The development and application of genome editing technology in ruminants: a review

doi:10.15302/J-FASE-2019302

Front. Agr. Sci. Eng.

2020, Vol. 7

Issue (2) : 171-180 https://doi.org/10.15302/J-FASE-2019302

REVIEW

The development and application of genome editing technology in ruminants: a review

Mengke YUAN^1,², Yuanpeng GAO^1,², Jing HAN^1,², Teng WU^1,², Jingcheng ZHANG^1,², Yongke WEI^1,², Yong ZHANG^1,²(

)

¹. College of Veterinary Medicine, Northwest A&F University, Yangling 712100, China
². Key Laboratory of Animal Biotechnology (Ministry of Agriculture), Northwest A&F University, Yangling 712100, China

Download: PDF(416 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

Transgenic ruminants are a valuable resource for both animal breeding and biomedical research. The development of transgenic breeding is proceeding slowly, because it suffers from low efficiency of gene transfer and possible safety problems from uncontrolled random integration. However, new breeding methods combined with genome editing and somatic cell nuclear transfer or microinjection can offer an economic and efficient way to produce gene-edited ruminants, which can serve as bioreactors or have improved disease resistance, animal welfare and product quality. Recent advances in precise genome editing technologies, especially clustered regularly interspaced short palindromic repeat (CRISPR)/Cas9 nucleases, are enabling the systematic development of gene-edited ruminant production. This review covers the development of gene-edited ruminants, the particulars of site-specific engineered nucleases and the state of the art and new insights into practical applications and social acceptance of genome editing technology in ruminants. It is concluded that the production of gene-edited ruminants is feasible and through improvements in genome editing technology it is possible to help feed the world.

Keywords bioreactors breeding engineered endonucleases genome editing ruminants

Corresponding Author(s): Yong ZHANG

Just Accepted Date: 19 December 2019 Online First Date: 13 January 2020 Issue Date: 28 April 2020

Cite this article:

Mengke YUAN,Yuanpeng GAO,Jing HAN, et al. The development and application of genome editing technology in ruminants: a review[J]. Front. Agr. Sci. Eng. , 2020, 7(2): 171-180.

URL:

https://academic.hep.com.cn/fase/EN/10.15302/J-FASE-2019302
https://academic.hep.com.cn/fase/EN/Y2020/V7/I2/171

Fig.1 Simplified diagram of the two methods for generating gene-edited cows via somatic cell nuclear transfer (SCNT) (a, b) and microinjection (c). OPU, ovum pick-up; GV, germinal vesicle; MII, metaphase II.

Tab.1 Advantages and disadvantages of somatic cell nuclear transfer (SCNT) and microinjection technology for gene-edited cows

Tab.2 Application of genome editing in ruminants

1	Y Gao, H Wu, Y Wang, X Liu, L Chen, Q Li, C Cui, X Liu, J Zhang, Y Zhang. Single Cas9 nickase induced generation of NRAMP1 knockin cattle with reduced off-target effects. Genome Biology, 2017, 18(1): 13 https://doi.org/10.1186/s13059-016-1144-4 pmid: 28143571
2	X Miao. Recent advances in the development of new transgenic animal technology. Cellular and Molecular Life Sciences, 2013, 70(5): 815–828 https://doi.org/10.1007/s00018-012-1081-7 pmid: 22833168
3	D F Carlson, C A Lancto, B Zang, E S Kim, M Walton, D Oldeschulte, C Seabury, T S Sonstegard, S C Fahrenkrug. Production of hornless dairy cattle from genome-edited cell lines. Nature Biotechnology, 2016, 34(5): 479–481 https://doi.org/10.1038/nbt.3560 pmid: 27153274
4	J Luo, Z Song, S Yu, D Cui, B Wang, F Ding, S Li, Y Dai, N Li. Efficient generation of myostatin (MSTN) biallelic mutations in cattle using zinc finger nucleases. PLoS One, 2014, 9(4): e95225 https://doi.org/10.1371/journal.pone.0095225 pmid: 24743319
5	R E Hammer, V G Pursel, C E Rexroad Jr, R J Wall, D J Bolt, K M Ebert, R D Palmiter, R L Brinster. Production of transgenic rabbits, sheep and pigs by microinjection. Nature, 1985, 315(6021): 680–683 https://doi.org/10.1038/315680a0 pmid: 3892305
6	S G Lillico, C Proudfoot, D F Carlson, D Stverakova, C Neil, C Blain, T J King, W A Ritchie, W Tan, A J Mileham, D G McLaren, S C Fahrenkrug, C B A Whitelaw. Live pigs produced from genome edited zygotes. Scientific Reports, 2013, 3(1): 2847 https://doi.org/10.1038/srep02847 pmid: 24108318
7	H Wu, Y Wang, Y Zhang, M Yang, J Lv, J Liu, Y Zhang. TALE nickase-mediated SP110 knockin endows cattle with increased resistance to tuberculosis. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(13): E1530–E1539 https://doi.org/10.1073/pnas.1421587112 pmid: 25733846
8	M R Capecchi. How close are we to implementing gene targeting in animals other than the mouse? Proceedings of the National Academy of Sciences of the United States of America, 2000, 97(3): 956–957 https://doi.org/10.1073/pnas.97.3.956 pmid: 10655465
9	A Baguisi, E Behboodi, D T Melican, J S Pollock, M M Destrempes, C Cammuso, J L Williams, S D Nims, C A Porter, P Midura, M J Palacios, S L Ayres, R S Denniston, M L Hayes, C A Ziomek, H M Meade, R A Godke, W G Gavin, E W Overström, Y Echelard. Production of goats by somatic cell nuclear transfer. Nature Biotechnology, 1999, 17(5): 456–461 https://doi.org/10.1038/8632 pmid: 10331804
10	J B Cibelli, S L Stice, P J Golueke, J J Kane, J Jerry, C Blackwell, F A Ponce de León, J M Robl. Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science, 1998, 280(5367): 1256–1258 https://doi.org/10.1126/science.280.5367.1256 pmid: 9596577
11	Y Kato, T Tani, Y Sotomaru, K Kurokawa, J Kato, H Doguchi, H Yasue, Y Tsunoda. Eight calves cloned from somatic cells of a single adult. Science, 1998, 282(5396): 2095–2098 https://doi.org/10.1126/science.282.5396.2095 pmid: 9851933
12	I Wilmut, A E Schnieke, J McWhir, A J Kind, K H S Campbell. Viable offspring derived from fetal and adult mammalian cells. Nature, 1997, 385(6619): 810–813 https://doi.org/10.1038/385810a0 pmid: 9039911
13	A E Schnieke, A J Kind, W A Ritchie, K Mycock, A R Scott, M Ritchie, I Wilmut, A Colman, K H S Campbell. Human factor IX transgenic sheep produced by transfer of nuclei from transfected fetal fibroblasts. Science, 1997, 278(5346): 2130–2133 https://doi.org/10.1126/science.278.5346.2130 pmid: 9405350
14	L C Garas, J D Murray, E A Maga. Genetically engineered livestock: ethical use for food and medical models. Annual Review of Animal Biosciences, 2015, 3(1): 559–575 https://doi.org/10.1146/annurev-animal-022114-110739 pmid: 25387117
15	P D Hsu, E S Lander, F Zhang. Development and applications of CRISPR-Cas9 for genome engineering. Cell, 2014, 157(6): 1262–1278 https://doi.org/10.1016/j.cell.2014.05.010 pmid: 24906146
16	T Gaj, C A Gersbach, C F Barbas 3rd. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends in Biotechnology, 2013, 31(7): 397–405 https://doi.org/10.1016/j.tibtech.2013.04.004 pmid: 23664777
17	A Kawahara, Y Hisano, S Ota, K Taimatsu. Site-specific integration of exogenous genes using genome editing technologies in zebrafish. International Journal of Molecular Sciences, 2016, 17(5): 727 https://doi.org/10.3390/ijms17050727 pmid: 27187373
18	K H Campbell, J McWhir, W A Ritchie, I Wilmut. Sheep cloned by nuclear transfer from a cultured cell line. Nature, 1996, 380(6569): 64–66 https://doi.org/10.1038/380064a0 pmid: 8598906
19	C B A Whitelaw, T P Sheets, S G Lillico, B P Telugu. Engineering large animal models of human disease. Journal of Pathology, 2016, 238(2): 247–256 https://doi.org/10.1002/path.4648 pmid: 26414877
20	K J McCreath, J Howcroft, K H S Campbell, A Colman, A E Schnieke, A J Kind. Production of gene-targeted sheep by nuclear transfer from cultured somatic cells. Nature, 2000, 405(6790): 1066–1069 https://doi.org/10.1038/35016604 pmid: 10890449
21	J San Filippo, P Sung, H Klein. Mechanism of eukaryotic homologous recombination. Annual Review of Biochemistry, 2008, 77(1): 229–257 https://doi.org/10.1146/annurev.biochem.77.061306.125255 pmid: 18275380
22	S Yu, J Luo, Z Song, F Ding, Y Dai, N Li. Highly efficient modification of β-lactoglobulin (BLG) gene via zinc-finger nucleases in cattle. Cell Research, 2011, 21(11): 1638–1640 https://doi.org/10.1038/cr.2011.153 pmid: 21912434
23	Z Sun, M Wang, S Han, S Ma, Z Zou, F Ding, X Li, L Li, B Tang, H Wang, N Li, H Che, Y Dai. Production of hypoallergenic milk from DNA-free β-lactoglobulin (BLG) gene knockout cow using zinc-finger nucleases mRNA. Scientific Reports, 2018, 8(1): 15430 https://doi.org/10.1038/s41598-018-32024-x pmid: 30337546
24	W Ni, J Qiao, S Hu, X Zhao, M Regouski, M Yang, I A Polejaeva, C Chen. Efficient gene knockout in goats using CRISPR/Cas9 system. PLoS One, 2014, 9(9): e106718 https://doi.org/10.1371/journal.pone.0106718 pmid: 25188313
25	W Zhou, Y Wan, R Guo, M Deng, K Deng, Z Wang, Y Zhang, F Wang. Generation of β-lactoglobulin knock-out goats using CRISPR/Cas9. PLoS One, 2017, 12(10): e0186056 https://doi.org/10.1371/journal.pone.0186056 pmid: 29016691
26	J Wei, S Wagner, P Maclean, B Brophy, S Cole, G Smolenski, D F Carlson, S C Fahrenkrug, D N Wells, G Laible. Cattle with a precise, zygote-mediated deletion safely eliminate the major milk allergen β-lactoglobulin. Scientific Reports, 2018, 8(1): 7661 https://doi.org/10.1038/s41598-018-25654-8 pmid: 29769555
27	X Liu, Y Wang, W Guo, B Chang, J Liu, Z Guo, F Quan, Y Zhang. Zinc-finger nickase-mediated insertion of the lysostaphin gene into the β-casein locus in cloned cows. Nature Communications, 2013, 4(1): 2565 https://doi.org/10.1038/ncomms3565 pmid: 24121612
28	P Rouet, F Smih, M Jasin. Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. Proceedings of the National Academy of Sciences of the United States of America, 1994, 91(13): 6064–6068 https://doi.org/10.1073/pnas.91.13.6064 pmid: 8016116
29	J D Murray, E A Maga. Genetically engineered livestock for agriculture: a generation after the first transgenic animal research conference. Transgenic Research, 2016, 25(3): 321–327 https://doi.org/10.1007/s11248-016-9927-7 pmid: 26820413
30	L Li, L P Wu, S Chandrasegaran. Functional domains in Fok I restriction endonuclease. Proceedings of the National Academy of Sciences of the United States of America, 1992, 89(10): 4275–4279 https://doi.org/10.1073/pnas.89.10.4275 pmid: 1584761
31	N P Pavletich, C O Pabo. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science, 1991, 252(5007): 809–817 https://doi.org/10.1126/science.2028256 pmid: 2028256
32	J K Joung, J D Sander. TALENs: a widely applicable technology for targeted genome editing. Nature Reviews. Molecular Cell Biology, 2013, 14(1): 49–55 https://doi.org/10.1038/nrm3486 pmid: 23169466
33	E M Händel, S Alwin, T Cathomen. Expanding or restricting the target site repertoire of zinc-finger nucleases: the inter-domain linker as a major determinant of target site selectivity. Molecular Therapy, 2009, 17(1): 104–111 https://doi.org/10.1038/mt.2008.233 pmid: 19002164
34	J He, Q Li, S Fang, Y Guo, T Liu, J Ye, Z Yu, R Zhang, Y Zhao, X Hu, X Bai, X Chen, N Li. PKD1 mono-allelic knockout is sufficient to trigger renal cystogenesis in a mini-pig model. International Journal of Biological Sciences, 2015, 11(4): 361–369 https://doi.org/10.7150/ijbs.10858 pmid: 25798056
35	C Cui, Y Song, J Liu, H Ge, Q Li, H Huang, L Hu, H Zhu, Y Jin, Y Zhang. Gene targeting by TALEN-induced homologous recombination in goats directs production of β-lactoglobulin-free, high-human lactoferrin milk. Scientific Reports, 2015, 5(1): 10482 https://doi.org/10.1038/srep10482 pmid: 25994151
36	F E Moore, D Reyon, J D Sander, S A Martinez, J S Blackburn, C Khayter, C L Ramirez, J K Joung, D M Langenau. Improved somatic mutagenesis in zebrafish using transcription activator-like effector nucleases (TALENs). PLoS One, 2012, 7(5): e37877 https://doi.org/10.1371/journal.pone.0037877 pmid: 22655075
37	A Xiao, Y Wu, Z Yang, Y Hu, W Wang, Y Zhang, L Kong, G Gao, Z Zhu, S Lin, B Zhang. EENdb: a database and knowledge base of ZFNs and TALENs for endonuclease engineering. Nucleic Acids Research, 2013, 41(Database Issue): D415–D422 pmid: 23203870
38	L Cade, D Reyon, W Y Hwang, S Q Tsai, S Patel, C Khayter, J K Joung, J D Sander, R T Peterson, J R J Yeh. Highly efficient generation of heritable zebrafish gene mutations using homo- and heterodimeric TALENs. Nucleic Acids Research, 2012, 40(16): 8001–8010 https://doi.org/10.1093/nar/gks518 pmid: 22684503
39	V Pattanayak, C L Ramirez, J K Joung, D R Liu. Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection. Nature Methods, 2011, 8(9): 765–770 https://doi.org/10.1038/nmeth.1670 pmid: 21822273
40	R Gabriel, A Lombardo, A Arens, J C Miller, P Genovese, C Kaeppel, A Nowrouzi, C C Bartholomae, J Wang, G Friedman, M C Holmes, P D Gregory, H Glimm, M Schmidt, L Naldini, C von Kalle. An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nature Biotechnology, 2011, 29(9): 816–823 https://doi.org/10.1038/nbt.1948 pmid: 21822255
41	J Grau, J Boch, S Posch. TALENoffer: genome-wide TALEN off-target prediction. Bioinformatics, 2013, 29(22): 2931–2932 https://doi.org/10.1093/bioinformatics/btt501 pmid: 23995255
42	E J Sontheimer, R Barrangou. The bacterial origins of the CRISPR genome-editing revolution. Human Gene Therapy, 2015, 26(7): 413–424 https://doi.org/10.1089/hum.2015.091 pmid: 26078042
43	E Deltcheva, K Chylinski, C M Sharma, K Gonzales, Y Chao, Z A Pirzada, M R Eckert, J Vogel, E Charpentier. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature, 2011, 471(7340): 602–607 https://doi.org/10.1038/nature09886 pmid: 21455174
44	M Jinek, K Chylinski, I Fonfara, M Hauer, J A Doudna, E Charpentier. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 2012, 337(6096): 816–821 https://doi.org/10.1126/science.1225829 pmid: 22745249
45	M F Bolukbasi, A Gupta, S A Wolfe. Creating and evaluating accurate CRISPR-Cas9 scalpels for genomic surgery. Nature Methods, 2016, 13(1): 41–50 https://doi.org/10.1038/nmeth.3684 pmid: 26716561
46	L Cong, F A Ran, D Cox, S Lin, R Barretto, N Habib, P D Hsu, X Wu, W Jiang, L A Marraffini, F Zhang. Multiplex genome engineering using CRISPR/Cas systems. Science, 2013, 339(6121): 819–823 https://doi.org/10.1126/science.1231143 pmid: 23287718
47	P Mali, L Yang, K M Esvelt, J Aach, M Guell, J E DiCarlo, J E Norville, G M Church. RNA-guided human genome engineering via Cas9. Science, 2013, 339(6121): 823–826 https://doi.org/10.1126/science.1232033 pmid: 23287722
48	T Ma, J Tao, M Yang, C He, X Tian, X Zhang, J Zhang, S Deng, J Feng, Z Zhang, J Wang, P Ji, Y Song, P He, H Han, J Fu, Z Lian, G Liu. An AANAT/ASMT transgenic animal model constructed with CRISPR/Cas9 system serving as the mammary gland bioreactor to produce melatonin-enriched milk in sheep. Journal of Pineal Research, 2017, 63(1): e12406 https://doi.org/10.1111/jpi.12406 pmid: 28273380
49	J A Richt, P Kasinathan, A N Hamir, J Castilla, T Sathiyaseelan, F Vargas, J Sathiyaseelan, H Wu, H Matsushita, J Koster, S Kato, I Ishida, C Soto, J M Robl, Y Kuroiwa. Production of cattle lacking prion protein. Nature Biotechnology, 2007, 25(1): 132–138 https://doi.org/10.1038/nbt1271 pmid: 17195841
50	C Denning, S Burl, A Ainslie, J Bracken, A Dinnyes, J Fletcher, T King, M Ritchie, W A Ritchie, M Rollo, P de Sousa, A Travers, I Wilmut, A J Clark. Deletion of the α(1,3)galactosyl transferase (GGTA1) gene and the prion protein (PrP) gene in sheep. Nature Biotechnology, 2001, 19(6): 559–562 https://doi.org/10.1038/89313 pmid: 11385461
51	S Shanthalingam, A Tibary, J E Beever, P Kasinathan, W C Brown, S Srikumaran. Precise gene editing paves the way for derivation of Mannheimia haemolytica leukotoxin-resistant cattle. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(46): 13186–13190 https://doi.org/10.1073/pnas.1613428113 pmid: 27799556
52	J Zhang, M L Cui, Y W Nie, B Dai, F R Li, D J Liu, H Liang, M Cang. CRISPR/Cas9-mediated specific integration of fat-1 at the goat MSTN locus. FEBS Journal, 2018, 285(15): 2828–2839 https://doi.org/10.1111/febs.14520 pmid: 29802684
53	Y Zhang, Y Wang, B Yulin, B Tang, M Wang, C Zhang, W Zhang, J Jin, T Li, R Zhao, X Yu, Q Zuo, B Li. CRISPR/Cas9-mediated sheep MSTN gene knockout and promote sSMSCs differentiation. Journal of Cellular Biochemistry, 2018, 120(2): 1794–1806 https://doi.org/10.1002/jcb.27474 pmid: 30242885
54	L R Bertolini, H Meade, C R Lazzarotto, L T Martins, K C Tavares, M Bertolini, J D Murray. The transgenic animal platform for biopharmaceutical production. Transgenic Research, 2016, 25(3): 329–343 https://doi.org/10.1007/s11248-016-9933-9 pmid: 26820414
55	L M Houdebine. Production of pharmaceutical proteins by transgenic animals. Comparative Immunology, Microbiology and Infectious Diseases, 2009, 32(2): 107–121 https://doi.org/10.1016/j.cimid.2007.11.005 pmid: 18243312
56	M Yamasaki, T J Sendall, M C Pearce, J C Whisstock, J A Huntington. Molecular basis of α1-antitrypsin deficiency revealed by the structure of a domain-swapped trimer. EMBO Reports, 2011, 12(10): 1011–1017 https://doi.org/10.1038/embor.2011.171 pmid: 21909074
57	B Wang, H Baldassarre, T Tao, M Gauthier, N Neveu, J F Zhou, M Leduc, F Duguay, A S Bilodeau, A Lazaris, C Keefer, C N Karatzas. Transgenic goats produced by DNA pronuclear microinjection of in vitro derived zygotes. Molecular Reproduction and Development, 2002, 63(4): 437–443 https://doi.org/10.1002/mrd.10199 pmid: 12412045
58	D Esslemont, M Kossaibati. Mastitis: how to get out of the dark ages. Veterinary Journal, 2002, 164(2): 85–86 https://doi.org/10.1053/tvjl.2002.0742 pmid: 12359461
59	P Rainard. Tackling mastitis in dairy cows. Nature Biotechnology, 2005, 23(4): 430–432 https://doi.org/10.1038/nbt0405-430 pmid: 15815667
60	R J Wall, A M Powell, M J Paape, D E Kerr, D D Bannerman, V G Pursel, K D Wells, N Talbot, H W Hawk. Genetically enhanced cows resist intramammary Staphylococcus aureus infection. Nature Biotechnology, 2005, 23(4): 445–451 https://doi.org/10.1038/nbt1078 pmid: 15806099
61	E R Oldham, M J Daley. Lysostaphin: use of a recombinant bactericidal enzyme as a mastitis therapeutic. Journal of Dairy Science, 1991, 74(12): 4175–4182 https://doi.org/10.3168/jds.S0022-0302(91)78612-8 pmid: 1787188
62	S E Lloyd, S Mead, J Collinge. Genetics of prion diseases. Current Opinion in Genetics & Development, 2013, 23(3): 345–351 https://doi.org/10.1016/j.gde.2013.02.012 pmid: 23518043
63	G A Wells, A C Scott, C T Johnson, R F Gunning, R D Hancock, M Jeffrey, M Dawson, R Bradley. A novel progressive spongiform encephalopathy in cattle. Veterinary Record, 1987, 121(18): 419–420 https://doi.org/10.1136/vr.121.18.419 pmid: 3424605
64	M Jeffrey, L González. Classical sheep transmissible spongiform encephalopathies: pathogenesis, pathological phenotypes and clinical disease. Neuropathology and Applied Neurobiology, 2007, 33(4): 373–394 https://doi.org/10.1111/j.1365-2990.2007.00868.x pmid: 17617870
65	P Aguilar-Calvo, C García, J C Espinosa, O Andreoletti, J M Torres. Prion and prion-like diseases in animals. Virus Research, 2015, 207: 82–93 https://doi.org/10.1016/j.virusres.2014.11.026 pmid: 25444937
66	S B Prusiner, D Groth, A Serban, R Koehler, D Foster, M Torchia, D Burton, S L Yang, S J DeArmond. Ablation of the prion protein (PrP) gene in mice prevents scrapie and facilitates production of anti-PrP antibodies. Proceedings of the National Academy of Sciences of the United States of America, 1993, 90(22): 10608–10612 https://doi.org/10.1073/pnas.90.22.10608 pmid: 7902565
67	M A Breider, R D Walker, F M Hopkins, T W Schultz, T L Bowersock. Pulmonary lesions induced by Pasteurella haemolytica in neutrophil sufficient and neutrophil deficient calves. Canadian Journal of Veterinary Research, 1988, 52(2): 205–209 pmid: 3370555
68	M L Mueller, J B Cole, T S Sonstegard, A L Van Eenennaam. Comparison of gene editing versus conventional breeding to introgress the POLLED allele into the US dairy cattle population. Journal of Dairy Science, 2019, 102(5): 4215–4226 https://doi.org/10.3168/jds.2018-15892 pmid: 30852022
69	A Regalado. Gene-edited cattle have a major screwup in their DNA. MIT Technology Review, 2019 [Published Online]
70	L A Norris, S S Lee, K J Greenlees, D A Tadesse, M F Miller, H Lombard. Template plasmid integration in germline genome-edited cattle. BioRxiv, 2019 [Published Online] doi:10.1101/715482
71	B P Kleinstiver, V Pattanayak, M S Prew, S Q Tsai, N T Nguyen, Z Zheng, J K Joung. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature, 2016, 529(7587): 490–495 https://doi.org/10.1038/nature16526 pmid: 26735016
72	I M Slaymaker, L Gao, B Zetsche, D A Scott, W X Yan, F Zhang. Rationally engineered Cas9 nucleases with improved specificity. Science, 2016, 351(6268): 84–88 https://doi.org/10.1126/science.aad5227 pmid: 26628643
73	S Q Tsai, N T Nguyen, J Malagon-Lopez, V V Topkar, M J Aryee, J K Joung. CIRCLE-seq: a highly sensitive in vitro screen for genome-wide CRISPR-Cas9 nuclease off-targets. Nature Methods, 2017, 14(6): 607–614 https://doi.org/10.1038/nmeth.4278 pmid: 28459458
74	S Q Tsai, Z Zheng, N T Nguyen, M Liebers, V V Topkar, V Thapar, N Wyvekens, C Khayter, A J Iafrate, L P Le, M J Aryee, J K Joung. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nature Biotechnology, 2015, 33(2): 187–197 https://doi.org/10.1038/nbt.3117 pmid: 25513782
75	B M Ehn, B Ekstrand, U Bengtsson, S Ahlstedt. Modification of IgE binding during heat processing of the cow’s milk allergen β-lactoglobulin. Journal of Agricultural and Food Chemistry, 2004, 52(5): 1398–1403 https://doi.org/10.1021/jf0304371 pmid: 14995152
76	B M Ehn, T Allmere, E Telemo, U Bengtsson, B Ekstrand. Modification of IgE binding to β-lactoglobulin by fermentation and proteolysis of cow’s milk. Journal of Agricultural and Food Chemistry, 2005, 53(9): 3743–3748 https://doi.org/10.1021/jf048121w pmid: 15853429
77	L Grobet, L J Martin, D Poncelet, D Pirottin, B Brouwers, J Riquet, A Schoeberlein, S Dunner, F Ménissier, J Massabanda, R Fries, R Hanset, M Georges. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nature Genetics, 1997, 17(1): 71–74 https://doi.org/10.1038/ng0997-71 pmid: 9288100
78	A Dove. Milking the genome for profit. Nature Biotechnology, 2000, 18(10): 1045–1048 https://doi.org/10.1038/80231 pmid: 11017040
79	B Brophy, G Smolenski, T Wheeler, D Wells, P L’Huillier, G Laible. Cloned transgenic cattle produce milk with higher levels of β-casein and κ-casein. Nature Biotechnology, 2003, 21(2): 157–162 https://doi.org/10.1038/nbt783 pmid: 12548290
80	A Colman. Somatic cell nuclear transfer in mammals: progress and applications. Cloning, 1999–2000, 1(4): 185–200 https://doi.org/10.1089/15204559950019825 pmid: 16218819
81	J P Zhang, X L Li, G H Li, W Chen, C Arakaki, G D Botimer, D Baylink, L Zhang, W Wen, Y W Fu, J Xu, N Chun, W Yuan, T Cheng, X B Zhang. Efficient precise knockin with a double cut HDR donor after CRISPR/Cas9-mediated double-stranded DNA cleavage. Genome Biology, 2017, 18(1): 35 https://doi.org/10.1186/s13059-017-1164-8 pmid: 28219395
82	J Song, D Yang, J Xu, T Zhu, Y E Chen, J Zhang. RS-1 enhances CRISPR/Cas9- and TALEN-mediated knock-in efficiency. Nature Communications, 2016, 7(1): 10548 https://doi.org/10.1038/ncomms10548 pmid: 26817820
83	S M Kipriyanov, G Moldenhauer, M Braunagel, U Reusch, B Cochlovius, F Le Gall, O A Kouprianova, C W Von der Lieth, M Little. Effect of domain order on the activity of bacterially produced bispecific single-chain Fv antibodies. Journal of Molecular Biology, 2003, 330(1): 99–111 https://doi.org/10.1016/S0022-2836(03)00526-6 pmid: 12818205
84	M Little, S M Kipriyanov, F Le Gall, G Moldenhauer. Of mice and men: hybridoma and recombinant antibodies. Immunology Today, 2000, 21(8): 364–370 https://doi.org/10.1016/S0167-5699(00)01668-6 pmid: 10916138
85	G Walsh. Biopharmaceutical benchmarks 2014. Nature Biotechnology, 2014, 32(10): 992–1000 https://doi.org/10.1038/nbt.3040 pmid: 25299917
86	L Grosse-Hovest, S Müller, R Minoia, E Wolf, V Zakhartchenko, H Wenigerkind, C Lassnig, U Besenfelder, M Müller, S D Lytton, G Jung, G Brem. Cloned transgenic farm animals produce a bispecific antibody for T cell-mediated tumor cell killing. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(18): 6858–6863 https://doi.org/10.1073/pnas.0308487101 pmid: 15105446
87	Z Fan, I V Perisse, C U Cotton, M Regouski, Q Meng, C Domb, A J Van Wettere, Z Wang, A Harris, K L White, I A Polejaeva. A sheep model of cystic fibrosis generated by CRISPR/Cas9 disruption of the CFTR gene. JCI Insight, 2018, 3(19): e123529 https://doi.org/10.1172/jci.insight.123529 pmid: 30282831
88	D K Williams, C Pinzón, S Huggins, J H Pryor, A Falck, F Herman, J Oldeschulte, M B Chavez, B L Foster, S H White, M E Westhusin, L J Suva, C R Long, D Gaddy. Genetic engineering a large animal model of human hypophosphatasia in sheep. Scientific Reports, 2018, 8(1): 16945 https://doi.org/10.1038/s41598-018-35079-y pmid: 30446691
89	S J Du, Z Y Gong, G L Fletcher, M A Shears, M J King, D R Idler, C L Hew. Growth enhancement in transgenic Atlantic salmon by the use of an “all fish” chimeric growth hormone gene construct. Bio-Technology, 1992, 10(2): 176–181 pmid: 1368229
90	J Kling. First US approval for a transgenic animal drug. Nature Biotechnology, 2009, 27(4): 302–304 https://doi.org/10.1038/nbt0409-302 pmid: 19352350
91	H A van Veen, J Koiter, C J M Vogelezang, N van Wessel, T van Dam, I Velterop, K van Houdt, L Kupers, D Horbach, M Salaheddine, J H Nuijens, M L M Mannesse. Characterization of recombinant human C1 inhibitor secreted in milk of transgenic rabbits. Journal of Biotechnology, 2012, 162(2–3): 319–326 https://doi.org/10.1016/j.jbiotec.2012.09.005 pmid: 22995741
92	C Sheridan. FDA approves ‘farmaceutical’ drug from transgenic chickens. Nature Biotechnology, 2016, 34(2): 117–119 https://doi.org/10.1038/nbt0216-117 pmid: 26849497
93	A Bruce. Genome edited animals: learning from GM crops? Transgenic Research, 2017, 26(3): 385–398 https://doi.org/10.1007/s11248-017-0017-2 pmid: 28432545
94	T Ishii. Genome-edited livestock: ethics and social acceptance. Animal Frontiers, 2017, 7(2): 24–32 https://doi.org/10.2527/af.2017.0115
95	S Schicktanz. Ethical considerations of the human-animal-relationship under conditions of asymmetry and ambivalence. Journal of Agricultural & Environmental Ethics, 2006, 19(1): 7–16 https://doi.org/10.1007/s10806-005-4374-0

[1]	Kunling CHEN, Caixia GAO. Genome-edited crops: how to move them from laboratory to market[J]. Front. Agr. Sci. Eng. , 2020, 7(2): 181-187.
[2]	Zachariah MCLEAN, Björn OBACK, Götz LAIBLE. Embryo-mediated genome editing for accelerated genetic improvement of livestock[J]. Front. Agr. Sci. Eng. , 2020, 7(2): 148-160.
[3]	Haoyi WANG, Sen WU, Mario R. CAPECCHI, Rudolf JAENISCH. A brief review of genome editing technology for generating animal models[J]. Front. Agr. Sci. Eng. , 2020, 7(2): 123-128.
[4]	Dongdong LI, Meng WANG, Xianyan KUANG, Wenxin LIU. Genetic study and molecular breeding for high phosphorus use efficiency in maize[J]. Front. Agr. Sci. Eng. , 2019, 6(4): 366-379.
[5]	Carlos GUZMÁN, Karim AMMAR, Velu GOVINDAN, Ravi SINGH. Genetic improvement of wheat grain quality at CIMMYT[J]. Front. Agr. Sci. Eng. , 2019, 6(3): 265-272.
[6]	Hongxiang MA, Xu ZHANG, Jinbao YAO, Shunhe CHENG. *Breeding for the resistance to Fusarium* head blight of wheat in China**[J]. Front. Agr. Sci. Eng. , 2019, 6(3): 251-264.
[7]	Alexey MORGOUNOV, Fatih OZDEMIR, Mesut KESER, Beyhan AKIN, Thomas PAYNE, Hans-Joachim BRAUN. International Winter Wheat Improvement Program: history, activities, impact and future[J]. Front. Agr. Sci. Eng. , 2019, 6(3): 240-250.
[8]	Zhonghu HE, Xianchun XIA, Yong ZHANG, Yan ZHANG, Yonggui XIAO, Xinmin CHEN, Simin LI, Yuanfeng HAO, Awais RASHEED, Zhiyong XIN, Qiaosheng ZHUANG, Ennian YANG, Zheru FAN, Jun YAN, Ravi SINGH, Hans-Joachim BRAUN. China-CIMMYT collaboration enhances wheat improvement in China[J]. Front. Agr. Sci. Eng. , 2019, 6(3): 233-239.
[9]	Jianwen CHEN, Kaiyuan PAN, Zhen CHEN, Biao DING, Dandan SONG, Wenbin BAO, Yunhai ZHANG. Construction of multiple shRNA vectors targeting PEDV and TGEV and production of transgenic SCNT porcine embryos in vitro[J]. Front. Agr. Sci. Eng. , 2019, 6(1): 66-72.
[10]	Chuanping YANG. *Research progress on genetic improvement of Betula platyphylla* Suk.**[J]. Front. Agr. Sci. Eng. , 2017, 4(4): 391-401.
[11]	Wenteng XU, Songlin CHEN. Genomics and genetic breeding in aquatic animals: progress and prospects[J]. Front. Agr. Sci. Eng. , 2017, 4(3): 305-318.
[12]	Huimin KANG, Lei ZHOU, Jianfeng LIU. Statistical considerations for genomic selection[J]. Front. Agr. Sci. Eng. , 2017, 4(3): 268-278.
[13]	Yueyi CHEN,Xinsheng GAO,Xiaofei ZHANG,Weimin TIAN. *Relationship between the number of tapping-induced secondary laticifer lines and rubber yield among Hevea* germplasm**[J]. Front. Agr. Sci. Eng. , 2016, 3(4): 363-367.
[14]	Wei HUA,Jing LIU,Hanzhong WANG. *Molecular regulation and genetic improvement of seed oil content in Brassica napus* L.**[J]. Front. Agr. Sci. Eng. , 2016, 3(3): 186-194.
[15]	Shihua CHENG,Xiaodeng ZHAN,Liyong CAO. Breeding strategies for increasing yield potential in super hybrid rice[J]. Front. Agr. Sci. Eng. , 2015, 2(4): 277-282.

Viewed

Full text

Abstract

Cited

Shared

Discussed