Abstract
The ability to precisely modify endogenous genes can significantly facilitate biological studies and disease treatment, and the clustered regularly interspaced short palindromic repeats (CRISPR) systems have the potential to be powerful tools for genome engineering. However, the target specificity of CRISPR systems is largely unknown. Here we demonstrate that CRISPR/Cas9 systems targeting the human hemoglobin β and C-C chemokine receptor type 5 genes have substantial off-target cleavage, especially within the hemoglobin δ and C-C chemokine receptor type 2 genes, respectively, causing gross chromosomal deletions. The guide strands of the CRISPR/Cas9 systems were designed to have a range of mismatches with the sequences of potential off-target sites. Off-target analysis was performed using the T7 endonuclease I mutation detection assay and Sanger sequencing. We found that the repair of the on-and off-target cleavage resulted in a wide variety of insertions, deletions and point mutations. Therefore, CRISPR/Cas9 systems need to be carefully designed to avoid potential off-target cleavage sites, including those with mismatches to the 12-bases proximal to the guide strand protospacer-adjacent motif.
MeSH Terms
CRISPR-Associated Proteins/metabolism
CRISPR-Cas Systems
Chromosome Deletion
DNA Cleavage
Endodeoxyribonucleases/metabolism
Genetic Loci
HEK293 Cells
Humans
Receptors, CCR5/genetics
beta-Globins/genetics
Chemicals
CCR5 protein, human
CRISPR-Associated Proteins
Receptors, CCR5
beta-Globins
Endodeoxyribonucleases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Cradick Thomas J
Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, GA 30332, USA.
Fine Eli J
Antico Christopher J
Bao Gang
References (31)
31 references, click to expand
-
Knockout rats via embryo microinjection of zinc-finger nucleases.
Science. 2009 Jul 24;325(5939):433
PMID: 19628861
-
Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria.
Proc Natl Acad Sci U S A. 2012 Sep 25;109(39):E2579-86
PMID: 22949671
-
Engineered zinc finger nickases induce homology-directed repair with reduced mutagenic effects.
Nucleic Acids Res. 2012 Jul;40(12):5560-8
PMID: 22373919
-
CRISPR/Cas, the immune system of bacteria and archaea.
Science. 2010 Jan 8;327(5962):167-70
PMID: 20056882
-
Synthesis-dependent microhomology-mediated end joining accounts for multiple types of repair junctions.
Nucleic Acids Res. 2010 Sep;38(17):5706-17
PMID: 20460465
-
An unbiased genome-wide analysis of zinc-finger nuclease specificity.
Nat Biotechnol. 2011 Aug 07;29(9):816-23
PMID: 21822255
-
The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli.
Nucleic Acids Res. 2011 Nov;39(21):9275-82
PMID: 21813460
-
High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells.
Nat Biotechnol. 2013 Sep;31(9):822-6
PMID: 23792628
-
RNA-guided human genome engineering via Cas9.
Science. 2013 Feb 15;339(6121):823-6
PMID: 23287722
-
RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex.
Cell. 2009 Nov 25;139(5):945-56
PMID: 19945378
-
Multiplex genome engineering using CRISPR/Cas systems.
Science. 2013 Feb 15;339(6121):819-23
PMID: 23287718
-
Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin.
Microbiology (Reading). 2005 Aug;151(Pt 8):2551-2561
PMID: 16079334
-
Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease.
Genetics. 2013 Aug;194(4):1029-35
PMID: 23709638
-
Short motif sequences determine the targets of the prokaryotic CRISPR defence system.
Microbiology (Reading). 2009 Mar;155(Pt 3):733-740
PMID: 19246744
-
A rapid and general assay for monitoring endogenous gene modification.
Methods Mol Biol. 2010;649:247-56
PMID: 20680839
-
RNA-guided editing of bacterial genomes using CRISPR-Cas systems.
Nat Biotechnol. 2013 Mar;31(3):233-9
PMID: 23360965
-
One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering.
Cell. 2013 May 9;153(4):910-8
PMID: 23643243
-
Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases.
Nat Biotechnol. 2008 Jul;26(7):808-16
PMID: 18587387
-
DNA targeting specificity of RNA-guided Cas9 nucleases.
Nat Biotechnol. 2013 Sep;31(9):827-32
PMID: 23873081
-
CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea.
Nat Rev Genet. 2010 Mar;11(3):181-90
PMID: 20125085
-
Targeted chromosomal deletions and inversions in zebrafish.
Genome Res. 2013 Jun;23(6):1008-17
PMID: 23478401
-
Quantification of zinc finger nuclease-associated toxicity.
Methods Mol Biol. 2010;649:237-45
PMID: 20680838
-
Targeted chromosomal deletions in human cells using zinc finger nucleases.
Genome Res. 2010 Jan;20(1):81-9
PMID: 19952142
-
Knockout rats generated by embryo microinjection of TALENs.
Nat Biotechnol. 2011 Aug 05;29(8):695-6
PMID: 21822240
-
Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish.
Nucleic Acids Res. 2013 Aug;41(14):e141
PMID: 23748566
-
The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA.
Nature. 2010 Nov 4;468(7320):67-71
PMID: 21048762
-
A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity.
Science. 2012 Aug 17;337(6096):816-21
PMID: 22745249
-
RNA-programmed genome editing in human cells.
Elife. 2013 Jan 29;2:e00471
PMID: 23386978
-
Genetic engineering of human pluripotent cells using TALE nucleases.
Nat Biotechnol. 2011 Jul 07;29(8):731-4
PMID: 21738127
-
Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection.
Nat Methods. 2011 Aug 07;8(9):765-70
PMID: 21822273
-
A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity.
Nucleic Acids Res. 2011 Nov;39(21):9283-93
PMID: 21813459