Advances in genetic engineering of domestic animals

Shaohua WANG, Kun ZHANG, Yunping DAI

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Front. Agr. Sci. Eng. ›› 2016, Vol. 3 ›› Issue (1) : 1-10. DOI: 10.15302/J-FASE-2016085
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Advances in genetic engineering of domestic animals

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Abstract

Global population will increase to over nine billion by 2050 with the doubling in demand for meat and milk. To overcome this challenge, it is necessary to breed highly efficient and productive livestock. Furthermore, livestock are also excellent models for human diseases and ideal bioreactors to produce pharmaceutical proteins. Thus, genetic engineering of domestic animals presents a critical and valuable tool to address these agricultural and biomedical applications. Overall, genetic engineering has evolved through three stages in history: transgenesis, gene targeting, and gene editing. Since the birth of the first transgenic pig, genetic engineering in livestock has been advancing slowly due to inherent technical limitations. A major breakthrough has been the advent of somatic cell nuclear transfer, which, for the first time, provided the technical ability to produce site-specific genome-modified domestic animals. However, the low efficiency of gene targeting events in somatic cells prohibits its wide use in agricultural and biomedical applications. Recently, rapid progress in tools and methods of genome engineering has been made, allowing genetic editing from mutation of a single base pair to the deletion of entire chromosomes. Here, we review the major advances of genetic engineering in domestic animals with emphasis placed on the introduction of latest designer nucleases.

Keywords

CRISPR / TALEN / ZFN / gene editing / livestock / pig / cattle

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Shaohua WANG, Kun ZHANG, Yunping DAI. Advances in genetic engineering of domestic animals. Front. Agr. Sci. Eng., 2016, 3(1): 1‒10 https://doi.org/10.15302/J-FASE-2016085

References

[1]
Niemann H, Kues W A. Application of transgenesis in livestock for agriculture and biomedicine. Animal Reproduction Science, 2003, 79(3–4): 291–317
CrossRef Google scholar
[2]
Liu X, Wang Y S, Guo W J, Chang B H, Liu J, Guo Z K, Quan F S, Zhang Y. Zinc-finger nickase-mediated insertion of the lysostaphin gene into the beta-casein locus in cloned cows. Nature Communications, 2013,4: 2565
[3]
Wall R J, Powell A M, Paape M J, Kerr D E, Bannerman D D, Pursel V G, Wells K D, Talbot N, Hawk H W. Genetically enhanced cows resist intramammary Staphylococcus aureus infection. Nature Biotechnology, 2005, 23(4): 445–451
CrossRef Google scholar
[4]
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, Fahrenkrug S C. Genome edited sheep and cattle. Transgenic Research, 2015, 24(1): 147–153
CrossRef Google scholar
[5]
Luo J, Song Z, Yu S, Cui D, Wang B, Ding F, Li S, Dai Y, Li N. Efficient generation of myostatin (MSTN) biallelic mutations in cattle using zinc finger nucleases. PLoS ONE, 2014, 9(4): e95225
CrossRef Google scholar
[6]
Yang P, Wang J, Gong G, Sun X, Zhang R, Du Z, Liu Y, Li R, Ding F, Tang B, Dai Y, Li N. Cattle mammary bioreactor generated by a novel procedure of transgenic cloning for large-scale production of functional human lactoferrin. PLoS ONE, 2008, 3(10): e3453
CrossRef Google scholar
[7]
Yu S, Luo J, Song Z, Ding F, Dai Y, Li N. Highly efficient modification of beta-lactoglobulin (BLG) gene via zinc-finger nucleases in cattle. Cell Research, 2011, 21(11): 1638–1640
CrossRef Google scholar
[8]
Brophy B, Smolenski G, Wheeler T, Wells D, L'Huillier P, Laible G. Cloned transgenic cattle produce milk with higher levels of β-casein and κ-casein. Nature Biotechnology, 2003, 21(2): 157–162
CrossRef Google scholar
[9]
Prather R S, Lorson M, Ross J W, Whyte J J, Walters E. Genetically engineered pig models for human diseases. Annual Review of Animal Biosciences, 2013, 1: 203–219
[10]
Cooper D K, Ekser B, Ramsoondar J, Phelps C, Ayares D. The role of genetically engineered pigs in xenotransplantation research. Journal of Pathology, 2016: 238(2): 288–299
[11]
Bosze Z, Baranyi M, Whitelaw C B. Producing recombinant human milk proteins in the milk of livestock species. Advances in Experimental Medicine and Biology, 2008, 606: 357–393
[12]
Hammer R E, Pursel V G, Rexroad C E Jr, Wall R J, Bolt D J, Ebert K M, Palmiter R D, Brinster R L. Production of transgenic rabbits, sheep and pigs by microinjection. Nature, 1985, 315(6021): 680–683
CrossRef Google scholar
[13]
Palmiter R D, Brinster R L, Hammer R E, Trumbauer M E, Rosenfeld M G, Birnberg N C, Evans R M. Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion genes. Nature, 1982, 300(5893): 611–615
CrossRef Google scholar
[14]
Lai L, Kolber-Simonds D, Park K W, Cheong H T, Greenstein J L, Im G S, Samuel M, Bonk A, Rieke A, Day B N, Murphy C N, Carter D B, Hawley R J, Prather R S. Production of α-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning. Science, 2002, 295(5557): 1089–1092
CrossRef Google scholar
[15]
Cong L, Ran F A, Cox D, Lin S L, Barretto R, Habib N, Hsu P D, Wu X B, Jiang W Y, Marraffini L A, Zhang F. Multiplex genome engineering using CRISPR/Cas systems. Science, 2013, 339(6121): 819–823
CrossRef Google scholar
[16]
Mali P, Yang L H, Esvelt K M, Aach J, Guell M, DiCarlo J E, Norville J E, Church G M. RNA-guided human genome engineering via Cas9. Science, 2013, 339(6121): 823–826
CrossRef Google scholar
[17]
Jackson D A, Symons R H, Berg P. Biochemical method for inserting new genetic information into DNA of Simian virus 40: circular Sv40 DNA molecules containing lambda phage genes and galactose operon of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 1972, 69(10): 2904–2909
CrossRef Google scholar
[18]
Gordon J W, Scangos G A, Plotkin D J, Barbosa J A, Ruddle F H. Genetic transformation of mouse embryos by microinjection of purified DNA. Proceedings of the National Academy of Sciences of the United States of America, 1980, 77(12): 7380–7384
CrossRef Google scholar
[19]
Jaenisch R. Germ line integration of moloney leukemia virus: effect of homozygosity at the m-mulV locus. Cell, 1977, 12(3): 691–696
CrossRef Google scholar
[20]
Jaenisch R, Mintz B. Simian virus 40 DNA sequences in DNA of healthy adult mice derived from preimplantation blastocysts injected with viral DNA. Proceedings of the National Academy of Sciences of the United States of America, 1974, 71(4): 1250–1254
CrossRef Google scholar
[21]
Krimpenfort P, Rademakers A, Eyestone W, van der Schans A, van den Broek S, Kooiman P, Kootwijk E, Platenburg G, Pieper F, Strijker R, de Boer H. Generation of transgenic dairy cattle using ‘in vitro’ embryo production. Biotechnology, 1991, 9(9): 844–847
CrossRef Google scholar
[22]
Niemann H. Transgenic pigs expressing plant genes. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(19): 7211–7212
CrossRef Google scholar
[23]
Hofmann A, Kessler B, Ewerling S, Weppert M, Vogg B, Ludwig H, Stojkovic M, Boelhauve M, Brem G, Wolf E, Pfeifer A. Efficient transgenesis in farm animals by lentiviral vectors. EMBO Reports, 2003, 4(11): 1054–1058
CrossRef Google scholar
[24]
Kubisch H M, Larson M A, Eichen P A, Wilson J M, Roberts R M. Adenovirus-mediated gene transfer by perivitelline microinjection of mouse, rat, and cow embryos. Biology of Reproduction, 1997, 56(1): 119–124
CrossRef Google scholar
[25]
Webster N L, Forni M, Bacci M L, Giovannoni R, Razzini R, Fantinati P, Zannoni A, Fusetti L, Dalpra L, Bianco M R, Papa M, Seren E, Sandrin M S, Mc Kenzie I F, Lavitrano M. Multi-transgenic pigs expressing three fluorescent proteins produced with high efficiency by sperm mediated gene transfer. Molecular Reproduction and Development, 2005, 72(1): 68–76
CrossRef Google scholar
[26]
Maga E A, Geoffrey Sargent R, Zeng H, Pati S, Zarling D A, Oppenheim S M, Collette N M B, Moyer A L, Conrad-Brink J S, Rowe J D, BonDurant R H, Anderson G B, Murray J D. BonDurant R H, Anderson G B, Murray J D. Increased efficiency of transgenic livestock production. Transgenic Research, 2003, 12(4): 485–496
CrossRef Google scholar
[27]
Scherer S, Davis R W. Replacement of chromosome segments with altered DNA sequences constructed in vitro. Proceedings of the National Academy of Sciences of the United States of America, 1979, 76(10): 4951–4955
CrossRef Google scholar
[28]
Thomas K R, Folger K R, Capecchi M R. High frequency targeting of genes to specific sites in the mammalian genome. Cell, 1986, 44(3): 419–428
CrossRef Google scholar
[29]
Smithies O, Gregg R G, Boggs S S, Koralewski M A, Kucherlapati R S. Insertion of DNA sequences into the human chromosomal β-globin locus by homologous recombination. Nature, 1985, 317(6034): 230–234
CrossRef Google scholar
[30]
Evans M J, Kaufman M H. Establishment in culture of pluripotential cells from mouse embryos. Nature, 1981, 292(5819): 154–156
CrossRef Google scholar
[31]
Schwartzberg P L, Goff S P, Robertson E J. Germ-line transmission of a c-abl mutation produced by targeted gene disruption in ES cells. Science, 1989, 246(4931): 799–803
CrossRef Google scholar
[32]
Hall B, Limaye A, Kulkarni A B. Overview: generation of gene knockout mice. Current Protocols in Cell Biology, 2009. doi: 10.1002/0471143030.cb1912s44 (Published online in Whiely Online Library)
[33]
Wilmut I, Schnieke A E, McWhir J, Kind A J, Campbell K H. Viable offspring derived from fetal and adult mammalian cells. Nature, 1997, 385(6619): 810–813
CrossRef Google scholar
[34]
Dai Y, Vaught T D, Boone J, Chen S H, Phelps C J, Ball S, Monahan J A, Jobst P M, McCreath K J, Lamborn A E, Cowell-Lucero J L, Wells K D, Colman A, Polejaeva I A, Ayares D L. Targeted disruption of the α1,3-galactosyltransferase gene in cloned pigs. Nature Biotechnology, 2002, 20(3): 251–255
CrossRef Google scholar
[35]
Sedivy J M, Sharp P A. Positive genetic selection for gene disruption in mammalian cells by homologous recombination. Proceedings of the National Academy of Sciences of the United States of America, 1989, 86(1): 227–231
CrossRef Google scholar
[36]
Vasquez K M, Marburger K, Intody Z, Wilson J H. Manipulating the mammalian genome by homologous recombination. Proceedings of the National Academy of Sciences of the United States of America, 2001, 98(15): 8403–8410
CrossRef Google scholar
[37]
Kuroiwa Y, Kasinathan P, Matsushita H, Sathiyaselan J, Sullivan E J, Kakitani M, Tomizuka K, Ishida I, Robl J M. Sequential targeting of the genes encoding immunoglobulin-mu and prion protein in cattle. Nature Genetics, 2004, 36(7): 775–780
CrossRef Google scholar
[38]
Mansour S L, Thomas K R, Capecchi M R. Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to non-selectable genes. Nature, 1988, 336(6197): 348–352
CrossRef Google scholar
[39]
Klymiuk N, Mundhenk L, Kraehe K, Wuensch A, Plog S, Emrich D, Langenmayer M C, Stehr M, Holzinger A, Kroner C, Richter A, Kessler B, Kurome M, Eddicks M, Nagashima H, Heinritzi K, Gruber A D, Wolf E. Sequential targeting of CFTR by BAC vectors generates a novel pig model of cystic fibrosis. Journal of Molecular Medcine, 2012, 90(5): 597–608
CrossRef Google scholar
[40]
Klymiuk N, Blutke A, Graf A, Krause S, Burkhardt K, Wuensch A, Krebs S, Kessler B, Zakhartchenko V, Kurome M, Kemter E, Nagashima H, Schoser B, Herbach N, Blum H, Wanke R, Aartsma-Rus A, Thirion C, Lochmuller H, Walter M C, Wolf E. Dystrophin-deficient pigs provide new insights into the hierarchy of physiological derangements of dystrophic muscle. Human Molecular Genetics, 2013, 22(21): 4368–4382
CrossRef Google scholar
[41]
Segal D J, Carroll D. Endonuclease-induced, targeted homologous extrachromosomal recombination in Xenopus oocytes. Proceedings of the National Academy of Sciences of the United States of America, 1995, 92(3): 806–810
CrossRef Google scholar
[42]
Rouet P, Smih F, Jasin M. 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
CrossRef Google scholar
[43]
Choulika A, Perrin A, Dujon B, Nicolas J F. Induction of homologous recombination in mammalian chromosomes by using the I-SceI system of Saccharomyces cerevisiae. Molecular and Cellular Biology, 1995, 15(4): 1968–1973
CrossRef Google scholar
[44]
Bibikova M, Carroll D, Segal D J, Trautman J K, Smith J, Kim Y G, Chandrasegaran S. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Molecular and Cellular Biology, 2001, 21(1): 289–297
CrossRef Google scholar
[45]
Kim H, Kim J S. A guide to genome engineering with programmable nucleases. Nature Reviews. Genetics, 2014, 15(5): 321–334
CrossRef Google scholar
[46]
Pavletich N P, Pabo C O. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science, 1991, 252(5007): 809–817
CrossRef Google scholar
[47]
Bibikova M, Golic M, Golic K G, Carroll D. Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics, 2002, 161(3): 1169–1175
[48]
Morton J, Davis M W, Jorgensen E M, Carroll D. Induction and repair of zinc-finger nuclease-targeted double-strand breaks in Caenorhabditis elegans somatic cells. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(44): 16370–16375
CrossRef Google scholar
[49]
Foley J E, Maeder M L, Pearlberg J, Joung J K, Peterson R T, Yeh J R. Targeted mutagenesis in zebrafish using customized zinc-finger nucleases. Nature Protocols, 2009, 4(12): 1855–1867
CrossRef Google scholar
[50]
Cui X, Ji D, Fisher D A, Wu Y, Briner D M, Weinstein E J. Targeted integration in rat and mouse embryos with zinc-finger nucleases. Nature Biotechnology, 2011, 29(1): 64–67
CrossRef Google scholar
[51]
Yu S, Luo J, Song Z, Ding F, Dai Y, Li N. Highly efficient modification of beta-lactoglobulin (BLG) gene via zinc-finger nucleases in cattle. Cell Research, 2011, 21(11): 1638–1640
CrossRef Google scholar
[52]
Hauschild J, Petersen B, Santiago Y, Queisser A L, Carnwath J W, Lucas-Hahn A, Zhang L, Meng X D, Gregory P D, Schwinzer R, Cost G J, Niemann H. Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(29): 12013–12017
CrossRef Google scholar
[53]
Whyte J J, Zhao J G, Wells K D, Samuel M S, Whitworth K M, Walters E M, Laughlin M H, Prather R S. Gene targeting with zinc finger nucleases to produce cloned eGFP knockout pigs. Molecular Reproduction and Development, 2011, 78(1): 2
CrossRef Google scholar
[54]
Boch J, Bonas U.Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annual Review of Phytopathology, 2010, 48: 419–436
[55]
Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U. Breaking the code of DNA binding specificity of TAL-type III effectors. Science, 2009, 326(5959): 1509–1512
CrossRef Google scholar
[56]
Moscou M J, Bogdanove A J. A simple cipher governs DNA recognition by TAL effectors. Science, 2009, 326(5959): 1501
CrossRef Google scholar
[57]
Christian M, Cermak T, Doyle E L, Schmidt C, Zhang F, Hummel A, Bogdanove A J, Voytas D F. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics, 2010, 186(2): 757–761
CrossRef Google scholar
[58]
Carlson D F, Tan W, Lillico S G, Stverakova D, Proudfoot C, Christian M, Voytas D F, Long C R, Whitelaw C B, Fahrenkrug S C. Efficient TALEN-mediated gene knockout in livestock. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(43): 17382–17387
CrossRef Google scholar
[59]
Butler J R, Ladowski J M, Martens G R, Tector M, Tector A J. Recent advances in genome editing and creation of genetically modified pigs. International Journal of Surgery, 2015, 23: 217–222
[60]
Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. Journal of Bacteriology, 1987, 169(12): 5429–5433
[61]
Mojica F J M, Díez-Villaseñor C, Soria E, Juez G. Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Molecular Microbiology, 2000, 36(1): 244–246
CrossRef Google scholar
[62]
Jansen R, Embden J D, Gaastra W, Schouls L M. Identification of genes that are associated with DNA repeats in prokaryotes. Molecular Microbiology, 2002, 43(6): 1565–1575
CrossRef Google scholar
[63]
Mojica F J, Diez-Villasenor C, Garcia-Martinez J, Soria E. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. Journal of Molecular Evolution, 2005, 60(2): 174–182
CrossRef Google scholar
[64]
Pourcel C, Salvignol G, Vergnaud G. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology, 2005, 151(3): 653–663
CrossRef Google scholar
[65]
Bolotin A, Quinquis B, Sorokin A, Ehrlich S D. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology, 2005, 151(8): 2551–2561
CrossRef Google scholar
[66]
Tang T H, Bachellerie J P, Rozhdestvensky T, Bortolin M L, Huber H, Drungowski M, Elge T, Brosius J, Huttenhofer A. Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proceedings of the National Academy of Sciences of the United States of America, 2002, 99(11): 7536–7541
CrossRef Google scholar
[67]
Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero D A, Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science, 2007, 315(5819): 1709–1712
CrossRef Google scholar
[68]
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, van der Oost J. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 2008, 321(5891): 960–964
CrossRef Google scholar
[69]
Marraffini L A, Sontheimer E J. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science, 2008, 322(5909): 1843–1845
CrossRef Google scholar
[70]
Garneau J E, Dupuis M E, Villion M, Romero D A, Barrangou R, Boyaval P, Fremaux C, Horvath P, Magadan A H, Moineau S. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature, 2010, 468(7320): 67–71
CrossRef Google scholar
[71]
Deltcheva E, Chylinski K, Sharma C M, Gonzales K, Chao Y, Pirzada Z A, Eckert M R, Vogel J, Charpentier E. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature, 2011, 471(7340): 602–607
CrossRef Google scholar
[72]
Yang H, Wang H Y, Shivalila C S, Cheng A W, Shi L Y, Jaenisch R. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell, 2013, 154(6): 1370–1379
CrossRef Google scholar
[73]
Li W, Teng F, Li T D, Zhou Q. Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems. Nature Biotechnology, 2013, 31(8): 684–686
CrossRef Google scholar
[74]
Hai T, Teng F, Guo R F, Li W, Zhou Q. One-step generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Research, 2014, 24(3): 372–375
CrossRef Google scholar
[75]
Niu Y Y, Shen B, Cui Y Q, Chen Y C, Wang J Y, Wang L, Kang Y, Zhao X Y, Si W, Li W, Xiang A P, Zhou J K, Guo X J, Bi Y, Si C Y, Hu B, Dong G Y, Wang H, Zhou Z M, Li T Q, Tan T, Pu X Q, Wang F, Ji S H, Zhou Q, Huang X X, Ji W Z, Sha J H. Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell, 2014, 156(4): 836–843
CrossRef Google scholar
[76]
Gilbert L A, Larson M H, Morsut L, Liu Z, Brar G A, Torres S E, Stern-Ginossar N, Brandman O, Whitehead E H, Doudna J A, Lim W A, Weissman J S, Qi L S. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell, 2013, 154(2): 442–451
CrossRef Google scholar
[77]
Cheng A W, Wang H, Yang H, Shi L, Katz Y, Theunissen T W, Rangarajan S, Shivalila C S, Dadon D B, Jaenisch R. Multiplexed activation of endogenous genes by CRISPR-on, an RNA-guided transcriptional activator system. Cell Research, 2013, 23(10): 1163–1171
CrossRef Google scholar
[78]
Tanenbaum M E, Gilbert L A, Qi L S, Weissman J S, Vale R D. A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell, 2014, 159(3): 635–646
CrossRef Google scholar
[79]
Qi L S, Larson M H, Gilbert L A, Doudna J A, Weissman J S, Arkin A P, Lim W A. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 2013, 152(5): 1173–1183
CrossRef Google scholar
[80]
Thakore P I, D'Ippolito A M, Song L Y, Safi A, Shivakumar N K, Kabadi A M, Reddy T E, Crawford G E, Gersbach C A. Highly specific epigenome editing by CRISPR-Cas9 repressors for silencing of distal regulatory elements. Nature Methods, 2015, 12(12): 1143–1149
CrossRef Google scholar
[81]
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, Huang B. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell, 2013, 155(7): 1479–1491
CrossRef Google scholar
[82]
Whitworth K M, Lee K, Benne J A, Beaton B P, Spate L D, Murphy S L, Samuel M S, Mao J D, O'Gorman C, Walters E M, Murphy C N, Driver J, Mileham A, McLaren D, Wells K D, Prather R S. Use of the CRISPR/Cas9 system to produce genetically engineered pigs from in vitro-derived oocytes and embryos. Biology of Reproduction, 2014, 91(3): 78
CrossRef Google scholar
[83]
Petersen B, Niemann H. Molecular scissors and their application in genetically modified farm animals. Transgenic Research, 2015, 24(3): 381–396
CrossRef Google scholar
[84]
Wang T, Wei J J, Sabatini D M, Lander E S. Genetic screens in human cells using the CRISPR-Cas9 system. Science, 2014, 343(6166): 80–84
CrossRef Google scholar
[85]
Kim S, Kim D, Cho S W, Kim J, Kim J S. Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Research, 2014, 24(6): 1012–1019
CrossRef Google scholar
[86]
Ran F A, Hsu P D, Lin C Y, Gootenberg J S, Konermann S, Trevino A E, Scott D A, Inoue A, Matoba S, Zhang Y, Zhang F. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell, 2013, 154(6): 1380–1389
CrossRef Google scholar
[87]
Fu Y F, Sander J D, Reyon D, Cascio V M, Joung J K. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nature Biotechnology, 2014, 32(3): 279–284
CrossRef Google scholar
[88]
Slaymaker I M, Gao L, Zetsche B, Scott D A, Yan W X, Zhang F. Rationally engineered Cas9 nucleases with improved specificity. Science, 2016, 351(6268): 84–88
CrossRef Google scholar
[89]
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, Zhang F. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell, 2015, 163(3): 759–771
CrossRef Google scholar

Acknowledgements

The work was funded by the One Hundred Talents Program of Zhejiang University.
Wang, Kun Zhang, and Yunping Dai declare that they have no conflict of interest or financial conflicts to disclose.
This article is a review and does not contain any studies with human or animal subjects performed by any of the authors.

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