Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery
Abstract
The CRISPR/Cas9 system is a robust genome editing technology that works in human cells, animals and plants based on the RNA-programmed DNA cleaving activity of the Cas9 enzyme. Building on previous work (Jinek et al., 2013), we show here that new genetic information can be introduced site-specifically and with high efficiency by homology-directed repair (HDR) of Cas9-induced site-specific double-strand DNA breaks using timed delivery of Cas9-guide RNA ribonucleoprotein (RNP) complexes. Cas9 RNP-mediated HDR in HEK293T, human primary neonatal fibroblast and human embryonic stem cells was increased dramatically relative to experiments in unsynchronized cells, with rates of HDR up to 38% observed in HEK293T cells. Sequencing of on- and potential off-target sites showed that editing occurred with high fidelity, while cell mortality was minimized. This approach provides a simple and highly effective strategy for enhancing site-specific genome engineering in both transformed and primary human cells.
- Authors:
-
- Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology
- Univ. of California, Berkeley, CA (United States). Computational Genomics Resource Laboratory. QB3
- Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst.; Univ. of California, Berkeley, CA, (United States). Dept. of Chemistry; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Dept. of Chemistry
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
- OSTI Identifier:
- 1628827
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- eLife
- Additional Journal Information:
- Journal Volume: 3; Journal ID: ISSN 2050-084X
- Publisher:
- eLife Sciences Publications, Ltd.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- Life Sciences & Biomedicine - Other Topics
Citation Formats
Lin, Steven, Staahl, Brett T., Alla, Ravi K., and Doudna, Jennifer A. Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery. United States: N. p., 2014.
Web. doi:10.7554/elife.04766.
Lin, Steven, Staahl, Brett T., Alla, Ravi K., & Doudna, Jennifer A. Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery. United States. https://doi.org/10.7554/elife.04766
Lin, Steven, Staahl, Brett T., Alla, Ravi K., and Doudna, Jennifer A. Mon .
"Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery". United States. https://doi.org/10.7554/elife.04766. https://www.osti.gov/servlets/purl/1628827.
@article{osti_1628827,
title = {Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery},
author = {Lin, Steven and Staahl, Brett T. and Alla, Ravi K. and Doudna, Jennifer A.},
abstractNote = {The CRISPR/Cas9 system is a robust genome editing technology that works in human cells, animals and plants based on the RNA-programmed DNA cleaving activity of the Cas9 enzyme. Building on previous work (Jinek et al., 2013), we show here that new genetic information can be introduced site-specifically and with high efficiency by homology-directed repair (HDR) of Cas9-induced site-specific double-strand DNA breaks using timed delivery of Cas9-guide RNA ribonucleoprotein (RNP) complexes. Cas9 RNP-mediated HDR in HEK293T, human primary neonatal fibroblast and human embryonic stem cells was increased dramatically relative to experiments in unsynchronized cells, with rates of HDR up to 38% observed in HEK293T cells. Sequencing of on- and potential off-target sites showed that editing occurred with high fidelity, while cell mortality was minimized. This approach provides a simple and highly effective strategy for enhancing site-specific genome engineering in both transformed and primary human cells.},
doi = {10.7554/elife.04766},
journal = {eLife},
number = ,
volume = 3,
place = {United States},
year = {Mon Dec 15 00:00:00 EST 2014},
month = {Mon Dec 15 00:00:00 EST 2014}
}
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- Jayavaradhan, Rajeswari; Pillis, Devin M.; Goodman, Michael
- Nature Communications, Vol. 10, Issue 1
Small molecules enhance CRISPR/Cas9-mediated homology-directed genome editing in primary cells
journal, August 2017
- Li, Guoling; Zhang, Xianwei; Zhong, Cuili
- Scientific Reports, Vol. 7, Issue 1
Site-specific chromosomal gene insertion: Flp recombinase versus Cas9 nuclease
journal, December 2017
- Phan, Quang Vinh; Contzen, Jörg; Seemann, Petra
- Scientific Reports, Vol. 7, Issue 1
CRISPR/Cas9 – An evolving biological tool kit for cancer biology and oncology
journal, March 2019
- Tian, Xueli; Gu, Tingxuan; Patel, Satyananda
- npj Precision Oncology, Vol. 3, Issue 1
Large genomic fragment deletion and functional gene cassette knock-in via Cas9 protein mediated genome editing in one-cell rodent embryos
journal, December 2015
- Wang, Liren; Shao, Yanjiao; Guan, Yuting
- Scientific Reports, Vol. 5, Issue 1
Systematic quantification of HDR and NHEJ reveals effects of locus, nuclease, and cell type on genome-editing
journal, March 2016
- Miyaoka, Yuichiro; Berman, Jennifer R.; Cooper, Samantha B.
- Scientific Reports, Vol. 6, Issue 1
Isozygous and selectable marker-free MSTN knockout cloned pigs generated by the combined use of CRISPR/Cas9 and Cre/LoxP
journal, August 2016
- Bi, Yanzhen; Hua, Zaidong; Liu, Ximei
- Scientific Reports, Vol. 6, Issue 1
CRISPR-Cas9 enables conditional mutagenesis of challenging loci
journal, September 2016
- Schick, Joel A.; Seisenberger, Claudia; Beig, Joachim
- Scientific Reports, Vol. 6, Issue 1
CRISPR/Cas9-mediated gene manipulation to create single-amino-acid-substituted and floxed mice with a cloning-free method
journal, February 2017
- Ma, Xiaolong; Chen, Chao; Veevers, Jennifer
- Scientific Reports, Vol. 7, Issue 1
Homology-directed repair in mouse cells increased by CasRx-mediated knockdown or co-expressing Kaposi’s sarcoma-associated herpesvirus ORF52
journal, October 2019
- Pan, Hong; Yu, Weina; Zhang, Ming
- Bioscience Reports, Vol. 39, Issue 10
Editor's cut: DNA cleavage by CRISPR RNA-guided nucleases Cas9 and Cas12a
journal, December 2019
- Swartjes, Thomas; Staals, Raymond H. J.; van der Oost, John
- Biochemical Society Transactions, Vol. 48, Issue 1
Quantitative microscopy reveals dynamics and fate of clustered IRE1α
journal, December 2019
- Belyy, Vladislav; Tran, Ngoc-Han; Walter, Peter
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 3
Antibody discovery and engineering by enhanced CRISPR-Cas9 integration of variable gene cassette libraries in mammalian cells
journal, September 2019
- Parola, Cristina; Neumeier, Daniel; Friedensohn, Simon
- mAbs, Vol. 11, Issue 8
Cutting back malaria: CRISPR/Cas9 genome editing of Plasmodium
journal, July 2019
- Lee, Marcus C. S.; Lindner, Scott E.; Lopez-Rubio, Jose-Juan
- Briefings in Functional Genomics, Vol. 18, Issue 5
Multiplex genome editing of microorganisms using CRISPR-Cas
journal, April 2019
- Adiego-Pérez, Belén; Randazzo, Paola; Daran, Jean Marc
- FEMS Microbiology Letters, Vol. 366, Issue 8
In vivoblunt-end cloning through CRISPR/Cas9-facilitated non-homologous end-joining
journal, January 2016
- Geisinger, Jonathan M.; Turan, Sören; Hernandez, Sophia
- Nucleic Acids Research, Vol. 44, Issue 8
Nuclear domain ‘knock-in’ screen for the evaluation and identification of small molecule enhancers of CRISPR-based genome editing
journal, October 2015
- Pinder, Jordan; Salsman, Jayme; Dellaire, Graham
- Nucleic Acids Research, Vol. 43, Issue 19
Co-incident insertion enables high efficiency genome engineering in mouse embryonic stem cells
journal, August 2016
- Shy, Brian R.; MacDougall, Matthew S.; Clarke, Ryan
- Nucleic Acids Research, Vol. 44, Issue 16
Clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 with improved proof-reading enhances homology-directed repair
journal, April 2018
- Kato-Inui, Tomoko; Takahashi, Gou; Hsu, Szuyin
- Nucleic Acids Research, Vol. 46, Issue 9
Highly efficient editing of the β-globin gene in patient-derived hematopoietic stem and progenitor cells to treat sickle cell disease
journal, May 2019
- Park, So Hyun; Lee, Ciaran M.; Dever, Daniel P.
- Nucleic Acids Research, Vol. 47, Issue 15
Simultaneous precise editing of multiple genes in human cells
journal, August 2019
- Riesenberg, Stephan; Chintalapati, Manjusha; Macak, Dominik
- Nucleic Acids Research, Vol. 47, Issue 19
Depletion of Abundant Sequences by Hybridization (DASH): Using Cas9 to remove unwanted high-abundance species in sequencing libraries and molecular counting applications
journal, November 2015
- Gu, W.; Ceawford, E. D.; O'Donovan, B. D.
- Genome Biology
Targeting repair pathways with small molecules increases precise genome editing in pluripotent stem cells
journal, May 2017
- Riesenberg, Stephan; Maricic, Tomislav
- Nature Communications
CRISPR-Cas9 interrogation of a putative fetal globin repressor in human erythroid cells
journal, May 2018
- Chung, Jennifer; Magis, Wendy; Vu, Jonathan
- PLOS ONE
Highly efficient scarless knock-in of reporter genes into human and mouse pluripotent stem cells via transient antibiotic selection
journal, July 2018
- Sluch, Valentin M.; Chamling, Xitiz; Wenger, Claire
- PLOS ONE
Increasing the efficiency of CRISPR-Cas9-VQR precise genome editing in rice
journal, August 2017
- Hu, Xixun; Meng, Xiangbing; Liu, Qing
- Plant Biotechnology Journal, Vol. 16, Issue 1
Universal intracellular biomolecule delivery with precise dosage control
journal, October 2018
- Cao, Y.; Chen, H.; Qiu, R.
- Science Advances, Vol. 4, Issue 10
The Impact of CRISPR/Cas9 Technology on Cardiac Research: From Disease Modelling to Therapeutic Approaches
journal, January 2017
- Motta, Benedetta M.; Pramstaller, Peter P.; Hicks, Andrew A.
- Stem Cells International, Vol. 2017
Efficient identification of CRISPR/Cas9-induced insertions/deletions by direct germline screening in zebrafish
journal, March 2016
- Brocal, Isabel; White, Richard J.; Dooley, Christopher M.
- BMC Genomics, Vol. 17, Issue 1
Resources for the design of CRISPR gene editing experiments
journal, November 2015
- Graham, Daniel B.; Root, David E.
- Genome Biology, Vol. 16, Issue 1
Efficient precise knockin with a double cut HDR donor after CRISPR/Cas9-mediated double-stranded DNA cleavage
journal, February 2017
- Zhang, Jian-Ping; Li, Xiao-Lan; Li, Guo-Hua
- Genome Biology, Vol. 18, Issue 1
Systematic evaluation of CRISPR-Cas systems reveals design principles for genome editing in human cells
journal, May 2018
- Wang, Yuanming; Liu, Kaiwen Ivy; Sutrisnoh, Norfala-Aliah Binte
- Genome Biology, Vol. 19, Issue 1
Targeted gene knockin in zebrafish using the 28S rDNA-specific non-LTR-retrotransposon R2Ol
journal, May 2019
- Kuroki-Kami, Azusa; Nichuguti, Narisu; Yatabe, Haruka
- Mobile DNA, Vol. 10, Issue 1
CRISPR/Cas9-mediated homology-directed repair by ssODNs in zebrafish induces complex mutational patterns resulting from genomic integration of repair-template fragments
journal, October 2018
- Boel, Annekatrien; De Saffel, Hanna; Steyaert, Wouter
- Disease Models & Mechanisms, Vol. 11, Issue 10
Successful CRISPR/Cas9 mediated homologous recombination in a chicken cell line
journal, January 2018
- Antonova, Ekaterina; Glazova, Olga; Gaponova, Anna
- F1000Research, Vol. 7
Regulation of Gene Editing Activity Directed by Single-Stranded Oligonucleotides and CRISPR/Cas9 Systems
journal, June 2015
- Bialk, Pawel; Rivera-Torres, Natalia; Strouse, Bryan
- PLOS ONE, Vol. 10, Issue 6
Generation of deletions and precise point mutations in Dictyostelium discoideum using the CRISPR nickase
journal, October 2019
- Iriki, Hoshie; Kawata, Takefumi; Muramoto, Tetsuya
- PLOS ONE, Vol. 14, Issue 10
Knock-In Rat Lines with Cre Recombinase at the Dopamine D1 and Adenosine 2a Receptor Loci
journal, August 2019
- Pettibone, Jeffrey R.; Yu, Jai Y.; Derman, Rifka C.
- eneuro, Vol. 6, Issue 5
CRISPR /Cas9‐mediated somatic correction of a novel coagulator factor IX gene mutation ameliorates hemophilia in mouse
journal, March 2016
- Guan, Yuting; Ma, Yanlin; Li, Qi
- EMBO Molecular Medicine, Vol. 8, Issue 5
Methods for Enhancing Clustered Regularly Interspaced Short Palindromic Repeats/Cas9-Mediated Homology-Directed Repair Efficiency
journal, June 2019
- Tang, Xi-Dian; Gao, Fei; Liu, Ming-Jie
- Frontiers in Genetics, Vol. 10
Modeling the Function of TATA Box Binding Protein in Transcriptional Changes Induced by HIV-1 Tat in Innate Immune Cells and the Effect of Methamphetamine Exposure
journal, February 2019
- Tjitro, Ryan; Campbell, Lee A.; Basova, Liana
- Frontiers in Immunology, Vol. 9
Gene Editing Preserves Visual Functions in a Mouse Model of Retinal Degeneration
journal, September 2019
- Vagni, Paola; Perlini, Laura E.; Chenais, Naïg A. L.
- Frontiers in Neuroscience, Vol. 13
Autologous Stem-Cell-Based Gene Therapy for Inherited Disorders: State of the Art and Perspectives
journal, October 2019
- Staal, Frank J. T.; Aiuti, Alessandro; Cavazzana, Marina
- Frontiers in Pediatrics, Vol. 7
CRISPR-Cas: Converting A Bacterial Defence Mechanism into A State-of-the-Art Genetic Manipulation Tool
journal, February 2019
- Loureiro, Alexandre; da Silva, Gabriela
- Antibiotics, Vol. 8, Issue 1
Applications of Alternative Nucleases in the Age of CRISPR/Cas9
journal, November 2017
- Guha, Tuhin; Edgell, David
- International Journal of Molecular Sciences, Vol. 18, Issue 12
Genome Editing for Mucopolysaccharidoses
journal, January 2020
- Poletto, Edina; Baldo, Guilherme; Gomez-Ospina, Natalia
- International Journal of Molecular Sciences, Vol. 21, Issue 2
Genome Editing for the Understanding and Treatment of Inherited Cardiomyopathies
journal, January 2020
- Nguyen,
- International Journal of Molecular Sciences, Vol. 21, Issue 3
Chitosan in Non-Viral Gene Delivery: Role of Structure, Characterization Methods, and Insights in Cancer and Rare Diseases Therapies
journal, April 2018
- Santos-Carballal, Beatriz; Fernández Fernández, Elena; Goycoolea, Francisco
- Polymers, Vol. 10, Issue 4
Establishment of Genome-edited Human Pluripotent Stem Cell Lines: From Targeting to Isolation
journal, February 2016
- Blair, John D.; Bateup, Helen S.; Hockemeyer, Dirk F.
- Journal of Visualized Experiments, Issue 108
An Overview Of The Crispr-Based Genomic- And Epigenome-Editing System: Function, Applications, And Challenges
journal, January 2019
- Mojarrad, Majid; Bozorg Qomi, Saeed; Asghari, Amir
- Advanced Biomedical Research, Vol. 8, Issue 1
Efficient And Versatile Crispr Engineering Of Human Neurons In Culture To Model Neurological Disorders
text, January 2016
- Shah, Ruth Rama; Cholewa-Waclaw, Justyna; Davies, Faith C. J.
- Zenodo
The road less traveled: strategies to enhance the frequency of homology-directed repair (HDR) for increased efficiency of CRISPR/Cas-mediated transgenesis
journal, September 2018
- Devkota, Sushil
- BMB Reports, Vol. 51, Issue 9
Correction: Multiplexed genetic engineering of human hematopoietic stem and progenitor cells using CRISPR/Cas9 and AAV6
journal, November 2018
- Bak, Rasmus O.; Dever, Daniel P.; Reinisch, Andreas
- eLife, Vol. 7
One-step efficient generation of dual-function conditional knockout and geno-tagging alleles in zebrafish
journal, October 2019
- Li, Wenyuan; Zhang, Yage; Han, Bingzhou
- eLife, Vol. 8