The neisseria meningitidis CRISPR-Cas9 system enables specific genome editing in mammalian cells

Molecular Therapy

Volumn 24, Issue 3, 2016, Pages 645-654

  Lee, Ciaran M ^a   Cradick, Thomas J ^b,c   Bao, Gang ^a  

^a Rice University   (United States)

^b Emory University   (United States)

^c CRISPR THERAPEUTICS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENOME; COMPARATIVE STUDY; CONTROLLED STUDY; CRISPR CAS SYSTEM; CRISPR CAS9 SYSTEM; DNA CLEAVAGE; GENE LOCUS; GENE STRUCTURE; GENE TARGETING; GENETIC ENGINEERING; GENETIC PARAMETERS; GENETIC PROCEDURES; GENOME ENGINEERING; MAMMAL CELL; NEISSERIA MENINGITIDIS; NONHUMAN; PROTOSPACER ADJACENT MOTIF; RNA LENGTH; SITE SPECIFIC CLEAVAGE; SPECIFIC GENOME EDITING; STREPTOCOCCUS PYOGENES; STRUCTURE ACTIVITY RELATION; BINDING SITE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EDITING; GENETICS; GENOME; HUMAN; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE; POSITION WEIGHT MATRIX;

GUIDE RNA; PROTEIN BINDING;

BASE SEQUENCE; BINDING SITES; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-CAS SYSTEMS; GENE EDITING; GENE TARGETING; GENETIC LOCI; GENOME; HUMANS; NEISSERIA MENINGITIDIS; NUCLEOTIDE MOTIFS; POSITION-SPECIFIC SCORING MATRICES; PROTEIN BINDING; RNA, GUIDE; SUBSTRATE SPECIFICITY;

EID: 84960449403     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2016.8     Document Type: Article

References (46)

1. Barrangou, R, Fremaux, C, Deveau, H, Richards, M, Boyaval, P, Moineau, S, et al. (2007). CRISPR provides acquired resistance against viruses in prokaryotes. Science 315: 1709-1712
2. Cho, SW, Kim, S, Kim, JM and Kim, JS. (2013). Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol 31: 230-232
3. DiCarlo, JE, Norville, JE, Mali, P, Rios, X, Aach, J and Church, GM. (2013). Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res 41: 4336-4343
4. Friedland, AE, Tzur, YB, Esvelt, KM, Colaiácovo, MP, Church, GM and Calarco, JA. (2013). Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat Methods 10: 741-743
5. Hwang, WY, Fu, Y, Reyon, D, Maeder, ML, Tsai, SQ, Sander, JD, et al. (2013). Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31: 227-229
6. Mali, P, Yang, L, Esvelt, KM, Aach, J, Guell, M, DiCarlo, JE, et al. (2013). RNA-guided human genome engineering via Cas9. Science 339: 823-826
7. Shen, B, Zhang, J, Wu, H, Wang, J, Ma, K, Li, Z, et al. (2013). Generation of genemodified mice via Cas9/RNA-mediated gene targeting. Cell Res 23: 720-723
8. Wang, H, Yang, H, Shivalila, CS, Dawlaty, MM, Cheng, AW, Zhang, F, et al. (2013). One-step generation of mice carrying mutations in multiple genes by CRISPR/Casmediated genome engineering. Cell 153: 910-918
9. Nekrasov, V, Staskawicz, B, Weigel, D, Jones, JD and Kamoun, S. (2013). Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31: 691-693
10. Jinek, M, Chylinski, K, Fonfara, I, Hauer, M, Doudna, JA and Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816-821
11. Urnov, FD, Miller, JC, Lee, YL, Beausejour, CM, Rock, JM, Augustus, S, et al. (2005). Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435: 646-651
12. Christian, M, Cermak, T, Doyle, EL, Schmidt, C, Zhang, F, Hummel, A, et al. (2010). Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186: 757-761
13. Fu, Y, Foden, JA, Khayter, C, Maeder, ML, Reyon, D, Joung, JK, et al. (2013). Highfrequency off-Target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31: 822-826
14. Hsu, PD, Scott, DA, Weinstein, JA, Ran, FA, Konermann, S, Agarwala, V, et al. (2013). DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31: 827-832
15. Cradick, TJ, Fine, EJ, Antico, CJ and Bao, G. (2013). CRISPR/Cas9 systems targeting-globin and CCR5 genes have substantial off-Target activity. Nucleic Acids Res 41: 9584-9592
16. Lin, Y, Cradick, TJ, Brown, MT, Deshmukh, H, Ranjan, P, Sarode, N, et al. (2014). CRISPR/Cas9 systems have off-Target activity with insertions or deletions between target DNA and guide RNA sequences. Nucleic Acids Res 42: 7473-7485
17. Tsai, SQ, Zheng, Z, Nguyen, NT, Liebers, M, Topkar, VV, Thapar, V, et al. (2015). GUIDE-seq enables genome-wide profiling of off-Target cleavage by CRISPR-Cas nucleases. Nat Biotechnol 33: 187-197
18. Frock, RL, Hu, J, Meyers, RM, Ho, YJ, Kii, E and Alt, FW. (2015). Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases. Nat Biotechnol 33: 179-186
19. Wang, X, Wang, Y, Wu, X, Wang, J, Wang, Y, Qiu, Z, et al. (2015). Unbiased detection of off-Target cleavage by CRISPR-Cas9 and TALENs using integrase-defective lentiviral vectors. Nat Biotechnol 33: 175-178
20. Kim, D, Bae, S, Park, J, Kim, E, Kim, S, Yu, HR, et al. (2015). Digenome-seq: genomewide profiling of CRISPR-Cas9 off-Target effects in human cells. Nat Methods 12: 237-43, 1 p following 243
21. Mali, P, Aach, J, Stranges, PB, Esvelt, KM, Moosburner, M, Kosuri, S, et al. (2013). CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol 31: 833-838
22. Ran, FA, Hsu, PD, Lin, CY, Gootenberg, JS, Konermann, S, Trevino, AE, et al. (2013). Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154: 1380-1389
23. Guilinger, JP, Thompson, DB and Liu, DR. (2014). Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotechnol 32: 577-582
24. Tsai, SQ, Wyvekens, N, Khayter, C, Foden, JA, Thapar, V, Reyon, D, et al. (2014). Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotechnol 32: 569-576
25. Aouida, M, Eid, A, Ali, Z, Cradick, TJ, Lee, CM, Deshmukh, H, et al. (2015). Efficient fdCas9 synthetic endonuclease with improved specificity for precise genome engineering. PLoS One 10: e0133373 (doi: 10.1371/journal.pone.0133373
26. Fonfara, I, Le Rhun, A, Chylinski, K, Makarova, KS, Lécrivain, AL, Bzdrenga, J, et al. (2014). Phylogeny of Cas9 determines functional exchangeability of dual-RNA and Cas9 among orthologous type II CRISPR-Cas systems. Nucleic Acids Res 42: 2577-2590
27. Ran, FA, Cong, L, Yan, WX, Scott, DA, Gootenberg, JS, Kriz, AJ, et al. (2015). In vivo genome editing using Staphylococcus aureus Cas9. Nature 520: 186-191
28. Müller, M, Lee, CM, Gasiunas, G, Davis, TH, Cradick, TJ, Siksnys, V, et al. (2015). Streptococcus thermophilus CRISPR-Cas9 systems enable specific editing of the human genome. Mol Ther (epub ahead of print). doi: 10.1038/mt.2015.218
29. Esvelt, KM, Mali, P, Braff, JL, Moosburner, M, Yaung, SJ and Church, GM. (2013). Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat Methods 10: 1116-1121
30. Hou, Z, Zhang, Y, Propson, NE, Howden, SE, Chu, LF, Sontheimer, EJ, et al. (2013). Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc Natl Acad Sci USA 110: 15644-15649
31. Fu, Y, Sander, JD, Reyon, D, Cascio, VM and Joung, JK. (2014). Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol 32: 279-284
32. Zhang, Y, Heidrich, N, Ampattu, BJ, Gunderson, CW, Seifert, HS, Schoen, C, et al. (2013). Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis. Mol Cell 50: 488-503
33. Cradick, TJ, Antico, CJ and Bao, G. (2014). High-Throughput cellular screening of engineered nuclease activity using the single-strand annealing assay and luciferase reporter. Methods Mol Biol 1114: 339-352
34. Cradick, TJ, Qiu, P, Lee, CM, Fine, EJ and Bao, G. (2014). COSMID: A Web-based Tool for Identifying and Validating CRISPR/Cas Off-Target Sites. Mol Ther Nucleic Acids 3: e214
35. Bae, S, Kweon, J, Kim, HS and Kim, JS. (2014). Microhomology-based choice of Cas9 nuclease target sites. Nat Methods 11: 705-706
36. Ma, E, Harrington, LB, Oconnell, MR, Zhou, K and Doudna, JA. (2015). Single-Stranded DNA Cleavage by Divergent CRISPR-Cas9 Enzymes. Mol Cell 60: 398-407
37. Zhang, Y, Rajan, R, Seifert, HS, Mondragón, A and Sontheimer, EJ. (2015). DNase H Activity of Neisseria meningitidis Cas9. Mol Cell 60: 242-255
38. Nishimasu, H, Ran, FA, Hsu, PD, Konermann, S, Shehata, SI, Dohmae, N, et al. (2014). Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell 156: 935-949
39. Nishimasu, H, Cong, L, Yan, WX, Ran, FA, Zetsche, B, Li, Y, et al. (2015). Crystal Structure of Staphylococcus aureus Cas9. Cell 162: 1113-1126
40. Kleinstiver, BP, Prew, MS, Tsai, SQ, Nguyen, NT, Topkar, VV, Zheng, Z, et al. (2015). Broadening the targeting range of Staphylococcus aureus CRISPR-Cas9 by modifying PAM recognition. Nat Biotechnol 33: 1293-1298
41. Friedland, AE, Baral, R, Singhal, P, Loveluck, K, Shen, S, Sanchez, M, et al. (2015). Characterization of Staphylococcus aureus Cas9: a smaller Cas9 for all-in-one adeno-Associated virus delivery and paired nickase applications. Genome Biol 16: 257
42. Cong, L, Ran, FA, Cox, D, Lin, S, Barretto, R, Habib, N, et al. (2013). Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819-823
43. Jiang, W, Bikard, D, Cox, D, Zhang, F and Marraffini, LA. (2013). RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31: 233-239
44. Wu, X, Scott, DA, Kriz, AJ, Chiu, AC, Hsu, PD, Dadon, DB, et al. (2014). Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat Biotechnol 32: 670-676
45. Reyon, D, Tsai, SQ, Khayter, C, Foden, JA, Sander, JD and Joung, JK. (2012). FLASH assembly of TALENs for high-Throughput genome editing. Nat Biotechnol 30: 460-465
46. Guschin, DY, Waite, AJ, Katibah, GE, Miller, JC, Holmes, MC and Rebar, EJ. (2010). A rapid and general assay for monitoring endogenous gene modification. Methods Mol Biol 649: 247-256