Open Access

Nature Protocols, volume 8, issue 11, pages 2281-2308

Genome engineering using the CRISPR-Cas9 system

Ran F Ann ^{1, 2, 3, 4, 5}

Hsu Patrick D. ^{1, 2, 3, 4, 5}

Wright Jason ¹

Agarwala Vineeta ^{1, 6, 7}

Scott David A ^{1, 3, 4, 5}

Zhang Feng ^{1, 3, 4, 5}

Hide authors affiliations Show authors affiliations: 7 affiliations

Broad Institute of Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, USA |

Department of Molecular and Cellular biology, Harvard University, Cambridge, USA |

Department of Biological Engineering, MIT, Cambridge, USA |

⁴

Department of Brain and Cognitive Sciences, MIT, Cambridge, Massachusetts, USA., |

⁵

McGovern Institute for Brain Research, Cambridge, USA |

⁶

Harvard-MIT Division of Health Sciences and Technology, MIT, Cambridge, USA |

⁷

Program in Biophysics, Harvard University, MIT, Cambridge, USA |

Publication type: Journal Article

Publication date: 2013-10-24

Springer Nature

Journal: Nature Protocols

Quartile SCImago

Quartile WOS

Impact factor: 14.8

ISSN: 17542189

DOI: 10.1038/nprot.2013.143

Copy DOI

PubMed ID: 24157548

General Biochemistry, Genetics and Molecular Biology

Abstract

Targeted nucleases are powerful tools for mediating genome alteration with high precision. The RNA-guided Cas9 nuclease from the microbial clustered regularly interspaced short palindromic repeats (CRISPR) adaptive immune system can be used to facilitate efficient genome engineering in eukaryotic cells by simply specifying a 20-nt targeting sequence within its guide RNA. Here we describe a set of tools for Cas9-mediated genome editing via nonhomologous end joining (NHEJ) or homology-directed repair (HDR) in mammalian cells, as well as generation of modified cell lines for downstream functional studies. To minimize off-target cleavage, we further describe a double-nicking strategy using the Cas9 nickase mutant with paired guide RNAs. This protocol provides experimentally derived guidelines for the selection of target sites, evaluation of cleavage efficiency and analysis of off-target activity. Beginning with target design, gene modifications can be achieved within as little as 1–2 weeks, and modified clonal cell lines can be derived within 2–3 weeks.

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Citations by journals

	50 100 150 200 250 300 350
Nature Communications	Nature Communications, 344, 4.09% Nature Communications 344 publications, 4.09%
Scientific Reports	Scientific Reports, 244, 2.9% Scientific Reports 244 publications, 2.9%
Cell Reports	Cell Reports, 202, 2.4% Cell Reports 202 publications, 2.4%
eLife	eLife, 165, 1.96% eLife 165 publications, 1.96%
Journal of Biological Chemistry	Journal of Biological Chemistry, 159, 1.89% Journal of Biological Chemistry 159 publications, 1.89%
Nucleic Acids Research	Nucleic Acids Research, 158, 1.88% Nucleic Acids Research 158 publications, 1.88%
International Journal of Molecular Sciences	International Journal of Molecular Sciences, 131, 1.56% International Journal of Molecular Sciences 131 publications, 1.56%
Methods in Molecular Biology	Methods in Molecular Biology, 130, 1.54% Methods in Molecular Biology 130 publications, 1.54%
Proceedings of the National Academy of Sciences of the United States of America	Proceedings of the National Academy of Sciences of the United States of America, 117, 1.39% Proceedings of the National Academy of Sciences of the United States of America 117 publications, 1.39%
PLoS ONE	PLoS ONE, 113, 1.34% PLoS ONE 113 publications, 1.34%
Molecular Cell	Molecular Cell, 110, 1.31% Molecular Cell 110 publications, 1.31%
Cell	Cell, 85, 1.01% Cell 85 publications, 1.01%
Journal of Cell Biology	Journal of Cell Biology, 80, 0.95% Journal of Cell Biology 80 publications, 0.95%
Nature	Nature, 77, 0.91% Nature 77 publications, 0.91%
Cells	Cells, 71, 0.84% Cells 71 publications, 0.84%
EMBO Journal	EMBO Journal, 70, 0.83% EMBO Journal 70 publications, 0.83%
Science advances	Science advances, 63, 0.75% Science advances 63 publications, 0.75%
Journal of Cell Science	Journal of Cell Science, 62, 0.74% Journal of Cell Science 62 publications, 0.74%
Stem Cell Research	Stem Cell Research, 59, 0.7% Stem Cell Research 59 publications, 0.7%
Nature Cell Biology	Nature Cell Biology, 58, 0.69% Nature Cell Biology 58 publications, 0.69%
Frontiers in Cell and Developmental Biology	Frontiers in Cell and Developmental Biology, 53, 0.63% Frontiers in Cell and Developmental Biology 53 publications, 0.63%
Science	Science, 53, 0.63% Science 53 publications, 0.63%
Cancers	Cancers, 51, 0.61% Cancers 51 publications, 0.61%
Oncogene	Oncogene, 46, 0.55% Oncogene 46 publications, 0.55%
FASEB Journal	FASEB Journal, 45, 0.53% FASEB Journal 45 publications, 0.53%
Frontiers in Immunology	Frontiers in Immunology, 43, 0.51% Frontiers in Immunology 43 publications, 0.51%
Human Molecular Genetics	Human Molecular Genetics, 41, 0.49% Human Molecular Genetics 41 publications, 0.49%
Molecular Therapy - Nucleic Acids	Molecular Therapy - Nucleic Acids, 41, 0.49% Molecular Therapy - Nucleic Acids 41 publications, 0.49%
Molecular Biology of the Cell	Molecular Biology of the Cell, 41, 0.49% Molecular Biology of the Cell 41 publications, 0.49%
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Citations by publishers

	200 400 600 800 1000 1200 1400 1600 1800 2000
Springer Nature	Springer Nature, 1805, 21.43% Springer Nature 1805 publications, 21.43%
Elsevier	Elsevier, 1490, 17.69% Elsevier 1490 publications, 17.69%
Wiley	Wiley, 453, 5.38% Wiley 453 publications, 5.38%
Multidisciplinary Digital Publishing Institute (MDPI)	Multidisciplinary Digital Publishing Institute (MDPI), 424, 5.04% Multidisciplinary Digital Publishing Institute (MDPI) 424 publications, 5.04%
Oxford University Press	Oxford University Press, 282, 3.35% Oxford University Press 282 publications, 3.35%
Frontiers Media S.A.	Frontiers Media S.A., 258, 3.06% Frontiers Media S.A. 258 publications, 3.06%
Public Library of Science (PLoS)	Public Library of Science (PLoS), 208, 2.47% Public Library of Science (PLoS) 208 publications, 2.47%
American Society for Biochemistry and Molecular Biology	American Society for Biochemistry and Molecular Biology, 189, 2.24% American Society for Biochemistry and Molecular Biology 189 publications, 2.24%
eLife Sciences Publications	eLife Sciences Publications, 165, 1.96% eLife Sciences Publications 165 publications, 1.96%
American Association for the Advancement of Science (AAAS)	American Association for the Advancement of Science (AAAS), 165, 1.96% American Association for the Advancement of Science (AAAS) 165 publications, 1.96%
Rockefeller University Press	Rockefeller University Press, 130, 1.54% Rockefeller University Press 130 publications, 1.54%
EMBO press	EMBO press, 125, 1.48% EMBO press 125 publications, 1.48%
The Company of Biologists	The Company of Biologists, 118, 1.4% The Company of Biologists 118 publications, 1.4%
Proceedings of the National Academy of Sciences (PNAS)	Proceedings of the National Academy of Sciences (PNAS), 117, 1.39% Proceedings of the National Academy of Sciences (PNAS) 117 publications, 1.39%
Taylor & Francis	Taylor & Francis, 93, 1.1% Taylor & Francis 93 publications, 1.1%
American Society for Microbiology	American Society for Microbiology, 80, 0.95% American Society for Microbiology 80 publications, 0.95%
American Chemical Society (ACS)	American Chemical Society (ACS), 79, 0.94% American Chemical Society (ACS) 79 publications, 0.94%
American Association for Cancer Research (AACR)	American Association for Cancer Research (AACR), 69, 0.82% American Association for Cancer Research (AACR) 69 publications, 0.82%
Cold Spring Harbor Laboratory	Cold Spring Harbor Laboratory, 61, 0.72% Cold Spring Harbor Laboratory 61 publications, 0.72%
American Society for Clinical Investigation	American Society for Clinical Investigation, 54, 0.64% American Society for Clinical Investigation 54 publications, 0.64%
Mary Ann Liebert	Mary Ann Liebert, 51, 0.61% Mary Ann Liebert 51 publications, 0.61%
Wolters Kluwer Health	Wolters Kluwer Health, 47, 0.56% Wolters Kluwer Health 47 publications, 0.56%
Federation of American Societies for Experimental Biology (FASEB)	Federation of American Societies for Experimental Biology (FASEB), 46, 0.55% Federation of American Societies for Experimental Biology (FASEB) 46 publications, 0.55%
Impact Journals	Impact Journals, 43, 0.51% Impact Journals 43 publications, 0.51%
American Society for Cell Biology (ASCB)	American Society for Cell Biology (ASCB), 41, 0.49% American Society for Cell Biology (ASCB) 41 publications, 0.49%
Royal Society of Chemistry (RSC)	Royal Society of Chemistry (RSC), 31, 0.37% Royal Society of Chemistry (RSC) 31 publications, 0.37%
American Society of Hematology	American Society of Hematology, 30, 0.36% American Society of Hematology 30 publications, 0.36%
The American Association of Immunologists	The American Association of Immunologists, 28, 0.33% The American Association of Immunologists 28 publications, 0.33%
BMJ	BMJ, 25, 0.3% BMJ 25 publications, 0.3%
	200 400 600 800 1000 1200 1400 1600 1800 2000

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GOST |

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GOST Copy

Ran F. A. et al. Genome engineering using the CRISPR-Cas9 system // Nature Protocols. 2013. Vol. 8. No. 11. pp. 2281-2308.

GOST all authors (up to 50) Copy

Ran F. A., Hsu P. D., Wright J., Agarwala V., Scott D. A., Zhang F. Genome engineering using the CRISPR-Cas9 system // Nature Protocols. 2013. Vol. 8. No. 11. pp. 2281-2308.

RIS |

Cite this

RIS Copy

TY - JOUR

DO - 10.1038/nprot.2013.143

UR - https://doi.org/10.1038%2Fnprot.2013.143

TI - Genome engineering using the CRISPR-Cas9 system

T2 - Nature Protocols

AU - Ran, F Ann

AU - Hsu, Patrick D.

AU - Wright, Jason

AU - Agarwala, Vineeta

AU - Scott, David A

AU - Zhang, Feng

PY - 2013

DA - 2013/10/24 00:00:00

PB - Springer Nature

SP - 2281-2308

IS - 11

VL - 8

PMID - 24157548

SN - 1754-2189

ER -

BibTex |

Cite this

BibTex Copy

@article{2013_Ran,

author = {F Ann Ran and Patrick D. Hsu and Jason Wright and Vineeta Agarwala and David A Scott and Feng Zhang},

title = {Genome engineering using the CRISPR-Cas9 system},

journal = {Nature Protocols},

year = {2013},

volume = {8},

publisher = {Springer Nature},

month = {oct},

url = {https://doi.org/10.1038%2Fnprot.2013.143},

number = {11},

pages = {2281--2308},

doi = {10.1038/nprot.2013.143}

}

MLA

Cite this

MLA Copy

Ran, F. Ann, et al. “Genome engineering using the CRISPR-Cas9 system.” Nature Protocols, vol. 8, no. 11, Oct. 2013, pp. 2281-2308. https://doi.org/10.1038%2Fnprot.2013.143.

Found error?

Publisher

Springer Nature

Journal

Nature Protocols

Quartile SCImago

Quartile WOS

Impact factor

14.8

ISSN

17542189 (Print)