Cited by 1,137CRISPR and Genetic EngineeringDNA Repair MechanismsRNA regulation and disease

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Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining

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Maruyama, Takeshi, Dougan, Stephanie K, Truttmann, Matthias C, Bilate, Angelina M, Ingram, Jessica R, Ploegh, Hidde L·2015·Nature Biotechnology

DOI 10.1038/nbt.3190PMC PMC4618510

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Abstract

Methods to introduce targeted double-strand breaks (DSBs) into DNA enable precise genome editing by increasing the rate at which externally supplied DNA fragments are incorporated into the genome through homologous recombination. The efficiency of these methods is limited by nonhomologous end joining (NHEJ), an alternative DNA repair pathway that competes with homology-directed repair (HDR). To promote HDR at the expense of NHEJ, we targeted DNA ligase IV, a key enzyme in the NHEJ pathway, using the inhibitor Scr7. Scr7 treatment increased the efficiency of HDR-mediated genome editing, using Cas9 in mammalian cell lines and in mice for all four genes examined, up to 19-fold. This approach should be applicable to other customizable endonucleases, such as zinc finger nucleases and transcription activator-like effector nucleases, and to nonmammalian cells with sufficiently conserved mechanisms of NHEJ and HDR.

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Robinson, J. T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E. S., Getz, G., & Mesirov, J. P. (2011) · Nature Biotechnology · doi:10.1038/nbt.1754 · Cited by 15,390
RNA-Guided Human Genome Engineering via Cas9
Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E., & Church, G. M. (2013) · Science · doi:10.1126/science.1232033 · Cited by 9,210
One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering
Wang, H., Yang, H., Shivalila, C. S., Dawlaty, M. M., Cheng, A. W., Zhang, F., & Jaenisch, R. (2013) · Cell · doi:10.1016/j.cell.2013.04.025 · Cited by 3,495
CRISPR-Cas systems for editing, regulating and targeting genomes
Sander, J. D., & Joung, J. K. (2014) · Nature Biotechnology · doi:10.1038/nbt.2842 · Cited by 3,153
Genetic screens in human cells using the CRISPR-Cas9 system
Wang, T., Wei, J. J., Sabatini, D. M., & Lander, E. S. (2014) · Science · doi:10.1126/science.1246981 · Cited by 2,856
RNA-guided editing of bacterial genomes using CRISPR-Cas systems
Jiang, W., Bikard, D., Cox, D., Zhang, F., & Marraffini, L. A. (2013) · Nature Biotechnology · doi:10.1038/nbt.2508 · Cited by 2,429
RNA-guided genetic silencing systems in bacteria and archaea
Wiedenheft, B., Sternberg, S. H., & Doudna, J. A. (2012) · Nature · doi:10.1038/nature10886 · Cited by 1,851
One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering
Yang, H., Wang, H., Shivalila, C. S., Cheng, A. W., Shi, L., & Jaenisch, R. (2013) · Cell · doi:10.1016/j.cell.2013.08.022 · Cited by 1,596
Double-strand break repair: 53BP1 comes into focus
Panier, S., & Boulton, S. J. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3719 · Cited by 1,168
Improved structure, function and compatibility for CellProfiler: modular high-throughput image analysis software
Kamentsky, L. D., Jones, T. R., Fraser, A. N., Bray, M., Logan, D. J., Madden, K. L., Ljosa, V., Rueden, C., Eliceiri, K. W., & Carpenter, A. E. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr095 · Cited by 1,002

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Wu, Y., Luna, M. J., Bonilla, L. S., Ryba, N. J. P., & Pickel, J. M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0193129 · Cited by 17
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Hillen, A. E. J., Hruzova, M., Rothgangl, T., Breur, M., Bugiani, M., van der Knaap, M. S., Schwank, G., & Heine, V. M. (2022) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2022.02.006 · Cited by 17
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Kannan, R., & Ventura, A. (2015) · Swiss Medical Weekly · doi:10.4414/smw.2015.14230 · Cited by 17
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Plosky, B. S. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.05.006 · Cited by 17
The application of CRISPR technology to high content screening in primary neurons
Callif, B. L., Maunze, B., Krueger, N. L., Simpson, M. T., & Blackmore, M. G. (2017) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2017.01.003 · Cited by 17
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Lee, K., Farrell, K., & Uh, K. (2019) · Reproduction Fertility and Development · doi:10.1071/rd19273 · Cited by 18
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Bhat, M. A., Bhat, M. A., Kumar, V., Wani, I. A., Bashir, H., Shah, A. A., Rahman, S., & Jan, A. T. (2020) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2020.09.013 · Cited by 17
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Mentani, A., Maresca, M., & Shiriaeva, A. (2025) · Cells · doi:10.3390/cells14040277 · Cited by 13
Production of genome-edited pluripotent stem cells and mice by CRISPR/Cas [Review]
Horii, T., & Hatada, I. (2016) · Endocrine Journal · doi:10.1507/endocrj.ej15-0734 · Cited by 12
The present and future of genome editing in cancer research
Li, X., Wu, R., & Ventura, A. (2016) · Human Genetics · doi:10.1007/s00439-016-1713-3 · Cited by 12
Enhanced CRISPR /Cas9‐mediated biallelic genome targeting with dual surrogate reporter‐integrated donors
Wu, Y., Xu, K., Ren, C., Li, X., Lv, H., Han, F., Wei, Z., Wang, X., & Zhang, Z. (2017) · FEBS Letters · doi:10.1002/1873-3468.12599 · Cited by 12
CRISPR/Cas9-based knockout pipeline for reverse genetics in mammalian cell culture
Spiegel, A., Bachmann, M., Jiménez, G. J., & Sarov, M. (2019) · Methods · doi:10.1016/j.ymeth.2019.04.016 · Cited by 12
A Broad Application of CRISPR Cas9 in Infectious Diseases of Central Nervous System
Bellizzi, A., Ahye, N., Jalagadugula, G. S., & Wollebo, H. S. (2019) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-019-09878-7 · Cited by 12
Mutation-Specific Guide RNA for Compound Heterozygous Porphyria On-target Scarless Correction by CRISPR/Cas9 in Stem Cells
Prat, F., Toutain, J., Boutin, J., Amintas, S., Cullot, G., Lalanne, M., Lamrissi‐Garcia, I., Moranvillier, I., Richard, E., Blouin, J., et al. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.07.015 · Cited by 13
CRISPR-Based Editing Techniques for Genetic Manipulation of Primary T Cells
Kotowski, M., & Sharma, S. (2020) · Methods and Protocols · doi:10.3390/mps3040079 · Cited by 14
Characterizing genes associated with cancer using the CRISPR/Cas9 system: A systematic review of genes and methodological approaches
Gonzalez-Salinas, F., Martínez-Amador, C., & Treviño, V. (2022) · Gene · doi:10.1016/j.gene.2022.146595 · Cited by 12
Gene-independent therapeutic interventions to maintain and restore light sensitivity in degenerating photoreceptors
Žužić, M., Striebel, J., Pawlick, J. S., Sharma, K., Holz, F. G., & Busskamp, V. (2022) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2022.101065 · Cited by 12
Application of CRISPR-Cas system in gene therapy: Pre-clinical progress in animal model
Guan, L., Han, Y., Zhu, S., & Lin, J. (2016) · DNA repair · doi:10.1016/j.dnarep.2016.07.004 · Cited by 13
An Overview of the CRISPR-Based Genomic- and Epigenome-Editing System: Function, Applications, and Challenges
Mojarrad, M., Qomi, S. B., & Asghari, A. (2019) · Advanced Biomedical Research · doi:10.4103/abr.abr_41_19 · Cited by 12
Enhanced homologous recombination by the modulation of targeting vector ends
Hirotsune, S., Kiyonari, H., Jin, M., Kumamoto, K., Yoshida, K., Shinohara, M., Watanabe, H., Wynshaw-Boris, A. J., & Matsuzaki, F. (2020) · Scientific Reports · doi:10.1038/s41598-020-58893-9 · Cited by 12
Beta human papillomavirus 8 E6 allows colocalization of non-homologous end joining and homologous recombination repair factors
Hu, C., Bugbee, T., Dacus, D., Palinski, R. M., & Wallace, N. A. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010275 · Cited by 13
How Crisp is CRISPR? CRISPR-Cas-mediated crop improvement with special focus on nutritional traits
Kaul, T., Sony, S. K., Raman, N. M., Eswaran, M., Verma, R., Prakash, A. T., Bharti, J., Motelb, K. F. A., & Kaul, R. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-818581-0.00011-5 · Cited by 12
Evaluation and prediction of guide RNA activities in genome-editing tools
Kim, H. K., & Kim, S. (2025) · Nature Reviews Bioengineering · doi:10.1038/s44222-025-00352-z · Cited by 12
Small-molecule activators specific to adenine base editors through blocking the canonical TGF-β pathway
Yang, Y., Zhang, C., Song, Y., Li, Y., Li, P., Huang, M., Meng, F., & Zhang, M. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac742 · Cited by 11
The Emerging Role of uORF-Encoded uPeptides and HLA uLigands in Cellular and Tumor Biology
Jürgens, L., & Wethmar, K. (2022) · Cancers · doi:10.3390/cancers14246031 · Cited by 13
Genome-edited rabbits: Unleashing the potential of a promising experimental animal model across diverse diseases
Han, Y., 吉林大学动物科学学院人畜共患病研究教育部重点实验室, 吉. 长. 1., Zhou, J., Zhang, R., Liang, Y., Lai, L., Li, Z., 中国科学院再生生物学重点实验室、广东省干细胞与再生医学重点实验室、中国科学院广州生物医药与健康研究院华南干细胞生物学与再生医学研究所, 广., 广州再生医学与健康广东实验室(GRMH-GDL), 广. 广. 5., & 中国科学院干细胞与再生研究所, 北. 1. (2023) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2023.201 · Cited by 11
One-step knock-in of two antimicrobial peptide transgenes at multiple loci of catfish by CRISPR/Cas9-mediated multiplex genome engineering
Wang, J., Torres, I. M., Shang, M., Al-Armanazi, J., Dilawar, H., Hettiarachchi, D. U., Paladines-Parrales, A., Chambers, B., Pottle, K. B., Soman, M., et al. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.129384 · Cited by 11
CRISPR/Cas9 Genome Editing in Oncology: Mechanisms, Therapeutic Platforms and Translational Challenges
Nguyen, D. A. H., & Quang, M. T. (2025) · Molecular Biotechnology · doi:10.1007/s12033-025-01533-2 · Cited by 12

Authors: Maruyama, T., Dougan, S. K., Truttmann, M. C., Bilate, A. M., Ingram, J. R., & Ploegh, H. L.
Affiliations: Whitehead Institute for Biomedical Research (US)
Corresponding author: Ploegh, Hidde L
ORCID: Maruyama, Takeshi
Dougan, Stephanie K
Truttmann, Matthias C
Bilate, Angelina M
Ingram, Jessica R
Ploegh, Hidde L
Venue: Nature Biotechnology
Publisher: Springer Science and Business Media LLC
Published: 2015-03-23
Volume: 33
Issue: 5
Pages: 538-542
ISSN: 0733-222X (ISSN-L)
1087-0156
1546-1696
DOI: 10.1038/nbt.3190
PMC: PMC4618510
OpenAlex: W2008147758
Cited by: 1,137
References: 32
Citations by year: 2026: 39 · 2025: 58 · 2024: 62 · 2023: 67 · 2022: 108 · 2021: 101 · 2020: 117 · 2019: 122 · 2018: 125 · 2017: 139 · 2016: 143 · 2015: 55
FWCI: 66.47
Type: journal article
Language: en
Update notices: erratum (2016-02-05)
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Biotechnology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-sa)
PMC
Funders: National Institute of Allergy and Infectious Diseases (R01AI087879)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
Keywords: CRISPR/Cas9, genome editing efficiency, non-homologous end joining, homology-directed repair, DNA ligase IV, DNA double-strand break repair, zinc finger nucleases, TALEN
MeSH terms: DNA Ligase ATP, Animals, Cell Line, DNA Repair, Genetic Engineering, DNA Ligases, Pyrimidines, Schiff Bases, Zinc Fingers, Genome, Mice, DNA Breaks, Double-Stranded, Homologous Recombination, DNA End-Joining Repair, CRISPR-Cas Systems

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Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining

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