22, 1115, 10.1038/sj.onc.1206263 Tennstedt, 2013, RAD51 overexpression is a negative prognostic marker for colorectal adenocarcinoma, Int. J. Cancer, 132, 2118, 10.1002/ijc.27907 Toledo, 2013, ATR prohibits replication catastrophe by preventing global exhaustion of RPA, Cell, 155, 1088, 10.1016/j.cell.2013.10.043 Venkatesh, 2002, RecX protein abrogates ATP hydrolysis and strand exchange promoted by RecA: insights into negative regulation of homologous recombination, Proc. Natl. Acad. Sci. USA, 99, 12091, 10.1073/pnas.192178999 Vierling, 2000, Transcriptional and mutational analyses of the Streptomyces lividans recX gene and its interference with RecA activity, J. Bacteriol., 182, 4005, 10.1128/JB.182.14.4005-4011.2000 Willis, 2014, BRCA1 controls homologous recombination at Tus/Ter-stalled mammalian replication forks, Nature, 510, 556, 10.1038/nature13295 Xia, 2006, Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2, Mol. Cell, 22, 719, 10.1016/j.molcel.2006.05.022 Xu, 2008, The basic cleft of RPA70N binds multiple checkpoint proteins, including RAD9, to regulate ATR signaling, Mol. Cell. Biol., 28, 7345, 10.1128/MCB.01079-08 Yuan, 2009, The annealing helicase HARP protects stalled replication forks, Genes Dev., 23, 2394, 10.1101/gad.1836409 Yusufzai, 2009, The annealing helicase HARP is recruited to DNA repair sites via an interaction with RPA, Genes Dev., 23, 2400, 10.1101/gad.1831509 Zellweger, 2015, Rad51-mediated replication fork reversal is a global response to genotoxic treatments in human cells, J. Cell Biol., 208, 563, 10.1083/jcb.201406099 Zou, 2017, DNA replication checkpoint: new ATR activator identified, Curr. Biol., 27, R33, 10.1016/j.cub.2016.11.025 Zou, 2003, Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes, Science, 300, 1542, 10.1126/science.1083430