Dramatic enhancement of genome editing by CRISPR/cas9 through improved guide RNA design

Genetics

Volumn 199, Issue 4, 2015, Pages 959-971

  Farboud, Behnom ^a   Meyer, Barbara J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

C. elegans; Cas9; Co conversion; CRISPR; Genome editing

Indexed keywords

CAS9 PROTEIN; GUIDE RNA; NUCLEASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA INTEGRATION; DNA TEMPLATE; EMBRYO; GENOME; IN VIVO STUDY; MUTAGENESIS; MUTANT; NONHUMAN; NUCLEOTIDE MOTIF; PHENOTYPE; PRIORITY JOURNAL; RNA EDITING; SEQUENCE ANALYSIS; ANIMAL; CHEMISTRY; CRISPR CAS SYSTEM; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

ANIMALIA; CAENORHABDITIS ELEGANS;

ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CRISPR-CAS SYSTEMS; GENOME, HELMINTH; MOLECULAR SEQUENCE DATA; RNA EDITING; RNA, GUIDE;

EID: 84926433352     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.115.175166     Document Type: Article

References (47)

1. Anders, C., O. Niewoehner, A. Duerst, and M. Jinek, 2014 Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513: 569–573
2. Arribere, J. A., R. T. Bell, B. X. Fu, K. L. Artiles, P. S. Hartman et al., 2014 Efficient marker-free recovery of custom genetic modifications with CRISPR/Cas9 in Caenorhabditis elegans. Genetics 198: 837–846
3. Bikard, D., W. Jiang, P. Samai, A. Hochschild, F. Zhang et al., 2013 Programmable repression and activation of bacterial gene expression using an engineered CRISPR-Cas system. Nucleic Acids Res. 41: 7429–7437
4. Brenner, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71–94
5. Carroll, D., 2014 Genome engineering with targetable nucleases. Annu. Rev. Biochem. 83: 409–439
6. Chen, B., L. A. Gilbert, B. A. Cimini, J. Schnitzbauer, W. Zhang et al., 2013 Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155: 1479–1491
7. Chen, X., F. Xu, C. Zhu, J. Ji, X. Zhou et al., 2014 Dual sgRNAdirected gene knockout using CRISPR/Cas9 technology in Caenorhabditis elegans. Sci. Rep. 4: 7581
8. Chiu, H., H. T. Schwartz, I. Antoshechkin, and P. W. Sternberg, 2013 Transgene-free genome editing in Caenorhabditis elegans using CRISPR-Cas. Genetics 195: 1167–1171
9. Cho, S. W., J. Lee, D. Carroll, J. S. Kim, and J. Lee, 2013 Heritable gene knockout in Caenorhabditis elegans by direct injection of Cas9-sgRNA ribonucleoproteins. Genetics 195: 1177–1180
10. Cong, L., F. A. Ran, D. Cox, S. Lin, R. Barretto et al., 2013 Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819–823
11. Dickinson, D. J., J. D. Ward, D. J. Reiner, and B. Goldstein, 2013 Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat. Methods 10: 1028–1034
12. Doench, J. G., E. Hartenian, D. B. Graham, Z. Tothova, M. Hegde et al., 2014 Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat. Biotechnol. 32: 1262–1267
13. Doudna, J. A., and E. Charpentier, 2014 Genome editing. The new frontier of genome engineering with CRISPR-Cas9 Science 346: 1258096
14. Friedland, A. E., Y. B. Tzur, K. M. Esvelt, M. P. Colaiacovo, G. M. Church et al., 2013 Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat. Methods 10: 741–743
15. Gagnon, J. A., E. Valen, S. B. Thyme, P. Huang, L. Ahkmetova et al., 2014 Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs. PLoS ONE 9: e98186
16. Garneau, J. E., M. E. Dupuis, M. Villion, D. A. Romero, R. Barrangou et al., 2010 The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468: 67–71
17. Gasiunas, G., R. Barrangou, P. Horvath, and V. Siksnys, 2012 Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc. Natl. Acad. Sci. USA 109: E2579–E2586
18. Gibson, D. G., 2011 Enzymatic assembly of overlapping DNA fragments. Methods Enzymol. 498: 349–361
19. Gilbert, L. A., M. A. Horlbeck, B. Adamson, J. E. Villalta, Y. Chen et al., 2014 Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159: 647–661
20. Hsu, P. D., E. S. Lander, and F. Zhang, 2014 Development and applications of CRISPR-Cas9 for genome engineering. Cell 157: 1262–1278
21. Jinek, M., K. Chylinski, I. Fonfara, M. Hauer, J. A. Doudna et al., 2012 A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816–821
22. Jinek, M., A. East, A. Cheng, S. Lin, E. Ma et al., 2013 RNAprogrammed genome editing in human cells. elife 2: e00471
23. Katic, I., and H. Grosshans, 2013 Targeted heritable mutation and gene conversion by Cas9-CRISPR in Caenorhabditis elegans. Genetics 195: 1173–1176
24. Kim, H., T. Ishidate, K. S. Ghanta, M. Seth, D. Conte, Jr. et al., 2014 A co-CRISPR strategy for efficient genome editing in Caenorhabditis elegans. Genetics 197: 1069–1080
25. Larson, M. H., L. A. Gilbert, X. Wang, W. A. Lim, J. S. Weissman et al., 2013 CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat. Protoc. 8: 2180–2196
26. Liu, P., L. Long, K. Xiong, B. Yu, N. Chang et al., 2014 Heritable/ conditional genome editing in C. elegans using a CRISPR-Cas9 feeding system. Cell Res. 24: 886–889
27. Lo, T. W., C. S. Pickle, S. Lin, E. J. Ralston, M. Gurling et al., 2013 Precise and heritable genome editing in evolutionarily diverse nematodes using TALENs and CRISPR/Cas9 to engineer insertions and deletions. Genetics 195: 331–348
28. Maeder, M. L., S. J. Linder, V. M. Cascio, Y. Fu, Q. H. Ho et al., 2013 CRISPR RNA-guided activation of endogenous human genes. Nat. Methods 10: 977–979
29. Mali, P., K. M. Esvelt, and G. M. Church, 2013 Cas9 as a versatile tool for engineering biology. Nat. Methods 10: 957–963
30. Mello, C., and A. Fire, 1995 DNA transformation. Methods Cell Biol. 48: 451–482
31. Mojica, F. J., C. Diez-Villasenor, J. Garcia-Martinez, and C. Almendros, 2009 Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155: 733–740
32. Paix, A., Y. Wang, H. E. Smith, C. Y. Lee, D. Calidas et al., 2014 Scalable and versatile genome editing using linear DNAs with microhomology to Cas9 sites in Caenorhabditis elegans. Genetics 198: 1347–1356
33. Perez-Pinera, P., D. D. Kocak, C. M. Vockley, A. F. Adler, A. M. Kabadi et al., 2013 RNA-guided gene activation by CRISPRCas9- based transcription factors. Nat. Methods 10: 973–976
34. Qi, L. S., M. H. Larson, L. A. Gilbert, J. A. Doudna, J. S. Weissman et al., 2013 Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152: 1173–1183
35. Ren, X., Z. Yang, J. Xu, J. Sun, D. Mao et al., 2014 Enhanced specificity and efficiency of the CRISPR/Cas9 system with optimized sgRNA parameters in Drosophila. Cell Reports 9: 1151–1162
36. Rosenbluth, R. E., C. Cuddeford, and D. L. Baillie, 1985 Mutagenesis in Caenorhabditis elegans. II. A spectrum of mutational events induced with 1500 r of gamma-radiation. Genetics 109: 493–511
37. Sapranauskas, R., G. Gasiunas, C. Fremaux, R. Barrangou, P. Horvath et al., 2011 The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res. 39: 9275–9282
38. Shen, Z., X. Zhang, Y. Chai, Z. Zhu, P. Yi et al., 2014 Conditional knockouts generated by engineered CRISPR-Cas9 endonuclease reveal the roles of coronin in C. elegans neural development. Dev. Cell 30: 625–636
39. Sternberg, S. H., S. Redding, M. Jinek, E. C. Greene, and J. A. Doudna, 2014 DNA interrogation by the CRISPR RNA-guided endonuclease Cas9 Nature 507: 62–67
40. Tanenbaum, M. E., L. A. Gilbert, L. S. Qi, J. S. Weissman, and R. D. Vale, 2014 A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159: 635–646
41. Tzur, Y. B., A. E. Friedland, S. Nadarajan, G. M. Church, J. A. Calarco et al., 2013 Heritable custom genomic modifications in Caenorhabditis elegans via a CRISPR-Cas9 system. Genetics 195: 1181–1185
42. Waaijers, S., and M. Boxem, 2014 Engineering the Caenorhabditis elegans genome with CRISPR/Cas9 Methods 68: 381–388
43. Waaijers, S., V. Portegijs, J. Kerver, B. B. Lemmens, M. Tijsterman et al., 2013 CRISPR/Cas9-targeted mutagenesis in Caenorhabditis elegans. Genetics 195: 1187–1191
44. Wang, T., J. J. Wei, D. M. Sabatini, and E. S. Lander, 2014 Genetic screens in human cells using the CRISPR-Cas9 system. Science 343: 80–84
45. Ward, J. D., 2014 Rapid and precise engineering of the Caenorhabditis elegans genome with lethal mutation co-conversion and inactivation of NHEJ repair. Genetics 199: 363–377
46. Wu, X., D. A. Scott, A. J. Kriz, A. C. Chiu, P. D. Hsu et al., 2014 Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat. Biotechnol. 32: 670–676
47. Zhao, P., Z. Zhang, H. Ke, Y. Yue, and D. Xue, 2014 Oligonucleotidebased targeted gene editing in C. elegans via the CRISPR/Cas9 system. Cell Res. 24: 247–250.