Performance of the Cas9 nickase system in Drosophila melanogaster

G3: Genes, Genomes, Genetics

Volumn 4, Issue 10, 2014, Pages 1955-1962

  Ren, Xingjie ^a   Yang, Zhihao ^a   Mao, Decai ^a   Chang, Zai ^b   Qiao, Huan Huan ^a   Wang, Xia ^a   Sun, Jin ^a   Hu, Qun ^b   Cui, Yan ^a   Liu, Lu Ping ^a,b   Ji, Jun Yuan ^c   Xu, Jiang ^a,d,e   Ni, Jian Quan ^a  

^a Tsinghua University   (China)

^b TSINGHUA UNIVERSITY   (China)

^c TEXAS A M COLLEGE OF MEDICINE   (United States)

^d WUHAN UNIVERSITY   (China)

^e HUBEI UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Cas9; CRISPR; Nickase; Off target; Piwi

Indexed keywords

CAS9 NICKASE; DNA NICKASE; ENZYME; PROTEIN CAS9; RNA; UNCLASSIFIED DRUG; ARGONAUTE PROTEIN; DEOXYRIBONUCLEASE I; DROSOPHILA PROTEIN; GUIDE RNA; PIWI PROTEIN, DROSOPHILA;

ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA REPAIR; DROSOPHILA MELANOGASTER; EMBRYO; GENE; GENE EXPRESSION; GENE SEQUENCE; GENOME; HOMOLOGY DIRECTED REPAIR; IN VITRO STUDY; INDEL MUTATION; NONHUMAN; PHENOTYPE; PIWI GENE; PLASMID; SITE DIRECTED MUTAGENESIS; ANIMAL; ANIMAL EMBRYO; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; ENZYMOLOGY; GENE VECTOR; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTAGENESIS; TRANSGENIC ANIMAL;

DROSOPHILA MELANOGASTER;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ARGONAUTE PROTEINS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; DEOXYRIBONUCLEASE I; DNA REPAIR; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GENETIC VECTORS; MUTAGENESIS; RNA, GUIDE;

EID: 84908403463     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.114.013821     Document Type: Article

References (51)

1. Aravin, A., D. Gaidatzis, S. Pfeffer, M. Lagos-Quintana, P. Landgraf et al., 2006 A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442: 203-207.
2. Baena-Lopez, L. A., C. Alexandre, A. Mitchell, L. Pasakarnis, and J. P. Vincent, 2013 Accelerated homologous recombination and subsequent genome modification in Drosophila. Development 140: 4818-4825.
3. Bassett, A. R., C. Tibbit, C. P. Ponting, and J. L. Liu, 2013 Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Reports 4: 220-228.
4. Bhaya, D., M. Davison, and R. Barrangou, 2011 CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 45: 273-297.
5. Certo, M. T., B. Y. Ryu, J. E. Annis, M. Garibov, J. Jarjour et al., 2011 Tracking genome engineering outcome at individual DNA breakpoints. Nat. Methods 8: 671-676.
6. Chan, S. H., B. L. Stoddard, and S. Y. Xu, 2011 Natural and engineered nicking endonucleases-from cleavage mechanism to engineering of strand-specificity. Nucleic Acids Res. 39: 1-18.
7. Cho, S. W., S. Kim, Y. Kim, J. Kweon, H. S. Kim et al., 2014 Analysis of offtarget effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res. 24: 132-141.
8. 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.
9. Cox, D. N., A. Chao, J. Baker, L. Chang, D. Qiao et al., 1998 A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 12: 3715-3727.
10. Davis, L., and N. Maizels, 2011 DNA nicks promote efficient and safe targeted gene correction. PLoS ONE 6: e23981.
11. Deltcheva, E., K. Chylinski, C. M. Sharma, K. Gonzales, Y. Chao et al., 2011 CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471: 602-607.
12. Deveau, H., J. E. Garneau, and S. Moineau, 2010 CRISPR/Cas system and its role in phage-bacteria interactions. Annu. Rev. Microbiol. 64: 475-493.
13. Fu, Y., J. A. Foden, C. Khayter, M. L. Maeder, D. Reyon et al., 2013 Highfrequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31: 822-826.
14. Gabsalilow, L., B. Schierling, P. Friedhoff, A. Pingoud, and W. Wende, 2013 Site- and strand-specific nicking of DNA by fusion proteins derived from MutH and I-SceI or TALE repeats. Nucleic Acids Res. 41: e83.
15. 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.
16. Girard, A., R. Sachidanandam, G. J. Hannon, and M. A. Carmell, 2006 A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442: 199-202.
17. Gratz, S. J., A. M. Cummings, J. N. Nguyen, D. C. Hamm, L. K. Donohue et al., 2013 Genome engineering of Drosophila with the CRISPR RNAguided Cas9 nuclease. Genetics 194: 1029-1035.
18. Gratz, S. J., F. P. Ukken, C. D. Rubinstein, G. Thiede, L. K. Donohue et al., 2014 Highly specific and efficient CRISPR/Cas9-catalyzed homologydirected repair in Drosophila. Genetics 196: 961-971.
19. Grivna, S. T., E. Beyret, Z. Wang, and H. Lin, 2006 A novel class of small RNAs in mouse spermatogenic cells. Genes Dev. 20: 1709-1714.
20. Horn, C., B. Jaunich, and E. A. Wimmer, 2000 Highly sensitive, fluorescent transformation marker for Drosophila transgenesis. Dev. Genes Evol. 210: 623-629.
21. Hsu, P. D., D. A. Scott, J. A. Weinstein, F. A. Ran, S. Konermann et al., 2013 DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31: 827-832.
22. Jin, Z., A. S. Flynt, and E. C. Lai, 2013 Drosophila piwi mutants exhibit germline stem cell tumors that are sustained by elevated Dpp signaling. Curr. Biol. 23: 1442-1448.
23. Jinek, M., F. Jiang, D. W. Taylor, S. H. Sternberg, E. Kaya et al., 2014 Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science 343: 1247997.
24. 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.
25. Katz, S. S., F. S. Gimble, and F. Storici, 2014 To nick or not to nick: Comparison of I-SceI single- and double-strand break-induced recombination in yeast and human cells. PLoS ONE 9: e88840.
26. Kim, E., S. Kim, D. H. Kim, B. S. Choi, I. Y. Choi et al., 2012 Precision genome engineering with programmable DNA-nicking enzymes. Genome Res. 22: 1327-1333.
27. Kondo, S., and R. Ueda, 2013 Highly improved gene targeting by germlinespecific cas9 expression in Drosophila. Genetics 195: 715-721.
28. Lau, N. C., A. G. Seto, J. Kim, S. Kuramochi-Miyagawa, T. Nakano et al., 2006 Characterization of the piRNA complex from rat testes. Science 313: 363-367.
29. Lin, H., and A. C. Spradling, 1997 A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124: 2463-2476.
30. Ma, X., S. Wang, T. Do, X. Song, M. Inaba et al., 2014 Piwi is required in multiple cell types to control germline stem cell lineage development in the Drosophila ovary. PLoS ONE 9: e90267.
31. Mali, P., J. Aach, P. B. Stranges, K. M. Esvelt, M. Moosburner et al., 2013a CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31: 833-838.
32. Mali, P., L. Yang, K. M. Esvelt, J. Aach, M. Guell et al., 2013b RNA-guided human genome engineering via Cas9. Science 339: 823-826.
33. Malone, C. D., J. Brennecke, M. Dus, A. Stark, W. R. McCombie et al., 2009 Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137: 522-535.
34. McConnell, S. A., R. Takeuchi, S. Pellenz, L. Davis, N. Maizels et al., 2009 Generation of a nicking enzyme that stimulates site-specific gene conversion from the I-AniI LAGLIDADG homing endonuclease. Proc. Natl. Acad. Sci. USA 106: 5099-5104.
35. Megosh, H. B., D. N. Cox, C. Campbell, and H. Lin, 2006 The role of PIWI and the miRNA machinery in Drosophila germline determination. Curr. Biol. 16: 1884-1894.
36. Metzger, M. J., A. McConnell-Smith, B. L. Stoddard, and A. D. Miller, 2011 Single-strand nicks induce homologous recombination with less toxicity than double-strand breaks using an AAV vector template. Nucleic Acids Res. 39: 926-935.
37. Ni, J. Q., M. Markstein, R. Binari, B. Pfeiffer, L. P. Liu et al., 2008 Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster. Nat. Methods 5: 49-51.
38. Nishimasu, H., F. A. Ran, P. D. Hsu, S. Konermann, S. I. Shehata et al., 2014 Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell 156: 935-949.
39. Port, F., H. M. Chen, T. Lee, and S. L. Bullock, 2014 Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. Proc. Natl. Acad. Sci. USA 111: E2967-E2976.
40. Ramirez, C. L., M. T. Certo, C. Mussolino, M. J. Goodwin, T. J. Cradick et al., 2012 Engineered zinc finger nickases induce homology-directed repair with reduced mutagenic effects. Nucleic Acids Res. 40: 5560-5568.
41. Ran, F. A., P. D. Hsu, C. Y. Lin, J. S. Gootenberg, S. Konermann et al., 2013 Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154: 1380-1389.
42. Ren, X., J. Sun, B. E. Housden, Y. Hu, C. Roesel et al., 2013 Optimized gene editing technology for Drosophila melanogaster using germ line-specific Cas9. Proc. Natl. Acad. Sci. USA 110: 19012-19017.
43. Sebo, Z. L., H. B. Lee, Y. Peng, and Y. Guo, 2013 A simplified and efficient germline-specific CRISPR/Cas9 system for Drosophila genomic engineering. Fly (Austin) 8: 52-57.
44. Szakmary, A., D. N. Cox, Z. Wang, and H. Lin, 2005 Regulatory relationship among piwi, pumilio, and bag-of-marbles in Drosophila germline stem cell self-renewal and differentiation. Curr. Biol. 15: 171-178.
45. Terns, M. P., and R. M. Terns, 2011 CRISPR-based adaptive immune systems. Curr. Opin. Microbiol. 14: 321-327.
46. van Nierop, G. P., A. A. de Vries, M. Holkers, K. R. Vrijsen, and M. A. Goncalves, 2009 Stimulation of homology-directed gene targeting at an endogenous human locus by a nicking endonuclease. Nucleic Acids Res. 37: 5725-5736.
47. Wiedenheft, B., S. H. Sternberg, and J. A. Doudna, 2012 RNA-guided genetic silencing systems in bacteria and archaea. Nature 482: 331-338.
48. Xu, S. Y., and Y. K. Gupta, 2013 Natural zinc ribbon HNH endonucleases and engineered zinc finger nicking endonuclease. Nucleic Acids Res. 41: 378-390.
49. Xue, Z., M. Ren, M. Wu, J. Dai, Y. S. Rong et al., 2014 Efficient gene knockout and knock-in with transgenic Cas9 in Drosophila. G3 (Bethesda) 4: 925-929.
50. Yu, Z., H. Chen, J. Liu, H. Zhang, Y. Yan et al., 2014 Various applications of TALEN- and CRISPR/Cas9-mediated homologous recombination to modify the Drosophila genome. Biol. Open 3: 271-280.
51. Yu, Z., M. Ren, Z. Wang, B. Zhang, Y. S. Rong et al., 2013 Highly efficient genome modifications mediated by CRISPR/Cas9 in Drosophila. Genetics 195: 289-291.