A convenientmethod to pre-screen candidate guide RNAs for CRISPR/Cas9 gene editing by NHEJ-mediated integration of a 'self-cleaving' GFP-expression plasmid

DNA Research

Volumn 24, Issue 6, 2017, Pages 609-621

  Tálas, András ^a,b   Kulcsár, Péter István ^b,c,d   Weinhardt, Nóra ^b,c,d   Borsy, Adrienn ^b   Tóth, Eszter ^b,c   Szebényi, Kornélia ^b   Krausz, Sarah Laura ^a,b   Huszár, Krisztina ^b,c   Vida, István ^b,e   Sturm, Ádám ^b   Gordos, Bianka ^b   Hoffmann, Orsolya Ivett ^f   Bencsura, Petra ^b,c   Nyeste, Antal ^b,c   Ligeti, Zoltán ^b   Fodor, Elfrieda ^c   Welker, Ervin ^b,c  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c INSTITUTE OF BIOCHEMISTRY   (Hungary)

^d UNIVERSITY OF SZEGED   (Hungary)

^e EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^f SZENT ISTVÁN UNIVERSITY   (Hungary)

Author keywords

Cas9; CRISPR; GRNA testing; NHEJ cloning; Reporter assay

Indexed keywords

ADULT; ARTICLE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DNA END JOINING REPAIR; FLOW CYTOMETRY; GENE EDITING; HUMAN; MAMMAL CELL; PLASMID; POLYMERASE CHAIN REACTION; ANIMAL; CRISPR CAS SYSTEM; GENETICS; GENOMICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; MOUSE; NIH 3T3 CELL LINE; PROCEDURES;

GREEN FLUORESCENT PROTEIN; GUIDE RNA;

ANIMALS; CRISPR-CAS SYSTEMS; DNA END-JOINING REPAIR; GENE EDITING; GENOMICS; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HELA CELLS; HUMANS; MICE; NIH 3T3 CELLS; PLASMIDS; RNA, GUIDE;

EID: 85030696088     PISSN: 13402838     EISSN: 17561663     Source Type: Journal    
DOI: 10.1093/dnares/dsx029     Document Type: Article

References (73)

1. 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, 816-21.
2. Mali, P., Yang, L., Esvelt, K. M., et al. 2013, RNA-guided human genome engineering via Cas9. Science, 339, 823-26.
3. Cong, L., Ran, F. A., Cox, D., et al. 2013, Multiplex genome engineering using CRISPR/Cas systems. Science, 339, 819-23.
4. Jinek, M., East, A., Cheng, A., Lin, S., Ma, E. and Doudna, J. 2013, RNA-programmed genome editing in human cells. Elife, 2, e00471.
5. Gilbert, L. A., Larson, M. H., Morsut, L., et al. 2013, CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell, 154, 442-51.
6. Shalem, O., Sanjana, N. E., Hartenian, E., et al. 2014, Genome-scale CRISPR-Cas9 knockout screening in human cells. Science, 343, 84-7.
7. Zalatan, J. G., Lee, M. E., Almeida, R., et al. 2015, Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds. Cell, 160, 339-50.
8. Gilbert, L. A., Horlbeck, M. A., Adamson, B., et al. 2014, Genome-scale CRISPR-mediated control of gene repression and activation. Cell, 159, 647-61.
9. Qi, L. S., Larson, M. H., Gilbert, L. A., et al. 2013, Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 152, 1173-83.
10. Ramakrishna, S., Dad, A.-B. K., Beloor, J., Gopalappa, R., Lee, S.-K. and Kim, H. 2014, Gene disruption by cell-penetrating peptide-mediated delivery of Cas9 protein and guide RNA. Genome Res., 24, 1020-7.
11. Mali, P., Aach, J., Stranges, P. B., et al. 2013, CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol., 31, 833-8.
12. Ran, F. A., Hsu, P. D., Lin, C.-Y., et al. 2013, Double nicking by RNAguided CRISPR Cas9 for enhanced genome editing specificity. Cell, 154, 1380-9.
13. Dow, L. E. 2015, Modeling Disease In Vivo With CRISPR/Cas9. Trends Mol. Med., 21, 609-21.
14. Kim, H. and Kim, J.-S. 2014, A guide to genome engineering with programmable nucleases. Nat. Rev. Genet., 15, 321-34.
15. Ramakrishna, S., Cho, S. W., Kim, S., et al. 2014, Surrogate reporterbased enrichment of cells containing RNA-guided Cas9 nuclease-induced mutations. Nat. Commun., 5, 3378.
16. Doench, J. G., Hartenian, E., Graham, D. B., et al. 2014, Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat. Biotechnol 32, 1262-7.
17. Wang, T., Wei, J. J., Sabatini, D.M. and Lander, E. S. 2014, Genetic screens in human cells using the CRISPR-Cas9 system. Science, 343, 80-4.
18. Chari, R., Mali, P., Moosburner, M. and Church, G. M. 2015, Unraveling CRISPR-Cas9 genome engineering parameters via a libraryon- library approach. Nat. Methods, 12, 823-6.
19. Moreno-Mateos, M. A., Vejnar, C. E., Beaudoin, J.-D., et al. 2015, CRISPRscan: designing highly efficient sgRNAs for CRISPR-Cas9 targeting in vivo. Nat. Methods, 12, 982-8.
20. Wong, N., Liu, W. and Wang, X. 2015, WU-CRISPR: characteristics of functional guide RNAs for the CRISPR/Cas9 system. Genome Biol., 16, 1-8.
21. Doench, J. G., Fusi, N., Sullender, M., et al. 2016, Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9. Nat. Biotechnol 34, 184-91.
22. Hinz, J. M., Laughery, M. F. and Wyrick, J. J. 2015, Nucleosomes inhibit Cas9 endonuclease activity in vitro. Biochemistry, 54, 7063-6.
23. Horlbeck, M. A., Witkowsky, L. B., Guglielmi, B., et al. 2016, Nucleosomes impede Cas9 access to DNA in vivo and in vitro. Elife, 5, e12677.
24. Hendel, A., Fine, E. J., Bao, G. and Porteus, M. H. 2015, Quantifying onand off-target genome editing. Trends Biotechnol., 33, 132-40.
25. Chapman, K. M., Medrano, G. A., Jaichander, P., et al. 2015, Targeted germline modifications in rats using CRISPR/Cas9 and spermatogonial stem cells. Cell Rep., 10, 1828-35.
26. Dow, L. E., Fisher, J., O'Rourke, K. P., et al. 2015, Inducible in vivo genome editing with CRISPR-Cas9. Nature Biotechnol., 33, 390-4.
27. Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A. and Zhang, F. 2013, Genome engineering using the CRISPR-Cas9 system. Nat. Protoc., 8, 2281-308.
28. Cho, S. W., Kim, S., Kim, J. M. and Kim, J.-S. 2013, Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol., 31, 230-2.
29. Qiu, P., Shandilya, H., D Alessio, J. M., O Connor, K., Durocher, J. and Gerard, G. F. 2004, Mutation detection using SurveyorTM nuclease. Biotechniques, 36, 702-7.
30. Dahlem, T. J., Hoshijima, K., Jurynec, M. J., et al. 2012, Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome. PLoS Genet., 8, e1002861.
31. Wang, X., Wang, Y., Wu, X., et al. 2015, Unbiased detection of off-target cleavage by CRISPR-Cas9 and TALENs using integrase-defective lentiviral vectors. Nat. Biotechnol., 33, 175-8.
32. Ramlee, M. K., Yan, T., Cheung, A. M., Chuah, C. T. and Li, S. 2015, High-throughput genotyping of CRISPR/Cas9-mediated mutants using fluorescent PCR-capillary gel electrophoresis. Sci. Rep., 5, 15587.
33. Brinkman, E. K., Chen, T., Amendola, M. and van Steensel, B. 2014, Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Res., 42, e168.
34. Yang, L., Guell, M., Byrne, S., et al. 2013, Optimization of scarless human stem cell genome editing. Nucleic Acids Res., 41, 9049-61.
35. Urnov, F. D., Miller, J. C., Lee, Y.-L., et al. 2005, Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature, 435, 646-51.
36. Wagner, J. C., Platt, R. J., Goldfless, S. J., Zhang, F. and Niles, J. C. 2014, Efficient CRISPR-Cas9-mediated genome editing in Plasmodium falciparum. Nat. Methods 11, 915-8.
37. Wang, H., Yang, H., Shivalila, C. S., et al. 2013, One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell, 153, 910-8.
38. Auer, T. O., Duroure, K., De Cian, A., Concordet, J.-P. and Del Bene, F. 2014, Highly efficient CRISPR/Cas9-mediated knock-in in zebrafish by homology-independent DNA repair. Genome Res., 24, 142-53.
39. Certo, M. T., Ryu, B. Y., Annis, J. E., et al. 2011, Tracking genome engineering outcome at individual DNA breakpoints. Nat. Methods, 8, 671-6.
40. Mashiko, D., Fujihara, Y., Satouh, Y., Miyata, H., Isotani, A. and Ikawa, M. 2013, Generation of mutant mice by pronuclear injection of circular plasmid expressing Cas9 and single guided RNA. Sci. Rep., 3, 3355.
41. Hockemeyer, D., Soldner, F., Beard, C., et al. 2009, Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat. Biotechnol., 27, 851-7.
42. Kim, H., Um, E., Cho, S.-R., Jung, C., Kim, H. and Kim, J.-S. 2011, Surrogate reporters for enrichment of cells with nuclease-induced mutations. Nat. Methods, 8, 941-3.
43. Orlando, S. J., Santiago, Y., DeKelver, R. C., et al. 2010, Zinc-finger nuclease-driven targeted integration into mammalian genomes using donors with limited chromosomal homology. Nucleic Acids Res., 38, e152.
44. Cristea, S., Freyvert, Y., Santiago, Y., et al. 2013, In vivo cleavage of transgene donors promotes nuclease-mediated targeted integration. Biotechnol. Bioeng., 110, 871-80.
45. Bachu, R., Bergareche, I. and Chasin, L. A. 2015, CRISPR-Cas targeted plasmid integration into mammalian cells via non-homologous end joining. Biotechnol. Bioeng 112, 2154-62.
46. Lackner, D. H., Carré, A., Guzzardo, P. M., et al. 2015, A generic strategy for CRISPR-Cas9-mediated gene tagging. Nat. Commun., 6, 10237.
47. Ma, H., Naseri, A., Reyes-Gutierrez, P., Wolfe, S. A., Zhang, S. and Pederson, T. 2015, Multicolor CRISPR labeling of chromosomal loci in human cells. Proc. Natl. Acad. Sci. USA, 112, 3002-7.
48. Tóth, E., Huszár, K., Bencsura, P., et al. 2014, Restriction enzyme body doubles and PCR cloning: on the general use of type IIs restriction enzymes for cloning. PloS One, 9, e90896.
49. Stewart, S. A., Dykxhoorn, D. M., Palliser, D., et al. 2003, Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA, 9, 493-501.
50. Iwamoto, M., Björklund, T., Lundberg, C., Kirik, D. and Wandless, T. J. 2010, A general chemical method to regulate protein stability in the mammalian central nervous system. Chem. Biol., 17, 981-8.
51. Perez-Pinera, P., Ousterout, D. G., Brown, M. T. and Gersbach, C. A. 2012, Gene targeting to the ROSA26 locus directed by engineered zinc finger nucleases. Nucleic Acids Res., 40, 3741-52.
52. Maresca, M., Lin, V. G., Guo, N. and Yang, Y. 2013, Obligate ligation-gated recombination (ObLiGaRe): custom-designed nuclease-mediated targeted integration through nonhomologous end joining. Genome Res., 23, 539-46.
53. Heigwer, F., Kerr, G. and Boutros, M. 2014, E-CRISP: fast CRISPR target site identification. Nat. Methods, 11, 122-3.
54. Aach, J., Mali, P. and Church, G. M. 2014, CasFinder: Flexible algorithm for identifying specific Cas9 targets in genomes. bioRxiv, 005074.
55. Xue, W., Chen, S., Yin, H., et al. 2014, CRISPR-mediated direct mutation of cancer genes in the mouse liver. Nature 514, 380-4.
56. Fujii, W., Kawasaki, K., Sugiura, K. and Naito, K. 2013, Efficient generation of large-scale genome-modified mice using gRNA and CAS9 endonuclease. Nucleic Acids Res., 41, e187.
57. Pinder, J., Salsman, J. and Dellaire, G. 2015, Nuclear domain 'knockin'screen for the evaluation and identification of small molecule enhancers of CRISPR-based genome editing. Nucleic Acids Res., 43, 9379-92.
58. Li, K., Wang, G., Andersen, T., Zhou, P. and Pu, W. T. 2014, Optimization of genome engineering approaches with the CRISPR/Cas9 system. Plos One., 9, e105779.
59. Geisinger, J. M., Turan, S., Hernandez, S., Spector, L. P. and Calos, M. P. 2016, In vivo blunt-end cloning through CRISPR/Cas9-facilitated non-homologous end-joining. Nucleic Acids Res., 44, e76-e76.
60. Slaymaker, I. M., Gao, L., Zetsche, B., Scott, D. A., Yan, W. X. and Zhang, F. 2016, Rationally engineered Cas9 nucleases with improved specificity. Science, 351, 84-8.
61. Kleinstiver, B. P., Pattanayak, V., Prew, M. S., et al. 2016, High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529, 490-5.
62. Mladenov, E. and Iliakis, G. 2011, Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways. Mutat. Res., 711, 61-72.
63. Bae, S., Kweon, J., Kim, H. S. and Kim, J.-S. 2014, Microhomology-based choice of Cas9 nuclease target sites. Nat. Methods, 11, 705-6.
64. McVey, M. and Lee, S. E. 2008, MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet., 24, 529-38.
65. Vouillot, L., Thélie, A. and Pollet, N. 2015, Comparison of T7E1 and surveyor mismatch cleavage assays to detect mutations triggered by engineered nucleases. G3, 5, 407-15.
66. Huang, Y., Zhao, S., Shi, M., Liu, J. and Liang, H. 2012, Microchip electrophoresis coupled with on-line magnetic separation and chemiluminescence detection for multiplexed immunoassay. Electrophoresis, 33, 1198-204.
67. Sakuma, T. 2015, Front-line of genome editing technology for animal cell engineering. BMC Proceed., 9, O1.
68. Liu, J., Gong, L., Chang, C., Liu, C., Peng, J. and Chen, J. 2012, Development of novel visual-plus quantitative analysis systems for studying DNA double-strand break repairs in zebrafish. J. Genet. Genomics, 39, 489-502.
69. Dai, J., Cui, X., Zhu, Z. and Hu, W. 2010, Non-homologous end joining plays a key role in transgene concatemer formation in transgenic zebrafish embryos. Int. J. Biol. Sci., 6, 756.
70. Hagmann, M., Bruggmann, R., Xue, L., et al. 1998, Homologous recombination and DNA-end joining reactions in zygotes and early embryos of zebrafish (Danio rerio) and Drosophila melanogaster. Biol. Chem., 379, 673-82.
71. Suzuki, K., Tsunekawa, Y., Hernandez-Benitez, R., et al. 2016, In vivo genome editing via CRISPR/Cas9 mediated homology-independent targeted integration. Nature, 540, 144-9.
72. Nakade, S., Tsubota, T., Sakane, Y., et al. 2014, Microhomology-mediated end-joining-dependent integration of donor DNA in cells and animals using TALENs and CRISPR/Cas9. Nat. Commun., 5, 5560.
73. Schmid-Burgk, J. L., Höning, K., Ebert, T. S. and Hornung, V. 2016, CRISPaint allows modular base-specific gene tagging using a ligase-4- dependent mechanism. Nat. Commun., 7, 12338