CRISPR/Cas9 systems targeting β-globin and CCR5 genes have substantial off-target activity

Nucleic Acids Research

Volumn 41, Issue 20, 2013, Pages 9584-9592

  Cradick, Thomas J ^a   Fine, Eli J ^a   Antico, Christopher J ^a   Bao, Gang ^a  

^a Emory University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; ENDONUCLEASE; HEMOGLOBIN BETA CHAIN; HEMOGLOBIN D;

ARTICLE; BASE MISPAIRING; CCR5 GENE; CHROMOSOME DELETION; CHROMOSOME REARRANGEMENT; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DNA CLEAVAGE; GENE; GENE INSERTION; GENE LOCATION; GENE LOCUS; GENE MUTATION; GENE TARGETING; HBB GENE; MUTATION RATE; POINT MUTATION; PRIORITY JOURNAL;

BETA-GLOBINS; CHROMOSOME DELETION; CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; DNA CLEAVAGE; ENDODEOXYRIBONUCLEASES; GENETIC LOCI; HEK293 CELLS; HUMANS; RECEPTORS, CCR5;

EID: 84884950106     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt714     Document Type: Article

References (31)

1. Perez, E.E., Wang, J., Miller, J.C., Jouvenot, Y., Kim, K.A., Liu, O., Wang, N., Lee, G., Bartsevich, V.V., Lee, Y.L. et al. (2008) Establishment of HIV-1 resistance in CD4+T cells by genome editing using zinc-finger nucleases. Nat. Biotechnol., 26, 808-816.
2. Geurts, A.M., Cost, G.J., Freyvert, Y., Zeitler, B., Miller, J.C., Choi, V.M., Jenkins, S.S., Wood, A., Cui, X., Meng, X. et al. (2009) Knockout rats via embryo microinjection of zinc-finger nucleases. Science, 325, 433.
3. Bolotin, A., Quinquis, B., Sorokin, A. and Ehrlich, S.D. (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology, 151, 2551-2561.
4. Horvath, P. and Barrangou, R. (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science, 327, 167-170.
5. Marraffini, L.A. and Sontheimer, E.J. (2010) CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat. Rev. Genet., 11, 181-190.
6. Garneau, J.E., Dupuis, M., Villion, M., Romero, D.A., Barrangou, R., Boyaval, P., Fremaux, C., Horvath, P., Magadá n, A.H. and Moineau, S. (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature, 468, 67-71.
7. Hale, C.R., Zhao, P., Olson, S., Duff, M.O., Graveley, B.R., Wells, L., Terns, R.M. and Terns, M.P. (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell, 139, 945-956.
8. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A. et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science, 339, 819-823.
9. Pattanayak, V., Ramirez, C.L., Joung, J.K. and Liu, D.R. (2011) Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection. Nat. Methods, 8, 765-770.
10. Gabriel, R., Lombardo, A., Arens, A., Miller, J.C., Genovese, P., Kaeppel, C., Nowrouzi, A., Bartholomae, C.C., Wang, J., Friedman, G. et al. (2011) An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat. Biotechnol., 29, 816-823.
11. Cornu, T.I. and Cathomen, T. (2010) Quantification of zinc finger nuclease-associated toxicity. Methods Mol. Biol., 649, 237-245.
12. Ramirez, C.L., Certo, M.T., Mussolino, C., Goodwin, M.J., Cradick, T.J., McCaffrey, A.P., Cathomen, T., Scharenberg, A.M. and Joung, J.K. (2012) Engineered zinc finger nickases induce homology-directed repair with reduced mutagenic effects. Nucleic Acids Res., 40, 5560-5568.
13. Tesson, L., Usal, C., Ménoret, S., Leung, E., Niles, B.J., Remy, S., Santiago, Y., Vincent, A.I., Meng, X., Zhang, L. et al. (2011) Knockout rats generated by embryo microinjection of TALENs. Nat. Biotechnol., 29, 695-696.
14. Hockemeyer, D., Wang, H., Kiani, S., Lai, C.S., Gao, Q., Cassady, J.P., Cost, G.J., Zhang, L., Santiago, Y., Miller, J.C. et al. (2011) Genetic engineering of human pluripotent cells using TALE nucleases. Nat. Biotechnol., 29, 731-734.
15. Mussolino, C., Morbitzer, R., Lutge, F., Dannemann, N., Lahaye, T. and Cathomen, T. (2011) A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res., 39, 9283-9293.
16. Gasiunas, G., Barrangou, R., Horvath, P. and Siksnys, V. (2012) Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc. Natl Acad. Sci. USA, 109, E2579-E2586.
17. Jinek, M., East, A., Cheng, A., Lin, S., Ma, E. and Doudna, J. (2013) RNA-programmed genome editing in human cells. Elife, 2, e00471.
18. Jiang, W., Bikard, D., Cox, D., Zhang, F. and Marraffini, L.A. (2013) RNA-guided editing of bacterial genomes using CRISPRCas systems. Nat. Biotechnol., 31, 233-239.
19. Hsu, P.D., Scott, D.A., Weinstein, J.A., Ran, F.A., Konermann, S., Agarwala, V., Li, Y., Fine, E.J., Wu, X. et al. (2013) DNA targeting specificity of the RNA-guided Cas9 nuclease. Nat. Biotechnol., 31, 827-832.
20. Sapranauskas, R., Gasiunas, G., Fremaux, C., Barrangou, R., Horvath, P. and Siksnys, V. (2011) The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res., 39, 9275-9282.
21. Guschin, D.Y., Waite, A.J., Katibah, G.E., Miller, J.C., Holmes, M.C. and Rebar, E.J. (2010) A rapid and general assay for monitoring endogenous gene modification. Methods Mol. Biol., 649, 247-256.
22. Fu, Y., Foden, J.A., Khayter, C., Maeder, M.L., Reyon, D., Joung, J.K. and Sander, J.D. (2013) High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol., 31, 822-826.
23. Lee, H.J., Kim, E. and Kim, J.S. (2010) Targeted chromosomal deletions in human cells using zinc finger nucleases. Genome Res., 20, 81-89.
24. Gupta, A., Hall, V.L., Kok, F.O., Shin, M., McNulty, J.C., Lawson, N.D. and Wolfe, S.A. (2013) Targeted chromosomal deletions and inversions in zebrafish. Genome Res., 23, 1008-1017.
25. Xiao, A., Wang, Z., Hu, Y., Wu, Y., Luo, Z., Yang, Z., Zu, Y., Li, W., Huang, P., Tong, X. et al. (2013) Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish. Nucleic Acids Res, 41, e141.
26. Gratz, S.J., Cummings, A.M., Nguyen, J.N., Hamm, D.C., Donohue, L.K., Harrison, M.M., Wildonger, J. and O'Connor- Giles, K.M. (2013) Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics, 194, 1029-1035.
27. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A. and Charpentier, E. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337, 816-821.
28. Yu, A.M. and McVey, M. (2010) Synthesis-dependent microhomology-mediated end joining accounts for multiple types of repair junctions. Nucleic Acids Res., 38, 5706-5717.
29. Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E. and Church, G.M. (2013) RNA-guided human genome engineering via Cas9. Science, 339, 823-826.
30. Mojica, F.J., Díez-Villaseňor, C., García- Martínez, J. and Almendros, C. (2009) Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology, 155, 733-740.
31. Wang, H., Yang, H., Shivalila, C.S., Dawlaty, M.M., Cheng, A.W., Zhang, F. and Jaenisch, R. (2013) One-Step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell, 153, 910-918.