Advances in genome editing through control of DNA repair pathways (original) (raw)
Cannan, W. J. & Pederson, D. S. Mechanisms and consequences of double-strand DNA break formation in chromatin. J. Cell. Physiol.231, 3–14 (2016). ArticleCASPubMedPubMed Central Google Scholar
Ranjha, L., Howard, S. M. & Cejka, P. Main steps in DNA double-strand break repair: an introduction to homologous recombination and related processes. Chromosoma127, 187–214 (2018). ArticleCASPubMed Google Scholar
Doudna, J. A. & Charpentier, E. The new frontier of genome engineering with CRISPR-Cas9. Science346, 1258096 (2014). ArticlePubMed Google Scholar
Urnov, F. D., Rebar, E. J., Holmes, M. C., Zhang, H. S. & Gregory, P. D. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet.11, 636–646 (2010). ArticleCASPubMed Google Scholar
Miller, J. C. et al. A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol.29, 143–148 (2011). ArticleCASPubMed Google Scholar
Haber, J. E. A life investigating pathways that repair broken chromosomes. Annu. Rev. Genet.50, 1–28 (2016). ArticleCASPubMed Google Scholar
Ward, J. F. DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and reparability. Prog. Nucleic Acid Res. Mol. Biol.35, 95–125 (1988). ArticleCASPubMed Google Scholar
Komor, A. C., Kim, Y. B., Packer, M. S., Zuris, J. A. & Liu, D. R. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature533, 420–424 (2016). ArticleCASPubMedPubMed Central Google Scholar
McConnell Smith, A. et al. Generation of a nicking enzyme that stimulates site-specific gene conversion from the I-AniI LAGLIDADG homing endonuclease. Proc. Natl Acad. Sci.106, 5099–5104 (2009). ArticleCASPubMedPubMed Central Google Scholar
Davis, L. & Maizels, N. Homology-directed repair of DNA nicks via pathways distinct from canonical double-strand break repair. Proc. Natl. Acad. Sci.111, E924–E932 (2014). ArticleCASPubMedPubMed Central Google Scholar
Davis, L. & Maizels, N. Two distinct pathways support gene correction by single-stranded donors at DNA nicks. Cell Rep.17, 1872–1881 (2016). ArticleCASPubMedPubMed Central Google Scholar
Schatz, D. G. & Ji, Y. Recombination centres and the orchestration of V(D)J recombination. Nat. Rev. Immunol.11, 251–263 (2011). ArticleCASPubMed Google Scholar
Baudat, F., Imai, Y. & de Massy, B. Meiotic recombination in mammals: localization and regulation. Nat. Rev. Genet.14, 794–806 (2013). ArticleCASPubMed Google Scholar
Mali, P. et al. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol.31, 833–838 (2013). ArticleCASPubMedPubMed Central Google Scholar
Richardson, C. D., Ray, G. J., DeWitt, M. A., Curie, G. L. & Corn, J. E. Enhancing homology-directed genome editing by catalytically active and inactive CRISPR-Cas9 using asymmetric donor DNA. Nat. Biotechnol.34, 339–344 (2016). ArticleCASPubMed Google Scholar
Sternberg, S. H., Redding, S., Jinek, M., Greene, E. C. & Doudna, J. A. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature507, 62–67 (2014). ArticleCASPubMedPubMed Central Google Scholar
Knight, S. C. et al. Dynamics of CRISPR-Cas9 genome interrogation in living cells. Science350, 823–826 (2015). ArticleCASPubMed Google Scholar
Clarke, R. et al. Enhanced bacterial immunity and mammalian genome editing via RNA-polymerase-mediated dislodging of Cas9 from double-strand DNA breaks. Mol. Cell71, 42–55.e8 (2018). ArticleCASPubMedPubMed Central Google Scholar
DiCarlo, J. E. et al. Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res.41, 4336–4343 (2013). ArticleCASPubMedPubMed Central Google Scholar
Mao, Z., Bozzella, M., Seluanov, A. & Gorbunova, V. Comparison of nonhomologous end joining and homologous recombination in human cells. DNA Repair (Amst.)7, 1765–1771 (2008). ArticleCAS Google Scholar
Chang, H. H. Y., Pannunzio, N. R., Adachi, N. & Lieber, M. R. Non-homologous DNA end joining and alternative pathways to double-strand break repair. Nat. Rev. Mol. Cell Biol.18, 495–506 (2017). ArticleCASPubMedPubMed Central Google Scholar
Mjelle, R. et al. Cell cycle regulation of human DNA repair and chromatin remodeling genes. DNA Repair (Amst.)30, 53–67 (2015). ArticleCAS Google Scholar
Ren, K. & Peña de Ortiz, S. Non-homologous DNA end joining in the mature rat brain. J. Neurochem.80, 949–959 (2002). ArticleCASPubMed Google Scholar
Bae, S., Kweon, J., Kim, H. S. & Kim, J.-S. Microhomology-based choice of Cas9 nuclease target sites. Nat. Methods11, 705–706 (2014). ArticleCASPubMed Google Scholar
Griffith, A. J., Blier, P. R., Mimori, T. & Hardin, J. A. Ku polypeptides synthesized in vitro assemble into complexes which recognize ends of double-stranded DNA. J. Biol. Chem.267, 331–338 (1992). ArticleCASPubMed Google Scholar
Spagnolo, L., Rivera-Calzada, A., Pearl, L. H. & Llorca, O. Three-dimensional structure of the human DNA-PKcs/Ku70/Ku80 complex assembled on DNA and its implications for DNA DSB repair. Mol. Cell22, 511–519 (2006). ArticleCASPubMed Google Scholar
Davis, A. J., Chen, B. P. C. & Chen, D. J. DNA-PK: a dynamic enzyme in a versatile DSB repair pathway. DNA Repair (Amst.)17, 21–29 (2014). ArticleCAS Google Scholar
Yang, S. et al. The SOSS1 single‐stranded DNA binding complex promotes DNA end resection in concert with Exo1. EMBO J.32, 126–139 (2013). ArticleCASPubMed Google Scholar
Mimitou, E. P. & Symington, L. S. Ku prevents Exo1 and Sgs1‐dependent resection of DNA ends in the absence of a functional MRX complex or Sae2. EMBO J.29, 3358–3369 (2010). ArticleCASPubMedPubMed Central Google Scholar
Shim, E. Y. et al. Saccharomyces cerevisiae Mre11/Rad50/Xrs2 and Ku proteins regulate association of Exo1 and Dna2 with DNA breaks. EMBO J.29, 3370–3380 (2010). ArticleCASPubMedPubMed Central Google Scholar
Mari, P.-O. et al. Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc. Natl. Acad. Sci.103, 18597–18602 (2006). ArticleCASPubMedPubMed Central Google Scholar
Bryans, M., Valenzano, M. C. & Stamato, T. D. Absence of DNA ligase IV protein in XR-1 cells: evidence for stabilization by XRCC4. Mutat. Res.433, 53–58 (1999). ArticleCASPubMed Google Scholar
Yano, K. & Chen, D. J. Live cell imaging of XLF and XRCC4 reveals a novel view of protein assembly in the non-homologous end-joining pathway. Cell Cycle7, 1321–1325 (2008). ArticleCASPubMed Google Scholar
Chang, H. H. Y., Watanabe, G. & Lieber, M. R. Unifying the DNA end-processing roles of the artemis nuclease: Ku-dependent artemis resection at blunt DNA ends. J. Biol. Chem.290, 24036–24050 (2015). ArticleCASPubMedPubMed Central Google Scholar
Mahaney, B. L., Meek, K. & Lees-Miller, S. P. Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous end-joining. Biochem. J.417, 639–650 (2009). ArticleCASPubMed Google Scholar
Riesenberg, S. & Maricic, T. Targeting repair pathways with small molecules increases precise genome editing in pluripotent stem cells. Nat. Commun.9, 2164 (2018). ArticlePubMedPubMed CentralCAS Google Scholar
Ninomiya, Y., Suzuki, K., Ishii, C. & Inoue, H. Highly efficient gene replacements in Neurospora strains deficient for nonhomologous end-joining. Proc. Natl. Acad. Sci. USA101, 12248–12253 (2004). ArticleCASPubMedPubMed Central Google Scholar
da Silva Ferreira, M. E. et al. The akuB KU80 mutant deficient for nonhomologous end joining is a powerful tool for analyzing pathogenicity in. Aspergillus fumigatus. Eukaryot. Cell5, 207–211 (2006). ArticlePubMedCAS Google Scholar
Fattah, F. J., Lichter, N. F., Fattah, K. R., Oh, S. & Hendrickson, E. A. Ku70, an essential gene, modulates the frequency of rAAV-mediated gene targeting in human somatic cells. Proc. Natl. Acad. Sci.105, 8703–8708 (2008). ArticleCASPubMedPubMed Central Google Scholar
Srivastava, M. et al. An inhibitor of nonhomologous end-joining abrogates double-strand break repair and impedes cancer progression. Cell151, 1474–1487 (2012). ArticleCASPubMed Google Scholar
Chu, V. T. et al. Increasing the efficiency of homology-directed repair for CRISPR-Cas9-induced precise gene editing in mammalian cells. Nat. Biotechnol.33, 543–548 (2015). ArticleCASPubMed Google Scholar
Beumer, K. J. et al. Efficient gene targeting in Drosophila by direct embryo injection with zinc-finger nucleases. Proc. Natl. Acad. Sci.105, 19821–19826 (2008). ArticleCASPubMedPubMed Central Google Scholar
Maruyama, T. et al. Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat. Biotechnol.33, 538–542 (2015). ArticleCASPubMedPubMed Central Google Scholar
Robert, F., Barbeau, M., Éthier, S., Dostie, J. & Pelletier, J. Pharmacological inhibition of DNA-PK stimulates Cas9-mediated genome editing. Genome Med.7, 93 (2015). ArticlePubMedPubMed CentralCAS Google Scholar
Singh, P., Schimenti, J. C. & Bolcun-Filas, E. A mouse geneticist’s practical guide to CRISPR applications. Genetics199, 1–15 (2015). ArticleCASPubMed Google Scholar
Hu, Z. et al. Ligase IV inhibitor SCR7 enhances gene editing directed by CRISPR-Cas9 and ssODN in human cancer cells. Cell Biosci.8, 12 (2018). ArticlePubMedPubMed CentralCAS Google Scholar
Zhang, J.-P. et al. Efficient precise knockin with a double cut HDR donor after CRISPR/Cas9-mediated double-stranded DNA cleavage. Genome Biol.18, 35 (2017). ArticlePubMedPubMed CentralCAS Google Scholar
Gutschner, T., Haemmerle, M., Genovese, G., Draetta, G. F. & Chin, L. Post-translational regulation of Cas9 during G1 enhances homology-directed repair. Cell Rep.14, 1555–1566 (2016). ArticleCASPubMed Google Scholar
Yang, D. et al. Enrichment of G2/M cell cycle phase in human pluripotent stem cells enhances HDR-mediated gene repair with customizable endonucleases. Sci. Rep.6, 21264 (2016). ArticleCASPubMedPubMed Central Google Scholar
Pinder, J., Salsman, J. & Dellaire, G. Nuclear domain ‘knock-in’ screen for the evaluation and identification of small molecule enhancers of CRISPR-based genome editing. Nucleic Acids Res.43, 9379–9392 (2015). ArticleCASPubMedPubMed Central Google Scholar
Greco, G. E. et al. SCR7 is neither a selective nor a potent inhibitor of human DNA ligase IV. DNA Repair (Amst.)43, 18–23 (2016). ArticleCAS Google Scholar
Truong, L. N. et al. Microhomology-mediated end joining and homologous recombination share the initial end resection step to repair DNA double-strand breaks in mammalian cells. Proc. Natl Acad. Sci.110, 7720–7725 (2013). ArticleCASPubMedPubMed Central Google Scholar
Yan, C. T. et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature449, 478–482 (2007). ArticleCASPubMed Google Scholar
Boboila, C. et al. Alternative end-joining catalyzes class switch recombination in the absence of both Ku70 and DNA ligase 4. J. Exp. Med.207, 417–427 (2010). ArticlePubMedPubMed CentralCAS Google Scholar
Anand, R., Ranjha, L., Cannavo, E. & Cejka, P. Phosphorylated CtIP functions as a co-factor of the MRE11-RAD50-NBS1 endonuclease in DNA end resection. Mol. Cell64, 940–950 (2016). ArticleCASPubMed Google Scholar
Shibata, A. et al. DNA double-strand break repair pathway choice is directed by distinct MRE11 nuclease activities. Mol. Cell53, 7–18 (2014). ArticleCASPubMed Google Scholar
Garcia, V., Phelps, S. E. L., Gray, S. & Neale, M. J. Bidirectional resection of DNA double-strand breaks by Mre11 and Exo1. Nature479, 241–244 (2011). ArticleCASPubMedPubMed Central Google Scholar
Zhou, Y., Caron, P., Legube, G. & Paull, T. T. Quantitation of DNA double-strand break resection intermediates in human cells. Nucleic Acids Res.42, e19 (2014). ArticleCASPubMed Google Scholar
Paull, T. T. & Gellert, M. The 3′ to 5′ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell1, 969–979 (1998). ArticleCASPubMed Google Scholar
Nakade, S. et al. Microhomology-mediated end-joining-dependent integration of donor DNA in cells and animals using TALENs and CRISPR/Cas9. Nat. Commun.5, 5560 (2014). ArticleCASPubMed Google Scholar
Kent, T., Chandramouly, G., McDevitt, S. M., Ozdemir, A. Y. & Pomerantz, R. T. Mechanism of microhomology-mediated end-joining promoted by human DNA polymerase θ. Nat. Struct. Mol. Biol.22, 230–237 (2015). ArticleCASPubMedPubMed Central Google Scholar
Liang, L. et al. Human DNA ligases I and III, but not ligase IV, are required for microhomology-mediated end joining of DNA double-strand breaks. Nucleic Acids Res.36, 3297–3310 (2008). ArticleCASPubMedPubMed Central Google Scholar
Audebert, M., Salles, B. & Calsou, P. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J. Biol. Chem.279, 55117–55126 (2004). ArticleCASPubMed Google Scholar
Wang, M. et al. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res.34, 6170–6182 (2006). ArticleCASPubMedPubMed Central Google Scholar
Haince, J.-F. et al. PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J. Biol. Chem.283, 1197–1208 (2008). ArticleCASPubMed Google Scholar
Mateos-Gomez, P. A. et al. The helicase domain of Polθ counteracts RPA to promote alt-NHEJ. Nat. Struct. Mol. Biol.24, 1116–1123 (2017). ArticleCASPubMedPubMed Central Google Scholar
Dutta, A. et al. Microhomology-mediated end joining is activated in irradiated human cells due to phosphorylation-dependent formation of the XRCC1 repair complex. Nucleic Acids Res.45, 2585–2599 (2017). CASPubMed Google Scholar
Allen, F. et al. Predicting the mutations generated by repair of Cas9-induced double-strand breaks. Nat. Biotechnol.37, 64–72 (2018). ArticleCAS Google Scholar
Shou, J., Li, J., Liu, Y. & Wu, Q. Precise and predictable CRISPR chromosomal rearrangements reveal principles of Cas9-mediated nucleotide insertion. Mol. Cell71, 498–509.e4 (2018). ArticleCASPubMed Google Scholar
Richardson, C. D. et al. CRISPR-Cas9 genome editing in human cells occurs via the Fanconi anemia pathway. Nat. Genet.50, 1132–1139 (2018). ArticleCASPubMed Google Scholar
Liang, F., Han, M., Romanienko, P. J. & Jasin, M. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc. Natl. Acad. Sci.95, 5172–5177 (1998). ArticleCASPubMedPubMed Central Google Scholar
Zhu, Z., Chung, W.-H., Shim, E. Y., Lee, S. E. & Ira, G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell134, 981–994 (2008). ArticleCASPubMedPubMed Central Google Scholar
Chen, R. & Wold, M. S. Replication protein A: single-stranded DNA’s first responder: dynamic DNA-interactions allow replication protein A to direct single-strand DNA intermediates into different pathways for synthesis or repair. BioEssays36, 1156–1161 (2014). ArticleCASPubMedPubMed Central Google Scholar
Ihry, R. J. et al. p53 inhibits CRISPR-Cas9 engineering in human pluripotent stem cells. Nat. Med.24, 939–946 (2018). ArticleCASPubMed Google Scholar
Haapaniemi, E., Botla, S., Persson, J., Schmierer, B. & Taipale, J. CRISPR-Cas9 genome editing induces a p53-mediated DNA damage response. Nat. Med.24, 927–930 (2018). ArticleCASPubMed Google Scholar
Nakanishi, K. et al. Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proc. Natl. Acad. Sci. USA102, 1110–1115 (2005). ArticleCASPubMedPubMed Central Google Scholar
Ceccaldi, R., Sarangi, P. & D’Andrea, A. D. The Fanconi anaemia pathway: new players and new functions. Nat. Rev. Mol. Cell Biol.17, 337–349 (2016). ArticleCASPubMed Google Scholar
Roques, C. et al. MRE11–RAD50–NBS1 is a critical regulator of FANCD2 stability and function during DNA double‐strand break repair. EMBO J.28, 2400–2413 (2009). ArticleCASPubMedPubMed Central Google Scholar
Unno, J. et al. FANCD2 binds CtIP and regulates DNA-end resection during DNA interstrand crosslink repair. Cell Rep.7, 1039–1047 (2014). ArticleCASPubMed Google Scholar
Howard, S. M., Yanez, D. A. & Stark, J. M. DNA damage response factors from diverse pathways, including DNA crosslink repair, mediate alternative end joining. PLoS Genet.11, e1004943 (2015). ArticlePubMedPubMed CentralCAS Google Scholar
Benitez, A. et al. FANCA promotes DNA double-strand break repair by catalyzing single-strand annealing and strand exchange. Mol. Cell71, 621–628.e4 (2018). ArticleCASPubMedPubMed Central Google Scholar
Sugiyama, T., Zaitseva, E. M. & Kowalczykowski, S. C. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem.272, 7940–7945 (1997). ArticleCASPubMed Google Scholar
Renkawitz, J., Lademann, C. A., Kalocsay, M. & Jentsch, S. Monitoring homology search during DNA double-strand break repair in vivo. Mol. Cell50, 261–272 (2013). ArticleCASPubMed Google Scholar
Sugawara, N., Ira, G. & Haber, J. E. DNA length dependence of the single-strand annealing pathway and the role of Saccharomyces cerevisiae RAD59 in double-strand break repair. Mol. Cell. Biol.20, 5300–5309 (2000). ArticleCASPubMedPubMed Central Google Scholar
Chun, J., Buechelmaier, E. S. & Powell, S. N. Rad51 paralog complexes BCDX2 and CX3 act at different stages in the BRCA1-BRCA2-dependent homologous recombination pathway. Mol. Cell. Biol.33, 387–395 (2013). ArticleCASPubMedPubMed Central Google Scholar
Zhang, S. et al. Structural basis for the functional role of the Shu complex in homologous recombination. Nucleic Acids Res.45, 13068–13079 (2017). ArticleCASPubMedPubMed Central Google Scholar
Liu, J., Doty, T., Gibson, B. & Heyer, W.-D. Human BRCA2 protein promotes RAD51 filament formation on RPA-covered single-stranded DNA. Nat. Struct. Mol. Biol.17, 1260–1262 (2010). ArticleCASPubMedPubMed Central Google Scholar
McVey, M., Khodaverdian, V. Y., Meyer, D., Cerqueira, P. G. & Heyer, W.-D. Eukaryotic DNA polymerases in homologous recombination. Annu. Rev. Genet.50, 393–421 (2016). ArticleCASPubMedPubMed Central Google Scholar
Goetz, J. D.-M., Motycka, T. A., Han, M., Jasin, M. & Tomkinson, A. E. Reduced repair of DNA double-strand breaks by homologous recombination in a DNA ligase I-deficient human cell line. DNA Repair (Amst.)4, 649–654 (2005). ArticleCAS Google Scholar
Bentley, D. et al. DNA ligase I is required for fetal liver erythropoiesis but is not essential for mammalian cell viability. Nat. Genet.13, 489–491 (1996). ArticleCASPubMed Google Scholar
Bugreev, D. V., Yu, X., Egelman, E. H. & Mazin, A. V. Novel pro- and anti-recombination activities of the Bloom’s syndrome helicase. Genes Dev.21, 3085–3094 (2007). ArticleCASPubMedPubMed Central Google Scholar
Hu, Y. et al. RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes Dev.21, 3073–3084 (2007). ArticleCASPubMedPubMed Central Google Scholar
Fugger, K. et al. Human Fbh1 helicase contributes to genome maintenance via pro- and anti-recombinase activities. J. Cell Biol.186, 655–663 (2009). ArticleCASPubMedPubMed Central Google Scholar
Simandlova, J. et al. FBH1 helicase disrupts RAD51 filaments in vitro and modulates homologous recombination in mammalian cells. J. Biol. Chem.288, 34168–34180 (2013). ArticleCASPubMedPubMed Central Google Scholar
Chu, W. K. et al. FBH1 influences DNA replication fork stability and homologous recombination through ubiquitylation of RAD51. Nat. Commun.6, 5931 (2015). ArticleCASPubMed Google Scholar
Jayathilaka, K. et al. A chemical compound that stimulates the human homologous recombination protein RAD51. Proc. Natl. Acad. Sci.105, 15848–15853 (2008). ArticleCASPubMedPubMed Central Google Scholar
Huang, F., Mazina, O. M., Zentner, I. J., Cocklin, S. & Mazin, A. V. Inhibition of homologous recombination in human cells by targeting RAD51 recombinase. J. Med. Chem.55, 3011–3020 (2012). ArticleCASPubMed Google Scholar
Ren, C., Yan, Q. & Zhang, Z. Minimum length of direct repeat sequences required for efficient homologous recombination induced by zinc finger nuclease in yeast. Mol. Biol. Rep.41, 6939–6948 (2014). ArticleCASPubMed Google Scholar
Liskay, R. M., Letsou, A. & Stachelek, J. L. Homology requirement for efficient gene conversion between duplicated chromosomal sequences in mammalian cells. Genetics115, 161–167 (1987). ArticleCASPubMedPubMed Central Google Scholar
Mortensen, U. H., Bendixen, C., Sunjevaric, I. & Rothstein, R. DNA strand annealing is promoted by the yeast Rad52 protein. Proc. Natl. Acad. Sci.93, 10729–10734 (1996). ArticleCASPubMedPubMed Central Google Scholar
Shinohara, A., Shinohara, M., Ohta, T., Matsuda, S. & Ogawa, T. Rad52 forms ring structures and co-operates with RPA in single-strand DNA annealing. Genes Cells3, 145–156 (1998). ArticleCASPubMed Google Scholar
Rothenberg, E., Grimme, J. M., Spies, M. & Ha, T. Human Rad52-mediated homology search and annealing occurs by continuous interactions between overlapping nucleoprotein complexes. Proc. Natl. Acad. Sci.105, 20274–20279 (2008). ArticleCASPubMedPubMed Central Google Scholar
Grimme, J. M. et al. Human Rad52 binds and wraps single-stranded DNA and mediates annealing via two hRad52-ssDNA complexes. Nucleic Acids Res.38, 2917–2930 (2010). ArticleCASPubMedPubMed Central Google Scholar
Han, J. et al. BRCA2 antagonizes classical and alternative nonhomologous end-joining to prevent gross genomic instability. Nat. Commun.8, 1470 (2017). ArticlePubMedPubMed CentralCAS Google Scholar
Ma, C. J., Kwon, Y., Sung, P. & Greene, E. C. Human RAD52 interactions with replication protein A and the RAD51 presynaptic complex. J. Biol. Chem.292, 11702–11713 (2017). ArticleCASPubMedPubMed Central Google Scholar
Feng, Z. et al. Rad52 inactivation is synthetically lethal with BRCA2 deficiency. Proc. Natl. Acad. Sci.108, 686–691 (2011). ArticleCASPubMed Google Scholar
Li, X. et al. Efficient SSA-mediated precise genome editing using CRISPR/Cas9. FEBS J.285, 3362–3375 (2018). ArticleCASPubMed Google Scholar
German, J. Bloom syndrome: a mendelian prototype of somatic mutational disease. Medicine (Baltimore)72, 393–406 (1993). ArticleCAS Google Scholar
Aylon, Y., Liefshitz, B. & Kupiec, M. The CDK regulates repair of double‐strand breaks by homologous recombination during the cell cycle. EMBO J.23, 4868–4875 (2004). ArticleCASPubMedPubMed Central Google Scholar
Ira, G. et al. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature431, 1011–1017 (2004). ArticleCASPubMedPubMed Central Google Scholar
Yun, M. H. & Hiom, K. CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature459, 460–463 (2009). ArticleCASPubMedPubMed Central Google Scholar
Buis, J., Stoneham, T., Spehalski, E. & Ferguson, D. O. Mre11 regulates CtIP-dependent double-strand break repair by interaction with CDK2. Nat. Struct. Mol. Biol.19, 246–252 (2012). ArticleCASPubMedPubMed Central Google Scholar
Peterson, S. E. et al. Cdk1 uncouples CtIP-dependent resection and Rad51 filament formation during M-phase double-strand break repair. J. Cell Biol.194, 705–720 (2011). ArticleCASPubMedPubMed Central Google Scholar
Bunting, S. F. et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell141, 243–254 (2010). ArticleCASPubMedPubMed Central Google Scholar
Escribano-Díaz, C. et al. A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol. Cell49, 872–883 (2013). ArticlePubMedCAS Google Scholar
Gupta, R. et al. DNA repair network analysis reveals shieldin as a key regulator of NHEJ and PARP inhibitor sensitivity. Cell173, 972–988.e23 (2018). ArticleCASPubMedPubMed Central Google Scholar
Paulsen, B. S. et al. Ectopic expression of RAD52 and dn53BP1 improves homology-directed repair during CRISPR-Cas9 genome editing. Nat. Biomed. Eng.1, 878–888 (2017). ArticleCASPubMedPubMed Central Google Scholar
Canny, M. D. et al. Inhibition of 53BP1 favors homology-dependent DNA repair and increases CRISPR-Cas9 genome-editing efficiency. Nat. Biotechnol.36, 95–102 (2018). ArticleCASPubMed Google Scholar
Ye, L. et al. Programmable DNA repair with CRISPRa/i enhanced homology-directed repair efficiency with a single Cas9. Cell Discov.4, 46 (2018). ArticlePubMedPubMed CentralCAS Google Scholar
Lin, S., Staahl, B. T., Alla, R. K. & Doudna, J. A. Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery. eLife3, e04766 (2014). ArticlePubMedPubMed Central Google Scholar
Lomova, A. et al. Improving gene editing outcomes in human hematopoietic stem and progenitor cells by temporal control of DNA repair. Stem Cells37, 284–294 (2018). ArticlePubMedPubMed CentralCAS Google Scholar
Storici, F., Snipe, J. R., Chan, G. K., Gordenin, D. A. & Resnick, M. A. Conservative repair of a chromosomal double-strand break by single-strand DNA through two steps of annealing. Mol. Cell. Biol.26, 7645–7657 (2006). ArticleCASPubMedPubMed Central Google Scholar
DeWitt, M. A. et al. Selection-free genome editing of the sickle mutation in human adult hematopoietic stem/progenitor cells. Sci. Transl. Med.8, 360ra134 (2016). ArticlePubMedPubMed CentralCAS Google Scholar
Kan, Y., Ruis, B., Takasugi, T. & Hendrickson, E. A. Mechanisms of precise genome editing using oligonucleotide donors. Genome Res.27, 1099–1111 (2017). ArticleCASPubMedPubMed Central Google Scholar
Bothmer, A. et al. Characterization of the interplay between DNA repair and CRISPR/Cas9-induced DNA lesions at an endogenous locus. Nat. Commun.8, 13905 (2017). ArticleCASPubMedPubMed Central Google Scholar
Shao, S. et al. Enhancing CRISPR/Cas9-mediated homology-directed repair in mammalian cells by expressing Saccharomyces cerevisiae Rad52. Int. J. Biochem. Cell Biol.92, 43–52 (2017). ArticleCASPubMed Google Scholar
Liang, X., Potter, J., Kumar, S., Ravinder, N. & Chesnut, J. D. Enhanced CRISPR/Cas9-mediated precise genome editing by improved design and delivery of gRNA, Cas9 nuclease, and donor DNA. J. Biotechnol.241, 136–146 (2017). ArticleCASPubMed Google Scholar
Renkawitz, J., Lademann, C. A. & Jentsch, S. Mechanisms and principles of homology search during recombination. Nat. Rev. Mol. Cell Biol.15, 369–383 (2014). ArticleCASPubMed Google Scholar
Ünal, E. et al. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell16, 991–1002 (2004). ArticlePubMed Google Scholar
Ström, L., Lindroos, H. B., Shirahige, K. & Sjögren, C. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell16, 1003–1015 (2004). ArticlePubMed Google Scholar
Miné-Hattab, J. & Rothstein, R. Increased chromosome mobility facilitates homology search during recombination. Nat. Cell Biol.14, 510–517 (2012). ArticlePubMedCAS Google Scholar
Savic, N. et al. Covalent linkage of the DNA repair template to the CRISPR-Cas9 nuclease enhances homology-directed repair. eLife7, e33761 (2018). ArticlePubMedPubMed Central Google Scholar
Aird, E. J., Lovendahl, K. N., St Martin, A., Harris, R. S. & Gordon, W. R. Increasing Cas9-mediated homology-directed repair efficiency through covalent tethering of DNA repair template. Commun. Biol.1, 54 (2018). ArticlePubMedPubMed CentralCAS Google Scholar
Eckstein, F. Phosphorothioates, essential components of therapeutic oligonucleotides. Nucleic Acid Ther.24, 374–387 (2014). ArticleCASPubMed Google Scholar
Kass, E. M., Lim, P. X., Helgadottir, H. R., Moynahan, M. E. & Jasin, M. Robust homology-directed repair within mouse mammary tissue is not specifically affected by Brca2 mutation. Nat. Commun.7, 13241 (2016). ArticleCASPubMedPubMed Central Google Scholar
Suzuki, K. et al. In vivo genome editing via CRISPR/Cas9 mediated homology-independent targeted integration. Nature540, 144–149 (2016). ArticleCASPubMedPubMed Central Google Scholar
van Overbeek, M. et al. DNA repair profiling reveals nonrandom outcomes at Cas9-mediated breaks. Mol. Cell63, 633–646 (2016). ArticlePubMedCAS Google Scholar
Taheri-Ghahfarokhi, A. et al. Decoding non-random mutational signatures at Cas9 targeted sites. Nucleic Acids Res.46, 8417–8434 (2018). ArticleCASPubMedPubMed Central Google Scholar
Wang, K. et al. Efficient generation of orthologous point mutations in pigs via CRISPR-assisted ssODN-mediated homology-directed repair. Mol. Ther. Nucleic Acids5, e396 (2016). ArticleCASPubMedPubMed Central Google Scholar