Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Concepts and tools for gene editing

Santiago Josa A B , Davide Seruggia A B C , Almudena Fernández A B and Lluis Montoliu A B D
+ Author Affiliations
- Author Affiliations

A Departamento de Biología Molecular y Celular, Centro Nacional de Biotecnología (CNB-CSIC), Darwin 3, 28049 Madrid, Spain.

B CIBERER, Instituto de Salud Carlos III, 28029 Madrid, Spain.

C Present address: Boston Children’s Hospital, Harvard Medical School, Dana-Farber Cancer Institute, Boston, MA 02215-5450 , USA.

D Corresponding author. Email: montoliu@cnb.csic.es

Reproduction, Fertility and Development 29(1) 1-7 https://doi.org/10.1071/RD16396
Published: 2 December 2016

Abstract

Gene editing is a relatively recent concept in the molecular biology field. Traditional genetic modifications in animals relied on a classical toolbox that, aside from some technical improvements and additions, remained unchanged for many years. Classical methods involved direct delivery of DNA sequences into embryos or the use of embryonic stem cells for those few species (mice and rats) where it was possible to establish them. For livestock, the advent of somatic cell nuclear transfer platforms provided alternative, but technically challenging, approaches for the genetic alteration of loci at will. However, the entire landscape changed with the appearance of different classes of genome editors, from initial zinc finger nucleases, to transcription activator-like effector nucleases and, most recently, with the development of clustered regularly interspaced short palindromic repeats (CRISPR) and CRISPR-associated proteins (Cas). Gene editing is currently achieved by CRISPR–Cas-mediated methods, and this technological advancement has boosted our capacity to generate almost any genetically altered animal that can be envisaged.

Additional keywords: genetically modified animals, genome-edited animals, knockin, knockout, transgenic animals.


References

Abudayyeh, O. O., Gootenberg, J. S., Konermann, S., Joung, J., Slaymaker, I. M., Cox, D. B., Shmakov, S., Makarova, K. S., Semenova, E., Minakhin, L., Severinov, K., Regev, A., Lander, E. S., Koonin, E. V., and Zhang, F. (2016). C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353, aaf5573.
C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector.CrossRef |

Basu, S., Aryan, A., Overcash, J. M., Samuel, G. H., Anderson, M. A., Dahlem, T. J., Myles, K. M., and Adelman, Z. N. (2015). Silencing of end-joining repair for efficient site-specific gene insertion after TALEN/CRISPR mutagenesis in Aedes aegypti. Proc. Natl Acad. Sci. USA 112, 4038–4043.
Silencing of end-joining repair for efficient site-specific gene insertion after TALEN/CRISPR mutagenesis in Aedes aegypti.CrossRef | 1:CAS:528:DC%2BC2MXksF2itL8%3D&md5=98ebc65475635d09944ba08e4c52dae4CAS |

Bedell, V. M., Wang, Y., Campbell, J. M., Poshusta, T. L., Starker, C. G., Krug, R. G., Tan, W., Penheiter, S. G., Ma, A. C., Leung, A. Y., Fahrenkrug, S. C., Carlson, D. F., Voytas, D. F., Clark, K. J., Essner, J. J., and Ekker, S. C. (2012). In vivo genome editing using a high-efficiency TALEN system. Nature 491, 114–118.
In vivo genome editing using a high-efficiency TALEN system.CrossRef | 1:CAS:528:DC%2BC38Xhtlylsr3K&md5=90163a0767c0236bc7a40cd5bea0720cCAS |

Bradley, A., Anastassiadis, K., Ayadi, A., Battey, J. F., Bell, C., Birling, M. C., Bottomley, J., Brown, S. D., Bürger, A., Bult, C. J., Bushell, W., Collins, F. S., Desaintes, C., Doe, B., Economides, A., Eppig, J. T., Finnell, R. H., Fletcher, C., Fray, M., Frendewey, D., Friedel, R. H., Grosveld, F. G., Hansen, J., Hérault, Y., Hicks, G., Hörlein, A., Houghton, R., Hrabé de Angelis, M., Huylebroeck, D., Iyer, V., de Jong, P. J., Kadin, J. A., Kaloff, C., Kennedy, K., Koutsourakis, M., Lloyd, K. C., Marschall, S., Mason, J., McKerlie, C., McLeod, M. P., von Melchner, H., Moore, M., Mujica, A. O., Nagy, A., Nefedov, M., Nutter, L. M., Pavlovic, G., Peterson, J. L., Pollock, J., Ramirez-Solis, R., Rancourt, D. E., Raspa, M., Remacle, J. E., Ringwald, M., Rosen, B., Rosenthal, N., Rossant, J., Ruiz Noppinger, P., Ryder, E., Schick, J. Z., Schnütgen, F., Schofield, P., Seisenberger, C., Selloum, M., Simpson, E. M., Skarnes, W. C., Smedley, D., Stanford, W. L., Stewart, A. F., Stone, K., Swan, K., Tadepally, H., Teboul, L., Tocchini-Valentini, G. P., Valenzuela, D., West, A. P., Yamamura, K., Yoshinaga, Y., and Wurst, W. (2012). The mammalian gene function resource: the International Knockout Mouse Consortium. Mamm. Genome 23, 580–586.
The mammalian gene function resource: the International Knockout Mouse Consortium.CrossRef |

Buehr, M., Meek, S., Blair, K., Yang, J., Ure, J., Silva, J., McLay, R., Hall, J., Ying, Q. L., and Smith, A. (2008). Capture of authentic embryonic stem cells from rat blastocysts. Cell 135, 1287–1298.
Capture of authentic embryonic stem cells from rat blastocysts.CrossRef | 1:CAS:528:DC%2BD1MXisFyisA%3D%3D&md5=70133a5c68c95881bdeb43aed8ca23daCAS |

Carbery, I. D., Ji, D., Harrington, A., Brown, V., Weinstein, E. J., Liaw, L., and Cui, X. (2010). Targeted genome modification in mice using zinc-finger nucleases. Genetics 186, 451–459.
Targeted genome modification in mice using zinc-finger nucleases.CrossRef | 1:CAS:528:DC%2BC3cXhsFOnt7rI&md5=c6611d7cca90286853a640ffa44b740bCAS |

Carlson, D. F., Tan, W., Lillico, S. G., Stverakova, D., Proudfoot, C., Christian, M., Voytas, D. F., Long, C. R., Whitelaw, C. B., and Fahrenkrug, S. C. (2012). Efficient TALEN-mediated gene knockout in livestock. Proc. Natl Acad. Sci. USA 109, 17 382–17 387.
Efficient TALEN-mediated gene knockout in livestock.CrossRef | 1:CAS:528:DC%2BC38XhvVSltL3K&md5=0b7dc6b97ece7d597e8decb3d3e7d1b2CAS |

Cermak, T., Starker, C. G., and Voytas, D. F. (2015). Efficient design and assembly of custom TALENs using the Golden Gate platform. Methods Mol. Biol. 1239, 133–159.
Efficient design and assembly of custom TALENs using the Golden Gate platform.CrossRef | 1:CAS:528:DC%2BC28XjtVyqtbk%3D&md5=05664738e56512029b5a26e2da38297aCAS |

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.
Multiplex genome engineering using CRISPR/Cas systems.CrossRef | 1:CAS:528:DC%2BC3sXit1ygtb8%3D&md5=25512c839e00286bbeabefc0702c321aCAS |

Crispo, M., Mulet, A. P., Tesson, L., Barrera, N., Cuadro, F., dos Santos-Neto, P. C., Nguyen, T. H., Crénéguy, A., Brusselle, L., Anegón, I., and Menchaca, A. (2015). Efficient Generation of myostatin knock-out sheep using CRISPR/Cas9 technology and microinjection into zygotes. PLoS One 10, e0136690.
Efficient Generation of myostatin knock-out sheep using CRISPR/Cas9 technology and microinjection into zygotes.CrossRef | 1:STN:280:DC%2BC287mt12juw%3D%3D&md5=cf377da78094a6b7a4c9e0a6237bdc3aCAS |

Cui, C., Song, Y., Liu, J., Ge, H., Li, Q., Huang, H., Hu, L., Zhu, H., Jin, Y., and Zhang, Y. (2015). Gene targeting by TALEN-induced homologous recombination in goats directs production of β-lactoglobulin-free, high-human lactoferrin milk. Sci. Rep. 5, 10482.
Gene targeting by TALEN-induced homologous recombination in goats directs production of β-lactoglobulin-free, high-human lactoferrin milk.CrossRef |

Daimon, T., Uchibori, M., Nakao, H., Sezutsu, H., and Shinoda, T. (2015). Knockout silkworms reveal a dispensable role for juvenile hormones in holometabolous life cycle. Proc. Natl Acad. Sci. USA 112, E4226–E4235.
Knockout silkworms reveal a dispensable role for juvenile hormones in holometabolous life cycle.CrossRef | 1:CAS:528:DC%2BC2MXhtF2hsrvN&md5=37b9066979c6752824f907887e3f8d74CAS |

Doudna, J. A., and Charpentier, E. (2014). Genome editing. The new frontier of genome engineering with CRISPR–Cas9. Science 346, 1258096.
Genome editing. The new frontier of genome engineering with CRISPR–Cas9.CrossRef |

Fischer, K., Kraner-Scheiber, S., Petersen, B., Rieblinger, B., Buermann, A., Flisikowska, T., Flisikowski, K., Christan, S., Edlinger, M., Baars, W., Kurome, M., Zakhartchenko, V., Kessler, B., Plotzki, E., Szczerbal, I., Switonski, M., Denner, J., Wolf, E., Schwinzer, R., Niemann, H., Kind, A., and Schnieke, A. (2016). Efficient production of multi-modified pigs for xenotransplantation by ‘combineering’, gene stacking and gene editing. Sci. Rep. 6, 29081.
Efficient production of multi-modified pigs for xenotransplantation by ‘combineering’, gene stacking and gene editing.CrossRef | 1:CAS:528:DC%2BC28XhtFSqt7jP&md5=850576167d7186a76cfe5b88b7e6f07cCAS |

Gao, F., Shen, X. Z., Jiang, F., Wu, Y., and Han, C. (2016). DNA-guided genome editing using the Natronobacterium gregoryi Argonaute. Nat. Biotechnol. 34, 768–773.
DNA-guided genome editing using the Natronobacterium gregoryi Argonaute.CrossRef | 1:CAS:528:DC%2BC28XmvFOqsro%3D&md5=44e55dd325ac2a2d297b2ddd9000b1d5CAS |

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. USA 109, E2579–E2586.
Cas9–crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria.CrossRef | 1:CAS:528:DC%2BC38XhsFCrsLfO&md5=ef3ec120b162e7a24bc169b48bb7410eCAS |

Geurts, A. M., Cost, G. J., Freyvert, Y., Zeitler, B., Miller, J. C., Choi, V. M., Jenkins, S. S., Wood, A., Cui, X., Meng, X., Vincent, A., Lam, S., Michalkiewicz, M., Schilling, R., Foeckler, J., Kalloway, S., Weiler, H., Ménoret, S., Anegon, I., Davis, G. D., Zhang, L., Rebar, E. J., Gregory, P. D., Urnov, F. D., Jacob, H. J., and Buelow, R. (2009). Knockout rats via embryo microinjection of zinc-finger nucleases. Science 325, 433.
Knockout rats via embryo microinjection of zinc-finger nucleases.CrossRef | 1:CAS:528:DC%2BD1MXovVChtrY%3D&md5=50ec324b2da01508979e08a47984569dCAS |

Guo, Y., Xu, Q., Canzio, D., Shou, J., Li, J., Gorkin, D. U., Jung, I., Wu, H., Zhai, Y., Tang, Y., Lu, Y., Wu, Y., Jia, Z., Li, W., Zhang, M. Q., Ren, B., Krainer, A. R., Maniatis, T., and Wu, Q. (2015). CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162, 900–910.
CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function.CrossRef | 1:CAS:528:DC%2BC2MXhtlCisLnI&md5=926496c6b774c35106405a23cd038889CAS |

Guo, R., Wan, Y., Xu, D., Cui, L., Deng, M., Zhang, G., Jia, R., Zhou, W., Wang, Z., Deng, K., Huang, M., Wang, F., and Zhang, Y. (2016). Generation and evaluation of myostatin knock-out rabbits and goats using CRISPR/Cas9 system. Sci. Rep. 6, 29855.
Generation and evaluation of myostatin knock-out rabbits and goats using CRISPR/Cas9 system.CrossRef |

Hai, T., Teng, F., Guo, R., Li, W., and Zhou, Q. (2014). One-step generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Res. 24, 372–375.
One-step generation of knockout pigs by zygote injection of CRISPR/Cas system.CrossRef | 1:CAS:528:DC%2BC2cXhsl2gsLk%3D&md5=0ca54353b0fa89ce7f239a371549edc5CAS |

Han, Y., Slivano, O. J., Christie, C. K., Cheng, A. W., and Miano, J. M. (2015). CRISPR–Cas9 genome editing of a single regulatory element nearly abolishes target gene expression in mice – brief report. Arterioscler. Thromb. Vasc. Biol. 35, 312–315.
CRISPR–Cas9 genome editing of a single regulatory element nearly abolishes target gene expression in mice – brief report.CrossRef | 1:CAS:528:DC%2BC2MXhtFyrtbY%3D&md5=8efaafa8b3cf8ab141d0dbf3a361b689CAS |

Harms, D. W., Quadros, R. M., Seruggia, D., Ohtsuka, M., Takahashi, G., Montoliu, L., and Gurumurthy, C. B. (2014). Mouse genome editing using the CRISPR/Cas system. Curr. Protoc. Hum. Genet. 83, 15.7.1–15.7.27.
Mouse genome editing using the CRISPR/Cas system.CrossRef |

Hauschild, J., Petersen, B., Santiago, Y., Queisser, A. L., Carnwath, J. W., Lucas-Hahn, A., Zhang, L., Meng, X., Gregory, P. D., Schwinzer, R., Cost, G. J., and Niemann, H. (2011). Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases. Proc. Natl Acad. Sci. USA 108, 12 013–12 017.
Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases.CrossRef | 1:CAS:528:DC%2BC3MXpsFyku7o%3D&md5=c6ec83c88f4fbf86ef4f5d7101d3ed84CAS |

Hermann, M., Maeder, M. L., Rector, K., Ruiz, J., Becher, B., Bürki, K., Khayter, C., Aguzzi, A., Joung, J. K., Buch, T., and Pelczar, P. (2012). Evaluation of OPEN zinc finger nucleases for direct gene targeting of the ROSA26 locus in mouse embryos. PLoS One 7, e41796.
Evaluation of OPEN zinc finger nucleases for direct gene targeting of the ROSA26 locus in mouse embryos.CrossRef | 1:CAS:528:DC%2BC38XhtlGitLfK&md5=6bf20bbed0d6f44d6f220b0a4779ee31CAS |

Hsu, P. D., Lander, E. S., and Zhang, F. (2014). Development and applications of CRISPR-Cas9 for genome engineering. Cell 157, 1262–1278.
Development and applications of CRISPR-Cas9 for genome engineering.CrossRef | 1:CAS:528:DC%2BC2cXpslagt7s%3D&md5=ab82238392af11007bb78f9794e894fcCAS |

Ikmi, A., McKinney, S. A., Delventhal, K. M., and Gibson, M. C. (2014). TALEN and CRISPR/Cas9-mediated genome editing in the early-branching metazoan Nematostella vectensis. Nat. Commun. 5, 5486.
TALEN and CRISPR/Cas9-mediated genome editing in the early-branching metazoan Nematostella vectensis.CrossRef | 1:CAS:528:DC%2BC2MXksVCjt7Y%3D&md5=3a771600fc4d17339c66b472615ca815CAS |

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.
A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity.CrossRef | 1:CAS:528:DC%2BC38XhtFOqsb3L&md5=03db2e35c779a9d33588e900c690d8d7CAS |

Kleinstiver, B. P., Prew, M. S., Tsai, S. Q., Topkar, V. V., Nguyen, N. T., Zheng, Z., Gonzales, A. P., Li, Z., Peterson, R. T., Yeh, J. R., Aryee, M. J., and Joung, J. K. (2015). Engineered CRISPR–Cas9 nucleases with altered PAM specificities. Nature 523, 481–485.
Engineered CRISPR–Cas9 nucleases with altered PAM specificities.CrossRef |

Kleinstiver, B. P., Pattanayak, V., Prew, M. S., Tsai, S. Q., Nguyen, N. T., Zheng, Z., and Joung, J. K. (2016). High-fidelity CRISPR–Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529, 490–495.
High-fidelity CRISPR–Cas9 nucleases with no detectable genome-wide off-target effects.CrossRef | 1:CAS:528:DC%2BC28Xns1GmsQ%3D%3D&md5=020e9b75025b977c59dcd0543c2152b3CAS |

Kwon, D. N., Lee, K., Kang, M. J., Choi, Y. J., Park, C., Whyte, J. J., Brown, A. N., Kim, J. H., Samuel, M., Mao, J., Park, K. W., Murphy, C. N., Prather, R. S., and Kim, J. H. (2013). Production of biallelic CMP–Neu5Ac hydroxylase knock-out pigs. Sci. Rep. 3, 1981.
Production of biallelic CMP–Neu5Ac hydroxylase knock-out pigs.CrossRef |

Lai, S., Wei, S., Zhao, B., Ouyang, Z., Zhang, Q., Fan, N., Liu, Z., Zhao, Y., Yan, Q., Zhou, X., Li, L., Xin, J., Zeng, Y., Lai, L., and Zou, Q. (2016). Generation of knock-in pigs carrying Oct4-tdTomato reporter through CRISPR/Cas9-mediated genome engineering. PLoS One 11, e0146562.
Generation of knock-in pigs carrying Oct4-tdTomato reporter through CRISPR/Cas9-mediated genome engineering.CrossRef |

Lillico, S. G., Proudfoot, C., King, T. J., Tan, W., Zhang, L., Mardjuki, R., Paschon, D. E., Rebar, E. J., Urnov, F. D., Mileham, A. J., McLaren, D. G., and Whitelaw, C. B. (2016). Mammalian interspecies substitution of immune modulatory alleles by genome editing. Sci. Rep. 6, 21645.
Mammalian interspecies substitution of immune modulatory alleles by genome editing.CrossRef | 1:CAS:528:DC%2BC28XivFGrt7s%3D&md5=b398810b5ae517ebc5588a333d71835eCAS |

Liu, X., Wang, Y., Guo, W., Chang, B., Liu, J., Guo, Z., Quan, F., and Zhang, Y. (2013). Zinc-finger nickase-mediated insertion of the lysostaphin gene into the beta-casein locus in cloned cows. Nat. Commun. 4, 2565.

Liu, H., Chen, Y., Niu, Y., Zhang, K., Kang, Y., Ge, W., Liu, X., Zhao, E., Wang, C., Lin, S., Jing, B., Si, C., Lin, Q., Chen, X., Lin, H., Pu, X., Wang, Y., Qin, B., Wang, F., Wang, H., Si, W., Zhou, J., Tan, T., Li, T., Ji, S., Xue, Z., Luo, Y., Cheng, L., Zhou, Q., Li, S., Sun, Y. E., and Ji, W. (2014a). TALEN-mediated gene mutagenesis in rhesus and cynomolgus monkeys. Cell Stem Cell 14, 323–328.
TALEN-mediated gene mutagenesis in rhesus and cynomolgus monkeys.CrossRef | 1:CAS:528:DC%2BC2cXisFCjtr4%3D&md5=0843a6117d48d4ea8daf35a5b3b6a071CAS |

Liu, X., Wang, Y., Tian, Y., Yu, Y., Gao, M., Hu, G., Su, F., Pan, S., Luo, Y., Guo, Z., Quan, F., and Zhang, Y. (2014b). Generation of mastitis resistance in cows by targeting human lysozyme gene to β-casein locus using zinc-finger nucleases. Proc. Biol. Sci. 281, 20133368.
Generation of mastitis resistance in cows by targeting human lysozyme gene to β-casein locus using zinc-finger nucleases.CrossRef |

Lupiáñez, D. G., Kraft, K., Heinrich, V., Krawitz, P., Brancati, F., Klopocki, E., Horn, D., Kayserili, H., Opitz, J. M., Laxova, R., Santos-Simarro, F., Gilbert-Dussardier, B., Wittler, L., Borschiwer, M., Haas, S. A., Osterwalder, M., Franke, M., Timmermann, B., Hecht, J., Spielmann, M., Visel, A., and Mundlos, S. (2015). Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161, 1012–1025.
Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions.CrossRef |

Lv, Q., Yuan, L., Deng, J., Chen, M., Wang, Y., Zeng, J., Li, Z., and Lai, L. (2016). Efficient generation of myostatin gene mutated rabbit by CRISPR/Cas9. Sci. Rep. 6, 25029.
Efficient generation of myostatin gene mutated rabbit by CRISPR/Cas9.CrossRef | 1:CAS:528:DC%2BC28XmvVCrtbc%3D&md5=d2206de1a0b912b824f35b0251a4af7bCAS |

Ma, Y., Ma, J., Zhang, X., Chen, W., Yu, L., Lu, Y., Bai, L., Shen, B., Huang, X., and Zhang, L. (2014). generation of eGFP and Cre knockin rats by CRISPR/Cas9. FEBS J. 281, 3779–3790.
generation of eGFP and Cre knockin rats by CRISPR/Cas9.CrossRef | 1:CAS:528:DC%2BC2cXhsVGgsrfI&md5=ef1c0bbc0d43f8c613c1e8b6ee04c4fbCAS |

Ma, L., Jeffery, W. R., Essner, J. J., and Kowalko, J. E. (2015). Genome editing using TALENs in blind Mexican cavefish, Astyanax mexicanus. PLoS One 10, e0119370.
Genome editing using TALENs in blind Mexican cavefish, Astyanax mexicanus.CrossRef |

Maddalo, D., Manchado, E., Concepcion, C. P., Bonetti, C., Vidigal, J. A., Han, Y. C., Ogrodowski, P., Crippa, A., Rekhtman, N., de Stanchina, E., Lowe, S. W., and Ventura, A. (2014). In vivo engineering of oncogenic chromosomal rearrangements with the CRISPR/Cas9 system. Nature 516, 423–427.
In vivo engineering of oncogenic chromosomal rearrangements with the CRISPR/Cas9 system.CrossRef | 1:CAS:528:DC%2BC2cXhvVemtrvL&md5=4ae9827c6a3c6bf763da2766a1c6621cCAS |

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.
RNA-guided human genome engineering via Cas9.CrossRef | 1:CAS:528:DC%2BC3sXit1ygtb0%3D&md5=cf687fdc12a92ed2f180522aa1539315CAS |

Meyer, M., de Angelis, M. H., Wurst, W., and Kühn, R. (2010). Gene targeting by homologous recombination in mouse zygotes mediated by zinc-finger nucleases. Proc. Natl Acad. Sci. USA 107, 15 022–15 026.
Gene targeting by homologous recombination in mouse zygotes mediated by zinc-finger nucleases.CrossRef | 1:CAS:528:DC%2BC3cXhtFSmt7vP&md5=2933bf844d31389d92cc8d8603ddba06CAS |

Mohanraju, P., Makarova, K. S., Zetsche, B., Zhang, F., Koonin, E. V., and van der Oost, J. (2016). Diverse evolutionary roots and mechanistic variations of the CRISPR–Cas systems. Science 353, .
Diverse evolutionary roots and mechanistic variations of the CRISPR–Cas systems.CrossRef | 1:CAS:528:DC%2BC28Xht1Oks7jJ&md5=7b185d2760610857e85e6f781cd55d3aCAS |

Mojica, F. J., and Montoliu, L. (2016). On the origin of CRISPR–Cas technology: from prokaryotes to mammals. Trends Microbiol. 24, 811–820.
On the origin of CRISPR–Cas technology: from prokaryotes to mammals.CrossRef | 1:CAS:528:DC%2BC28XhtVKntr%2FO&md5=9972c775f4adbfa8ea62d835657c3575CAS |

Montoliu, L. (2002). Gene transfer strategies in animal transgenesis. Cloning Stem Cells 4, 39–46.
Gene transfer strategies in animal transgenesis.CrossRef | 1:CAS:528:DC%2BD38Xjt1Gku7s%3D&md5=d3c867f40f50fc34eb2f1fb2b733037eCAS |

Ni, W., Qiao, J., Hu, S., Zhao, X., Regouski, M., Yang, M., Polejaeva, I. A., and Chen, C. (2014). Efficient gene knockout in goats using CRISPR/Cas9 system. PLoS One 9, e106718.
Efficient gene knockout in goats using CRISPR/Cas9 system.CrossRef |

Niemann, H., and Petersen, B. (2016). The production of multi-transgenic pigs: update and perspectives for xenotransplantation. Transgenic Res. 25, 361–374.
The production of multi-transgenic pigs: update and perspectives for xenotransplantation.CrossRef | 1:CAS:528:DC%2BC28XhsFyrur4%3D&md5=9390a947570b7c67441f038a3e0dfcd1CAS |

Palmiter, R. D., and Brinster, R. L. (1986). Germ-line transformation of mice. Annu. Rev. Genet. 20, 465–499.
Germ-line transformation of mice.CrossRef | 1:CAS:528:DyaL2sXmtFyksg%3D%3D&md5=3c2c0b8d84257770cb63fff9a30c85ffCAS |

Panda, S. K., Wefers, B., Ortiz, O., Floss, T., Schmid, B., Haass, C., Wurst, W., and Kühn, R. (2013). Highly efficient targeted mutagenesis in mice using TALENs. Genetics 195, 703–713.
Highly efficient targeted mutagenesis in mice using TALENs.CrossRef | 1:CAS:528:DC%2BC2cXhtlGjtLg%3D&md5=3375f396c72195d7fda8f7568824da46CAS |

Park, T. S., Lee, H. J., Kim, K. H., Kim, J. S., and Han, J. Y. (2014). Targeted gene knockout in chickens mediated by TALENs. Proc. Natl Acad. Sci. USA 111, 12 716–12 721.
Targeted gene knockout in chickens mediated by TALENs.CrossRef | 1:CAS:528:DC%2BC2cXhsVarsbfM&md5=124082565c188c4415fbc2a44751b2caCAS |

Peng, J., Wang, Y., Jiang, J., Zhou, X., Song, L., Wang, L., Ding, C., Qin, J., Liu, L., Wang, W., Liu, J., Huang, X., Wei, H., and Zhang, P. (2015). Production of human albumin in pigs through CRISPR/Cas9-mediated knockin of human cDNA into swine albumin locus in the zygotes. Sci. Rep. 5, 16705.
Production of human albumin in pigs through CRISPR/Cas9-mediated knockin of human cDNA into swine albumin locus in the zygotes.CrossRef |

Petersen, B., and Niemann, H. (2015). Advances in genetic modification of farm animals using zinc-finger nucleases (ZFN). Chromosome Res. 23, 7–15.
Advances in genetic modification of farm animals using zinc-finger nucleases (ZFN).CrossRef | 1:CAS:528:DC%2BC2MXpvFWjtg%3D%3D&md5=7d89144dd80364db585586362c6e6e45CAS |

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., Anderson, D. G., Hacohen, N., Regev, A., Feng, G., Sharp, P. A., and Zhang, F. (2014). CRISPR–Cas9 knockin mice for genome editing and cancer modeling. Cell 159, 440–455.
CRISPR–Cas9 knockin mice for genome editing and cancer modeling.CrossRef | 1:CAS:528:DC%2BC2cXhs1agsbbE&md5=661718a6fcfae19cdeb940dd1d67cb5eCAS |

Proudfoot, C., Carlson, D. F., Huddart, R., Long, C. R., Pryor, J. H., King, T. J., Lillico, S. G., Mileham, A. J., McLaren, D. G., Whitelaw, C. B., and Fahrenkrug, S. C. (2015). Genome edited sheep and cattle. Transgenic Res. 24, 147–153.
Genome edited sheep and cattle.CrossRef | 1:CAS:528:DC%2BC2cXhsFSgsLrF&md5=f3d7aa43e5eeaa88e71227ee26a7f714CAS |

Pyzocha, N. K., Ran, F. A., Hsu, P. D., and Zhang, F. (2014). RNA-guided genome editing of mammalian cells. Methods Mol. Biol. 1114, 269–277.
RNA-guided genome editing of mammalian cells.CrossRef | 1:CAS:528:DC%2BC2MXnvVWgs7w%3D&md5=9fc3c845453bf0b6b329bd727f06367eCAS |

Qian, L., Tang, M., Yang, J., Wang, Q., Cai, C., Jiang, S., Li, H., Jiang, K., Gao, P., Ma, D., Chen, Y., An, X., Li, K., and Cui, W. (2015). Targeted mutations in myostatin by zinc-finger nucleases result in double-muscled phenotype in Meishan pigs. Sci. Rep. 5, 14435.
Targeted mutations in myostatin by zinc-finger nucleases result in double-muscled phenotype in Meishan pigs.CrossRef | 1:CAS:528:DC%2BC2MXhsFGksbbI&md5=4b8efea0498441cb40e46a198e352649CAS |

Rémy, S., Tesson, L., Ménoret, S., Usal, C., Scharenberg, A. M., and Anegon, I. (2010). Zinc-finger nucleases: a powerful tool for genetic engineering of animals. Transgenic Res. 19, 363–371.
Zinc-finger nucleases: a powerful tool for genetic engineering of animals.CrossRef |

Saiki, R. K., Bugawan, T. L., Horn, G. T., Mullis, K. B., and Erlich, H. A. (1986). Analysis of enzymatically amplified beta-globin and HLA-DQ alpha DNA with allele-specific oligonucleotide probes. Nature 324, 163–166.
Analysis of enzymatically amplified beta-globin and HLA-DQ alpha DNA with allele-specific oligonucleotide probes.CrossRef | 1:CAS:528:DyaL2sXksV2qtQ%3D%3D&md5=6b8d98a6b9578be0b7cb85a8708e0bbeCAS |

Sander, J. D., and Joung, J. K. (2014). CRISPR–Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol. 32, 347–355.
CRISPR–Cas systems for editing, regulating and targeting genomes.CrossRef | 1:CAS:528:DC%2BC2cXjtlyrsLo%3D&md5=cb76350de539ebff0481a277856fe78cCAS |

Seruggia, D., and Montoliu, L. (2014). The new CRISPR–Cas system: RNA-guided genome engineering to efficiently produce any desired genetic alteration in animals. Transgenic Res. 23, 707–716.
The new CRISPR–Cas system: RNA-guided genome engineering to efficiently produce any desired genetic alteration in animals.CrossRef | 1:CAS:528:DC%2BC2cXht1KgsbzM&md5=5e0493848f428049b1d8ef6acbe8d842CAS |

Seruggia, D., Fernández, A., Cantero, M., Pelczar, P., and Montoliu, L. (2015). Functional validation of mouse tyrosinase non-coding regulatory DNA elements by CRISPR–Cas9-mediated mutagenesis. Nucleic Acids Res. 43, 4855–4867.
Functional validation of mouse tyrosinase non-coding regulatory DNA elements by CRISPR–Cas9-mediated mutagenesis.CrossRef | 1:CAS:528:DC%2BC2MXhsFaitL3F&md5=d1a6eee5f3f8a4cf95de5923126b88dfCAS |

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, 84–88.
Rationally engineered Cas9 nucleases with improved specificity.CrossRef | 1:CAS:528:DC%2BC2MXitV2nt7nE&md5=419fe90ad4754d1595a13482d02f13e4CAS |

Sommer, D., Peters, A. E., Baumgart, A. K., and Beyer, M. (2015). TALEN-mediated genome engineering to generate targeted mice. Chromosome Res. 23, 43–55.
TALEN-mediated genome engineering to generate targeted mice.CrossRef | 1:CAS:528:DC%2BC2MXpvFSqsg%3D%3D&md5=f7045d90ddcbeb5bc88370bc68b4b30cCAS |

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.
Knockout mice created by TALEN-mediated gene targeting.CrossRef | 1:CAS:528:DC%2BC3sXltVCksg%3D%3D&md5=a0d1792b0ac7504ec97db221647c43f4CAS |

Swarts, D. C., Jore, M. M., Westra, E. R., Zhu, Y., Janssen, J. H., Snijders, A. P., Wang, Y., Patel, D. J., Berenguer, J., Brouns, S. J., and van der Oost, J. (2014). DNA-guided DNA interference by a prokaryotic Argonaute. Nature 507, 258–261.
DNA-guided DNA interference by a prokaryotic Argonaute.CrossRef | 1:CAS:528:DC%2BC2cXktV2rt7o%3D&md5=98e768604f75bd125282a40b7eba2de1CAS |

Tan, W., Carlson, D. F., Lancto, C. A., Garbe, J. R., Webster, D. A., Hackett, P. B., and Fahrenkrug, S. C. (2013). Efficient nonmeiotic allele introgression in livestock using custom endonucleases. Proc. Natl Acad. Sci. USA 110, 16 526–16 531.
Efficient nonmeiotic allele introgression in livestock using custom endonucleases.CrossRef | 1:CAS:528:DC%2BC3sXhs1Kju7%2FL&md5=739a1fd1657e80b34b9e6d5afd9d29c0CAS |

Tan, W., Proudfoot, C., Lillico, S. G., and Whitelaw, C. B. (2016). Gene targeting, genome editing: from Dolly to editors. Transgenic Res. 25, 273–287.
Gene targeting, genome editing: from Dolly to editors.CrossRef | 1:CAS:528:DC%2BC28XitVWhs74%3D&md5=a4a0d79cf07257514bd2b5e343f073ffCAS |

Tesson, L., Usal, C., Ménoret, S., Leung, E., Niles, B. J., Remy, S., Santiago, Y., Vincent, A. I., Meng, X., Zhang, L., Gregory, P. D., Anegon, I., and Cost, G. J. (2011). Knockout rats generated by embryo microinjection of TALENs. Nat. Biotechnol. 29, 695–696.
Knockout rats generated by embryo microinjection of TALENs.CrossRef | 1:CAS:528:DC%2BC3MXpvVOlurY%3D&md5=59fc39760e2eb4855393b2b3dffa50c3CAS |

Trounson, A. O. (2006). Future and applications of cloning. Methods Mol. Biol. 348, 319–331.
Future and applications of cloning.CrossRef |

Wang, Z. (2015). Genome engineering in cattle: recent technological advancements. Chromosome Res. 23, 17–29.
Genome engineering in cattle: recent technological advancements.CrossRef | 1:CAS:528:DC%2BC2MXpvFSqtQ%3D%3D&md5=7e2ad5691a9b8e1a38b044b6f8178d60CAS |

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.
One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering.CrossRef | 1:CAS:528:DC%2BC3sXmvF2nt7w%3D&md5=d53fe22f23b031ff45616107b067c966CAS |

Wang, X., Yu, H., Lei, A., Zhou, J., Zeng, W., Zhu, H., Dong, Z., Niu, Y., Shi, B., Cai, B., Liu, J., Huang, S., Yan, H., Zhao, X., Zhou, G., He, X., Chen, X., Yang, Y., Jiang, Y., Shi, L., Tian, X., Wang, Y., Ma, B., Huang, X., Qu, L., and Chen, Y. (2015). Generation of gene-modified goats targeting MSTN and FGF5 via zygote injection of CRISPR/Cas9 system. Sci. Rep. 5, 13878.
Generation of gene-modified goats targeting MSTN and FGF5 via zygote injection of CRISPR/Cas9 system.CrossRef |

Wang, X., Cao, C., Huang, J., Yao, J., Hai, T., Zheng, Q., Wang, X., Zhang, H., Qin, G., Cheng, J., Wang, Y., Yuan, Z., Zhou, Q., Wang, H., and Zhao, J. (2016). One-step generation of triple gene-targeted pigs using CRISPR/Cas9 system. Sci. Rep. 6, 20620.
One-step generation of triple gene-targeted pigs using CRISPR/Cas9 system.CrossRef | 1:CAS:528:DC%2BC28Xitlymurs%3D&md5=e8fb2efb5ab74935ebefec70cd4288f9CAS |

Wefers, B., Panda, S. K., Ortiz, O., Brandl, C., Hensler, S., Hansen, J., Wurst, W., and Kühn, R. (2013). Generation of targeted mouse mutants by embryo microinjection of TALEN mRNA. Nat. Protoc. 8, 2355–2379.
Generation of targeted mouse mutants by embryo microinjection of TALEN mRNA.CrossRef | 1:CAS:528:DC%2BC3sXhslSnsL%2FF&md5=261e617c299c1ccd3d5168a9bb526bfbCAS |

Wei, J., Wagner, S., Lu, D., Maclean, P., Carlson, D. F., Fahrenkrug, S. C., and Laible, G. (2015). Efficient introgression of allelic variants by embryo-mediated editing of the bovine genome. Sci. Rep. 5, 11735.
Efficient introgression of allelic variants by embryo-mediated editing of the bovine genome.CrossRef |

Wilmut, I., Schnieke, A. E., McWhir, J., Kind, A. J., and Campbell, K. H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–813.
Viable offspring derived from fetal and adult mammalian cells.CrossRef | 1:CAS:528:DyaK2sXhsFamsLs%3D&md5=4da75c47ce70dd651256dd157af053c1CAS |

Wu, H., Wang, Y., Zhang, Y., Yang, M., Lv, J., Liu, J., and Zhang, Y. (2015). TALE nickase-mediated SP110 knockin endows cattle with increased resistance to tuberculosis. Proc. Natl Acad. Sci. USA 112, E1530–E1539.
TALE nickase-mediated SP110 knockin endows cattle with increased resistance to tuberculosis.CrossRef | 1:CAS:528:DC%2BC2MXjs1Gqsr4%3D&md5=59f83b550b1f8f4aea62dfa47fc3d2d5CAS |

Xiao, A., Wang, Z., Hu, Y., Wu, Y., Luo, Z., Yang, Z., Zu, Y., Li, W., Huang, P., Tong, X., Zhu, Z., Lin, S., and Zhang, B. (2013). Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish. Nucleic Acids Res. 41, e141.
Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish.CrossRef | 1:CAS:528:DC%2BC3sXht1CktLbK&md5=02d2ad561b5694edf11c7cb124ea80ebCAS |

Xin, J., Yang, H., Fan, N., Zhao, B., Ouyang, Z., Liu, Z., Zhao, Y., Li, X., Song, J., Yang, Y., Zou, Q., Yan, Q., Zeng, Y., and Lai, L. (2013). Highly efficient generation of GGTA1 biallelic knockout inbred mini-pigs with TALENs. PLoS One 8, e84250.
Highly efficient generation of GGTA1 biallelic knockout inbred mini-pigs with TALENs.CrossRef |

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.
One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering.CrossRef | 1:CAS:528:DC%2BC3sXhtlGqtr%2FN&md5=7872cc94fdd1278b5bca2ebe2d2826daCAS |

Yang, H., Wang, H., and Jaenisch, R. (2014). Generating genetically modified mice using CRISPR/Cas-mediated genome engineering. Nat. Protoc. 9, 1956–1968.
Generating genetically modified mice using CRISPR/Cas-mediated genome engineering.CrossRef | 1:CAS:528:DC%2BC2cXht1WlurbE&md5=926043f63cccac45c54769c60cd7d8f7CAS |

Yang, L., Güell, M., Niu, D., George, H., Lesha, E., Grishin, D., Aach, J., Shrock, E., Xu, W., Poci, J., Cortazio, R., Wilkinson, R. A., Fishman, J. A., and Church, G. (2015). Genome-wide inactivation of porcine endogenous retroviruses (PERVs). Science 350, 1101–1104.
Genome-wide inactivation of porcine endogenous retroviruses (PERVs).CrossRef | 1:CAS:528:DC%2BC2MXhvFamtLrM&md5=33664ea10014981e93ac02dab9c0b567CAS |

Yu, S., Luo, J., Song, Z., Ding, F., Dai, Y., and Li, N. (2011). Highly efficient modification of beta-lactoglobulin (BLG) gene via zinc-finger nucleases in cattle. Cell Res. 21, 1638–1640.
Highly efficient modification of beta-lactoglobulin (BLG) gene via zinc-finger nucleases in cattle.CrossRef | 1:CAS:528:DC%2BC3MXhsVags7%2FF&md5=ca344fc15102237758c57d9c9f589a70CAS |

Zetsche, B., Gootenberg, J. S., Abudayyeh, O. O., Slaymaker, I. M., Makarova, K. S., Essletzbichler, P., Volz, S. E., Joung, J., van der Oost, J., Regev, A., Koonin, E. V., and Zhang, F. (2015). Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR–Cas system. Cell 163, 759–771.
Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR–Cas system.CrossRef | 1:CAS:528:DC%2BC2MXhsFKqtLvI&md5=09623b5f40b8744fc32d15ec5a8a4c77CAS |

Zhang, L., Jia, R., Palange, N. J., Satheka, A. C., Togo, J., An, Y., Humphrey, M., Ban, L., Ji, Y., Jin, H., Feng, X., and Zheng, Y. (2015). Large genomic fragment deletions and insertions in mouse using CRISPR/Cas9. PLoS One 10, e0120396.
Large genomic fragment deletions and insertions in mouse using CRISPR/Cas9.CrossRef |

Zu, Y., Tong, X., Wang, Z., Liu, D., Pan, R., Li, Z., Hu, Y., Luo, Z., Huang, P., Wu, Q., Zhu, Z., Zhang, B., and Lin, S. (2013). TALEN-mediated precise genome modification by homologous recombination in zebrafish. Nat. Methods 10, 329–331.
TALEN-mediated precise genome modification by homologous recombination in zebrafish.CrossRef | 1:CAS:528:DC%2BC3sXivFyls7c%3D&md5=ec1512b8be3e6f9ba363704ac781211aCAS |



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