Genome-wide detection of CRISPR editing in vivo using GUIDE-tag
Open accessAbstract
Analysis of off-target editing is an important aspect of the development of safe nuclease-based genome editing therapeutics. in vivo assessment of nuclease off-target activity has primarily been indirect (based on discovery in vitro, in cells or via computational prediction) or through ChIP-based detection of double-strand break (DSB) DNA repair factors, which can be cumbersome. Herein we describe GUIDE-tag, which enables one-step, off-target genome editing analysis in mouse liver and lung. The GUIDE-tag system utilizes tethering between the Cas9 nuclease and the DNA donor to increase the capture rate of nuclease-mediated DSBs and UMI incorporation via Tn5 tagmentation to avoid PCR bias. These components can be delivered as SpyCas9-mSA ribonucleoprotein complexes and biotin-dsDNA donor for in vivo editing analysis. GUIDE-tag enables detection of off-target sites where editing rates are ≥ 0.2%. UDiTaS analysis utilizing the same tagmented genomic DNA detects low frequency translocation events with off-target sites and large deletions in vivo. The SpyCas9-mSA and biotin-dsDNA system provides a method to capture DSB loci in vivo in a variety of tissues with a workflow that is amenable to analysis of gross genomic alterations that are associated with genome editing.
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GUIDE-tag was derived from GUIDE-seq but with an improved dsODN capture system to increase the discovery rate of DSBs.
“GUIDE-tag was derived from GUIDE-seq but with an improved dsODN capture system to increase the discovery rate of DSBs (Liang et al., 2022).”
From Off-target effects in CRISPR/Cas9 gene editing (2023) · cites this paper as Liang et al., 2022
The Results section, “One step quantification of on-target insertion and genome-wide off-target sites in vivo” (page unavailable), links GUIDE-tag to GUIDE-seq’s DNA-tagging approach. The Results section, “Examining alternate forms of biotinylated donors for GUIDE-tag analysis” (page unavailable), reports only a modest increase in synthetic donor integration in mice and higher integration for an internally biotinylated dsODN in cell culture. These passages support improved tag capture in some conditions, but do not establish an increased DSB discovery rate relative to GUIDE-seq. (LLM, conf=0.84)
Experimental — accuracy not yet measuredAmong the 26 off-target sites originally detected by Discover-seq, GUIDE-tag successfully captures 24, and GUIDE-tag uncovers 16 new off-target sites that were not discovered by Discover-seq.
“Among the 26 off-target sites that were originally detected by Discover-seq, GUIDE-tag successfully captures 24. In addition, GUIDE-tag uncovers 16 new off-target sites that were not discovered by Discover-seq (Liang et al., 2022).”
From Off-target effects in CRISPR/Cas9 gene editing (2023) · cites this paper as Liang et al., 2022
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Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · 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
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
Gentleman R: R: A language for data analysis and graphics
Ihaka, R., & Gentleman, R. (1996) · Journal of Computational and Graphical Statistics · doi:10.1080/10618600.1996.10474713 · Cited by 11,747 · see citing works
Genome engineering using the CRISPR-Cas9 system
Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A., & Zhang, F. (2013) · Nature Protocols · doi:10.1038/nprot.2013.143 · Cited by 11,133 · see citing works
A robust and high-throughput Cre reporting and characterization system for the whole mouse brain
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907 · see citing works
DNA targeting specificity of RNA-guided Cas9 nucleases
Hsu, P. D., Scott, D. A., Weinstein, J. A., Ran, F. A., Konermann, S., Agarwala, V., Li, Y., Fine, E. J., Wu, X., Shalem, O., et al. (2013) · Nature Biotechnology · doi:10.1038/nbt.2647 · Cited by 4,741 · see citing works
Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9
Doench, J. G., Fusi, N., Sullender, M., Hegde, M., Vaimberg, E. W., Donovan, K. F., Smith, I., Tothova, Z., Wilen, C., Orchard, R., et al. (2016) · Nature Biotechnology · doi:10.1038/nbt.3437 · Cited by 4,637 · see citing works
High-Frequency off-Target Mutagenesis Induced by CRISPR-Cas Nucleases in Human Cells
Fu, Y., Foden, J. A., Khayter, C., Maeder, M. L., Reyon, D., Joung, J. K., & Sander, J. D. (2013) · Nature Biotechnology · doi:10.1038/nbt.2623 · Cited by 3,292 · see citing works
In vivo genome editing using Staphylococcus aureus Cas9
Ran, F. A., Cong, L., Yan, W. X., Scott, D. A., Gootenberg, J. S., Kriz, A. J., Zetsche, B., Shalem, O., Wu, X., Makarova, K. S., et al. (2015) · Nature · doi:10.1038/nature14299 · Cited by 2,687 · see citing works
High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects
Kleinstiver, B. P., Pattanayak, V., Prew, M. S., Tsai, S. Q., Nguyen, N. T., Zheng, Z., & Joung, J. K. (2016) · Nature · doi:10.1038/nature16526 · Cited by 2,673 · see citing works
Rationally engineered Cas9 nucleases with improved specificity
Slaymaker, I. M., Gao, L., Zetsche, B., Scott, D. A., Yan, W. X., & Zhang, F. (2016) · Science · doi:10.1126/science.aad5227 · Cited by 2,414 · see citing works
GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases
Tsai, S. Q., Zheng, Z., Nguyen, N. T., Liebers, M., Topkar, V. V., Thapar, V., Wyvekens, N., Khayter, C., Iafrate, A. J., Le, L. P., et al. (2015) · Nature Biotechnology · doi:10.1038/nbt.3117 · Cited by 2,268 · see citing works
Improving CRISPR-Cas nuclease specificity using truncated guide RNAs
Fu, Y., Sander, J. D., Reyon, D., Cascio, V. M., & Joung, J. K. (2014) · Nature Biotechnology · doi:10.1038/nbt.2808 · Cited by 1,993 · see citing works
Kosicki, M., Tomberg, K., & Bradley, A. (2018) · Nature Biotechnology · doi:10.1038/nbt.4192 · Cited by 1,883 · see citing works
Evolved Cas9 variants with broad PAM compatibility and high DNA specificity
Hu, J. H., Miller, S. M., Geurts, M. H., Tang, W., Chen, L., Sun, N., Zeina, C. M., Gao, X., Rees, H. A., Lin, Z., et al. (2018) · Nature · doi:10.1038/nature26155 · Cited by 1,552 · see citing works
The chemical evolution of oligonucleotide therapies of clinical utility
Khvorova, A., & Watts, J. K. (2017) · Nature Biotechnology · doi:10.1038/nbt.3765 · Cited by 1,216 · see citing works
Self-citationEnhanced proofreading governs CRISPR-Cas9 targeting accuracy
Chen, J. S., Dagdas, Y. S., Kleinstiver, B. P., Welch, M. M., Sousa, A. A., Harrington, L. B., Sternberg, S. H., Joung, J. K., Yildiz, A., & Doudna, J. A. (2017) · Nature · doi:10.1038/nature24268 · Cited by 1,168 · see citing works
In vivo genome editing via CRISPR/Cas9 mediated homology-independent targeted integration
Suzuki, K., Tsunekawa, Y., Hernandez-Benitez, R., Wu, J., Zhu, J., Kim, E. J., Hatanaka, F., Yamamoto, M., Araoka, T., Li, Z., et al. (2016) · Nature · doi:10.1038/nature20565 · Cited by 1,150 · see citing works
Digenome-seq: Genome-wide profiling of CRISPR-cas9 off-target effects in human cells
Kim, D., Bae, S., Park, J., Kim, E., Kim, S., Yu, H. R., Hwang, J., Kim, J.-I., & Kim, J.-S. (2015) · Nature Methods · doi:10.1038/nmeth.3284 · Cited by 992 · see citing works
Yin, H., Song, C.-Q., Dorkin, J. R., Zhu, L. J., Li, Y., Wu, Q., Park, A., Yang, J., Suresh, S., Bizhanova, A., et al. (2016) · Nature Biotechnology · doi:10.1038/nbt.3471 · Cited by 876 · see citing works
Self-citationCIRCLE-Seq: A highly sensitive in vitro screen for genome-wide CRISPR-cas9 nuclease off-targets
Tsai, S. Q., Nguyen, N. T., Malagon-Lopez, J., Topkar, V. V., Aryee, M. J., & Joung, J. K. (2017) · Nature Methods · doi:10.1038/nmeth.4278 · Cited by 814 · see citing works
Vakulskas, C. A., Dever, D. P., Rettig, G. R., Turk, R., Jacobi, A. M., Collingwood, M. A., Bode, N. M., McNeill, M. S., Yan, S., Camarena, J., et al. (2018) · Nature Medicine · doi:10.1038/s41591-018-0137-0 · Cited by 782 · see citing works
Kleinstiver, B. P., Sousa, A. A., Walton, R. T., Tak, Y. E., Hsu, J. Y., Clement, K., Welch, M. M., Horng, J. E., Malagon-Lopez, J., Scarfò, I., et al. (2019) · Nature Biotechnology · doi:10.1038/s41587-018-0011-0 · Cited by 680 · see citing works
Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases
Frock, R. L., Hu, J., Meyers, R. M., Ho, Y.-J., Kii, E., & Alt, F. W. (2015) · Nature Biotechnology · doi:10.1038/nbt.3101 · Cited by 673 · see citing works
Highly efficient CRISPR/Cas9-mediated knock-in in zebrafish by homology-independent DNA repair
Auer, T. O., Duroure, K., De Cian, A., Concordet, J.-P., & Del Bene, F. (2014) · Genome Research · doi:10.1101/gr.161638.113 · Cited by 631 · see citing works
Humanized Mouse Models of Clinical Disease
Walsh, N. C., Kenney, L. L., Jangalwe, S., Aryee, K., Greiner, D. L., Brehm, M. A., & Shultz, L. D. (2016) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-052016-100332 · Cited by 565 · see citing works
CRISPR-Based Therapeutic Genome Editing: Strategies and In Vivo Delivery by AAV Vectors
Wang, D., Zhang, F., & Gao, G. (2020) · Cell · doi:10.1016/j.cell.2020.03.023 · Cited by 526 · see citing works
Directed evolution of CRISPR-Cas9 to increase its specificity
Lee, J. K., Jeong, E., Lee, J., Jung, M., Shin, E., Kim, Y.-H., Lee, K., Jung, I., Kim, D., Kim, S., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05477-x · Cited by 525 · see citing works
Self-citationHighly efficient therapeutic gene editing of human hematopoietic stem cells
Wu, Y., Zeng, J., Roscoe, B. P., Liu, P., Yao, Q., Lazzarotto, C. R., Clement, K., Cole, M. A., Luk, K., Baricordi, C., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0401-y · Cited by 515 · see citing works
Self-citationA highly specific SpCas9 variant is identified by in vivo screening in yeast
Casini, A., Olivieri, M., Petris, G., Montagna, C., Reginato, G., Maule, G., Lorenzin, F., Prandi, D., Romanel, A., Demichelis, F., et al. (2018) · Nature Biotechnology · doi:10.1038/nbt.4066 · Cited by 493 · see citing works
Mapping the genomic landscape of CRISPR-Cas9 cleavage
Cameron, P., Fuller, C. K., Donohoue, P. D., Jones, B. N., Thompson, M. S., Carter, M. M., Gradia, S., Vidal, B., Garner, E., Slorach, E. M., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4284 · Cited by 443 · see citing works
Unbiased detection of CRISPR off-targets in vivo using DISCOVER-Seq
Wienert, B., Wyman, S. K., Richardson, C. D., Yeh, C. D., Akcakaya, P., Porritt, M. J., Morlock, M., Vu, J. T., Kazane, K. R., Watry, H. L., et al. (2019) · Science · doi:10.1126/science.aav9023 · Cited by 434 · see citing works
Long-term evaluation of AAV-CRISPR genome editing for Duchenne muscular dystrophy
Nelson, C. E., Wu, Y., Gemberling, M. P., Oliver, M. L., Waller, M. A., Bohning, J. D., Robinson-Hamm, J. N., Bulaklak, K., Rivera, R. M. C., Collier, J. H., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0344-3 · Cited by 426 · see citing works
BLISS is a versatile and quantitative method for genome-wide profiling of DNA double-strand breaks
Yan, W. X., Mirzazadeh, R., Garnerone, S., Scott, D., Schneider, M. W., Kallas, T., Custodio, J., Wernersson, E., Li, Y., Gao, L., et al. (2017) · Nature Communications · doi:10.1038/ncomms15058 · Cited by 369 · see citing works
Grompe, M., al-Dhalimy, M., Finegold, M., Ou, C. N., Burlingame, T., Kennaway, N. G., & Soriano, P. (1993) · Genes & Development · doi:10.1101/gad.7.12a.2298 · Cited by 355 · see citing works
Staahl, B. T., Benekareddy, M., Coulon-Bainier, C., Banfal, A. A., Floor, S. N., Sabo, J. K., Urnes, C., Munares, G. A., Ghosh, A., & Doudna, J. A. (2017) · Nature Biotechnology · doi:10.1038/nbt.3806 · Cited by 355 · see citing works
Increasing the specificity of CRISPR systems with engineered RNA secondary structures
Kocak, D. D., Josephs, E. A., Bhandarkar, V., Adkar, S. S., Kwon, J. B., & Gersbach, C. A. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0095-1 · Cited by 351 · see citing works
Hydrodynamic Gene Delivery: Its Principles and Applications
Suda, T., & Liu, D. (2007) · Molecular Therapy · doi:10.1038/sj.mt.6300314 · Cited by 349 · see citing works
He, X., Tan, C., Wang, F., Wang, Y., Zhou, R., Cui, D., You, W., Zhao, H., Ren, J., & Feng, B. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw064 · Cited by 338 · see citing works
Gu, B., Pósfai, E., & Rossant, J. (2018) · Nature Biotechnology · doi:10.1038/nbt.4166 · Cited by 324 · see citing works
In vivo CRISPR editing with no detectable genome-wide off-target mutations
Akçakaya, P., Bobbin, M. L., Guo, J. A., Malagon-Lopez, J., Clement, K., Garcia, S. P., Fellows, M. D., Porritt, M. J., Firth, M. A., Carreras, A., et al. (2018) · Nature · doi:10.1038/s41586-018-0500-9 · Cited by 316 · see citing works
Nguyen, D. N., Roth, T. L., Li, P. J., Chen, P. A., Apathy, R., Mamedov, M. R., Vo, L. T., Tobin, V. R., Goodman, D. B., Shifrut, E., et al. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0325-6 · Cited by 315 · see citing works
CHANGE-seq reveals genetic and epigenetic effects on CRISPR–Cas9 genome-wide activity
Lazzarotto, C. R., Malinin, N. L., Li, Y., Zhang, R., Yang, Y., Lee, G., Cowley, E., He, Y., Lan, X., Jividen, K., et al. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0555-7 · Cited by 283 · see citing works
Improved prime editors enable pathogenic allele correction and cancer modelling in adult mice
Liu, P., Liang, S.-Q., Zheng, C., Mintzer, E., Zhao, Y. G., Ponnienselvan, K., Mir, A., Sontheimer, E. J., Gao, G., Flotte, T. R., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22295-w · Cited by 273 · see citing works
Self-citationAird, E. J., Lovendahl, K. N., Martin, A. S., Harris, R. S., & Gordon, W. R. (2018) · Communications Biology · doi:10.1038/s42003-018-0054-2 · Cited by 248 · see citing works
Partial DNA-guided Cas9 enables genome editing with reduced off-target activity
Yin, H., Song, C.-Q., Suresh, S., Kwan, S.-Y., Wu, Q., Walsh, S., Ding, J., Bogorad, R. L., Zhu, L. J., Wolfe, S. A., et al. (2018) · Nature Chemical Biology · doi:10.1038/nchembio.2559 · Cited by 240 · see citing works
Self-citationHighly Parallel Profiling of Cas9 Variant Specificity
Schmid-Burgk, J. L., Gao, L., Li, D., Gardner, Z., Strecker, J., Lash, B., & Zhang, F. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.02.023 · Cited by 197 · see citing works
Zhu, L. J., Holmes, B. R., D, N. A. M., & Brodsky, M. H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108424 · Cited by 190 · see citing works
Self-citationEvaluating and enhancing target specificity of gene-editing nucleases and deaminases
Kim, D., Luk, K., Wolfe, S. A., & Kim, J.-S. (2019) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-013118-111730 · Cited by 171 · see citing works
Self-citationRapid Quantitative Evaluation of CRISPR Genome Editing by TIDE and TIDER
Brinkman, E. K., & van Steensel, B. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9170-9_3 · Cited by 171 · see citing works
Savić, N., Ringnalda, F. C. A. S., Lindsay, H. A., Berk, C., Bargsten, K., Li, Y., Neri, D., Robinson, M. D., Ciaudo, C., Hall, J., et al. (2018) · eLife · doi:10.7554/elife.33761 · Cited by 169 · see citing works
Rogers, Z. N., McFarland, C. D., Winters, I. P., Naranjo, S., Chuang, C.-H., Petrov, D. A., & Winslow, M. M. (2017) · Nature Methods · doi:10.1038/nmeth.4297 · Cited by 139 · see citing works
Microhomologies are prevalent at Cas9-induced larger deletions
Owens, D. D. G., Caulder, A., Frontera, V., Harman, J. R., Allan, A. J., Bucakci, A., Greder, L., Codner, G. F., Hublitz, P., McHugh, P. J., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz459 · Cited by 136 · see citing works
UDiTaS™, a genome editing detection method for indels and genome rearrangements
Giannoukos, G., Ciulla, D., Marco, E., Abdulkerim, H. S., Barrera, L. A., Bothmer, A., Dhanapal, V., Gloskowski, S. W., Jayaram, H., Maeder, M. L., et al. (2018) · BMC Genomics · doi:10.1186/s12864-018-4561-9 · Cited by 131 · 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
Krishnamurthy, S., Wohlford-Lenane, C., KANDIMALLA, S., Sartre, G., Meyerholz, D. K., Théberge, V., Hallée, S., Duperré, A.-M., Del’Guidice, T., Lepetit-Stoffaes, J.-P., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12922-y · Cited by 115 · see citing works
Lessard, S., Francioli, L. C., Alföldi, J., Tardif, J., Ellinor, P. T., MacArthur, D. G., Lettre, G., Orkin, S. H., & Canver, M. C. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1714640114 · Cited by 112 · see citing works
DIG-Seq: A genome-wide CRISPR off-target profiling method using chromatin DNA
Kim, D., & Kim, J.-S. (2018) · Genome Research · doi:10.1101/gr.236620.118 · Cited by 108 · see citing works
Ling, X., Xie, B., Gao, X., Chang, L., Zheng, W., Chen, H., Huang, Y., Tan, L., Li, M., & Liu, T. (2020) · Science Advances · doi:10.1126/sciadv.aaz0051 · Cited by 108 · see citing works
Enhanced Cas12a editing in mammalian cells and zebrafish
Liu, P., Luk, K., Shin, M., Idrizi, F., Kwok, S. F., Roscoe, B. P., Mintzer, E., Suresh, S., Morrison, K. S., Frazão, J. B., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz184 · Cited by 103 · see citing works
Self-citationHighsmith, W. E., Burch, L. H., Zhou, Z., Olsen, J. C., Strong, T. V., Smith, T., Friedman, K. J., Silverman, L. M., Boucher, R. C., Collins, F. S., et al. (1997) · Human Mutation · doi:10.1002/(sici)1098-1004(1997)9:4 · Cited by 89 · see citing works
iGUIDE: an improved pipeline for analyzing CRISPR cleavage specificity
Nobles, C. L., Reddy, S. G., Salas-McKee, J., Liu, X., June, C. H., Melenhorst, J. J., Suhoski, M. M., Zhao, Y., & Bushman, F. D. (2019) · Genome biology · doi:10.1186/s13059-019-1625-3 · Cited by 82 · see citing works
Kubo, S., Sun, M., Miyahara, M., Umeyama, K., Urakami, K.-I., Yamamoto, T., Jakobs, C., Matsuda, I., & Endo, F. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.16.9552 · Cited by 77 · see citing works
5′-Modifications improve potency and efficacy of DNA donors for precision genome editing
Ghanta, K. S., Chen, Z., Mir, A., Dokshin, G. A., Krishnamurthy, P. M., Yoon, Y., Gallant, J., Xu, P., Zhang, X.-O., Ozturk, A. R., et al. (2021) · eLife · doi:10.7554/elife.72216 · Cited by 76 · see citing works
Self-citationCas9-nickase–mediated genome editing corrects hereditary tyrosinemia in rats
Shao, Y., Wang, L., Guo, N., Wang, S., Yang, L., Li, Y., Wang, M., Yin, S., Han, H., Zeng, L., et al. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra117.000347 · Cited by 75 · see citing works
Yao, X., Wang, X., Liu, J., Hu, X., Shi, L., Shen, X., Ying, W., Sun, X.-Y., Wang, X., Huang, P., et al. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.05.015 · Cited by 74 · see citing works
Curing hemophilia A by NHEJ-mediated ectopic F8 insertion in the mouse
Zhang, J., Cheng, X., Zhao, M., Li, G., Xu, J., Zhang, F., Yin, M., Meng, F., Dai, X., Fu, Y.-W., et al. (2019) · Genome biology · doi:10.1186/s13059-019-1907-9 · Cited by 70 · see citing works
Shapiro, J., Iancu, O., Jacobi, A. M., McNeill, M., Turk, R., Rettig, G. R., Amit, I., Tovin, A., Yakhini, Z., Behlke, M. A., et al. (2020) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2020.04.027 · Cited by 70 · see citing works
A versatile reporter system for CRISPR-mediated chromosomal rearrangements
Li, Y., Park, A. I., Mou, H., Colpan, C., Bizhanova, A., Akama‐Garren, E. H., Joshi, N., Hendrickson, E. A., Feldser, D. M., Yin, H., et al. (2015) · Genome biology · doi:10.1186/s13059-015-0680-7 · Cited by 64 · see citing works
Self-citationBreton, C. A., Clark, P., Wang, L., Greig, J. A., & Wilson, J. M. (2020) · BMC Genomics · doi:10.1186/s12864-020-6655-4 · Cited by 57 · see citing works
Engineering designer beta cells with a CRISPR-Cas9 conjugation platform
Lim, D., Sreekanth, V., Cox, K. J., Law, B. K., Wagner, B. K., Karp, J. M., & Choudhary, A. (2020) · Nature Communications · doi:10.1038/s41467-020-17725-0 · Cited by 57 · see citing works
Rose, J. C., Popp, N. A., Richardson, C. D., Stephany, J. J., Mathieu, J., Wei, C. T., Corn, J. E., Maly, D. J., & Fowler, D. M. (2020) · Nature Communications · doi:10.1038/s41467-020-16542-9 · Cited by 56 · see citing works
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Liu, P., Liang, S., Zheng, C., Mintzer, E., Zhao, Y. G., Ponnienselvan, K., Mir, A., Sontheimer, E. J., Gao, G., Flotte, T. R., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.15.422970 · Cited by 42 · see citing works
Self-citationGUIDEseq: a bioconductor package to analyze GUIDE-Seq datasets for CRISPR-Cas nucleases
Zhu, L. J., Lawrence, M., Gupta, A., Pagès, H., Küçükural, A., Garber, M. G., & Wolfe, S. A. (2017) · BMC Genomics · doi:10.1186/s12864-017-3746-y · Cited by 41 · see citing works
Self-citationOrthogonal Cas9–Cas9 chimeras provide a versatile platform for genome editing
Bolukbasi, M. F., Liu, P., Luk, K., Kwok, S. F., Gupta, A., Amrani, N., Sontheimer, E. J., Zhu, L. J., & Wolfe, S. A. (2018) · Nature Communications · doi:10.1038/s41467-018-07310-x · Cited by 30 · see citing works
Self-citationCRISPR-SONIC: targeted somatic oncogene knock-in enables rapid in vivo cancer modeling
Mou, H., Özata, D. M., Smith, J. L., Sheel, A., Kwan, S., Hough, S. H., Küçükural, A., Kennedy, Z., Cao, Y., & Xue, W. (2019) · Genome Medicine · doi:10.1186/s13073-019-0627-9 · Cited by 22 · see citing works
Self-citation5′ Modifications Improve Potency and Efficacy of DNA Donors for Precision Genome EditingPreprint
Ghanta, K. S., Chen, Z., Mir, A., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/354480 · Cited by 19 · see citing works
Genome-wide detection and analysis of CRISPR-Cas off-targets
Rodríguez, T., Dadafarin, S., Pratt, H., Liu, P., Amrani, N., & Zhu, L. J. (2021) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2021.01.012 · Cited by 18 · see citing works
Self-citationRose, J. C., Popp, N. A., Richardson, C. D., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/597849 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
“When the indels are deposited at the coding sequences of a given gene, NHEJ can cause frameshift mutations, resulting in nonsense-mediated mRNA decay and gene silencing (Wang et al., 2016a; Zischewski et al., 2017; Lindeboom et al., 2019).”
BackgroundMethodInfluentialCurrent Bioinformatics Tools to Optimize CRISPR/Cas9 Experiments to Reduce Off-Target Effects
Naeem, M., & Alkhnbashi, O. S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076261 · Cited by 70 · see citing works
Cromer, M. K., Majeti, K. R., Rettig, G. R., Murugan, K., Kurgan, G. L., Bode, N. M., Hampton, J. P., Vakulskas, C. A., Behlke, M. A., & Porteus, M. H. (2023) · Molecular Therapy · doi:10.1016/j.ymthe.2023.02.011 · Cited by 42 · see citing works
Kwon, J., Kim, M., Hwang, W., Jo, A., Hwang, G.-H., Jung, M., Kim, U. G., Cui, G., Kim, H., Eom, J.-H., et al. (2023) · Genome biology · doi:10.1186/s13059-022-02842-4 · Cited by 24 · see citing works
Self-citation
- Authors
- Liang, S.-Q., Liu, P., Smith, J. L., Mintzer, E., Maitland, S., Dong, X., Yang, Q., Lee, J., Haynes, C. M., Zhu, L. J., Watts, J. K., Sontheimer, E. J., Wolfe, S. A., & Xue, W.
- Affiliations
- University of Massachusetts Chan Medical School (US)
- Corresponding author
- Wolfe, Scot A.
- Xue, Wen
- ORCID
- Venue
- Nature Communications
- Published
- 2022-01-21
- Volume
- 13
- Issue
- 1
- Pages
- 437-437
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC8782884
- OpenAlex
- W4206225117
- Cited by
- 54
- References
- 81
- Citations by year
- 2026: 7 · 2025: 11 · 2024: 14 · 2023: 17 · 2022: 5
- FWCI
- 3.83
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- American Cancer Society (129056-RSG-16-093)
- 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 › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
- Keywords
- in vivo gene editing, Cas9 nuclease, unique molecular identifiers, translocation, large deletions, mouse liver, mouse lung
- MeSH terms
- Gene Editing, CRISPR-Associated Protein 9, RNA, Guide, CRISPR-Cas Systems, Animals, Base Sequence, Biotin, DNA, Liver, Lung, Ribonucleoproteins, Genome, Genes, Reporter, Biotinylation, Cell Line, Tumor, Mice, CRISPR-Cas Systems
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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