Highly efficient mouse genome editing by CRISPR ribonucleoprotein electroporation of zygotes

Journal of Biological Chemistry

Volumn 291, Issue 28, 2016, Pages 14457-14467

  Chen, Sean ^a   Lee, Benjamin ^a   Lee, Angus Yiu Fai ^a   Modzelewski, Andrew J ^a   He, Lin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMMINUTION; GENES; THROUGHPUT;

ELECTROPORATION; HIGH THROUGHPUT; LABOR INTENSIVE; MICRO-INJECTION; MODEL ORGANISMS; PROOF-OF-PRINCIPLE EXPERIMENTS; RIBONUCLEOPROTEINS; SEQUENCE MODIFICATION;

MAMMALS;

CRISPR ASSOCIATED PROTEIN; MESSENGER RNA; MONOPHENOL MONOOXYGENASE; RIBONUCLEOPROTEIN; GUIDE RNA;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; FEMALE; GENE DELETION; GENE EXPRESSION; GENE TARGETING; GENOME ANALYSIS; GENOTYPE; INDEL MUTATION; MALE; MOUSE; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SURVIVAL RATE; TYR GENE; ZYGOTE; ANIMAL; C57BL MOUSE; CELL LINE; CRISPR CAS SYSTEM; GENE EDITING; GENE INACTIVATION; GENETICS; METABOLISM; MUTATION; PROCEDURES;

ANIMALS; CELL LINE; CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; ELECTROPORATION; FEMALE; GENE EDITING; GENE KNOCKOUT TECHNIQUES; MALE; MICE; MICE, INBRED C57BL; MUTATION; RIBONUCLEOPROTEINS; RNA, GUIDE; ZYGOTE;

EID: 84978967275     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.733154     Document Type: Article

References (49)

1. Martin, G. R. (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. U.S.A. 78, 7634-7638
2. Evans, M. J., and Kaufman, M. H. (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156
3. Thomas, K. R., and Capecchi, M. R. (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51, 503-512
4. Doetschman, T., Gregg, R. G., Maeda, N., Hooper, M. L., Melton, D. W., Thompson, S., and Smithies, O. (1987) Targetted correction of a mutant HPRT gene in mouse embryonic stem cells. Nature 330, 576-578
5. Mansour, S. L., Thomas, K. R., and Capecchi, M. R. (1988) Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to non-selectable genes. Nature 336, 348-352
6. Zijlstra, M., Li, E., Sajjadi, F., Subramani, S., and Jaenisch, R. (1989) Germline transmission of a disrupted β2-microglobulin gene produced by homologous recombination in embryonic stem cells. Nature 342, 435-438
7. Capecchi, M. R. (2005) Gene targeting in mice: functional analysis of the mammalian genome for the twenty-first century. Nat. Rev. Genet. 6, 507-512
8. Bibikova, M., Golic, M., Golic, K. G., and Carroll, D. (2002) Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161, 1169-1175
9. Bibikova, M., Beumer, K., Trautman, J. K., and Carroll, D. (2003) Enhancing gene targeting with designed zinc finger nucleases. Science 300, 764
10. Urnov, F. D., Miller, J. C., Lee, Y.-L., Beausejour, C. M., Rock, J. M., Augustus, S., Jamieson, A. C., Porteus, M. H., Gregory, P. D., and Holmes, M. C. (2005) Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435, 646-651
11. Meyer, M., de Angelis, M. H., Wurst, W., and Kühn, R. (2010) Gene targeting by homologous recombination in mouse zygotes mediated by zincfinger nucleases. Proc. Natl. Acad. Sci. U.S.A. 107, 15022-15026
12. Carroll, D. (2011) Genome engineering with zinc-finger nucleases. Genetics 188, 773-782
13. Carbery, I. D., Ji, D., Harrington, A., Brown, V., Weinstein, E. J., Liaw, L., and Cui, X. (2010) Targeted genome modification in mice using zincfinger nucleases. Genetics 186, 451-459
14. Sung, Y. H., Baek, I.-J., Kim, D. H., Jeon, J., Lee, J., Lee, K., Jeong, D., Kim, J.-S., and Lee, H.-W. (2013) Knockout mice created by TALEN-mediated gene targeting. Nat. Biotechnol. 31, 23-24
15. Wang, H., Yang, H., Shivalila, C. S., Dawlaty, M. M., Cheng, A. W., Zhang, F., and Jaenisch, R. (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/cas-mediated genome engineering. Cell 153, 910-918
16. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D. A., and Horvath, P. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709-1712
17. Brouns, S. J., Jore, M. M., Lundgren, M., Westra, E. R., Slijkhuis, R. J., Snijders, A. P., Dickman, M. J., Makarova, K. S., Koonin, E. V., and van der Oost, J. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321, 960-964
18. 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, 816-821
19. Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., and Zhang, F. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823
20. Jinek, M., East, A., Cheng, A., Lin, S., Ma, E., and Doudna, J. (2013) RNAprogrammed genome editing in human cells. Elife 2, e00471
21. Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E., and Church, G. M. (2013) RNA-guided human genome engineering via Cas9. Science 339, 823-826
22. Platt, R. J., Chen, S., Zhou, Y., Yim, M. J., Swiech, L., Kempton, H. R., Dahlman, J. E., Parnas, O., Eisenhaure, T. M., Jovanovic, M., Graham, D. B., Jhunjhunwala, S., Heidenreich, M., Xavier, R. J., Langer, R., et al. (2014) CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell 159, 440-455
23. Wang, B., Li, K., Wang, A., Reiser, M., Saunders, T., Lockey, R. F., and Wang, J.-W. (2015) Highly efficient CRISPR/HDR-mediated knock-in for mouse embryonic stem cells and zygotes. BioTechniques 59, 201-202
24. Mizuno, S., Dinh, T. T., Kato, K., Mizuno-Iijima, S., Tanimoto, Y., Daitoku, Y., Hoshino, Y., Ikawa, M., Takahashi, S., Sugiyama, F., and Yagami, K. (2014) Simple generation of albino C57BL/6J mice with G291T mutation in the tyrosinase gene by the CRISPR/Cas9 system. Mamm. Genome 25, 327-334
25. Zhu, W., Xie, K., Xu, Y., Wang, L., Chen, K., Zhang, L., and Fang, J. (2016) CRISPR/Cas9 produces anti-hepatitis B virus effect in hepatoma cells and transgenic mouse. Virus Res. 217, 125-132
26. Nelson, C. E., Hakim, C. H., Ousterout, D. G., Thakore, P. I., Moreb, E. A., Castellanos Rivera, R. M., Madhavan, S., Pan, X., Ran, F. A., Yan, W. X., Asokan, A., Zhang, F., Duan, D., and Gersbach, C. A. (2016) In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351, 403-407
27. Blasco, R. B., Karaca, E., Ambrogio, C., Cheong, T.-C., Karayol, E., Minero, V. G., Voena, C., and Chiarle, R. (2014) Simple and rapid in vivo generation of chromosomal rearrangements using CRISPR/Cas9 technology. Cell Rep. 9, 1219-1227
28. Yang, H., Wang, H., Shivalila, C. S., Cheng, A. W., Shi, L., and Jaenisch, R. (2013) One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154, 1370-1379
29. Brinster, R. L., Chen, H. Y., Trumbauer, M. E., Yagle, M. K., and Palmiter, R. D. (1985) Factors affecting the efficiency of introducing foreign DNA into mice by microinjecting eggs. Proc. Natl. Acad. Sci. U.S.A. 82, 4438-4442
30. Qin, W., Dion, S. L., Kutny, P. M., Zhang, Y., Cheng, A. W., Jillette, N. L., Malhotra, A., Geurts, A. M., Chen, Y.-G., and Wang, H. (2015) Efficient CRISPR/Cas9-mediated genome editing in mice by zygote electroporation of nuclease. Genetics 200, 423-430
31. Takahashi, G., Gurumurthy, C. B., Wada, K., Miura, H., Sato, M., and Ohtsuka, M. (2015) GONAD: genome-editing via oviductal nucleic acids delivery system: a novel microinjection independent genome engineering method in mice. Sci. Rep. 5, 11406
32. Hashimoto, M., and Takemoto, T. (2015) Electroporation enables the efficient mRNA delivery into the mouse zygotes and facilitates CRISPR/Cas9-based genome editing. Sci. Rep. 5, 11315
33. Gasiunas, G., Barrangou, R., Horvath, P., and Siksnys, V. (2012) Cas9- crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc. Natl. Acad. Sci. U.S.A. 109, E2579-E2586
34. Nishimasu, H., Ran, F. A., Hsu, P. D., Konermann, S., Shehata, S. I., Dohmae, N., Ishitani, R., Zhang, F., and Nureki, O. (2014) Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell 156, 935-949
35. Jinek, M., Jiang, F., Taylor, D. W., Sternberg, S. H., Kaya, E., Ma, E., Anders, C., Hauer, M., Zhou, K., Lin, S., Kaplan, M., Iavarone, A. T., Charpentier, E., Nogales, E., and Doudna, J. A. (2014) Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science 343, 1247997
36. Cho, S. W., Lee, J., Carroll, D., Kim, J.-S., and Lee, J. (2013) Heritable gene knockout in Caenorhabditis elegans by direct injection of Cas9-sgRNA ribonucleoproteins. Genetics 195, 1177-1180 (2013)
37. Lin, S., Staahl, B. T., Alla, R. K., and Doudna, J. A. (2014) Enhanced homology- directed human genome engineering by controlled timing of CRISPR/Cas9 delivery. Elife 3, e04766
38. Gratz, S. J., Cummings, A. M., Nguyen, J. N., Hamm, D. C., Donohue, L. K., Harrison, M. M., Wildonger, J., and O'Connor-Giles, K. M. (2013) Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics 194, 1029-1035
39. Sung, Y. H., Kim, J. M., Kim, H.-T., Lee, J., Jeon, J., Jin, Y., Choi, J.-H., Ban, Y. H., Ha, S.-J., Kim, C.-H., Lee, H.-W., and Kim, J.-S. (2014) Highly efficient gene knockout in mice and zebrafish with RNA-guided endonucleases. Genome Res. 24, 125-131
40. Xu, H., Xiao, T., Chen, C.-H., Li, W., Meyer, C. A., Wu, Q., Wu, D., Cong, L., Zhang, F., Liu, J. S., Brown, M., and Liu, X. S. (2015) Sequence determinants of improved CRISPR sgRNA design. Genome Res. 25, 1147-1157
41. Doench, J. G., Fusi, N., Sullender, M., Hegde, M., Vaimberg, E. W., Donovan, K. F., Smith, I., Tothova, Z., Wilen, C., Orchard, R., Virgin, H. W., Listgarten, J., and Root, D. E. (2016) Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9. Nat. Biotechnol. 34, 184-191
42. Montague, T. G., Cruz, J. M., Gagnon, J. A., Church, G. M., and Valen, E. (2014) CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res. 42, W401-W407
43. Hsu, P. D., Scott, D. A., Weinstein, J. A., Ran, F. A., Konermann, S., Agarwala, V., Li, Y., Fine, E. J., Wu, X., Shalem, O., Cradick, T. J., Marraffini, L. A., Bao, G., and Zhang, F. (2013) DNA targeting specificity of RNAguided Cas9 nucleases. Nat. Biotechnol. 31, 827-832
44. Qiu, P., Shandilya, H., D'Alessio, J. M., O'Connor, K., Durocher, J., and Gerard, G. F. (2004) Mutation detection using Surveyor nuclease. Bio- Techniques 36, 702-707
45. Chen, B., Gilbert, L. A., Cimini, B. A., Schnitzbauer, J., Zhang, W., Li, G.-W., Park, J., Blackburn, E. H., Weissman, J. S., Qi, L. S., and Huang, B. (2013) Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155, 1479-1491
46. Rohland, N., and Reich, D. (2012) Cost-effective, high throughput DNA sequencing libraries for multiplexed target capture. Genome Res. 22, 939-946
47. Basrur, V., Yang, F., Kushimoto, T., Higashimoto, Y., Yasumoto, K., Valencia, J., Muller, J., Vieira, W. D., Watabe, H., Shabanowitz, J., Hearing, V. J., Hunt, D. F., and Appella, E. (2003) Proteomic analysis of early melanosomes: identification of novel melanosomal proteins. J. Proteome Res. 2, 69-79
48. Paterson, E. K., Fielder, T. J., MacGregor, G. R., Ito, S., Wakamatsu, K., Gillen, D. L., Eby, V., Boissy, R. E., and Ganesan, A. K. (2015) Tyrosinase depletion prevents the maturation of melanosomes in the mouse hair Follicle. PLoS ONE 10, e0143702
49. Wang, W., Kutny, P. M., Byers, S. L., Longstaff, C. J., DaCosta, M. J., Pang, C., Zhang, Y., Taft, R. A., Buaas, F. W., and Wang, H. (2016) Delivery of Cas9 protein into mouse zygotes through a series of electroporation dramatically increased the efficiency of model creation. J. Genet. Genomics 10.1016/j.jgg.2016.02.004