A history of genome editing in mammals

Mammalian Genome

Volumn 28, Issue 7-8, 2017, Pages 237-246

  Fernández, Almudena ^a,b   Josa, Santiago ^a,b   Montoliu, Lluis ^a,b  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CRISPR ASSOCIATED PROTEIN; DNA; NUCLEASE; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; ZINC FINGER NUCLEASE;

ARTICLE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DNA REPAIR; DNA SEQUENCE; DOUBLE STRANDED DNA BREAK; GENE EDITING; HUMAN; INDEL MUTATION; MAMMALIAN GENETICS; NONHUMAN; ANIMAL; CRISPR CAS SYSTEM; GENOME; MAMMAL; METABOLISM; PROCEDURES;

ANIMALS; CRISPR-CAS SYSTEMS; GENE EDITING; GENOME; HUMANS; MAMMALS; TRANSCRIPTION ACTIVATOR-LIKE EFFECTOR NUCLEASES; ZINC FINGER NUCLEASES;

EID: 85020310565     PISSN: 09388990     EISSN: 14321777     Source Type: Journal    
DOI: 10.1007/s00335-017-9699-2     Document Type: Article

References (114)

1. Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM, Cox DB, Shmakov S, Makarova KS, Semenova E, Minakhin L, Severinov K, Regev A, Lander ES, Koonin EV, Zhang F (2016) C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353(6299):aaf5573
2. Bevacqua RJ, Fernandez-Martín R, Savy V, Canel NG, Gismondi MI, Kues WA, Carlson DF, Fahrenkrug SC, Niemann H, Taboga OA, Ferraris S, Salamone DF (2016) Efficient edition of the bovine PRNP prion gene in somatic cells and IVF embryos using the CRISPR/Cas9 system. Theriogenology 86:1886–1896
3. Bibikova M, Carroll D, Segal DJ, Trautman JK, Smith J, Kim YG, Chandrasegaran S (2001) Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol Cell Biol 21:289–297
4. Biffi A (2015) Clinical translation of TALENS: treating SCID-X1 by gene editing in iPSCs. Cell Stem Cell 16:348–349
5. Birling MC, Schaeffer L, André P, Lindner L, Maréchal D, Ayadi A, Sorg T, Pavlovic G, Hérault Y (2017) Efficient and rapid generation of large genomic variants in rats and mice using CRISMERE. Sci Rep 7:43331
6. Bochtler M (2012) Structural basis of the TAL effector-DNA interaction. Biol Chem 393:1055–1066
7. Brinster RL, Braun RE, Lo D, Avarbock MR, Oram F, Palmiter RD (1989) Targeted correction of a major histocompatibility class II E alpha gene by DNA microinjected into mouse eggs. Proc Natl Acad Sci USA 86:7087–7091
8. Buehr M, Meek S, Blair K, Yang J, Ure J, Silva J, McLay R, Hall J, Ying QL, Smith A (2008) Capture of authentic embryonic stem cells from rat blastocysts. Cell 135:1287–1298
9. Burstein D, Harrington LB, Strutt SC, Probst AJ, Anantharaman K, Thomas BC, Doudna JA, Banfield JF (2017) New CRISPR-Cas systems from uncultivated microbes. Nature 542:237–241
10. Carbery ID, Ji D, Harrington A, Brown V, Weinstein EJ, Liaw L, Cui X (2010) Targeted genome modification in mice using zinc-finger nucleases. Genetics 186:451–459
11. Carlson DF, Tan W, Lillico SG, Stverakova D, Proudfoot C, Christian M, Voytas DF, Long CR, Whitelaw CB, Fahrenkrug SC (2012) Efficient TALEN-mediated gene knockout in livestock. Proc Natl Acad Sci USA 109:17382–17387
12. Cermak T, Starker CG, Voytas DF (2015) Efficient design and assembly of custom TALENs using the Golden Gate platform. Methods Mol Biol 1239:133–159
13. Choulika A, Perrin A, Dujon B, Nicolas JF (1995) Induction of homologous recombination in mammalian chromosomes by using the I-SceI system of Saccharomyces cerevisiae. Mol Cell Biol 15:1968–1973
14. Cohen-Tannoudji M, Robine S, Choulika A, Pinto D, El Marjou F, Babinet C, Louvard D, Jaisser F (1998) I-SceI-induced gene replacement at a natural locus in embryonic stem cells. Mol Cell Biol 18:1444–1448
15. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823
16. Crispo M, Mulet AP, Tesson L, Barrera N, Cuadro F, dos Santos-Neto PC, Nguyen TH, Crénéguy A, Brusselle L, Anegón I, Menchaca A (2015) Efficient generation of Myostatin knock-out sheep using CRISPR/Cas9 technology and microinjection into zygotes. PLoS ONE 10:e0136690
17. Cui C, Song Y, Liu J, Ge H, Li Q, Huang H, Hu L, Zhu H, Jin Y, 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
18. Ellis BL, Hirsch ML, Porter SN, Samulski RJ, Porteus MH (2013) Zinc-finger nuclease-mediated gene correction using single AAV vector transduction and enhancement by Food and Drug Administration-approved drugs. Gene Ther 20:35–42
19. Fenina M, Simon-Chazottes D, Vandormael-Pournin S, Soueid J, Langa F, Cohen-Tannoudji M, Bernard BA, Panthier JJ (2012) I-SceI-mediated double-strand break does not increase the frequency of homologous recombination at the Dct locus in mouse embryonic stem cells. PLoS ONE 7:e39895
20. 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, Schnieke A (2016) Efficient production of multi-modified pigs for xenotransplantation by ‘combineering’, gene stacking and gene editing. Sci Rep 6:29081
21. Flynn R, Grundmann A, Renz P, Hänseler W, James WS, Cowley SA, Moore MD (2015) CRISPR-mediated genotypic and phenotypic correction of a chronic granulomatous disease mutation in human iPS cells. Exp Hematol 43:838–848
22. Gao Y, Wu H, Wang Y, Liu X, Chen L, Li Q, Cui C, Liu X, Zhang J, Zhang Y (2017) Single Cas9 nickase induced generation of NRAMP1 knockin cattle with reduced off-target effects. Genome Biol 18:13
23. Garate Z, Quintana-Bustamante O, Crane AM, Olivier E, Poirot L, Galetto R, Kosinski P, Hill C, Kung C, Agirre X, Orman I, Cerrato L, Alberquilla O, Rodriguez-Fornes F, Fusaki N, Garcia-Sanchez F, Maia TM, Ribeiro ML, Sevilla J, Prosper F, Jin S, Mountford J, Guenechea G, Gouble A, Bueren JA, Davis BR, Segovia JC (2015) Generation of a high number of healthy erythroid cells from gene-edited pyruvate kinase deficiency patient-specific induced pluripotent stem cells. Stem Cell Rep 5:1053–1066
24. Gasiunas G, Barrangou R, Horvath P, Siksnys V (2012) Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci USA 109:E2579–E2586
25. Geurts AM, Cost GJ, Freyvert Y, Zeitler B, Miller JC, Choi VM, Jenkins SS, 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 GD, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jacob HJ, Buelow R (2009) Knockout rats via embryo microinjection of zinc-finger nucleases. Science 325:433
26. Grizot S, Smith J, Daboussi F, Prieto J, Redondo P, Merino N, Villate M, Thomas S, Lemaire L, Montoya G, Blanco FJ, Pâques F, Duchateau P (2009) Efficient targeting of a SCID gene by an engineered single-chain homing endonuclease. Nucleic Acids Res 37:5405–5419
27. Guo Y, Xu Q, Canzio D, Shou J, Li J, Gorkin DU, Jung I, Wu H, Zhai Y, Tang Y, Lu Y, Wu Y, Jia Z, Li W, Zhang MQ, Ren B, Krainer AR, Maniatis T, Wu Q (2015) CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162:900–910
28. Guo R, Wan Y, Xu D, Cui L, Deng M, Zhang G, Jia R, Zhou W, Wang Z, Deng K, Huang M, Wang F, Zhang Y (2016) Generation and evaluation of Myostatin knock-out rabbits and goats using CRISPR/Cas9 system. Sci Rep 6:29855
29. Hai T, Teng F, Guo R, Li W, Zhou Q (2014) One-step generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Res 24:372–375
30. Han Y, Slivano OJ, Christie CK, Cheng AW, Miano JM (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
31. Harms DW, Quadros RM, Seruggia D, Ohtsuka M, Takahashi G, Montoliu L, Gurumurthy CB (2014) Mouse genome editing using the CRISPR/Cas system. Curr Protoc Hum Genet 83:1–27
32. Hasty P, Rivera-Pérez J, Chang C, Bradley A (1991) Target frequency and integration pattern for insertion and replacement vectors in embryonic stem cells. Mol Cell Biol 11:4509–4517
33. Hauschild J, Petersen B, Santiago Y, Queisser AL, Carnwath JW, Lucas-Hahn A, Zhang L, Meng X, Gregory PD, Schwinzer R, Cost GJ, Niemann H (2011) Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases. Proc Natl Acad Sci USA 108:12013–12017
34. Hermann M, Maeder ML, Rector K, Ruiz J, Becher B, Bürki K, Khayter C, Aguzzi A, Joung JK, Buch T, Pelczar P (2012) Evaluation of OPEN zinc finger nucleases for direct gene targeting of the ROSA26 locus in mouse embryos. PLoS ONE 7:e41796
35. Jacquier A, Dujon B (1985) An intron encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene. Cell 41:383–394
36. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821
37. Kang X, He W, Huang Y, Yu Q, Chen Y, Gao X, Sun X, Fan Y (2016) Introducing precise genetic modifications into human 3PN embryos by CRISPR/Cas-mediated genome editing. J Assist Reprod Genet 33:581–588
38. Kleinstiver BP, Prew MS, Tsai SQ, Topkar VV, Nguyen NT, Zheng Z, Gonzales AP, Li Z, Peterson RT, Yeh JR, Aryee MJ, Joung JK (2015) Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 523:481–485
39. Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT, Zheng Z, Joung JK (2016) High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529:490–495
40. Kucherlapati RS, Eves EM, Song KY, Morse BS, Smithies O (1984) Homologous recombination between plasmids in mammalian cells can be enhanced by treatment of input DNA. Proc Natl Acad Sci USA 81:3153–3157
41. Kwon DN, Lee K, Kang MJ, Choi YJ, Park C, Whyte JJ, Brown AN, Kim JH, Samuel M, Mao J, Park KW, Murphy CN, Prather RS, Kim JH (2013) Production of biallelic CMP-Neu5Ac hydroxylase knock-out pigs. Sci Rep 3:1981
42. 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, Zou Q (2016) Generation of knock-in pigs carrying Oct4-tdTomato reporter through CRISPR/Cas9-mediated genome engineering. PLoS ONE 11:e0146562
43. Liang P, Xu Y, Zhang X, Ding C, Huang R, Zhang Z, Lv J, Xie X, Chen Y, Li Y, Sun Y, Bai Y, Songyang Z, Ma W, Zhou C, Huang J (2015) CRISPR/Cas9-mediated gene editing in human tripronuclear zygotes. Protein Cell 6:363–372
44. Lillico SG, Proudfoot C, King TJ, Tan W, Zhang L, Mardjuki R, Paschon DE, Rebar EJ, Urnov FD, Mileham AJ, McLaren DG, Whitelaw CB (2016) Mammalian interspecies substitution of immune modulatory alleles by genome editing. Sci Rep 6:21645
45. Liu X, Wang Y, Guo W, Chang B, Liu J, Guo Z, Quan F, Zhang Y (2013) Zinc-finger nickase-mediated insertion of the lysostaphin gene into the beta-casein locus in cloned cows. Nat Commun 4:2565
46. 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 YE, Ji W (2014a) TALEN-mediated gene mutagenesis in rhesus and cynomolgus monkeys. Cell Stem Cell 14:323–328
47. Liu X, Wang Y, Tian Y, Yu Y, Gao M, Hu G, Su F, Pan S, Luo Y, Guo Z, Quan F, 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
48. Low BE, Krebs MP, Joung JK, Tsai SQ, Nishina PM, Wiles MV (2014) Correction of the Crb1rd8 allele and retinal phenotype in C57BL/6 N mice via TALEN-mediated homology-directed repair. Invest Ophthalmol Vis Sci 55:387–395
49. Lupiáñez DG, Kraft K, Heinrich V, Krawitz P, Brancati F, Klopocki E, Horn D, Kayserili H, Opitz JM, Laxova R, Santos-Simarro F, Gilbert-Dussardier B, Wittler L, Borschiwer M, Haas SA, Osterwalder M, Franke M, Timmermann B, Hecht J, Spielmann M, Visel A, Mundlos S (2015) Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161:1012–1025
50. Lv Q, Yuan L, Deng J, Chen M, Wang Y, Zeng J, Li Z, Lai L (2016) Efficient generation of myostatin gene mutated rabbit by CRISPR/Cas9. Sci Rep 6:25029
51. Ma Y, Ma J, Zhang X, Chen W, Yu L, Lu Y, Bai L, Shen B, Huang X, Zhang L (2014) Generation of eGFP and Cre knockin rats by CRISPR/Cas9. FEBS J 281:3779–3790
52. Maddalo D, Manchado E, Concepcion CP, Bonetti C, Vidigal JA, Han YC, Ogrodowski P, Crippa A, Rekhtman N, de Stanchina E, Lowe SW, Ventura A (2014) In vivo engineering of oncogenic chromosomal rearrangements with the CRISPR/Cas9 system. Nature 516:423–427
53. Maier DA, Brennan AL, Jiang S, Binder-Scholl GK, Lee G, Plesa G, Zheng Z, Cotte J, Carpenito C, Wood T, Spratt SK, Ando D, Gregory P, Holmes MC, Perez EE, Riley JL, Carroll RG, June CH, Levine BL (2013) Efficient clinical scale gene modification via zinc finger nuclease-targeted disruption of the HIV co-receptor CCR5. Hum Gene Ther 24:245–258
54. Mak TW (2007) Gene targeting in embryonic stem cells scores a knockout in Stockholm. Cell 131:1027–1031
55. Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA, Saunders SJ, Barrangou R, Brouns SJ, Charpentier E, Haft DH, Horvath P, Moineau S, Mojica FJ, Terns RM, Terns MP, White MF, Yakunin AF, Garrett RA, van der Oost J, Backofen R, Koonin EV (2015) An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol 13:722–736
56. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339:823–826
57. Mani M, Smith J, Kandavelou K, Berg JM, Chandrasegaran S (2005) Binding of two zinc finger nuclease monomers to two specific sites is required for effective double-strand DNA cleavage. Biochem Biophys Res Commun 334:1191–1197
58. Mattapallil MJ, Wawrousek EF, Chan CC, Zhao H, Roychoudhury J, Ferguson TA, Caspi RR (2012) The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6 N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes. Invest Ophthalmol Vis Sci 53:2921–2927
59. Ménoret S, Fontanière S, Jantz D, Tesson L, Thinard R, Rémy S, Usal C, Ouisse LH, Fraichard A, Anegon I (2013) Generation of Rag1-knockout immunodeficient rats and mice using engineered meganucleases. FASEB J 27:703–711
60. Meyer M, de Angelis MH, Wurst W, Kühn R (2010) Gene targeting by homologous recombination in mouse zygotes mediated by zinc-finger nucleases. Proc Natl Acad Sci USA 107:15022–15026
61. Mojica FJ, Montoliu L (2016) On the origin of CRISPR-Cas technology: from prokaryotes to mammals. Trends Microbiol 24:811–820
62. Mussolino C, Cathomen T (2012) TALE nucleases: tailored genome engineering made easy. Curr Opin Biotechnol 23:644–650
63. Nelson CE, Hakim CH, Ousterout DG, Thakore PI, Moreb EA, Castellanos Rivera RM, Madhavan S, Pan X, Ran FA, Yan WX, Asokan A, Zhang F, Duan D, Gersbach CA (2016) In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351:403–407
64. Ni W, Qiao J, Hu S, Zhao X, Regouski M, Yang M, Polejaeva IA, Chen C (2014) Efficient gene knockout in goats using CRISPR/Cas9 system. PLoS ONE 9:e106718
65. Niemann H, Petersen B (2016) The production of multi-transgenic pigs: update and perspectives for xenotransplantation. Transgenic Res 25:361–374
66. Osborn MJ, Starker CG, McElroy AN, Webber BR, Riddle MJ, Xia L, DeFeo AP, Gabriel R, Schmidt M, von Kalle C, Carlson DF, Maeder ML, Joung JK, Wagner JE, Voytas DF, Blazar BR, Tolar J (2013) TALEN-based gene correction for epidermolysis bullosa. Mol Ther 21:1151–1159
67. Overlack N, Goldmann T, Wolfrum U, Nagel-Wolfrum K (2012) Gene repair of an Usher syndrome causing mutation by zinc-fingernuclease mediated homologous recombination. Invest Ophthalmol Vis Sci 53:4140–4146
68. Pan FC, Chen Y, Loeber J, Henningfeld K, Pieler T (2006) I-SceI meganuclease-mediated transgenesis in Xenopus. Dev Dyn 235:247–252
69. Panda SK, Wefers B, Ortiz O, Floss T, Schmid B, Haass C, Wurst W, Kühn R (2013) Highly efficient targeted mutagenesis in mice using TALENs. Genetics 195:703–713
70. Park KE, Kaucher AV, Powell A, Waqas MS, Sandmaier SE, Oatley MJ, Park CH, Tibary A, Donovan DM, Blomberg LA, Lillico SG, Whitelaw CB, Mileham A, Telugu BP, Oatley JM (2017) Generation of germline ablated male pigs by CRISPR/Cas9 editing of the NANOS2 gene. Sci Rep 7:40176
71. 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, 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
72. Periwal V (2016) A comprehensive overview of computational resources to aid in precision genome editing with engineered nucleases. Brief Bioinform bbw052
73. Petersen B, Niemann H (2015) Advances in genetic modification of farm animals using zinc-finger nucleases (ZFN). Chromosome Res 23:7–15
74. Platt RJ, Chen S, Zhou Y, Yim MJ, Swiech L, Kempton HR, Dahlman JE, Parnas O, Eisenhaure TM, Jovanovic M, Graham DB, Jhunjhunwala S, Heidenreich M, Xavier RJ, Langer R, Anderson DG, Hacohen N, Regev A, Feng G, Sharp PA, Zhang F (2014) CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell 159:440–455
75. Porteus M (2008) Design and testing of zinc finger nucleases for use in mammalian cells. Methods Mol Biol 435:47–61
76. Proudfoot C, Carlson DF, Huddart R, Long CR, Pryor JH, King TJ, Lillico SG, Mileham AJ, McLaren DG, Whitelaw CB, Fahrenkrug SC (2015) Genome edited sheep and cattle. Transgenic Res 24:147–153
77. 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, Cui W (2015) Targeted mutations in myostatin by zinc-finger nucleases result in double-muscled phenotype in Meishan pigs. Sci Rep 5:14435
78. Radecke S, Radecke F, Cathomen T, Schwarz K (2010) Zinc-finger nuclease-induced gene repair with oligodeoxynucleotides: wanted and unwanted target locus modifications. Mol Ther 18:743–753
79. Ramalingam S, Annaluru N, Kandavelou K, Chandrasegaran S (2014) TALEN-mediated generation and genetic correction of disease-specific human induced pluripotent stem cells. Curr Gene Ther 14:461–472
80. Rémy S, Tesson L, Ménoret S, Usal C, Scharenberg AM, Anegon I (2010) Zinc-finger nucleases: a powerful tool for genetic engineering of animals. Transgenic Res 19:363–371
81. Sakuma T, Yamamoto T (2016) Engineering customized TALENs using the platinum gate TALEN Kit. Methods Mol Biol 1338:61–70
82. Seruggia D, 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
83. Seruggia D, Fernández A, Cantero M, Pelczar P, Montoliu L (2015) Functional validation of mouse tyrosinase non-coding regulatory DNA elements by CRISPR-Cas9-mediated mutagenesis. Nucleic Acids Res 43:4855–4867
84. Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, Zhang F (2016) Rationally engineered Cas9 nucleases with improved specificity. Science 351:84–88
85. Smithies O, Koralewski MA, Song KY, Kucherlapati RS (1984) Homologous recombination with DNA introduced into mammalian cells. Cold Spring Harb Symp Quant Biol 49:161–170
86. Smithies O, Gregg RG, Boggs SS, Koralewski MA, Kucherlapati RS (1985) Insertion of DNA sequences into the human chromosomal beta-globin locus by homologous recombination. Nature 317:230–234
87. Sung YH, Baek IJ, Kim DH, Jeon J, Lee J, Lee K, Jeong D, Kim JS, Lee HW (2013) Knockout mice created by TALEN-mediated gene targeting. Nat Biotechnol 31:23–24
88. Suzuki K, Tsunekawa Y, Hernandez-Benitez R, Wu J, Zhu J, Kim EJ, Hatanaka F, Yamamoto M, Araoka T, Li Z, Kurita M, Hishida T, Li M, Aizawa E, Guo S, Chen S, Goebl A, Soligalla RD, Qu J, Jiang T, Fu X, Jafari M, Esteban CR, Berggren WT, Lajara J, Nuñez-Delicado E, Guillen P, Campistol JM, Matsuzaki F, Liu GH, Magistretti P, Zhang K, Callaway EM, Zhang K, Belmonte JC (2016) In vivo genome editing via CRISPR/Cas9 mediated homology-independent targeted integration. Nature 540:144–149
89. Swarthout JT, Raisinghani M, Cui X (2011) Zinc finger nucleases: a new era for transgenic animals. Ann Neurosci 18:25–28
90. Tan W, Carlson DF, Lancto CA, Garbe JR, Webster DA, Hackett PB, Fahrenkrug SC (2013) Efficient nonmeiotic allele introgression in livestock using custom endonucleases. Proc Natl Acad Sci USA 110:16526–16531
91. Tan W, Proudfoot C, Lillico SG, Whitelaw CB (2016) Gene targeting, genome editing: from Dolly to editors. Transgenic Res 25:273–287
92. Tebas P, Stein D, Tang WW, Frank I, Wang SQ, Lee G, Spratt SK, Surosky RT, Giedlin MA, Nichol G, Holmes MC, Gregory PD, Ando DG, Kalos M, Collman RG, Binder-Scholl G, Plesa G, Hwang WT, Levine BL, June CH (2014) Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N Engl J Med 370:901–910
93. Tesson L, Usal C, Ménoret S, Leung E, Niles BJ, Remy S, Santiago Y, Vincent AI, Meng X, Zhang L, Gregory PD, Anegon I, Cost GJ (2011) Knockout rats generated by embryo microinjection of TALENs. Nat Biotechnol 29:695–696
94. Thermes V, Grabher C, Ristoratore F, Bourrat F, Choulika A, Wittbrodt J, Joly JS (2002) I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech Dev 118:91–98
95. Urnov FD, Miller JC, Lee YL, Beausejour CM, Rock JM, Augustus S, Jamieson AC, Porteus MH, Gregory PD, Holmes MC (2005) Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435:646–651
96. Wang Z (2015) Genome engineering in cattle: recent technological advancements. Chromosome Res 23(1):17–29
97. Wang H, Hu YC, Markoulaki S, Welstead GG, Cheng AW, Shivalila CS, Pyntikova T, Dadon DB, Voytas DF, Bogdanove AJ, Page DC, Jaenisch R (2013a) TALEN-mediated editing of the mouse Y chromosome. Nat Biotechnol 31:530–532
98. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R (2013b) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153:910–918
99. Wang Y, Zhou XY, Xiang PY, Wang LL, Tang H, Xie F, Li L, Wei H (2014) The meganuclease I-SceI containing nuclear localization signal (NLS-I-SceI) efficiently mediated mammalian germline transgenesis via embryo cytoplasmic microinjection. PLoS ONE 9:e108347
100. 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, Chen Y (2015) Generation of gene-modified goats targeting MSTN and FGF5 via zygote injection of CRISPR/Cas9 system. Sci Rep 5:13878
101. 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, Zhao J (2016) One-step generation of triple gene-targeted pigs using CRISPR/Cas9 system. Sci Rep 6:20620
102. Wefers B, Panda SK, Ortiz O, Brandl C, Hensler S, Hansen J, Wurst W, Kühn R (2013) Generation of targeted mouse mutants by embryo microinjection of TALEN mRNA. Nat Protoc 8:2355–2379
103. Wei J, Wagner S, Lu D, Maclean P, Carlson DF, Fahrenkrug SC, Laible G (2015) Efficient introgression of allelic variants by embryo-mediated editing of the bovine genome. Sci Rep 5:11735
104. Whitelaw CB, Sheets TP, Lillico SG, Telugu BP (2016) Engineering large animal models of human disease. J Pathol 238:247–256
105. Wu H, Wang Y, Zhang Y, Yang M, Lv J, Liu J, Zhang Y (2015) TALE nickase-mediated SP110 knockin endows cattle with increased resistance to tuberculosis. Proc Natl Acad Sci USA 112:E1530–E1539
106. Wu J, Platero-Luengo A, Sakurai M, Sugawara A, Gil MA, Yamauchi T, Suzuki K, Bogliotti YS, Cuello C, Morales Valencia M, Okumura D, Luo J, Vilariño M, Parrilla I, Soto DA, Martinez CA, Hishida T, Sánchez-Bautista S, Martinez-Martinez ML, Wang H, Nohalez A, Aizawa E, Martinez-Redondo P, Ocampo A, Reddy P, Roca J, Maga EA, Esteban CR, Berggren WT, Nuñez Delicado E, Lajara J, Guillen I, Guillen P, Campistol JM, Martinez EA, Ross PJ, Izpisua Belmonte JC (2017) Interspecies chimerism with mammalian pluripotent stem cells. Cell 168:473–486
107. Xiao A, Wang Z, Hu Y, Wu Y, Luo Z, Yang Z, Zu Y, Li W, Huang P, Tong X, Zhu Z, Lin S, Zhang B (2013) Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish. Nucleic Acids Res 41:e141
108. 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, Lai L (2013) Highly efficient generation of GGTA1 biallelic knockout inbred mini-pigs with TALENs. PLoS ONE 8:e84250
109. Yang H, Wang H, Shivalila CS, Cheng AW, Shi L, Jaenisch R (2013) One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154:1370–1379
110. Yang L, Güell M, Niu D, George H, Lesha E, Grishin D, Aach J, Shrock E, Xu W, Poci J, Cortazio R, Wilkinson RA, Fishman JA, Church G (2015) Genome-wide inactivation of porcine endogenous retroviruses (PERVs). Science 350:1101–1104
111. Yin H, Song CQ, Dorkin JR, Zhu LJ, Li Y, Wu Q, Park A, Yang J, Suresh S, Bizhanova A, Gupta A, Bolukbasi MF, Walsh S, Bogorad RL, Gao G, Weng Z, Dong Y, Koteliansky V, Wolfe SA, Langer R, Xue W, Anderson DG (2016) Therapeutic genome editing by combined viral and non-viral delivery of CRISPR system components in vivo. Nat Biotechnol 34:328–333
112. Yu S, Luo J, Song Z, Ding F, Dai Y, Li N (2011) Highly efficient modification of beta-lactoglobulin (BLG) gene via zinc-finger nucleases in cattle. Cell Res 21:1638–1640
113. Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, van der Oost J, Regev A, Koonin EV, Zhang F (2015) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:759–771
114. Zhang L, Jia R, Palange NJ, Satheka AC, Togo J, An Y, Jin H, Feng X, Zheng Y (2015) Large genomic fragment deletions and insertions in mouse using CRISPR/Cas9. PLoS ONE 10:e0120396