Off-target Effects in CRISPR/Cas9-mediated Genome Engineering

Molecular Therapy - Nucleic Acids - Tập 4 - Trang e264 - 2015
Xiao-Hui Zhang1,2, Louis Y Tee3, Xiao-Gang Wang4, Qun-Shan Huang1, Shi-Hua Yang1
1Guangdong Provincial Key Laboratory of Prevention and Control for Severe Clinical Animal Diseases, College of Veterinary Medicine, South China Agricultural University, Guangzhou, China
2Faculty of Life Science and Technology, Kunming University of Science and Technology, Kunming, China
3McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
4Department of Cell Biology & Institute of Biomedicine, College of Life Science and Technology, Jinan University, Guangzhou, China

Tài liệu tham khảo

Mali, 2013, RNA-guided human genome engineering via Cas9, Science, 339, 823, 10.1126/science.1232033 Cong, 2013, Multiplex genome engineering using CRISPR/Cas systems, Science, 339, 819, 10.1126/science.1231143 Hsu, 2014, Development and applications of CRISPR-Cas9 for genome engineering, Cell, 157, 1262, 10.1016/j.cell.2014.05.010 Doudna, 2014, Genome editing. The new frontier of genome engineering with CRISPR-Cas9, Science, 346, 1258096, 10.1126/science.1258096 Cox, 2015, Therapeutic genome editing: prospects and challenges, Nat Med, 21, 121, 10.1038/nm.3793 Smith, 2015, Efficient and allele-specific genome editing of disease loci in human iPSCs, Mol Ther, 23, 570, 10.1038/mt.2014.226 Mali, 2013, CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering, Nat Biotechnol, 31, 833, 10.1038/nbt.2675 Hsu, 2013, DNA targeting specificity of RNA-guided Cas9 nucleases, Nat Biotechnol, 31, 827, 10.1038/nbt.2647 Pattanayak, 2013, High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity, Nat Biotechnol, 31, 839, 10.1038/nbt.2673 Fu, 2013, High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells, Nat Biotechnol, 31, 822, 10.1038/nbt.2623 Cho, 2014, Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases, Genome Res, 24, 132, 10.1101/gr.162339.113 Corrigan-Curay, 2015, Genome editing technologies: defining a path to clinic, Mol Ther, 23, 796, 10.1038/mt.2015.54 Horvath, 2010, CRISPR/Cas, the immune system of bacteria and archaea, Science, 327, 167, 10.1126/science.1179555 Gasiunas, 2012, Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria, Proc Natl Acad Sci USA, 109, E2579, 10.1073/pnas.1208507109 Jinek, 2012, A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity, Science, 337, 816, 10.1126/science.1225829 Mojica, 2009, Short motif sequences determine the targets of the prokaryotic CRISPR defence system, Microbiology, 155, 733, 10.1099/mic.0.023960-0 Sternberg, 2014, DNA interrogation by the CRISPR RNA-guided endonuclease Cas9, Nature, 507, 62, 10.1038/nature13011 Anders, 2014, Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease, Nature, 513, 569, 10.1038/nature13579 Nishimasu, 2014, Crystal structure of Cas9 in complex with guide RNA and target DNA, Cell, 156, 935, 10.1016/j.cell.2014.02.001 Jinek, 2014, Structures of Cas9 endonucleases reveal RNA-mediated conformational activation, Science, 343, 1247997, 10.1126/science.1247997 Wu, 2014, Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells, Nat Biotechnol, 32, 670, 10.1038/nbt.2889 Duan, 2014, Genome-wide identification of CRISPR/Cas9 off-targets in human genome, Cell Res, 24, 1009, 10.1038/cr.2014.87 Jiang, 2013, RNA-guided editing of bacterial genomes using CRISPR-Cas systems, Nat Biotechnol, 31, 233, 10.1038/nbt.2508 Cencic, 2014, Protospacer adjacent motif (PAM)-distal sequences engage CRISPR Cas9 DNA target cleavage, PLoS One, 9, e109213, 10.1371/journal.pone.0109213 Wang, 2014, Genetic screens in human cells using the CRISPR-Cas9 system, Science, 343, 80, 10.1126/science.1246981 Doench, 2014, Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation, Nat Biotechnol, 32, 1262, 10.1038/nbt.3026 Ren, 2014, Enhanced specificity and efficiency of the CRISPR/Cas9 system with optimized sgRNA parameters in Drosophila, Cell Rep, 9, 1151, 10.1016/j.celrep.2014.09.044 Gagnon, 2014, Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs, PLoS One, 9, e98186, 10.1371/journal.pone.0098186 Moreno-Mateos, 2015, CRISPRscan: designing highly efficient sgRNAs for CRISPR-Cas9 targeting in vivo, Nat Methods, 12, 982, 10.1038/nmeth.3543 Kuscu, 2014, Genome-wide analysis reveals characteristics of off-target sites bound by the Cas9 endonuclease, Nat Biotechnol, 32, 677, 10.1038/nbt.2916 Zhang, 2014, Comparison of non-canonical PAMs for CRISPR/Cas9-mediated DNA cleavage in human cells, Sci Rep, 4, 5405, 10.1038/srep05405 Kleinstiver, 2015, Engineered CRISPR-Cas9 nucleases with altered PAM specificities, Nature, 523, 481, 10.1038/nature14592 Kim, 2014, Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins, Genome Res, 24, 1012, 10.1101/gr.171322.113 Ramakrishna, 2014, Gene disruption by cell-penetrating peptide-mediated delivery of Cas9 protein and guide RNA, Genome Res, 24, 1020, 10.1101/gr.171264.113 Smith, 2014, Whole-genome sequencing analysis reveals high specificity of CRISPR/Cas9 and TALEN-based genome editing in human iPSCs, Cell Stem Cell, 15, 12, 10.1016/j.stem.2014.06.011 Veres, 2014, Low incidence of off-target mutations in individual CRISPR-Cas9 and TALEN targeted human stem cell clones detected by whole-genome sequencing, Cell Stem Cell, 15, 27, 10.1016/j.stem.2014.04.020 Yu, 2015, Small molecules enhance CRISPR genome editing in pluripotent stem cells, Cell Stem Cell, 16, 142, 10.1016/j.stem.2015.01.003 Gabriel, 2015, Mapping the precision of genome editing, Nat Biotechnol, 33, 150, 10.1038/nbt.3142 Cho, 2013, Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease, Nat Biotechnol, 31, 230, 10.1038/nbt.2507 Kim, 2009, Targeted genome editing in human cells with zinc finger nucleases constructed via modular assembly, Genome Res, 19, 1279, 10.1101/gr.089417.108 Ran, 2013, Genome engineering using the CRISPR-Cas9 system, Nat Protoc, 8, 2281, 10.1038/nprot.2013.143 Heigwer, 2014, E-CRISP: fast CRISPR target site identification, Nat Methods, 11, 122, 10.1038/nmeth.2812 Singh, 2015, Cas9-chromatin binding information enables more accurate CRISPR off-target prediction, Nucleic Acids Res, 43, e118, 10.1093/nar/gkv575 Hendel, 2015, Quantifying on- and off-target genome editing, Trends Biotechnol, 33, 132, 10.1016/j.tibtech.2014.12.001 Tsai, 2015, GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases, Nat Biotechnol, 33, 187, 10.1038/nbt.3117 Frock, 2015, Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases, Nat Biotechnol, 33, 179, 10.1038/nbt.3101 Gabriel, 2011, An unbiased genome-wide analysis of zinc-finger nuclease specificity, Nat Biotechnol, 29, 816, 10.1038/nbt.1948 Osborn, 2013, TALEN-based gene correction for epidermolysis bullosa, Mol Ther, 21, 1151, 10.1038/mt.2013.56 Wang, 2015, Unbiased detection of off-target cleavage by CRISPR-Cas9 and TALENs using integrase-defective lentiviral vectors, Nat Biotechnol, 33, 175, 10.1038/nbt.3127 Kim, 2015, Digenome-seq: genome-wide profiling of CRISPR-Cas9 off-target effects in human cells, Nat Methods, 12, 237, 10.1038/nmeth.3284 Paulis, 2015, A pre-screening FISH-based method to detect CRISPR/Cas9 off-targets in mouse embryonic stem cells, Sci Rep, 5, 12327, 10.1038/srep12327 Iyer, 2015, Off-target mutations are rare in Cas9-modified mice, Nat Methods, 12, 479, 10.1038/nmeth.3408 Shen, 2013, Generation of gene-modified mice via Cas9/RNA-mediated gene targeting, Cell Res, 23, 720, 10.1038/cr.2013.46 Hai, 2014, One-step generation of knockout pigs by zygote injection of CRISPR/Cas system, Cell Res, 24, 372, 10.1038/cr.2014.11 Wan, 2015, One-step generation of p53 gene biallelic mutant Cynomolgus monkey via the CRISPR/Cas system, Cell Res, 25, 258, 10.1038/cr.2014.158 Niu, 2014, Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos, Cell, 156, 836, 10.1016/j.cell.2014.01.027 Shen, 2014, Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects, Nat Methods, 11, 399, 10.1038/nmeth.2857 Li, 2013, Heritable gene targeting in the mouse and rat using a CRISPR-Cas system, Nat Biotechnol, 31, 681, 10.1038/nbt.2661 Fu, 2014, Improving CRISPR-Cas nuclease specificity using truncated guide RNAs, Nat Biotechnol, 32, 279, 10.1038/nbt.2808 Rusk, 2015, Next-generation CRISPRs, Nat Methods, 12, 36, 10.1038/nmeth.3237 Ran, 2013, Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity, Cell, 154, 1380, 10.1016/j.cell.2013.08.021 Guilinger, 2014, Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification, Nat Biotechnol, 32, 577, 10.1038/nbt.2909 Tsai, 2014, Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing, Nat Biotechnol, 32, 569, 10.1038/nbt.2908 Wyvekens, 2015, Dimeric CRISPR RNA-Guided FokI-dCas9 Nucleases Directed by Truncated gRNAs for Highly Specific Genome Editing, Hum Gene Ther, 26, 425, 10.1089/hum.2015.084 Maruyama, 2015, Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining, Nat Biotechnol, 33, 538, 10.1038/nbt.3190 Hendel, 2015, Chemically modified guide RNAs enhance CRISPR-Cas genome editing in human primary cells, Nat Biotechnol, 6, 1 Sanjana, 2014, Improved vectors and genome-wide libraries for CRISPR screening, Nat Methods, 11, 783, 10.1038/nmeth.3047 Konermann, 2015, Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex, Nature, 517, 583, 10.1038/nature14136 Gilbert, 2013, CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes, Cell, 154, 442, 10.1016/j.cell.2013.06.044 Maeder, 2013, CRISPR RNA-guided activation of endogenous human genes, Nat Methods, 10, 977, 10.1038/nmeth.2598 Qi, 2013, Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression, Cell, 152, 1173, 10.1016/j.cell.2013.02.022 Cheng, 2013, Multiplexed activation of endogenous genes by CRISPR-on, an RNA-guided transcriptional activator system, Cell Res, 23, 1163, 10.1038/cr.2013.122 Zetsche, 2015, A split-Cas9 architecture for inducible genome editing and transcription modulation, Nat Biotechnol, 33, 139, 10.1038/nbt.3149 Ranganathan, 2014, Expansion of the CRISPR-Cas9 genome targeting space through the use of H1 promoter-expressed guide RNAs, Nat Commun, 5, 4516, 10.1038/ncomms5516 Zetsche, 2015, Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system, Cell, 163, 1, 10.1016/j.cell.2015.09.038 Smith, 2013, DNA methylation: roles in mammalian development, Nat Rev Genet, 14, 204, 10.1038/nrg3354 Deisseroth, 2011, Optogenetics, Nat Methods, 8, 26, 10.1038/nmeth.f.324 Polstein, 2015, A light-inducible CRISPR-Cas9 system for control of endogenous gene activation, Nat Chem Biol, 11, 198, 10.1038/nchembio.1753 Gondo, 2008, Trends in large-scale mouse mutagenesis: from genetics to functional genomics, Nat Rev Genet, 9, 803, 10.1038/nrg2431 Lada, 2013, Genome-wide mutation avalanches induced in diploid yeast cells by a base analog or an APOBEC deaminase, PLoS Genet, 9, e1003736, 10.1371/journal.pgen.1003736 Bauer, 1968, The interaction of closed circular DNA with intercalative dyes. I. The superhelix density of SV40 DNA in the presence and absence of dye, J Mol Biol, 33, 141, 10.1016/0022-2836(68)90286-6