DNA-binding-domain fusions enhance the targeting range and precision of Cas9

Nature Methods

Volumn 12, Issue 12, 2015, Pages 1150-1156

  Bolukbasi, Mehmet Fatih ^a   Gupta, Ankit ^a   Oikemus, Sarah ^a   Derr, Alan G ^a   Garber, Manuel ^a   Brodsky, Michael H ^a   Zhu, Lihua Julie ^a   Wolfe, Scot A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL POPULATION; CRISPR CAS SYSTEM; CRISPR CAS9 SYSTEM; DNA BINDING; DNA CLEAVAGE; EMBRYO; ENZYME ACTIVITY; GENE TARGETING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN GENOME; PRIORITY JOURNAL; PROMOTER REGION; WESTERN BLOTTING; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; GENETICS; HEK293 CELL LINE; PROCEDURES; TRANSCRIPTION INITIATION;

CRISPR ASSOCIATED PROTEIN; DNA BINDING PROTEIN; GUIDE RNA; ZINC FINGER PROTEIN;

CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; DNA CLEAVAGE; DNA-BINDING PROTEINS; GENE TARGETING; HEK293 CELLS; HUMANS; RNA, GUIDE; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; ZINC FINGERS;

EID: 84949087122     PISSN: 15487091     EISSN: 15487105     Source Type: Journal    
DOI: 10.1038/nmeth.3624     Document Type: Article

References (63)

1. Doudna, J.A., & Charpentier, E. Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346, 1258096 (2014
2. Sander, J.D., & Joung, J.K. CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol. 32, 347-355 (2014
3. Hsu, P.D., Lander, E.S., & Zhang, F. Development and applications of CRISPR-Cas9 for genome engineering. Cell 157, 1262-1278 (2014
4. Jinek, M., et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821 (2012
5. Sternberg, S.H., Redding, S., Jinek, M., Greene, E.C., & Doudna, J.A DNA Interrogation by the CRISPR RNA-guided Endonuclease Cas9. Nature 507, 62-67 (2014
6. Szczelkun, M.D., et al. Direct observation of R-loop formation by single RNA-guided Cas9 and Cascade effector complexes. Proc. Natl. Acad. Sci. USA 111, 9798-9803 (2014
7. Anders, C., Niewoehner, O., Duerst, A., & Jinek, M. Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513, 569-573 (2014
8. Jiang, F., Zhou, K., Ma, L., Gressel, S., & Doudna, J.A. A Cas9-guide RNA complex preorganized for target DNA recognition. Science 348, 1477-1481 (2015
9. Hsu, P.D., et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31, 827-832 (2013
10. Tsai, S.Q., et al. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol. 32, 569-576 (2014
11. Zhang, Y., et al. Comparison of non-canonical PAMs for CRISPR/Cas9-mediated DNA cleavage in human cells. Sci. Rep. 4, 5405 (2014
12. Gabriel, R., von Kalle, C., & Schmidt, M. Mapping the precision of genome editing. Nat. Biotechnol. 33, 150-152 (2015
13. Ledford, H. CRISPR, the disruptor. Nature 522, 20-24 (2015
14. Fu, Y., et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31, 822-826 (2013
15. 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
16. Pattanayak, V., et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 31, 839-843 (2013
17. 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
18. Frock, R.L., et al. Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases. Nat. Biotechnol. 33, 179-186 (2015
19. Kim, D., et al. Digenome-seq: genome-wide profiling of CRISPR-Cas9 off-target effects in human cells. Nat. Methods 12, 237-243 (2015
20. Wang, X., et al. Unbiased detection of off-target cleavage by CRISPR-Cas9 and TALENs using integrase-defective lentiviral vectors. Nat. Biotechnol. 33, 175-178 (2015
21. Zhu, L.J., Holmes, B.R., Aronin, N., & Brodsky, M.H. CRISPRseek: a bioconductor package to identify target-specific guide RNAs for CRISPR-Cas9 genome-editing systems. PLoS One 9, e108424 (2014
22. Zhu, L.J. Overview of guide RNA design tools for CRISPR-Cas9 genome editing technology. Front. Biol. 10, 289-296 (2015
23. Brunet, E., et al. Chromosomal translocations induced at specified loci in human stem cells. Proc. Natl. Acad. Sci. USA 106, 10620-10625 (2009
24. Lee, H.J., Kim, E., & Kim, J.-S. Targeted chromosomal deletions in human cells using zinc finger nucleases. Genome Res. 20, 81-89 (2010
25. Fu, Y., Sander, J.D., Reyon, D., Cascio, V.M., & Joung, J.K. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol. 32, 279-284 (2014
26. Cho, S.W., et al. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res. 24, 132-141 (2014
27. Ran, F.A., et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389 (2013
28. Mali, P., et al. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31, 833-838 (2013
29. 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
30. Zetsche, B., Volz, S.E., & Zhang, F. A split-Cas9 architecture for inducible genome editing and transcription modulation. Nat. Biotechnol. 33, 139-142 (2015
31. Nihongaki, Y., Kawano, F., Nakajima, T., & Sato, M. Photoactivatable CRISPR-Cas9 for optogenetic genome editing. Nat. Biotechnol. 33, 755-760 (2015
32. Wright, A.V., et al. Rational design of a split-Cas9 enzyme complex. Proc. Natl. Acad. Sci. USA 112, 2984-2989 (2015
33. Davis, K.M., Pattanayak, V., Thompson, D.B., Zuris, J.A., & Liu, D.R. Small molecule-triggered Cas9 protein with improved genome-editing specificity. Nat. Chem. Biol. 11, 316-318 (2015
34. Kleinstiver, B.P., et al. Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 523, 481-485 (2015
35. Kim, S., Kim, D., Cho, S.W., Kim, J., & Kim, J.-S. Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Res. 24, 1012-1019 (2014
36. Ramakrishna, S., et al. Gene disruption by cell-penetrating peptide-mediated delivery of Cas9 protein and guide RNA. Genome Res. 24, 1020-1027 (2014
37. 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
38. Tsai, S.Q., & Joung, J.K. What's changed with genome editing?. Cell Stem Cell 15, 3-4 (2014
39. Urnov, F.D., Rebar, E.J., Holmes, M.C., Zhang, H.S., & Gregory, P.D. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11, 636-646 (2010
40. Joung, J.K., & Sander, J.D. TALENs: a widely applicable technology for targeted genome editing. Nat. Rev. Mol. Cell Biol. 14, 49-55 (2013
41. Persikov, A.V., et al. A systematic survey of the Cys2His2 zinc finger DNA-binding landscape. Nucleic Acids Res. 43, 1965-1984 (2015
42. Hubbard, B.P., et al. Continuous directed evolution of DNA-binding proteins to improve TALEN specificity. Nat. Methods 12, 939-942 (2015
43. Boissel, S., et al. megaTALs: a rare-cleaving nuclease architecture for therapeutic genome engineering. Nucleic Acids Res. 42, 2591-2601 (2014
44. Khalil, A.S., et al. A synthetic biology framework for programming eukaryotic transcription functions. Cell 150, 647-658 (2012
45. Meckler, J.F., et al. Quantitative analysis of TALE-DNA interactions suggests polarity effects. Nucleic Acids Res. 41, 4118-4128 (2013
46. Wilson, K.A., Chateau, M.L., & Porteus, M.H. Design and development of artificial zinc finger transcription factors and zinc finger nucleases to the hTERT locus. Mol. Ther. Nucleic Acids 2, e87 (2013
47. Atkinson, H., & Chalmers, R. Delivering the goods: viral and non-viral gene therapy systems and the inherent limits on cargo DNA and internal sequences. Genetica 138, 485-498 (2010
48. Klemm, J.D., & Pabo, C.O. Oct-1 POU domain-DNA interactions: cooperative binding of isolated subdomains and effects of covalent linkage. Genes Dev. 10, 27-36 (1996
49. Hou, Z., et al. Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 110, 15644-15649 (2013
50. Ran, F.A., et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature 520, 186-191 (2015
51. Kearns, N.A., et al. Cas9 effector-mediated regulation of transcription and differentiation in human pluripotent stem cells. Development 141, 219-223 (2014
52. Villefranc, J.A., Amigo, J., & Lawson, N.D. Gateway compatible vectors for analysis of gene function in the zebrafish. Dev. Dyn. 236, 3077-3087 (2007
53. Gupta, A., et al. An optimized two-finger archive for ZFN-mediated gene targeting. Nat. Methods 9, 588-590 (2012
54. Zhu, C., et al. Using defined finger-finger interfaces as units of assembly for constructing zinc-finger nucleases. Nucleic Acids Res. 41, 2455-2465 (2013
55. 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
56. Kok, F.O., Gupta, A., Lawson, N.D., & Wolfe, S.A. Construction and application of site-specific artificial nucleases for targeted gene editing. Methods Mol. Biol. 1101, 267-303 (2014
57. Gupta, A., et al. Targeted chromosomal deletions and inversions in zebrafish. Genome Res. 23, 1008-1017 (2013
58. Schneider, C.A., Rasband, W.S., & Eliceiri, K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675 (2012
59. Gupta, A., Meng, X., Zhu, L.J., Lawson, N.D., & Wolfe, S.A. Zinc finger protein-dependent and -independent contributions to the in vivo off-target activity of zinc finger nucleases. Nucleic Acids Res. 39, 381-392 (2011
60. Ihaka, R., & Gentleman, R.R. A language for data analysis and graphics. J. Comput. Graph. Stat. 5, 299-314 (1996
61. Benjamini, Y., & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289-300 (1995
62. Zhu, L.J., et al. ChIPpeakAnno: a Bioconductor package to annotate ChIP-seq and ChIP-chip data. BMC Bioinformatics 11, 237 (2010
63. Zhu, L.J. Integrative analysis of ChIP-chip and ChIP-seq dataset. in Methods in Molecular Biology 1067 (eds. Lee, T.-L., & Shui Luk, A.C.) 105-124 (Humana Press, 2013