Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins

Genome Research

Volumn 24, Issue 6, 2014, Pages 1012-1019

  Kim, Sojung ^a,b   Kim, Daesik ^a,b   Cho, Seung Woo ^a,b   Kim, Jungeun ^a,b   Kim, Jin Soo ^a,b  

^a Seoul National University   (South Korea)

^b Institute for Basic Science   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; DNA; GUIDE RNA; NUCLEASE; OLIGONUCLEOTIDE; PROTEIN; PROTEIN TALEN; RECOMBINANT PROTEIN; RIBONUCLEOPROTEIN; RIBONUCLEOPROTEIN CAS 9; RNA; RNA GUIDED ENGINEERED NUCLEASE; UNCLASSIFIED DRUG; ZINC FINGER NUCLEASE;

ARTICLE; CHROMOSOME; CHROMOSOME DELETION; DNA TRANSFECTION; ELECTROPORATION; EMBRYONIC STEM CELL; FIBROBLAST; GENE LOCUS; GENE MUTATION; GENETIC PROCEDURES; GENOME EDITING; HUMAN; HUMAN CELL; HYBRIDIZATION; PLASMID; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; CELL CULTURE; CRISPR CAS SYSTEM; GENETICS; HUMAN GENOME; METABOLISM; POINT MUTATION; PROCEDURES; RNA EDITING; SITE DIRECTED MUTAGENESIS; TUMOR CELL LINE;

CELL LINE, TUMOR; CELLS, CULTURED; CRISPR-CAS SYSTEMS; FIBROBLASTS; GENOME, HUMAN; HUMANS; MUTAGENESIS, SITE-DIRECTED; PLURIPOTENT STEM CELLS; POINT MUTATION; RIBONUCLEOPROTEINS; RNA EDITING; RNA, GUIDE;

EID: 84901834420     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.171322.113     Document Type: Article

References (55)

1. Bae S, Park J, Kim JS. 2014. Cas-OFFinder: a fast and versatile algorithm that searches for potential off-target sites of Cas9 RNA-guided endonucleases. Bioinformatics doi: 10.1093/bioinformatics/btu048.
2. Bibikova M, Beumer K, Trautman JK, Carroll D. 2003. Enhancing gene targeting with designed zinc finger nucleases. Science 300: 764. (Pubitemid 36532104)
3. Brunet E, Simsek D, Tomishima M, DeKelver R, Choi VM, Gregory P, Urnov F, Weinstock DM, Jasin M. 2009. Chromosomal translocations induced at specified loci in human stem cells. Proc Natl Acad Sci 106: 10620-10625.
4. Budman J, Chu G. 2005. Processing of DNA for nonhomologous end-joining by cell-free extract. EMBO J 24: 849-860. (Pubitemid 40396113)
5. Carlson DF, Tan W, Lillico SG, Stverakova D, Proudfoot C, Christian M, Voytas DF, Long CR, Whitelaw CB, Fahrenkrug SC. 2012. Efficient TALEN-mediated gene knockout in livestock. Proc Natl Acad Sci 109:17382-17387.
6. Chen F, Pruett-Miller SM, Huang Y, Gjoka M, Duda K, Taunton J, Collingwood TN, Frodin M, Davis GD. 2011. High-frequency genome editing using ssDNA oligonucleotides with zinc-finger nucleases. Nat Methods 8: 753-755.
7. Cho SW, Kim S, Kim JM, Kim JS. 2013a. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol 31: 230-232.
8. Cho SW, Lee J, Carroll D, Kim JS. 2013b. Heritable gene knockout in Caenorhabditis elegans by direct injection of Cas9-sgRNA ribonucleoproteins. Genetics 195: 1177-1180.
9. Cho SW, Kim S, Kim Y, Kweon J, Kim HS, Bae S, Kim JS. 2014. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res 24: 132-141.
10. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819-823.
11. Cradick TJ, Fine EJ, Antico CJ, Bao G. 2013. CRISPR/Cas9 systems targeting β-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res 41: 9584-9592.
12. Dickinson DJ, Ward JD, Reiner DJ, Goldstein B. 2013. Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat Methods 10: 1028-1034.
13. Friedland AE, Tzur YB, Esvelt KM, Colaiacovo MP, Church GM, Calarco JA. 2013. Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat Methods 10: 741-743.
14. Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD. 2013. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31: 822-826.
15. Fu Y, Sander JD, Reyon D, Cascio VM, Joung JK. 2014. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol 32: 279-284.
16. Gabriel R, Lombardo A, Arens A, Miller JC, Genovese P, Kaeppel C, Nowrouzi A, Bartholomae CC, Wang J, Friedman G, et al. 2011. An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat Biotechnol 29: 816-823.
17. Gaj T, Guo J, Kato Y, Sirk SJ, Barbas CF III. 2012. Targeted gene knockout by direct delivery of zinc-finger nuclease proteins. Nat Methods 9: 805-807.
18. Gratz SJ, Cummings AM, Nguyen JN, Hamm DC, Donohue LK, Harrison MM, Wildonger J, O'Connor-Giles KM. 2013. Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics 194: 1029-1035.
19. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, Matsumoto M, Hoshino K, Wagner H, Takeda K, et al. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745. (Pubitemid 32015992)
20. Horvath P, Barrangou R. 2010. CRISPR/Cas, the immune system of bacteria and archaea. Science 327: 167-170.
21. Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li Y, Fine EJ, Wu X, Shalem O, et al. 2013. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31: 827-832.
22. Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK. 2013. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31: 227-229.
23. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. 2013. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31: 233-239.
24. Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J. 2013. RNA-programmed genome editing in human cells. eLife 2: e00471.
25. Kim H, Kim JS. 201 4. A guide to genome engineering with programmable nucleases. Nat Rev Genet 15: 321-334.
26. Kim HJ, Lee HJ, Kim H, Cho SW, Kim JS. 2009. Targeted genome editing in human cells with zinc finger nucleases constructed via modular assembly. Genome Res 19: 1279-1288.
27. Kim JS, Lee HJ, Carroll D. 2010. Genome editing with modularly assembled zinc-finger nucleases. Nat Methods 7: 91 (author reply 91-92).
28. Kim S, Lee MJ, Kim H, Kang M, Kim JS. 2011. Preassembled zinc-finger arrays for rapid construction of ZFNs. Nat Methods 8: 7.
29. Kim E, Kim S, Kim DH, Choi BS, Choi IY, Kim JS. 2012. Precision genome engineering with programmable DNA-nicking enzymes. Genome Res 22: 1327-1333.
30. Kim Y, Kweon J, Kim A, Chon JK, Yoo JY, Kim HJ, Kim S, Lee C, Jeong E, Chung E, et al. 2013a. A library of TAL effector nucleases spanning the human genome. Nat Biotechnol 31: 251-258.
31. Kim Y, Kweon J, Kim JS. 2013b. TALENs and ZFNs are associated with different mutation signatures. Nat Methods 10: 185.
32. Kim JM, Kim D, Kim S, Kim JS. 2014. Genotyping with CRISPR-Cas-derived RNA-guided endonucleases. Nat Commun 5: 3157.
33. Lee HJ, Kim E, Kim JS. 2010. Targeted chromosomal deletions in human cells using zinc finger nucleases. Genome Res 20: 81-89.
34. Lee HJ, Kweon J, Kim E, Kim S, Kim JS. 2012. Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleases. Genome Res 22: 539-548.
35. Li D, Qiu Z, Shao Y, Chen Y, Guan Y, Liu M, Li Y, Gao N, Wang L, Lu X, et al. 2013a. Heritable gene targeting in the mouse and rat using a CRISPR-Cas system. Nat Biotechnol 31: 681-683.
36. Li JF, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Church GM, Sheen J. 2013b. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31: 688-691.
37. Li W, Teng F, Li T, Zhou Q. 2013c. Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems. Nat Biotechnol 31: 684-686.
38. Liu J, Gaj T, Patterson JT, Sirk SJ, Barbas Iii CF. 2014. Cell-penetrating peptide-mediated delivery of TALEN proteins via bioconjugation for genome engineering. PLoS ONE 9: e85755.
39. Mali P, Aach J, Stranges PB, Esvelt KM, Moosburner M, Kosuri S, Yang L, Church GM. 2013a. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol 31: 833-838.
40. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. 2013b. RNA-guided human genome engineering via Cas9. Science 339: 823-826.
41. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Meng X, Paschon DE, Leung E, Hinkley SJ, et al. 2011. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29: 143-148.
42. Nekrasov V, Staskawicz B, Weigel D, Jones JD, Kamoun S. 2013. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31: 691-693.
43. Pattanayak V, Lin S, Guilinger JP, Ma E, Doudna JA, Liu DR. 2013. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat Biotechnol 31: 839-843.
44. Pauwels K, Podevin N, Breyer D, Carroll D, Herman P. 2014. Engineering nucleases for gene targeting: safety and regulatory considerations. New Biotechnol 31: 18-27.
45. Podevin N, Davies HV, Hartung F, Nogue F, Casacuberta JM. 2013. Site-directed nucleases: a paradigm shift in predictable, knowledge-based plant breeding. Trends Biotechnol 31: 375-383.
46. Porteus MH, Baltimore D. 2003. Chimeric nucleases stimulate gene targeting in human cells. Science 300: 763. (Pubitemid 36532103)
47. Ramakrishna S, Kwaku Dad AB, Beloor J, Gopalappa R, Lee SK, Kim H. 2014. Gene disruption by cell-penetrating peptide-mediated delivery of Cas9 protein and guide RNA. Genome Res (this issue). doi: 10.1101/gr.171264.113.
48. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, et al. 2013. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154: 1380-1389.
49. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, et al. 2013. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31: 686-688.
50. Sun L, Wu J, Du F, Chen X, Chen ZJ. 2013. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339: 786-791.
51. Sung YH, Baek IJ, Kim DH, Jeon J, Lee J, Lee K, Jeong D, Kim JS, Lee HW. 2013. Knockout mice created by TALEN-mediated gene targeting. Nat Biotechnol 31: 23-24.
52. Sung YH, Kim JM, Kim HT, Lee J, Jeon J, Jin Y, Choi JH, Ban YH, Ha SJ, Kim CH, et al. 2014. Highly efficient gene knockout in mice and zebrafish with RNA-guided endonucleases. Genome Res 24: 125-131.
53. Wagner H. 2001. Toll meets bacterial CpG-DNA. Immunity 14: 499-502. (Pubitemid 32520861)
54. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R. 2013. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153: 910-918.
55. Wiedenheft B, Sternberg SH, Doudna JA. 2012. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482: 331-338.