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Genome editing and genetic engineering in livestock for advancing agricultural and biomedical applications

Abstract

Genetic modification of livestock has a longstanding and successful history, starting with domestication several thousand years ago. Modern animal breeding strategies predominantly based on marker-assisted and genomic selection, artificial insemination, and embryo transfer have led to significant improvement in the performance of domestic animals, and are the basis for regular supply of high quality animal derived food. However, the current strategy of breeding animals over multiple generations to introduce novel traits is not realistic in responding to the unprecedented challenges such as changing climate, pandemic diseases, and feeding an anticipated 3 billion increase in global population in the next three decades. Consequently, sophisticated genetic modifications that allow for seamless introgression of novel alleles or traits and introduction of precise modifications without affecting the overall genetic merit of the animal are required for addressing these pressing challenges. The requirement for precise modifications is especially important in the context of modeling human diseases for the development of therapeutic interventions. The animal science community envisions the genome editors as essential tools in addressing these critical priorities in agriculture and biomedicine, and for advancing livestock genetic engineering for agriculture, biomedical as well as “dual purpose” applications.

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References

  • Alberio R, Croxall N, Allegrucci C (2010) Pig epiblast stem cells depend on activin/nodal signaling for pluripotency and self renewal. Stem Cells Dev 19:1627–1636

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Barry JS, Anthony RV (2008) The pregnant sheep as a model for human pregnancy. Theriogenology 69:55–67

    CAS  PubMed  Article  Google Scholar 

  • Betteridge KJ (2003) A history of farm animal embryo transfer and some associated techniques. Anim Reprod Sci 79:203–244

    PubMed  Article  Google Scholar 

  • Bleck GT, White BR, Miller DJ, Wheeler MB (1998) Production of bovine alpha-lactalbumin in the milk of transgenic pigs. J Anim Sci 76:3072–3078

    CAS  PubMed  Article  Google Scholar 

  • Brinster RL, Chen HY, Trumbauer M, Senear AW, Warren R, Palmiter RD (1981) Somatic expression of herpes thymidine kinase in mice following injection of a fusion gene into eggs. Cell 27:223–231

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Brinster RL, Sandgren EP, Behringer RR, Palmiter RD (1989) No simple solution for making transgenic mice. Cell 59:239–241

    CAS  PubMed  Article  Google Scholar 

  • Buhler TA, Bruyere T, Went DF, Stranzinger G, Burki K (1990) Rabbit beta-casein promoter directs secretion of human interleukin-2 into the milk of transgenic rabbits. Biotechnology (N Y) 8, 140–143

    CAS  PubMed  Google Scholar 

  • Cabot RA, Kuhholzer B, Chan AW, Lai L, Park KW, Chong KY, Schatten G, Murphy CN, Abeydeera LR, Day BN, Prather RS (2001) Transgenic pigs produced using in vitro matured oocytes infected with a retroviral vector. Anim Biotechnol 12:205–214

    CAS  PubMed  Article  Google Scholar 

  • Campbell KH, McWhir J, Ritchie WA, Wilmut I (1996) Sheep cloned by nuclear transfer from a cultured cell line. Nature 380:64–66

    CAS  PubMed  Article  Google Scholar 

  • Camus S, Ko WK, Pioli E, Bezard E (2015) Why bother using non-human primate models of cognitive disorders in translational research? Neurobiol Learn Mem. doi:10.1016/j.nlm.2015.06.012

    PubMed  Google Scholar 

  • Capecchi MR (1980) High efficiency transformation by direct microinjection of DNA into cultured mammalian cells. Cell 22:479–488

    CAS  PubMed  Article  Google Scholar 

  • Capecchi MR (1989) Altering the genome by homologous recombination. Science 244:1288–1292

    CAS  PubMed  Article  Google Scholar 

  • Carlson DF, Geurts AM, Garbe JR, Park CW, Rangel-Filho A, O’Grady SM, Jacob HJ, Steer CJ, Largaespada DA, Fahrenkrug SC (2011) Efficient mammalian germline transgenesis by cis-enhanced Sleeping Beauty transposition. Transgenic Res 20:29–45

    CAS  PubMed  Article  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Carvalho-Oliveira I, Scholte BJ, Penque D (2007) What have we learned from mouse models for cystic fibrosis? Expert Rev Mol Diagn 7:407–417

    CAS  PubMed  Article  Google Scholar 

  • Casal M, Haskins M (2006) Large animal models and gene therapy. Eur J Hum Genet 14:266–272

    CAS  PubMed  Article  Google Scholar 

  • Chang K, Qian J, Jiang M, Liu YH, Wu MC, Chen CD, Lai CK, Lo HL, Hsiao CT, Brown L, Bolen J Jr, Huang HI, Ho PY, Shih PY, Yao CW, Lin WJ, Chen CH, Wu FY, Lin YJ, Xu J, Wang K (2002) Effective generation of transgenic pigs and mice by linker based sperm-mediated gene transfer. BMC Biotechnol 2:5

    PubMed  PubMed Central  Article  Google Scholar 

  • Chen F, Wang Y, Yuan Y, Zhang W, Ren Z, Jin Y, Liu X, Xiong Q, Chen Q, Zhang M, Li X, Zhao L, Li Z, Wu Z, Zhang Y, Hu F, Huang J, Li R, Dai Y (2015) Generation of B cell-deficient pigs by highly efficient CRISPR/Cas9-mediated gene targeting. J Genet Genom 42:437–444

    Article  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–761

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Cibelli JB, Stice SL, Golueke PJ, Kane JJ, Jerry J, Blackwell C, Ponce de Leon FA, Robl JM (1998) Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science 280:1256–1258

    CAS  PubMed  Article  Google Scholar 

  • Clark KJ, Carlson DF, Fahrenkrug SC (2007) Pigs taking wing with transposons and recombinases. Genome Biol 8(Suppl 1):S13

    PubMed  PubMed Central  Article  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Cuffee Y, Ogedegbe C, Williams NJ, Ogedegbe G, Schoenthaler A (2014) Psychosocial risk factors for hypertension: an update of the literature. Curr Hypertens Rep 16:483

    PubMed  PubMed Central  Article  Google Scholar 

  • Denning C, Burl S, Ainslie A, Bracken J, Dinnyes A, Fletcher J, King T, Ritchie M, Ritchie WA, Rollo M, de Sousa P, Travers A, Wilmut I, Clark AJ (2001) Deletion of the alpha(1,3)galactosyl transferase (GGTA1) gene and the prion protein (PrP) gene in sheep. Nat Biotechnol 19:559–562

    CAS  PubMed  Article  Google Scholar 

  • Ebert KM, Selgrath JP, DiTullio P, Denman J, Smith TE, Memon MA, Schindler JE, Monastersky GM, Vitale JA, Gordon K (1991) Transgenic production of a variant of human tissue-type plasminogen activator in goat milk: Generation of transgenic goats and analysis of expression. Nat Biotechnol 9:835–838

    CAS  Article  Google Scholar 

  • Federspiel MJ, Hughes SH (1997) Retroviral gene delivery. Methods Cell Biol 52:179–214

    CAS  PubMed  Article  Google Scholar 

  • Gafni O, Weinberger L, Mansour AA, Manor YS, Chomsky E, Ben-Yosef D, Kalma Y, Viukov S, Maza I, Zviran A, Rais Y, Shipony Z, Mukamel Z, Krupalnik V, Zerbib M, Geula S, Caspi I, Schneir D, Shwartz T, Gilad S, Amann-Zalcenstein D, Benjamin S, Amit I, Tanay A, Massarwa R, Novershtern N, Hanna JH (2013) Derivation of novel human ground state naive pluripotent stem cells. Nature 504:282–286

    CAS  PubMed  Article  Google Scholar 

  • Galli C, Lagutina I, Perota A, Colleoni S, Duchi R, Lucchini F, Lazzari G (2012) Somatic cell nuclear transfer and transgenesis in large animals: current and future insights. Reprod Domest Anim 47(Suppl 3):2–11

    PubMed  Article  Google Scholar 

  • Gandolfi F (2000) Sperm-mediated transgenesis. Theriogenology 53:127–137

    CAS  PubMed  Article  Google Scholar 

  • Geijsen N, Horoschak M, Kim K, Gribnau J, Eggan K, Daley GQ (2004) Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 427:148–154

    CAS  PubMed  Article  Google Scholar 

  • Goliasova E, Wolf J (2004) Impact of the ESR gene on litter size and production traits in Czech Large White pigs. Anim Genet 35:293–297

    CAS  PubMed  Article  Google Scholar 

  • Golovan SP, Meidinger RG, Ajakaiye A, Cottrill M, Wiederkehr MZ, Barney DJ, Plante C, Pollard JW, Fan MZ, Hayes MA, Laursen J, Hjorth JP, Hacker RR, Phillips JP, Forsberg CW (2001) Pigs expressing salivary phytase produce low-phosphorus manure. Nat Biotechnol 19:741–745

    CAS  PubMed  Article  Google Scholar 

  • Gordon JW, Scangos GA, Plotkin DJ, Barbosa JA, Ruddle FH (1980) Genetic transformation of mouse embryos by microinjection of purified DNA. Proc Natl Acad Sci USA 77:7380–7384

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Graessmann A, Graessmann M, Topp WC, Botchan M (1979) Retransformation of a simian virus 40 revertant cell line, which is resistant to viral and DNA infections, by microinjection of viral DNA. J Virol 32:989–994

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grubb BR, Boucher RC (1999) Pathophysiology of gene-targeted mouse models for cystic fibrosis. Physiol Rev 79:S193–S214

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Hammer RE, Pursel VG, Rexroad CE Jr, Wall RJ, Bolt DJ, Ebert KM, Palmiter RD, Brinster RL (1985) Production of transgenic rabbits, sheep and pigs by microinjection. Nature 315:680–683

    CAS  Article  Google Scholar 

  • Harris MJ, Juriloff DM (2010) An update to the list of mouse mutants with neural tube closure defects and advances toward a complete genetic perspective of neural tube closure. Birth defects research. Birth Defects Res A 88:653–669

    CAS  Article  Google Scholar 

  • Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M (2011) Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146:519–532

    CAS  PubMed  Article  Google Scholar 

  • Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M (2012) Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science 338:971–975

    CAS  PubMed  Article  Google Scholar 

  • Hofmann A, Kessler B, Ewerling S, Weppert M, Vogg B, Ludwig H, Stojkovic M, Boelhauve M, Brem G, Wolf E, Pfeifer A (2003) Efficient transgenesis in farm animals by lentiviral vectors. EMBO Rep 4:1054–1060

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Honaramooz A, Megee S, Zeng W, Destrempes MM, Overton SA, Luo J, Galantino-Homer H, Modelski M, Chen F, Blash S, Melican DT, Gavin WG, Ayres S, Yang F, Wang PJ, Echelard Y, Dobrinski I (2008) Adeno-associated virus (AAV)-mediated transduction of male germ line stem cells results in transgene transmission after germ cell transplantation. FASEB J 22:374–382

    CAS  PubMed  Article  Google Scholar 

  • Houde C, Banks KG, Coulombe N, Rasper D, Grimm E, Roy S, Simpson EM, Nicholson DW (2004) Caspase-7 expanded function and intrinsic expression level underlies strain-specific brain phenotype of caspase-3-null mice. J Neurosci 24:9977–9984

    CAS  PubMed  Article  Google Scholar 

  • Huang TT, Naeemuddin M, Elchuri S, Yamaguchi M, Kozy HM, Carlson EJ, Epstein CJ (2006) Genetic modifiers of the phenotype of mice deficient in mitochondrial superoxide dismutase. Hum Mol Genet 15:1187–1194

    CAS  PubMed  Article  Google Scholar 

  • Hubner K, Fuhrmann G, Christenson LK, Kehler J, Reinbold R, De La Fuente R, Wood J, Strauss JF 3rd, Boiani M, Scholer HR (2003) Derivation of oocytes from mouse embryonic stem cells. Science 300:1251–1256

    PubMed  Article  CAS  Google Scholar 

  • Jabed A, Wagner S, McCracken J, Wells DN, Laible G (2012) Targeted microRNA expression in dairy cattle directs production of beta-lactoglobulin-free, high-casein milk. Proc Natl Acad Sci USA 109:16811–16816

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 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

    CAS  PubMed  Article  Google Scholar 

  • Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J (2013) RNA-programmed genome editing in human cells. eLife 2:e00471

    PubMed  PubMed Central  Article  Google Scholar 

  • Kang JT, Ryu J, Cho B, Lee EJ, Yun YJ, Ahn S, Lee J, Ji DY, Lee K, Park KW (2016) Generation of RUNX3 knockout pigs using CRISPR/Cas9-mediated gene targeting. Reprod Domest Anim 51:970–978

    CAS  PubMed  Article  Google Scholar 

  • Kass EM, Jasin M (2010) Collaboration and competition between DNA double-strand break repair pathways. FEBS Lett 584, 3703–3708

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci USA 93:1156–1160

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kong BW, Carlson DF, Fahrenkrug SC, Foster DN (2008) Application of the Sleeping Beauty transposon system to avian cells. Anim Genet 39:180–186

    CAS  PubMed  Article  Google Scholar 

  • Kuroiwa Y, Kasinathan P, Matsushita H, Sathiyaselan J, Sullivan EJ, Kakitani M, Tomizuka K, Ishida I, Robl JM (2004) Sequential targeting of the genes encoding immunoglobulin-mu and prion protein in cattle. Nat Genet 36:775–780

    CAS  PubMed  Article  Google Scholar 

  • Lai L, Kang JX, Li R, Wang J, Witt WT, Yong HY, Hao Y, Wax DM, Murphy CN, Rieke A, Samuel M, Linville ML, Korte SW, Evans RW, Starzl TE, Prather RS, Dai Y (2006) Generation of cloned transgenic pigs rich in omega-3 fatty acids. Nat Biotechnol 24:435–436

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Lavine G (2009) FDA approves first biological product derived from transgenic animal. Am J Health-System Pharm 66:518

    Article  Google Scholar 

  • Lavitrano M, Forni M, Varzi V, Pucci L, Bacci ML, Di Stefano C, Fioretti D, Zoraqi G, Moioli B, Rossi M, Lazzereschi D, Stoppacciaro A, Seren E, Alfani D, Cortesini R, Frati L (1997) Sperm-mediated gene transfer: production of pigs transgenic for a human regulator of complement activation. Transplant Proc 29:3508–3509

    CAS  PubMed  Article  Google Scholar 

  • Lavitrano M, Busnelli M, Cerrito MG, Giovannoni R, Manzini S, Vargiolu A (2006) Sperm-mediated gene transfer. Reprod Fertil Dev 18:19–23

    CAS  PubMed  Article  Google Scholar 

  • Li XJ, Li S (2012) Influence of species differences on the neuropathology of transgenic Huntington’s disease animal models. J Genet Genom 39:239–245

    CAS  Article  Google Scholar 

  • 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. Scientific reports 6:21645

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Lyall J, Irvine RM, Sherman A, McKinley TJ, Nunez A, Purdie A, Outtrim L, Brown IH, Rolleston-Smith G, Sang H, Tiley L (2011) Suppression of avian influenza transmission in genetically modified chickens. Science 331:223–226

    CAS  PubMed  Article  Google Scholar 

  • Macdonald J, Glover JD, Taylor L, Sang HM, McGrew MJ (2010) Characterisation and germline transmission of cultured avian primordial germ cells. PLoS ONE 5:e15518

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Maga EA, Cullor JS, Smith W, Anderson GB, Murray JD (2006a) Human lysozyme expressed in the mammary gland of transgenic dairy goats can inhibit the growth of bacteria that cause mastitis and the cold-spoilage of milk. Foodborne Pathog Dis 3:384–392

    CAS  PubMed  Article  Google Scholar 

  • Maga EA, Walker RL, Anderson GB, Murray JD (2006b) Consumption of milk from transgenic goats expressing human lysozyme in the mammary gland results in the modulation of intestinal microflora. Transgenic Res 15:515–519

    CAS  PubMed  Article  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • McNatty KP, Smith P, Moore LG, Reader K, Lun S, Hanrahan JP, Groome NP, Laitinen M, Ritvos O, Juengel JL (2005) Oocyte-expressed genes affecting ovulation rate. Mol Cell Endocrinol 234:57–66

    CAS  PubMed  Article  Google Scholar 

  • Meurens F, Summerfield A, Nauwynck H, Saif L, Gerdts V (2012) The pig: a model for human infectious diseases. Trends Microbiol 20:50–57

    CAS  PubMed  Article  Google Scholar 

  • Montier T, Delepine P, Pichon C, Ferec C, Porteous DJ, Midoux P (2004) Non-viral vectors in cystic fibrosis gene therapy: progress and challenges. Trends Biotechnol 22:586–592

    CAS  PubMed  Article  Google Scholar 

  • Morton AJ, Howland DS (2013) Large genetic animal models of Huntington’s Disease. J Huntingtons Dis 2:3–19

    PubMed  Google Scholar 

  • Navarro SJ, Trinh T, Lucas CA, Ross AJ, Waymire KG, Macgregor GR (2012) The C57BL/6 J mouse strain background modifies the effect of a mutation in Bcl2l2. G3 2:99–102

  • Ni J, Clark KJ, Fahrenkrug SC, Ekker SC (2008) Transposon tools hopping in vertebrates. Brief Funct Genom Proteom 7:444–453

    CAS  Article  Google Scholar 

  • Nicholson A, Reifsnyder PC, Malcolm RD, Lucas CA, MacGregor GR, Zhang W, Leiter EH (2010) Diet-induced obesity in two C57BL/6 substrains with intact or mutant nicotinamide nucleotide transhydrogenase (Nnt) gene. Obesity 18:1902–1905

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Nowak-Imialek M, Niemann H (2012) Pluripotent cells in farm animals: state of the art and future perspectives. Reprod Fertil Dev 25:103–128

    PubMed  Article  Google Scholar 

  • Onishi A, Iwamoto M, Akita T, Mikawa S, Takeda K, Awata T, Hanada H, Perry AC (2000) Pig cloning by microinjection of fetal fibroblast nuclei. Science 289:1188–1190

    CAS  PubMed  Article  Google Scholar 

  • 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 (2017a) Generation of germline ablated male pigs by CRISPR/Cas9 editing of the NANOS2 gene. Sci Rep 7:40176

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Park KE, Powell A, Sandmaier SE, Kim CM, Mileham A, Donovan DM, Telugu BP (2017b) Targeted gene knock-in by CRISPR/Cas ribonucleoproteins in porcine zygotes. Sci Rep 7:42458

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Patterson JK, Lei XG, Miller DD (2008) The pig as an experimental model for elucidating the mechanisms governing dietary influence on mineral absorption. Exp Biol Med 233:651–664

    CAS  Article  Google Scholar 

  • 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

    PubMed  PubMed Central  Article  Google Scholar 

  • Petersen B, Niemann H (2015) Molecular scissors and their application in genetically modified farm animals. Transgenic Res 24:381–396

    CAS  PubMed  Article  Google Scholar 

  • Petersen B, Frenzel A, Lucas-Hahn A, Herrmann D, Hassel P, Klein S, Ziegler M, Hadeler KG, Niemann H (2016) Efficient production of biallelic GGTA1 knockout pigs by cytoplasmic microinjection of CRISPR/Cas9 into zygotes. Xenotransplantation 23:338–346

    PubMed  Article  Google Scholar 

  • Plasterk RH, Izsvak Z, Ivics Z (1999) Resident aliens: the Tc1/mariner superfamily of transposable elements. Trends Genet 15, 326–332

    CAS  PubMed  Article  Google Scholar 

  • Porter TE, Couger GS, Morpurgo B (1995) Evidence that somatotroph differentiation during chicken embryonic development is stimulated by a blood-borne signal. Endocrinology 136:3721–3728

    CAS  PubMed  Article  Google Scholar 

  • Prather RS, Shen M, Dai Y (2008) Genetically modified pigs for medicine and agriculture. Biotechnol Genet Eng Rev 25:245–265

    CAS  PubMed  Google Scholar 

  • Pursel VG, Mitchell AD, Bee G, Elsasser TH, McMurtry JP, Wall RJ, Coleman ME, Schwartz RJ (2004) Growth and tissue accretion rates of swine expressing an insulin-like growth factor I transgene. Anim Biotechnol 15:33–45

    CAS  PubMed  Article  Google Scholar 

  • Rouet P, Smih F, Jasin M (1994) Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol Cell Biol 14:8096–8106

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Scheerlinck JP, Snibson KJ, Bowles VM, Sutton P (2008) Biomedical applications of sheep models: from asthma to vaccines. Trends Biotechnol 26:259–266

    CAS  PubMed  Article  Google Scholar 

  • Schmidt C (2006) Belated approval of first recombinant protein from animal. Nat Biotechnol 24:877

    CAS  PubMed  Article  Google Scholar 

  • Smith C (1989) Cloning and genetic improvement of beef cattle. Anim Prod 49:49–62

    CAS  Article  Google Scholar 

  • Solaiman F, Zink MA, Xu G, Grunkemeyer J, Cosgrove D, Saenz J, Hodgson CP (2000) Modular retro-vectors for transgenic and therapeutic use. Mol Reprod Dev 56:309–315

    CAS  PubMed  Article  Google Scholar 

  • Swindle MM, Makin A, Herron AJ, Clubb FJ Jr, Frazier KS (2012) Swine as models in biomedical research and toxicology testing. Vet Pathol 49:344–356

    CAS  PubMed  Article  Google Scholar 

  • Symington LS, Gautier J (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45:247–271

    CAS  PubMed  Article  Google Scholar 

  • Szybalska EH, Szybalski W (1962) Genetics of human cess line. IV. DNA-mediated heritable transformation of a biochemical trait. Proc Natl Acad Sci USA 48:2026–2034

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Tan W, Proudfoot C, Lillico SG, Whitelaw CB (2016) Gene targeting, genome editing: from Dolly to editors. Transgenic Res. doi:10.1007/s11248-016-9932-x

    PubMed  PubMed Central  Google Scholar 

  • Tanihara F, Takemoto T, Kitagawa E, Rao S, Do LT, Onishi A, Yamashita Y, Kosugi C, Suzuki H, Sembon S, Suzuki S, Nakai M, Hashimoto M, Yasue A, Matsuhisa M, Noji S, Fujimura T, Fuchimoto D, Otoi T (2016) Somatic cell reprogramming-free generation of genetically modified pigs. Sci Adv 2:e1600803

    PubMed  PubMed Central  Article  Google Scholar 

  • Telugu BP, Ezashi T, Roberts RM (2010) Porcine induced pluripotent stem cells analogous to naive and primed embryonic stem cells of the mouse. Int J Dev Biol 54:1703–1711

    CAS  PubMed  Article  Google Scholar 

  • Telugu BP, Ezashi T, Sinha S, Alexenko AP, Spate L, Prather RS, Roberts RM (2011) Leukemia inhibitory factor (LIF)-dependent, pluripotent stem cells established from inner cell mass of porcine embryos. J Biol Chem 286:28948–28953

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Threadgill DW, Dlugosz AA, Hansen LA, Tennenbaum T, Lichti U, Yee D, LaMantia C, Mourton T, Herrup K, Harris RC et al (1995) Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269:230–234

    CAS  PubMed  Article  Google Scholar 

  • Tickle C (2004) The contribution of chicken embryology to the understanding of vertebrate limb development. Mech Dev 121:1019–1029

    CAS  PubMed  Article  Google Scholar 

  • van Veen HA, Koiter J, Vogelezang CJ, van Wessel N, van Dam T, Velterop I, van Houdt K, Kupers L, Horbach D, Salaheddine M, Nuijens JH, Mannesse ML (2012) Characterization of recombinant human C1 inhibitor secreted in milk of transgenic rabbits. J Biotechnol 162:319–326

    PubMed  Article  CAS  Google Scholar 

  • Vize PD (1988) Introduction of a porcine growth hormone fusion gene into transgenic pigs promotes growth. J Cell Sci 90:295–300

    CAS  PubMed  Google Scholar 

  • Wall RJ, Powell AM, Paape MJ, Kerr DE, Bannerman DD, Pursel VG, Wells KD, Talbot N, Hawk HW (2005) Genetically enhanced cows resist intramammary Staphylococcus aureus infection. Nat Biotechnol 23:445–451

    CAS  PubMed  Article  Google Scholar 

  • Wang K, Ouyang H, Xie Z, Yao C, Guo N, Li M, Jiao H, Pang D (2015a) Efficient generation of myostatin mutations in pigs using the CRISPR/Cas9 system. Sci Rep 5:16623

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 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 (2015b) Generation of gene-modified goats targeting MSTN and FGF5 via zygote injection of CRISPR/Cas9 system. Sci Rep 5:13878

    PubMed  PubMed Central  Article  Google Scholar 

  • Wang X, Zhou J, Cao C, Huang J, Hai T, Wang Y, Zheng Q, Zhang H, Qin G, Miao X, Wang H, Cao S, Zhou Q, Zhao J (2015c) Efficient CRISPR/Cas9-mediated biallelic gene disruption and site-specific knockin after rapid selection of highly active sgRNAs in pigs. Sci Rep 5:13348

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Wang Y, Du Y, Shen B, Zhou X, Li J, Liu Y, Wang J, Zhou J, Hu B, Kang N, Gao J, Yu L, Huang X, Wei H (2015d) Efficient generation of gene-modified pigs via injection of zygote with Cas9/sgRNA. Sci Rep 5:8256

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Whitelaw CB, Sheets TP, Lillico SG, Telugu BP (2016) Engineering large animal models of human disease. J Pathol 238:247–256

    PubMed  Article  Google Scholar 

  • Whitworth KM, Lee K, Benne JA, Beaton BP, Spate LD, Murphy SL, Samuel MS, Mao J, O’Gorman C, Walters EM, Murphy CN, Driver J, Mileham A, McLaren D, Wells KD, Prather RS (2014) Use of the CRISPR/Cas9 system to produce genetically engineered pigs from in vitro-derived oocytes and embryos. Biol Reprod 91:78

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Whitworth KM, Rowland RR, Ewen CL, Trible BR, Kerrigan MA, Cino-Ozuna AG, Samuel MS, Lightner JE, McLaren DG, Mileham AJ, Wells KD, Prather RS (2016) Gene-edited pigs are protected from porcine reproductive and respiratory syndrome virus. Nat Biotechnol 34:20–22

    CAS  PubMed  Article  Google Scholar 

  • Whyte JJ, Prather RS (2011) Genetic modifications of pigs for medicine and agriculture. Mol Reprod Dev 78:879–891

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Wilke M, Buijs-Offerman RM, Aarbiou J, Colledge WH, Sheppard DN, Touqui L, Bot A, Jorna H, de Jonge HR, Scholte BJ (2011) Mouse models of cystic fibrosis: phenotypic analysis and research applications. J Cyst Fibros 10 Suppl 2, S152–171

    Article  Google Scholar 

  • Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH (1997) Viable offspring derived from fetal and adult mammalian cells. Nature 385:810–813

    CAS  PubMed  Article  Google Scholar 

  • Wright G, Carver A, Cottom D, Reeves D, Scott A, Simons P, Wilmut I, Garner I, Colman A (1991) High level expression of active human alpha-1-antitrypsin in the milk of transgenic sheep. Bio/Technology 9, 830–834

    CAS  PubMed  Google Scholar 

  • Wu CL, Melton DW (1993) Production of a model for Lesch-Nyhan syndrome in hypoxanthine phosphoribosyltransferase-deficient mice. Nat Genet 3:235–240

    CAS  PubMed  Article  Google Scholar 

  • Yin XJ, Lee HS, Lee YH, Seo YI, Jeon SJ, Choi EG, Cho SJ, Cho SG, Min W, Kang SK, Hwang WS, Kong IK (2005) Cats cloned from fetal and adult somatic cells by nuclear transfer. Reproduction 129:245–249

    CAS  PubMed  Article  Google Scholar 

  • Yong Z, Yuqiang L (1998) Nuclear-cytoplasmic interaction and development of goat embryos reconstructed by nuclear transplantation: production of goats by serially cloning embryos. Biol Reprod 58:266–269

    CAS  PubMed  Article  Google Scholar 

  • Yu G, Chen J, Yu H, Liu S, Chen J, Xu X, Sha H, Zhang X, Wu G, Xu S, Cheng G (2006) Functional disruption of the prion protein gene in cloned goats. J Gen Virol 87:1019–1027

    CAS  PubMed  Article  Google Scholar 

  • Zhou X, Xin J, Fan N, Zou Q, Huang J, Ouyang Z, Zhao Y, Zhao B, Liu Z, Lai S, Yi X, Guo L, Esteban MA, Zeng Y, Yang H, Lai L (2015) Generation of CRISPR/Cas9-mediated gene-targeted pigs via somatic cell nuclear transfer. Cell Mol Life Sci 72:1175–1184

    CAS  PubMed  Article  Google Scholar 

  • Zhou X, Wang L, Du Y, Xie F, Li L, Liu Y, Liu C, Wang S, Zhang S, Huang X, Wang Y, Wei H (2016) Efficient generation of gene-modified pigs harboring precise orthologous human mutation via CRISPR/Cas9-induced homology-directed repair in zygotes. Hum Mutat 37:110–118

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

The primary author was supported by Agriculture and Food Research Initiative Competitive Grant # 2015-67015-22845 from the USDA National Institute of Food and Agriculture, and Maryland Agricultural Experiment Station.

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Correspondence to Bhanu P. Telugu.

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Drs. Bhanu Telugu and Ki-Eun Park are co-founders of RenOVAte Biosciences Inc, a large animal genome editing company.

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Telugu, B.P., Park, KE. & Park, CH. Genome editing and genetic engineering in livestock for advancing agricultural and biomedical applications. Mamm Genome 28, 338–347 (2017). https://doi.org/10.1007/s00335-017-9709-4

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  • DOI: https://doi.org/10.1007/s00335-017-9709-4

Keywords

  • Genome Editing
  • Somatic Cell Nuclear Transfer (SCNT)
  • Sperm-mediated Gene Transfer (SMGT)
  • African Swine Fever
  • Transgenic Pigs