Genome editing comes of age

Nature Protocols

Volumn 11, Issue 9, 2016, Pages 1573-1578

  Kim, Jin Soo ^a,b  

^a Institute for Basic Science   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CRISPR ASSOCIATED PROTEIN; CRISPR ASSOCIATED PROTEIN 9; ENDONUCLEASE; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; UNCLASSIFIED DRUG; ZINC FINGER NUCLEASE; DEOXYRIBONUCLEASE;

CHROMOSOME REARRANGEMENT; CRISPR CAS SYSTEM; DNA MODIFICATION; GENE DELIVERY SYSTEM; GENE TARGETING; GENE THERAPY; GENETIC ENGINEERING; GENETIC PROCEDURES; GENOME EDITING; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA EDITING; ANIMAL; CHROMOSOME; GENE EDITING; GENETICS; GENOME; METABOLISM; PROCEDURES;

ANIMALS; CHROMOSOMES; CRISPR-CAS SYSTEMS; DEOXYRIBONUCLEASES; GENE EDITING; GENETIC THERAPY; GENOME; HUMANS;

EID: 84981283748     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2016.104     Document Type: Review

References (88)

1. Kim, H. & Kim, J.S. A guide to genome engineering with programmable nucleases. Nat. Rev. Genet. 15, 321-334 (2014).
2. Cho, S.W., Kim, S., Kim, J.M. & Kim, J.S. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31, 230-232 (2013).
3. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013).
4. Mali, P. et al. RNA-guided human genome engineering via Cas9. Science 339, 823-826 (2013).
5. Jinek, M. et al. RNA-programmed genome editing in human cells. eLife 2, e00471 (2013).
6. Cho, S.W., Lee, J., Carroll, D., Kim, J.S. & Lee, J. Heritable gene knockout in Caenorhabditis elegans by direct injection of Cas9-sgRNA ribonucleoproteins. Genetics 195, 1177-1180 (2013).
7. Hwang, W.Y. et al. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat. Biotechnol. 31, 227-229 (2013).
8. Wang, H. et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153, 910-918 (2013).
9. Sung, Y.H. et al. Highly efficient gene knockout in mice and zebrafish with RNA-guided endonucleases. Genome Res. 24, 125-131 (2014).
10. Shan, Q. et al. Targeted genome modification of crop plants using a CRISPRCas system. Nat. Biotechnol. 31, 686-688 (2013).
11. Woo, J.W. et al. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat. Biotechnol. 33, 1162-1164 (2015).
12. Gilbert, L.A. et al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154, 442-451 (2013).
13. Qi, L.S. et al. Repurposing CRISPR as an RNA-guided platform for sequencespecific control of gene expression. Cell 152, 1173-1183 (2013).
14. Hilton, I.B. et al. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat. Biotechnol. 33, 510-517 (2015).
15. Thakore, P.I. et al. Highly specific epigenome editing by CRISPR-Cas9 repressors for silencing of distal regulatory elements. Nat. Methods 12, 1143-1149 (2015).
16. Gaj, T., Gersbach, C.A. & Barbas, C.F. III. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 31, 397-405 (2013).
17. Capecchi, M.R. Gene targeting in mice: functional analysis of the mammalian genome for the twenty-first century. Nat. Rev. Genet. 6, 507-512 (2005).
18. Rudin, N. & Haber, J.E. Efficient repair of HO-induced chromosomal breaks in Saccharomyces cerevisiae by recombination between flanking homologous sequences. Mol. Cell. Biol. 8, 3918-3928 (1988).
19. Rouet, P., Smih, F. & Jasin, M. Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol. Cell. Biol. 14, 8096-8106 (1994).
20. Epinat, J.C. et al. A novel engineered meganuclease induces homologous recombination in yeast and mammalian cells. Nucleic Acids Res. 31, 2952-2962 (2003).
21. Li, L., Wu, L.P. & Chandrasegaran, S. Functional domains in Fok I restriction endonuclease. Proc. Natl. Acad. Sci. USA 89, 4275-4279 (1992).
22. Kim, Y.G. & Chandrasegaran, S. Chimeric restriction endonuclease. Proc. Natl. Acad. Sci. USA 91, 883-887 (1994).
23. Kim, Y.G., Cha, J. & Chandrasegaran, S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc. Natl. Acad. Sci. USA 93, 1156-1160 (1996).
24. Pavletich, N.P. & Pabo, C.O. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science 252, 809-817 (1991).
25. Desjarlais, J.R. & Berg, J.M. Redesigning the DNA-binding specificity of a zinc finger protein: a data base-guided approach. Proteins 12, 101-104 (1992).
26. Rebar, E.J. & Pabo, C.O. Zinc finger phage: affinity selection of fingers with new DNA-binding specificities. Science 263, 671-673 (1994).
27. Bibikova, M., Golic, M., Golic, K.G. & Carroll, D. Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161, 1169-1175 (2002).
28. Bibikova, M., Beumer, K., Trautman, J.K. & Carroll, D. Enhancing gene targeting with designed zinc finger nucleases. Science 300, 764 (2003).
29. Morton, J., Davis, M.W., Jorgensen, E.M. & Carroll, D. Induction and repair of zinc-finger nuclease-targeted double-strand breaks in Caenorhabditis elegans somatic cells. Proc. Natl. Acad. Sci. USA 103, 16370-16375 (2006).
30. Doyon, Y. et al. Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat. Biotechnol. 26, 702-708 (2008).
31. Meng, X., Noyes, M.B., Zhu, L.J., Lawson, N.D. & Wolfe, S.A. Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat. Biotechnol. 26, 695-701 (2008).
32. Lloyd, A., Plaisier, C.L., Carroll, D. & Drews, G.N. Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc. Natl. Acad. Sci. USA 102, 2232-2237 (2005).
33. Townsend, J.A. et al. High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459, 442-445 (2009).
34. Kim, H.J., Lee, H.J., Kim, H., Cho, S.W. & Kim, J.S. Targeted genome editing in human cells with zinc finger nucleases constructed via modular assembly. Genome Res. 19, 1279-1288 (2009).
35. Porteus, M.H. & Baltimore, D. Chimeric nucleases stimulate gene targeting in human cells. Science 300, 763 (2003).
36. Urnov, F.D. et al. Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435, 646-651 (2005).
37. Maeder, M.L. et al. Rapid "open-source" engineering of customized zincfinger nucleases for highly efficient gene modification. Mol. Cell 31, 294-301 (2008).
38. Ramirez, C.L. et al. Unexpected failure rates for modular assembly of engineered zinc fingers. Nat. Methods 5, 374-375 (2008).
39. Kim, J.S., Lee, H.J. & Carroll, D. Genome editing with modularly assembled zinc-finger nucleases. Nat. Methods 7, 91 (2010).
40. Kim, S., Lee, M.J., Kim, H., Kang, M. & Kim, J.S. Preassembled zinc-finger arrays for rapid construction of ZFNs. Nat. Methods 8, 7 (2011).
41. Miller, J.C. et al. An improved zinc-finger nuclease architecture for highly specific genome editing. Nat. Biotechnol. 25, 778-785 (2007).
42. Bhakta, M.S. et al. Highly active zinc-finger nucleases by extended modular assembly. Genome Res. 23, 530-538 (2013).
43. Sander, J.D. et al. Selection-free zinc-finger-nuclease engineering by context-dependent assembly (CoDA). Nat. Methods 8, 67-69 (2011).
44. Szczepek, M. et al. Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat. Biotechnol. 25, 786-793 (2007).
45. Gupta, A. et al. An optimized two-finger archive for ZFN-mediated gene targeting. Nat. Methods 9, 588-590 (2012).
46. Moscou, M.J. & Bogdanove, A.J. A simple cipher governs DNA recognition by TAL effectors. Science 326, 1501 (2009).
47. Boch, J. et al. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326, 1509-1512 (2009).
48. Miller, J.C. et al. A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29, 143-148 (2011).
49. Cermak, T. et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, e82 (2011).
50. Briggs, A.W. et al. Iterative capped assembly: rapid and scalable synthesis of repeat-module DNA such as TAL effectors from individual monomers. Nucleic Acids Res. 40, e117 (2012).
51. Reyon, D. et al. FLASH assembly of TALENs for high-throughput genome editing. Nat. Biotechnol. 30, 460-465 (2012).
52. Kim, Y. et al. A library of TAL effector nucleases spanning the human genome. Nat. Biotechnol. 31, 251-258 (2013).
53. Jinek, M. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821 (2012).
54. Cradick, T.J., Fine, E.J., Antico, C.J. & Bao, G. CRISPR/Cas9 systems targeting b-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res. 41, 9584-9592 (2013).
55. Fu, Y. et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31, 822-826 (2013).
56. Pattanayak, V. et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 31, 839-843 (2013).
57. Cho, S.W. et al. Analysis of off-target effects of CRISPR/Cas-derived RNAguided endonucleases and nickases. Genome Res. 24, 132-141 (2014).
58. Lin, Y. et al. CRISPR/Cas9 systems have off-target activity with insertions or deletions between target DNA and guide RNA sequences. Nucleic Acids Res. 42, 7473-7485 (2014).
59. Koo, T., Lee, J. & Kim, J.S. Measuring and reducing off-target activities of programmable nucleases including CRISPR-Cas9. Mol. Cells 38, 475-481 (2015).
60. Kim, D. et al. Digenome-seq: genome-wide profiling of CRISPR-Cas9 offtarget effects in human cells. Nat. Methods 12, 237-243, 1, 243 (2015).
61. Tsai, S.Q. et al. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat. Biotechnol. 33, 187-197 (2015).
62. Kleinstiver, B.P. et al. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529, 490-495 (2016).
63. Slaymaker, I.M. et al. Rationally engineered Cas9 nucleases with improved specificity. Science 351, 84-88 (2016).
64. Fu, Y., Sander, J.D., Reyon, D., Cascio, V.M. & Joung, J.K. Improving CRISPRCas nuclease specificity using truncated guide RNAs. Nat. Biotechnol. 32, 279-284 (2014).
65. Tsai, S.Q. et al. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol. 32, 569-576 (2014).
66. Guilinger, J.P., Thompson, D.B. & Liu, D.R. Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat. Biotechnol. 32, 577-582 (2014).
67. Bolukbasi, M.F. et al. DNA-binding-domain fusions enhance the targeting range and precision of Cas9. Nat. Methods 12, 1150-1156 (2015).
68. Mali, P. et al. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31, 833-838 (2013).
69. Ramirez, C.L. et al. Engineered zinc finger nickases induce homology-directed repair with reduced mutagenic effects. Nucleic Acids Res. 40, 5560-5568 (2012).
70. Ran, F.A. et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389 (2013).
71. Kim, E. et al. Precision genome engineering with programmable DNA-nicking enzymes. Genome Res. 22, 1327-1333 (2012).
72. Gaj, T., Guo, J., Kato, Y., Sirk, S.J. & Barbas, C.F., III. Targeted gene knockout by direct delivery of zinc-finger nuclease proteins. Nat. Methods 9, 805-807 (2012).
73. Kim, S., Kim, D., Cho, S.W., Kim, J. & Kim, J.S. Highly efficient RNAguided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Res. 24, 1012-1019 (2014).
74. Zuris, J.A. et al. Cationic lipid-mediated delivery of proteins enables efficient protein-based genome editing in vitro and in vivo. Nat. Biotechnol. 33, 73-80 (2015).
75. Ramakrishna, S. et al. Gene disruption by cell-penetrating peptide-mediated delivery of Cas9 protein and guide RNA. Genome Res. 24, 1020-1027 (2014).
76. Lee, H.J., Kim, E. & Kim, J.S. Targeted chromosomal deletions in human cells using zinc finger nucleases. Genome Res. 20, 81-89 (2010).
77. Lee, H.J., Kweon, J., Kim, E., Kim, S. & Kim, J.S. Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleases. Genome Res. 22, 539-548 (2012).
78. Brunet, E. et al. Chromosomal translocations induced at specified loci in human stem cells. Proc. Natl. Acad. Sci. USA 106, 10620-10625 (2009).
79. Park, C.Y. et al. Targeted inversion and reversion of the blood coagulation factor 8 gene in human iPS cells using TALENs. Proc. Natl. Acad. Sci. USA 111, 9253-9258 (2014).
80. Park, C.Y. et al. Functional correction of large factor VIII gene chromosomal inversions in hemophilia A patient-derived iPSCs using CRISPR-Cas9. Cell Stem Cell 17, 213-220 (2015).
81. Young, C.S. et al. A single CRISPR-Cas9 deletion strategy that targets the majority of DMD patients restores dystrophin function in hiPSC-derived muscle cells. Cell Stem Cell 18, 533-540 (2016).
82. Beerli, R.R., Dreier, B. & Barbas, C.F., III. Positive and negative regulation of endogenous genes by designed transcription factors. Proc. Natl. Acad. Sci. USA 97, 1495-1500 (2000).
83. Park, K.S., Jang, Y.S., Lee, H. & Kim, J.S. Phenotypic alteration and target gene identification using combinatorial libraries of zinc finger proteins in prokaryotic cells. J. Bacteriol. 187, 5496-5499 (2005).
84. Blancafort, P., Magnenat, L. & Barbas, C.F., III. Scanning the human genome with combinatorial transcription factor libraries. Nat. Biotechnol. 21, 269-274 (2003).
85. Park, K.S. et al. Phenotypic alteration of eukaryotic cells using randomized libraries of artificial transcription factors. Nat. Biotechnol. 21, 1208-1214 (2003).
86. Komor, A.C., Kim, Y.B., Packer, M.S., Zuris, J.A. & Liu, D.R. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533, 420-424 (2016).
87. Zetsche, B. et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163, 759-771 (2015).
88. Kim, D. et al. Genome-wide analysis reveals specificities of Cpf1 endonucleases in human cells. Nat. Biotechnol. http://dx.doi.org/10.1038/nbt.3609 (2016).