Cytosine, but not adenine, base editors induce genome-wide off-target mutations in rice
Abstract
Spotting off-targets from gene editing Unintended genomic modifications limit the potential therapeutic use of gene-editing tools. Available methods to find off-targets generally do not work in vivo or detect single-nucleotide changes. Three papers in this issue report new methods for monitoring gene-editing tools in vivo (see the Perspective by Kempton and Qi). Wienert et al. followed the recruitment of a DNA repair protein to DNA breaks induced by CRISPR-Cas9, enabling unbiased detection of off-target editing in cellular and animal models. Zuo et al. identified off-targets without the interference of natural genetic heterogeneity by injecting base editors into one blastomere of a two-cell mouse embryo and leaving the other genetically identical blastomere unedited. Jin et al. performed whole-genome sequencing on individual, genome-edited rice plants to identify unintended mutations. Cytosine, but not adenine, base editors induced numerous single-nucleotide variants in both mouse and rice. Science , this issue p. 286 , p. 289 , p. 292 ; see also p. 234
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CBE and ABE create new formats of off-target effects such as RNA editing and sgRNA-independent DNA editing.
“they create new formats of off-target effects such as RNA editing and sgRNA-independent DNA editing”
From Off-target effects in CRISPR/Cas9 gene editing (2023) · cites this paper as Jin et al., 2019
CBE and ABE greatly reduce classic off-target effects of CRISPR/Cas9 systems.
“Although CBE and ABE greatly reduce the classic off-target effects of CRISPR/Cas9 systems”
From Off-target effects in CRISPR/Cas9 gene editing (2023) · cites this paper as Jin et al., 2019
Previously it has been shown that cytidine but not adenine base editors result in significant, genome-wide, off-target effects.
“Previously it has been shown that cytidine but not adenine base editors result in significant, genome-wide, off-target effects57,69.”
From One-step generation of tumor models by base editor multiplexing in adult stem cell-derived organoids (2023) · cites this paper as [57]
Cites
The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041 · see citing works
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607 · see citing works
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., et al. (2010) · Genome Research · doi:10.1101/gr.107524.110 · Cited by 27,895 · see citing works
BEDTools: a flexible suite of utilities for comparing genomic features
Quinlan, A. R., & Hall, I. M. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq033 · Cited by 27,437 · see citing works
HISAT: a fast spliced aligner with low memory requirements
Kim, D., Langmead, B., & Salzberg, S. L. (2015) · Nature Methods · doi:10.1038/nmeth.3317 · Cited by 24,112 · see citing works
Fast and accurate long-read alignment with Burrows-Wheeler transform.
Li, H., & Durbin, R. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp698 · Cited by 12,063 · see citing works
Cingolani, P., Platts, A., Wang, L. L., Coon, M., Nguyen, T., Wang, L., Land, S. J., Lu, X., & Ruden, D. M. (2012) · Fly · doi:10.4161/fly.19695 · Cited by 11,816 · see citing works
Circos: An information aesthetic for comparative genomicsPreprint
Krzywinski, M. I., Schein, J. E., Birol, İ., Connors, J. M., Gascoyne, R. D., Horsman, D. E., Jones, S. J. M., & Marra, M. A. (2009) · Genome Research · doi:10.1101/gr.092759.109 · Cited by 10,838 · see citing works
Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration
Thorvaldsdottir, H., Robinson, J. T., & Mesirov, J. P. (2013) · Briefings in Bioinformatics · doi:10.1093/bib/bbs017 · Cited by 9,049 · see citing works
Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage
Komor, A. C., Kim, Y. B., Packer, M. S., Zuris, J. A., & Liu, D. R. (2016) · Nature · doi:10.1038/nature17946 · Cited by 5,437 · see citing works
Programmable base editing of A•T to G•C in genomic DNA without DNA cleavage
Gaudelli, N. M., Komor, A. C., Rees, H. A., Packer, M. S., Badran, A. H., Bryson, D. I., & Liu, D. R. (2017) · Nature · doi:10.1038/nature24644 · Cited by 4,184 · see citing works
VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R
Chen, H., & Boutros, P. C. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-35 · Cited by 3,150 · see citing works
ClinVar: public archive of interpretations of clinically relevant variants
Landrum, M. J., Lee, J. M., Benson, M., Brown, G., Chao, C., Chitipiralla, S., Gu, B., Hart, J., Hoffman, D., Hoover, J., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkv1222 · Cited by 2,758 · see citing works
Bae, S., Park, J., & Kim, J.-S. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu048 · Cited by 2,339 · see citing works
Base editing: precision chemistry on the genome and transcriptome of living cells
Rees, H. A., & Liu, D. R. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0059-1 · Cited by 1,675 · see citing works
Strelka2: fast and accurate calling of germline and somatic variants
Kim, S., Scheffler, K., Halpern, A. L., Bekritsky, M. A., Noh, E., Källberg, M., Chen, X., Kim, Y., Beyter, D., Krusche, P., et al. (2018) · Nature Methods · doi:10.1038/s41592-018-0051-x · Cited by 1,643 · see citing works
Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems
Nishida, K., Arazoe, T., Yachie, N., Banno, S., Kakimoto, M., Tabata, M., Mochizuki, M., Miyabe, A., Araki, M., Hara, K. Y., et al. (2016) · Science · doi:10.1126/science.aaf8729 · Cited by 1,349 · see citing works
Wilm, A., Aw, P. P. K., Bertrand, D., Yeo, G. H. T., Ong, S. H., Wong, C. H., Khor, C. C., Petric, R., Hibberd, M. L., & Nagarajan, N. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks918 · Cited by 1,338 · see citing works
Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion
Zong, Y., Wang, Y., Li, C., Zhang, R., Chen, K., Ran, Y., Qiu, J., Wang, D., & Gao, C. (2017) · Nature Biotechnology · doi:10.1038/nbt.3811 · Cited by 875 · see citing works
Cytosine base editor generates substantial off-target single-nucleotide variants in mouse embryos
Zuo, E., Sun, Y., Wei, W., Yuan, T., Ying, W., Sun, H., Yuan, L., Steinmetz, L. M., Li, Y., & Yang, H. (2019) · Science · doi:10.1126/science.aav9973 · Cited by 782 · see citing works
Kim, Y. B., Komor, A. C., Levy, J. M., Packer, M. S., Zhao, K. T., & Liu, D. R. (2017) · Nature Biotechnology · doi:10.1038/nbt.3803 · Cited by 756 · see citing works
RNA Editing Enzyme APOBEC1 and Some of Its Homologs Can Act as DNA Mutators
Harris, R. S., Petersen‐Mahrt, S. K., & Neuberger, M. S. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00742-6 · Cited by 604 · see citing works
Expanded base editing in rice and wheat using a Cas9-adenosine deaminase fusion
Li, C., Zong, Y., Wang, Y., Jin, S., Zhang, D., Song, Q., Zhang, R., & Gao, C. (2018) · Genome biology · doi:10.1186/s13059-018-1443-z · Cited by 499 · see citing works
An APOBEC3A-Cas9 base editor with minimized bystander and off-target activities
Gehrke, J. M., Cervantes, O., Clement, K., Wu, Y., Zeng, J., Bauer, D. E., Pinello, L., & Joung, J. K. (2018) · Nature Biotechnology · doi:10.1038/nbt.4199 · Cited by 433 · see citing works
Rees, H. A., Komor, A. C., Yeh, W.-H., Caetano‐Lopes, J., Warman, M. L., Edge, A. S. B., & Liu, D. R. (2017) · Nature Communications · doi:10.1038/ncomms15790 · Cited by 422 · see citing works
Single-Nucleotide Mutations for Plant Functional Genomics
Henikoff, S., & Comai, L. (2003) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.54.031902.135009 · Cited by 325 · see citing works
Rogozin, I. B., Iyer, L. M., Liang, L., Glazko, G. V., Liston, V. G., Pavlov, Y. I., Aravind, L., & Pancer, Z. (2007) · Nature Immunology · doi:10.1038/ni1463 · Cited by 311 · see citing works
Rapid and Efficient Gene Modification in Rice and Brachypodium Using TALENs
Shan, Q., Wang, Y., Chen, K., Liang, Z., Li, J., Zhang, Y., Zhang, K., Liu, J., Voytas, D. F., Zheng, X., et al. (2013) · Molecular Plant · doi:10.1093/mp/sss162 · Cited by 288 · see citing works
Genome-wide target specificities of CRISPR RNA-guided programmable deaminases
Kim, D., Lim, K., Kim, S., Yoon, S.-H., Kim, K., Ryu, S.-M., & Kim, J. (2017) · Nature Biotechnology · doi:10.1038/nbt.3852 · Cited by 275 · see citing works
MiR408 Regulates Grain Yield and Photosynthesis via a Phytocyanin Protein
Zhang, J., Yu, Y., Feng, Y., Zhou, Y.-F., Zhang, F., Yang, Y., Lei, M.-Q., Zhang, Y., & Chen, Y.-Q. (2017) · PLANT PHYSIOLOGY · doi:10.1104/pp.17.01169 · Cited by 174 · see citing works
Genome-wide profiling of adenine base editor specificity by EndoV-seq
Liang, P., Xie, X., Zhi, S., Sun, H., Zhang, X., Chen, Y., Chen, Y., Xiong, Y., Ma, W., Liu, D., et al. (2019) · Nature Communications · doi:10.1038/s41467-018-07988-z · Cited by 148 · see citing works
Targeting fidelity of adenine and cytosine base editors in mouse embryos
Lee, H., Willi, M., Miller, S. M., Kim, S., Liu, C., Liu, D. R., & Hennighausen, L. G. (2018) · Nature Communications · doi:10.1038/s41467-018-07322-7 · Cited by 82 · see citing works
Tian, Y., Ma, X., Lv, C., Sheng, X., Li, X., Zhao, R., Song, Y., Andl, T., Plikus, M. V., Sun, J., et al. (2017) · eLife · doi:10.7554/elife.29538 · Cited by 69 · see citing works
Radany, E. H., Dornfeld, K. J., Sanderson, R. J., Savage, M. K., Majumdar, A., Seidman, M. M., & Mosbaugh, D. W. (2000) · Mutation Research/DNA Repair · doi:10.1016/s0921-8777(00)00040-9 · Cited by 41 · see citing works
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Genome editing with CRISPR–Cas nucleases, base editors, transposases and prime editors
Anzalone, A. V., Koblan, L. W., & Liu, D. R. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0561-9 · Cited by 2,237 · see citing works
The next generation of CRISPR–Cas technologies and applications
Pickar-Oliver, A., & Gersbach, C. A. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0131-5 · Cited by 1,459 · see citing works
Genome engineering for crop improvement and future agriculture
Gao, C. (2021) · Cell · doi:10.1016/j.cell.2021.01.005 · Cited by 1,037 · see citing works
Cytosine base editor generates substantial off-target single-nucleotide variants in mouse embryos
Zuo, E., Sun, Y., Wei, W., Yuan, T., Ying, W., Sun, H., Yuan, L., Steinmetz, L. M., Li, Y., & Yang, H. (2019) · Science · doi:10.1126/science.aav9973 · Cited by 782 · see citing works
Off-target effects in CRISPR/Cas9 gene editing
Guo, C., Ma, X., Gao, F., & Guo, Y. (2023) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2023.1143157 · Cited by 625 · see citing works
“Although CBE and ABE greatly reduce the classic off-target effects of CRISPR/Cas9 systems, they create new formats of offtarget effects such as RNA editing and sgRNA-independent DNA editing (Grünewald et al., 2019; Jin et al., 2019; Zhou et al., 2019; Zuo et al., 2019).”
BackgroundLineage tracing meets single-cell omics: opportunities and challenges
Wagner, D. E., & Klein, A. M. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-0223-2 · Cited by 594 · see citing works
Prime editing for precise and highly versatile genome manipulation
Chen, P. J., & Liu, D. R. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-022-00541-1 · Cited by 621 · see citing works
Directed evolution of adenine base editors with increased activity and therapeutic application
Gaudelli, N. M., Lam, D. K., Rees, H. A., Solá-Esteves, N. M., Barrera, L. A., Born, D. A., Edwards, A., Gehrke, J. M., Lee, S., Liquori, A., et al. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0491-6 · Cited by 518 · see citing works
Off-target RNA mutation induced by DNA base editing and its elimination by mutagenesis
Zhou, C., Sun, Y., Yan, R., Liu, Y., Zuo, E., Gu, C., Han, L., Wei, Y., Hu, X., Zeng, R., et al. (2019) · Nature · doi:10.1038/s41586-019-1314-0 · Cited by 482 · see citing works
Evaluation and minimization of Cas9-independent off-target DNA editing by cytosine base editors
Doman, J. L., Raguram, A., Newby, G. A., & Liu, D. R. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0414-6 · Cited by 473 · see citing works
Base editing: advances and therapeutic opportunities
Porto, E. M., Komor, A. C., Slaymaker, I. M., & Yeo, G. W.-M. (2020) · Nature Reviews Drug Discovery · doi:10.1038/s41573-020-0084-6 · Cited by 475 · see citing works
A cytosine deaminase for programmable single-base RNA editing
Abudayyeh, O. O., Gootenberg, J. S., Franklin, B., Koob, J. G., Kellner, M. J., Ladha, A., Joung, J., Kirchgatterer, P. C., Cox, D. B. T., & Zhang, F. (2019) · Science · doi:10.1126/science.aax7063 · Cited by 456 · see citing works
Latest Developed Strategies to Minimize the Off-Target Effects in CRISPR-Cas-Mediated Genome Editing
Naeem, M., Majeed, S., Hoque, M. Z., & Ahmad, I. (2020) · Cells · doi:10.3390/cells9071608 · Cited by 457 · see citing works
Targeted, random mutagenesis of plant genes with dual cytosine and adenine base editors
Li, C., Zhang, R., Meng, X., Chen, S., Zong, Y., Lu, C., Qiu, J., Chen, Y., Li, J., & Gao, C. (2020) · Nature Biotechnology · doi:10.1038/s41587-019-0393-7 · Cited by 410 · see citing works
Precise plant genome editing using base editors and prime editors
Molla, K. A., Sretenovic, S., Bansal, K. C., & Qi, Y. (2021) · Nature Plants · doi:10.1038/s41477-021-00991-1 · Cited by 387 · see citing works
The emerging and uncultivated potential of CRISPR technology in plant science
Zhang, Y., Malzahn, A. A., Sretenovic, S., & Qi, Y. (2019) · Nature Plants · doi:10.1038/s41477-019-0461-5 · Cited by 404 · see citing works
In vivo adenine base editing of PCSK9 in macaques reduces LDL cholesterol levels
Rothgangl, T., Dennis, M. K., Lin, P. J. C., Oka, R., Witzigmann, D., Villiger, L., Qi, W., Hruzova, M., Kissling, L., Lenggenhager, D., et al. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-00933-4 · Cited by 378 · see citing works
Manghwar, H., Li, B., Ding, X. L., Hussain, A., Lindsey, K., Zhang, X., & Jin, S. (2020) · Advanced Science · doi:10.1002/advs.201902312 · Cited by 394 · see citing works
Continuous evolution of SpCas9 variants compatible with non-G PAMs
Miller, S. M., Wang, T., Randolph, P. B., Arbab, M., Shen, M. W., Huang, T. P., Matuszek, Ż., Newby, G. A., Rees, H. A., & Liu, D. R. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0412-8 · Cited by 347 · see citing works
CRISPR/Cas-Mediated Base Editing: Technical Considerations and Practical Applications
Molla, K. A., & Yang, Y. (2019) · Trends in biotechnology · doi:10.1016/j.tibtech.2019.03.008 · Cited by 336 · see citing works
Analysis and minimization of cellular RNA editing by DNA adenine base editors
Rees, H. A., Wilson, C., Doman, J. L., & Liu, D. R. (2019) · Science Advances · doi:10.1126/sciadv.aax5717 · Cited by 278 · see citing works
Programmable RNA editing by recruiting endogenous ADAR using engineered RNAs
Qu, L., Yi, Z., Zhu, S., Wang, C., Cao, Z., Zhou, Z. L., Yuan, P., Yu, Y. F., Tian, F., Liu, Z., et al. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0178-z · Cited by 287 · see citing works
Next-generation stem cells — ushering in a new era of cell-based therapies
Kimbrel, E. A., & Lanza, R. (2020) · Nature Reviews Drug Discovery · doi:10.1038/s41573-020-0064-x · Cited by 280 · see citing works
Neugebauer, M. E., Hsu, A., Arbab, M., Krasnow, N. A., McElroy, A. N., Pandey, S., Doman, J. L., Huang, T. P., Raguram, A., Banskota, S., et al. (2022) · Nature Biotechnology · doi:10.1038/s41587-022-01533-6 · Cited by 273 · see citing works
Dual base editor catalyzes both cytosine and adenine base conversions in human cells
Zhang, X., Zhu, B., Chen, L., Xie, L., Yu, W., Wang, Y., Li, L., Yin, S., Yang, L., Hu, H., et al. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0527-y · Cited by 270 · see citing works
Precision genome editing in plants: state-of-the-art in CRISPR/Cas9-based genome engineering
Wada, N., Ueta, R., Osakabe, Y., & Osakabe, K. (2020) · BMC Plant Biology · doi:10.1186/s12870-020-02385-5 · Cited by 271 · see citing works
CRISPR technologies for genome, epigenome and transcriptome editing
Villiger, L., Joung, J., Koblan, L. W., Weissman, J. S., Abudayyeh, O. O., & Gootenberg, J. S. (2024) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00697-6 · Cited by 264 · see citing works
Delivery of CRISPR-Cas tools for in vivo genome editing therapy: Trends and challenges
Taha, E. A., Lee, J., & Hotta, A. (2022) · Journal of Controlled Release · doi:10.1016/j.jconrel.2022.01.013 · Cited by 259 · see citing works
Anti-CRISPR protein applications: natural brakes for CRISPR-Cas technologies
Marino, N. D., Pinilla‐Redondo, R., Csörgő, B., & Bondy‐Denomy, J. (2020) · Nature Methods · doi:10.1038/s41592-020-0771-6 · Cited by 240 · see citing works
Precise correction of Duchenne muscular dystrophy exon deletion mutations by base and prime editing
Chemello, F., Chai, A. C., Li, H. Z., Rodríguez-Caycedo, C., Sanchez‐Ortiz, E., Atmanli, A., Mireault, A. A., Liu, N., Bassel‐Duby, R., & Olson, E. N. (2021) · Science Advances · doi:10.1126/sciadv.abg4910 · Cited by 250 · see citing works
Venn diagrams in bioinformatics
Jia, A., Xu, L., & Wang, Y. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab108 · Cited by 243 · see citing works
Webber, B. R., Lonetree, C.-L., Kluesner, M. G., Johnson, M. J., Pomeroy, E. J., Diers, M. D., Lahr, W. S., Draper, G. M., Slipek, N. J., Smeester, B. A., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-13007-6 · Cited by 232 · see citing works
Base editing in crops: current advances, limitations and future implications
Mishra, R., Joshi, R. K., & Zhao, K. (2019) · Plant Biotechnology Journal · doi:10.1111/pbi.13225 · Cited by 231 · see citing works
Treatment of a Mouse Model of ALS by In Vivo Base Editing
Lim, C. K. W., Gapinske, M., Brooks, A. K., Woods, W. S., Powell, J. E., C., M. A. Z., Winter, J., Pérez‐Piñera, P., & Gaj, T. (2020) · Molecular Therapy · doi:10.1016/j.ymthe.2020.01.005 · Cited by 225 · see citing works
CRISPR-Based Adenine Editors Correct Nonsense Mutations in a Cystic Fibrosis Organoid Biobank
Geurts, M. H., de Poel, E., Amatngalim, G. D., Oka, R., Meijers, F. M., Kruisselbrink, E., van Mourik, P., Berkers, G., de Winter-de Groot, K. M., Michel, S., et al. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.01.019 · Cited by 222 · see citing works
Zhao, H., Li, Y., He, L., Pu, W., Yu, W., Li, Y., Wu, Y., Xu, C., Wei, Y., Ding, Q., et al. (2019) · Circulation · doi:10.1161/circulationaha.119.042476 · Cited by 212 · see citing works
Assessing and advancing the safety of CRISPR-Cas tools: from DNA to RNA editing
Tao, J., Bauer, D. E., & Chiarle, R. (2023) · Nature Communications · doi:10.1038/s41467-023-35886-6 · Cited by 215 · see citing works
Highly efficient DSB-free base editing for streptomycetes with CRISPR-BEST
Tong, Y., Whitford, C. M., Robertsen, H. L., Blin, K., Jørgensen, T. S., Klitgaard, A., Gren, T., Jiang, X., Weber, T., & Lee, S. Y. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1913493116 · Cited by 201 · see citing works
Engineered materials for in vivo delivery of genome-editing machinery
Tong, S., Moyo, B., Lee, C. M., Leong, K. W., & Bao, G. (2019) · Nature Reviews Materials · doi:10.1038/s41578-019-0145-9 · Cited by 206 · see citing works
Recent advances in the CRISPR genome editing tool set
Moon, S. B., Kim, D. Y., Ko, J., & Kim, Y.-S. (2019) · Experimental & Molecular Medicine · doi:10.1038/s12276-019-0339-7 · Cited by 208 · see citing works
Engineering a precise adenine base editor with minimal bystander editing
Chen, L., Zhang, S., Xue, N., Hong, M., Zhang, X., Zhang, D., Yang, J., Bai, S., Huang, Y., Meng, H., et al. (2023) · Nature Chemical Biology · doi:10.1038/s41589-022-01163-8 · Cited by 202 · see citing works
In vivo somatic cell base editing and prime editing
Newby, G. A., & Liu, D. R. (2021) · Molecular Therapy · doi:10.1016/j.ymthe.2021.09.002 · Cited by 192 · see citing works
Yu, Y., Leete, T., Born, D. A., Young, L., Barrera, L. A., Lee, S., Rees, H. A., Ciaramella, G., & Gaudelli, N. M. (2020) · Nature Communications · doi:10.1038/s41467-020-15887-5 · Cited by 190 · see citing works
Gene editing and CRISPR in the clinic: current and future perspectives
Hirakawa, M. P., Krishnakumar, R., Timlin, J. A., Carney, J. P., & Butler, K. S. (2020) · Bioscience Reports · doi:10.1042/bsr20200127 · Cited by 197 · see citing works
CRISPR-Cas Tools and Their Application in Genetic Engineering of Human Stem Cells and Organoids
Hendriks, D. F. G., Clevers, H. C., & Artegiani, B. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.10.014 · Cited by 196 · see citing works
Yi, Z., Qu, L., Tang, H., Liu, Z., Liu, Y., Tian, F., Wang, C., Zhang, X., Feng, Z., Yu, Y. F., et al. (2022) · Nature Biotechnology · doi:10.1038/s41587-021-01180-3 · Cited by 185 · see citing works
Yeh, W.-H., Shubina-Oleinik, O., Levy, J. M., Pan, B., Newby, G. A., Wornow, M., Burt, R., Chen, J. C., Holt, J. R., & Liu, D. R. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.aay9101 · Cited by 179 · see citing works
Development of CRISPR-Cas systems for genome editing and beyond
Zhang, F. (2019) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583519000052 · Cited by 185 · see citing works
Fine-tuning sugar content in strawberry
Xing, S., Chen, K., Zhu, H., Zhang, R., Zhang, H., Li, B., & Gao, C. (2020) · Genome biology · doi:10.1186/s13059-020-02146-5 · Cited by 178 · see citing works
Rationally designed APOBEC3B cytosine base editors with improved specificity
Jin, S., Fei, H., Zhu, Z., Luo, Y., Liu, J., Gao, S., Zhang, F., Chen, Y.-H., Wang, Y., & Gao, C. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.07.005 · Cited by 159 · see citing works
Perspectives on the Application of Genome-Editing Technologies in Crop Breeding
Hua, K., Zhang, J., Botella, J. R., Ma, C., Kong, F., Liu, B., & Zhu, J. (2019) · Molecular Plant · doi:10.1016/j.molp.2019.06.009 · Cited by 170 · see citing works
Engineering source-sink relations by prime editing confers heat-stress resilience in tomato and rice
Lou, H. F., Li, S., Shi, Z., Zou, Y.-P., Zhang, Y., Huang, X., Yang, D., Yang, Y., Li, Z., & Cao, X. (2024) · Cell · doi:10.1016/j.cell.2024.11.005 · Cited by 167 · see citing works
Suh, S., Choi, E. H., Leinonen, H., Foik, A. T., Newby, G. A., Yeh, W.-H., Dong, Z., Kiser, P. D., Lyon, D. C., Liu, D. R., et al. (2020) · Nature Biomedical Engineering · doi:10.1038/s41551-020-00632-6 · Cited by 162 · see citing works
Everette, K. A., Newby, G. A., Levine, R. M., Mayberry, K. D., Jang, Y., Mayuranathan, T., Nimmagadda, N., Dempsey, E., Li, Y., Bhoopalan, S. V., et al. (2023) · Nature Biomedical Engineering · doi:10.1038/s41551-023-01026-0 · Cited by 167 · see citing works
Zuo, E., Sun, Y., Yuan, T., He, B., Zhou, C., Ying, W., Liu, J., Wu, W., Zeng, R., Li, Y., et al. (2020) · Nature Methods · doi:10.1038/s41592-020-0832-x · Cited by 164 · see citing works
Chen, L., Zhu, B., Ru, G., Meng, H., Yan, Y., Hong, M., Zhang, D., Luan, C., Zhang, S., Wu, H., et al. (2023) · Nature Biotechnology · doi:10.1038/s41587-022-01532-7 · Cited by 156 · see citing works
Ahmad, S., Wei, X., Sheng, Z., Hu, P., & Tang, S. (2019) · Briefings in Functional Genomics · doi:10.1093/bfgp/elz041 · Cited by 153 · see citing works
Current Status and Challenges of DNA Base Editing Tools
Jeong, Y. K., Song, B., & Bae, S. (2020) · Molecular Therapy · doi:10.1016/j.ymthe.2020.07.021 · Cited by 153 · see citing works
Improved plant cytosine base editors with high editing activity, purity, and specificity
Ren, Q., Sretenovic, S., Liu, G., Zhong, Z., Wang, J., Huang, L., Tang, X., Guo, Y., Liu, L., Wu, Y., et al. (2021) · Plant Biotechnology Journal · doi:10.1111/pbi.13635 · Cited by 131 · see citing works
Evaluating CRISPR-based prime editing for cancer modeling and CFTR repair in organoids
Geurts, M. H., de Poel, E., Pleguezuelos-Manzano, C., Oka, R., Carrillo, L., Andersson-Rolf, A., Boretto, M., Brunsveld, J. E., van Boxtel, R., Beekman, J. M., et al. (2021) · Life Science Alliance · doi:10.26508/lsa.202000940 · Cited by 151 · see citing works
Construct design for CRISPR/Cas-based genome editing in plants
Hassan, M. M., Zhang, Y., Yuan, G., De, K., Chen, J., Muchero, W., Tuskan, G. A., Qi, Y., & Yang, X. (2021) · Trends in Plant Science · doi:10.1016/j.tplants.2021.06.015 · Cited by 136 · see citing works
Adenine base editors catalyze cytosine conversions in human cells
Kim, H. S., Jeong, Y. K., Hur, J. K., Kim, J., & Bae, S. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0254-4 · Cited by 127 · see citing works
Improved cytosine base editors generated from TadA variants
Lam, D. K., Feliciano, P. R., Arif, A., Bohnuud, T., Fernandez, T. P., Gehrke, J. M., Grayson, P., Lee, K. D., Ortega, M. A., Sawyer, C. B., et al. (2023) · Nature Biotechnology · doi:10.1038/s41587-022-01611-9 · Cited by 138 · see citing works
CRISPR–Cas applications in agriculture and plant research
Tuncel, A., Pan, C., Clem, J. S., Liu, D., & Qi, Y. (2025) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-025-00834-3 · Cited by 139 · see citing works
Genome-wide specificity of prime editors in plants
Jin, S., Lin, Q., Luo, Y., Zhu, Z., Liu, G., Li, Y., Chen, K., Qiu, J., & Gao, C. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-00891-x · Cited by 127 · see citing works
Mitochondrial base editor induces substantial nuclear off-target mutations
Lei, Z.-X., Meng, H., Liu, L., Zhao, H., Rao, X., Yan, Y., Wu, H., Liu, M., He, A., & Yi, C. (2022) · Nature · doi:10.1038/s41586-022-04836-5 · Cited by 118 · see citing works
The Solanum tuberosum GBSSI gene: a target for assessing gene and base editing in tetraploid potato
Veillet, F., Chauvin, L., Kermarrec, M.-P., Sevestre, F., Merrer, M., Terret, Z., Szydlowski, N., Devaux, P., Gallois, J.-L., & Chauvin, J.-E. (2019) · Plant Cell Reports · doi:10.1007/s00299-019-02426-w · Cited by 124 · see citing works
Genome editing for plant research and crop improvement
Zhan, X., Lu, Y., Zhu, J., & Botella, J. R. (2020) · Journal of Integrative Plant Biology · doi:10.1111/jipb.13063 · Cited by 121 · see citing works
Efficient base editing for multiple genes and loci in pigs using base editors
Xie, J., Ge, W., Li, N., Liu, Q., Chen, F., Yang, X., Huang, X., Ouyang, Z., Zhang, Q., Zhao, Y., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10421-8 · Cited by 122 · see citing works
Sürün, D., Schneider, A., Mircetic, J., Neumann, K., Lansing, F., Paszkowski‐Rogacz, M., Hänchen, V., Lee‐Kirsch, M. A., & Buchholz, F. (2020) · Genes · doi:10.3390/genes11050511 · Cited by 121 · see citing works
Base editing in plants: Current status and challenges
Bharat, S. S., Li, S., Li, J., Yan, L., & Xia, L. (2019) · The Crop Journal · doi:10.1016/j.cj.2019.10.002 · Cited by 123 · see citing works
CRISPR Modeling and Correction of Cardiovascular Disease
Liu, N., & Olson, E. N. (2022) · Circulation Research · doi:10.1161/circresaha.122.320496 · Cited by 118 · see citing works
Neumann, E. N., Bertozzi, T. M., Wu, E., Serack, F. E., Harvey, J. W., Brauer, P. P., Pirtle, C. P., Coffey, A. A., Howard, M., Kamath, N., et al. (2024) · Science · doi:10.1126/science.ado7082 · Cited by 120 · see citing works
Plant Genome Editing and the Relevance of Off-Target Changes
Graham, N. D., Patil, G., Bubeck, D. M., Dobert, R. C., Glenn, K. C., Gutsche, A. T., Kumar, S., Lindbo, J. A., Maas, L., May, G. D., et al. (2020) · PLANT PHYSIOLOGY · doi:10.1104/pp.19.01194 · Cited by 118 · see citing works
Target base editing in soybean using a modified CRISPR/Cas9 system
Cai, Y., Chen, L., Zhang, Y., Yuan, S., Su, Q., Sun, S., Wu, C., Yao, W., Han, T., & Hou, W. (2020) · Plant Biotechnology Journal · doi:10.1111/pbi.13386 · Cited by 112 · see citing works
Efficient precise in vivo base editing in adult dystrophic mice
Xu, L. M., Zhang, C., Bailin, P. L., Wang, P., Gao, Y., Mohler, P. J., Mokadam, N. A., Ma, J., Arnold, W. D., & Han, R. (2021) · Nature Communications · doi:10.1038/s41467-021-23996-y · Cited by 109 · see citing works
CRISPR-Based Gene Therapies: From Preclinical to Clinical Treatments
Laurent, M., Geoffroy, M., Pavani, G., & Guiraud, S. (2024) · Cells · doi:10.3390/cells13100800 · Cited by 122 · see citing works
Tools for experimental and computational analyses of off-target editing by programmable nucleases
Bao, X. R., Pan, Y., Lee, C. M., Davis, T. H., & Bao, G. (2021) · Nature Protocols · doi:10.1038/s41596-020-00431-y · Cited by 106 · see citing works
CRISPR/Cas brings plant biology and breeding into the fast lane
Schindele, A., Dorn, A., & Puchta, H. (2019) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2019.08.006 · Cited by 110 · see citing works
Li, Y., Zhu, J., Wu, H., Liu, C., Huang, C., Lan, J., Zhao, Y., & Xie, C. (2019) · The Crop Journal · doi:10.1016/j.cj.2019.10.001 · Cited by 112 · see citing works
Structure-based functional mechanisms and biotechnology applications of anti-CRISPR proteins
Jia, N., & Patel, D. J. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00371-9 · Cited by 108 · see citing works
Allogeneic CAR-T Therapy Technologies: Has the Promise Been Met?
Lonez, C., & Breman, E. (2024) · Cells · doi:10.3390/cells13020146 · Cited by 113 · see citing works
CRISPR technologies for stem cell engineering and regenerative medicine
Hsu, M., Chang, Y., Truong, V. A., Lai, P., Nguyen, T. K. N., & Hu, Y. (2019) · Biotechnology Advances · doi:10.1016/j.biotechadv.2019.107447 · Cited by 105 · see citing works
Eliminating base-editor-induced genome-wide and transcriptome-wide off-target mutations
Wang, L., Xue, W., Zhang, H., Gao, R., Qiu, H.-Y., Wei, J., Zhou, L., Lei, Y.-N., Wu, X., Li, X., et al. (2021) · Nature Cell Biology · doi:10.1038/s41556-021-00671-4 · Cited by 103 · see citing works
CRISPR engineering in organoids for gene repair and disease modelling
Geurts, M. H., & Clevers, H. (2023) · Nature Reviews Bioengineering · doi:10.1038/s44222-022-00013-5 · Cited by 103 · see citing works
Generating broad-spectrum tolerance to ALS-inhibiting herbicides in rice by base editing
Zhang, R., Chen, S., Meng, X., Chai, Z., Wang, D., Yuan, Y., Chen, K., Jiang, L., Li, J., & Gao, C. (2020) · Science China Life Sciences · doi:10.1007/s11427-020-1800-5 · Cited by 101 · see citing works
Wang, Y., Wang, Z., Chen, Y., Hua, X., Yu, Y., & Ji, Q. (2019) · Cell chemical biology · doi:10.1016/j.chembiol.2019.09.003 · Cited by 93 · see citing works
Green Revolution to Gene Revolution: Technological Advances in Agriculture to Feed the World
Hamdan, M. F., Noor, S. N. M., Abd-Aziz, N., Pua, T., & Tan, B. C. (2022) · Plants · doi:10.3390/plants11101297 · Cited by 101 · see citing works
Nadakuduti, S. S., & Enciso-Rodríguez, F. E. (2021) · Frontiers in Plant Science · doi:10.3389/fpls.2020.637159 · Cited by 98 · see citing works
Reverse-genetics studies of lncRNAs—what we have learnt and paths forward
Gao, F., Cai, Y., Kapranov, P., & Xu, D. (2020) · Genome biology · doi:10.1186/s13059-020-01994-5 · Cited by 92 · see citing works
High-purity production and precise editing of DNA base editing ribonucleoproteins
Jang, H.-K., Jo, D. H., Lee, S.-N., Cho, C. S., Jeong, Y. K., Jung, Y., Yu, J., Kim, J. H., Woo, J.-S., & Bae, S. (2021) · Science Advances · doi:10.1126/sciadv.abg2661 · Cited by 93 · see citing works
Off-Target Editing by CRISPR-Guided DNA Base Editors
Park, S., & Beal, P. A. (2019) · Biochemistry · doi:10.1021/acs.biochem.9b00573 · Cited by 92 · see citing works
CRISPR/Cas genome editing improves abiotic and biotic stress tolerance of crops
Li, Y., Wu, X., Zhang, Y., & Zhang, Q. (2022) · Frontiers in Genome Editing · doi:10.3389/fgeed.2022.987817 · Cited by 96 · see citing works
Plant base editing and prime editing: The current status and future perspectives
Li, J., Zhang, C., He, Y., Li, S., Yan, L., Li, Y., Zhu, Z., & Xia, L. (2022) · Journal of Integrative Plant Biology · doi:10.1111/jipb.13425 · Cited by 93 · see citing works
Fei, H., Li, Y., Liu, Y., Wei, J., Chen, A. A., & Gao, C. (2025) · Cell · doi:10.1016/j.cell.2025.06.014 · Cited by 92 · see citing works
Development and Application of Base Editors
Yang, B., Yang, L. C., & Chen, J. (2019) · The CRISPR Journal · doi:10.1089/crispr.2019.0001 · Cited by 86 · see citing works
Glycosylase-based base editors for efficient T-to-G and C-to-G editing in mammalian cells
Ye, L., Zhao, D., Li, J., Wang, Y., Li, B., Yang, Y., Hou, X., Wang, H., Wei, Z., Liu, X., et al. (2024) · Nature Biotechnology · doi:10.1038/s41587-023-02050-w · Cited by 88 · see citing works
Base editing with high efficiency in allotetraploid oilseed rape by A3A‐PBE system
Cheng, H., Hao, M., Ding, B., Mei, D., Wang, W., Wang, H., Zhou, R., Liu, J., Li, C., & Hu, Q. (2020) · Plant Biotechnology Journal · doi:10.1111/pbi.13444 · Cited by 83 · see citing works
Rationally Designed Base Editors for Precise Editing of the Sickle Cell Disease Mutation
Chu, S. H., Packer, M. S., Rees, H. A., Lam, D. K., Yu, Y., Marshall, J., Cheng, L.-I., Lam, D., Olins, J., Ran, F. A., et al. (2021) · The CRISPR Journal · doi:10.1089/crispr.2020.0144 · Cited by 79 · see citing works
- Authors
- Jin, S., Zong, Y., Gao, Q., Zhu, Z., Wang, Y., Qin, P., Liang, C., Wang, D., Qiu, J.-L., Zhang, F., & Gao, C.
- Affiliations
- Chinese Academy of Sciences (CN)
- Sichuan Agricultural University (CN)
- University of Minnesota (US)
- Corresponding author
- Jin, Shuai
- Zong, Yuan
- Gao, Qiang
- Gao, Caixia
- ORCID
- Venue
- Science
- Published
- 2019-04-19
- Volume
- 364
- Issue
- 6437
- Pages
- 292-295
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2917855738
- Cited by
- 665
- References
- 34
- Citations by year
- 2026: 49 · 2025: 59 · 2024: 74 · 2023: 85 · 2022: 91 · 2021: 98 · 2020: 124 · 2019: 83
- FWCI
- 32.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (31788103)
- Chinese Academy of Sciences (QYZDY-SSW-SMC030)
- National Key Research and Development Program of China (2016YFD0101804)
- college of biological sciences, University of Minnesota startup funding
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Genetic and Mutation Studies
- Keywords
- base editors, cytosine base editors, adenine base editors, off-target mutations, single nucleotide variants, CRISPR/Cas9, genome editing, rice, single-cell whole-genome sequencing
- MeSH terms
- Gene Editing, Whole Genome Sequencing, Adenine, Cytosine, DNA Mutational Analysis, Mutation, Oryza, Polymorphism, Single Nucleotide, Agrobacterium
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