• 1.

    Niemann H, Kues WA. Application of transgenesis in livestock for agriculture and biomedicine. Anim Reprod Sci. 2003;79:291–317.

    CAS 
    PubMed 

    Google Scholar
     

  • 2.

    Klymiuk N, Aigner B, Brem G, Wolf E. Genetic modification of pigs as organ donors for xenotransplantation. Mol Reprod Dev. 2010;77:209–21.

    CAS 

    Google Scholar
     

  • 3.

    Zeyland J, Lipinski D, Slomski R. The current state of xenotransplantation. J Appl Genet. 2015;56:211–8.

    CAS 
    PubMed 

    Google Scholar
     

  • 4.

    Cooper DK. Xenoantigens and xenoantibodies. Xenotransplantation. 1998;5:6–17.

    CAS 
    PubMed 

    Google Scholar
     

  • 5.

    Galili U, Shohet SB, Kobrin E, Stults CL, Macher BA. Man, apes, and Old World monkeys differ from other mammals in the expression of alpha-galactosyl epitopes on nucleated cells. J Biol Chem. 1988;263:17755–62.

    CAS 
    PubMed 

    Google Scholar
     

  • 6.

    Fan N, Lai L. Genetically modified pig models for human diseases. J Genet Genomics. 2013;40:67–73.

    CAS 
    PubMed 

    Google Scholar
     

  • 7.

    Tan W, Proudfoot C, Lillico SG, Whitelaw CB. Gene targeting, genome editing: from Dolly to editors. Transgenic Res. 2016;25:273–87.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 8.

    Kim YG, Cha J, Chandrasegaran S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci U S A. 1996;93:1156–60.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 9.

    Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics. 2010;186:757–61.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 10.

    Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339:819–23.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 11.

    Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. RNA-guided human genome engineering via Cas9. Science. 2013;339:823–6.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 12.

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

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 13.

    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. Somatic cell reprogramming-free generation of genetically modified pigs. Sci Adv. 2016;2:e1600803.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 14.

    Kurome M, Geistlinger L, Kessler B, Zakhartchenko V, Klymiuk N, Wuensch A, Richter A, Baehr A, Kraehe K, Burkhardt K, Flisikowski K, Flisikowska T, Merkl C, Landmann M, Durkovic M, Tschukes A, Kraner S, Schindelhauer D, Petri T, Kind A, Nagashima H, Schnieke A, Zimmer R, Wolf E. Factors influencing the efficiency of generating genetically engineered pigs by nuclear transfer: multi-factorial analysis of a large data set. BMC Biotechnol. 2013;13:43.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 15.

    Cheng W, Zhao H, Yu H, Xin J, Wang J, Zeng L, Yuan Z, Qing Y, Li H, Jia B, Yang C, Shen Y, Zhao L, Pan W, Zhao HY, Wang W, Wei HJ. Efficient generation of GGTA1-null Diannan miniature pigs using TALENs combined with somatic cell nuclear transfer. Reprod Biol Endocrinol. 2016;14:77.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 16.

    Phelps CJ, Koike C, Vaught TD, Boone J, Wells KD, Chen SH, Ball S, Specht SM, Polejaeva IA, Monahan JA, Jobst PM, Sharma SB, Lamborn AE, Garst AS, Moore M, Demetris AJ, Rudert WA, Bottino R, Bertera S, Trucco M, Starzl TE, Dai Y, Ayares DL. Production of alpha 1,3-galactosyltransferase-deficient pigs. Science. 2003;299:411–4.

    CAS 
    PubMed 

    Google Scholar
     

  • 17.

    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. Highly efficient generation of GGTA1 biallelic knockout inbred mini-pigs with TALENs. PLoS One. 2013;8:e84250.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 18.

    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. Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases. Proc Natl Acad Sci U S A. 2011;108:12013–7.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 19.

    Gao H, Zhao C, Xiang X, Li Y, Zhao Y, Li Z, Pan D, Dai Y, Hara H, Cooper DK, Cai Z, Mou L. Production of alpha1,3-galactosyltransferase and cytidine monophosphate-N-acetylneuraminic acid hydroxylase gene double-deficient pigs by CRISPR/Cas9 and handmade cloning. J Reprod Dev. 2017;63:17–26.

    CAS 
    PubMed 

    Google Scholar
     

  • 20.

    Petersen B, Frenzel A, Lucas-Hahn A, Herrmann D, Hassel P, Klein S, Ziegler M, Hadeler KG, Niemann H. Efficient production of biallelic GGTA1 knockout pigs by cytoplasmic microinjection of CRISPR/Cas9 into zygotes. Xenotransplantation. 2016;23:338–46.

    PubMed 

    Google Scholar
     

  • 21.

    Nishio K, Tanihara F, Nguyen TV, Kunihara T, Nii M, Hirata M, Takemoto T, Otoi T. Effects of voltage strength during electroporation on the development and quality of in vitro-produced porcine embryos. Reprod Domest Anim. 2018;53:313–8.

    CAS 
    PubMed 

    Google Scholar
     

  • 22.

    Brinkman EK, Chen T, Amendola M, van Steensel B. Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Res. 2014;42:e168.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 23.

    Barman A, Deb B, Chakraborty S. A glance at genome editing with CRISPR-Cas9 technology. Curr Genet. 2019.

  • 24.

    Kimberland ML, Hou W, Alfonso-Pecchio A, Wilson S, Rao Y, Zhang S, Lu Q. Strategies for controlling CRISPR/Cas9 off-target effects and biological variations in mammalian genome editing experiments. J Biotechnol. 2018;284:91–101.

    CAS 
    PubMed 

    Google Scholar
     

  • 25.

    Le QA, Hirata M, Nguyen NT, Takebayashi K, Wittayarat M, Sato Y, Namula Z, Nii M, Tanihara F, Otoi T. Effects of electroporation treatment using different concentrations of Cas9 protein with gRNA targeting Myostatin (MSTN) genes on the development and gene editing of porcine zygotes. Anim Sci J. 2020;91:e13386.

    PubMed 

    Google Scholar
     

  • 26.

    Cho SW, Kim S, Kim Y, Kweon J, Kim HS, Bae S, Kim JS. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res. 2014;24:132–41.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 27.

    Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol. 2013;31:822–6.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 28.

    Dong Y, Li H, Zhao L, Koopman P, Zhang F, Huang JX. Genome-Wide Off-Target Analysis in CRISPR-Cas9 Modified Mice and Their Offspring. G3 (Bethesda). 2019;9:3645–51.

    CAS 

    Google Scholar
     

  • 29.

    Kang Y, Chu C, Wang F, Niu Y. CRISPR/Cas9-mediated genome editing in nonhuman primates. Dis Model Mech. 2019;12.

  • 30.

    Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, Zhang F. Rationally engineered Cas9 nucleases with improved specificity. Science. 2016;351:84–8.

    CAS 
    PubMed 

    Google Scholar
     

  • 31.

    Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT, Zheng Z, Joung JK. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature. 2016;529:490–5.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 32.

    Lee JK, Jeong E, Lee J, Jung M, Shin E, Kim YH, Lee K, Jung I, Kim D, Kim S, Kim JS. Directed evolution of CRISPR-Cas9 to increase its specificity. Nat Commun. 2018;9:3048.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 33.

    Tanihara F, Hirata M, Nguyen NT, Le QA, Hirano T, Takemoto T, Nakai M, Fuchimoto DI, Otoi T. Generation of a TP53-modified porcine cancer model by CRISPR/Cas9-mediated gene modification in porcine zygotes via electroporation. PLoS One. 2018;13:e0206360.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 34.

    Tanihara F, Hirata M, Nguyen NT, Le QA, Hirano T, Takemoto T, Nakai M, Fuchimoto DI, Otoi T. Generation of PDX-1 mutant porcine blastocysts by introducing CRISPR/Cas9-system into porcine zygotes via electroporation. Anim Sci J. 2019;90:55–61.

    CAS 
    PubMed 

    Google Scholar
     

  • 35.

    Tanihara F, Hirata M, Thi Nguyen N, Anh Le Q, Hirano T, Otoi T. Generation of viable PDX1 gene-edited founder pigs as providers of nonmosaics. Mol Reprod Dev. 2020;87:471–81.

    CAS 
    PubMed 

    Google Scholar
     

  • 36.

    Wang RG, Ruan M, Zhang RJ, Chen L, Li XX, Fang B, Li C, Ren XY, Liu JY, Xiong Q, Zhang LN, Jin Y, Li L, Li R, Wang Y, Yang HY, Dai YF. Antigenicity of tissues and organs from GGTA1/CMAH/beta4GalNT2 triple gene knockout pigs. J Biomed Res. 2018.

  • 37.

    Sharma A, Naziruddin B, Cui C, Martin MJ, Xu H, Wan H, Lei Y, Harrison C, Yin J, Okabe J, Mathews C, Stark A, Adams CS, Houtz J, Wiseman BS, Byrne GW, Logan JS. Pig cells that lack the gene for alpha1-3 galactosyltransferase express low levels of the gal antigen. Transplantation. 2003;75:430–6.

    CAS 
    PubMed 

    Google Scholar
     

  • 38.

    Lai L, Kolber-Simonds D, Park KW, Cheong HT, Greenstein JL, Im GS, Samuel M, Bonk A, Rieke A, Day BN, Murphy CN, Carter DB, Hawley RJ, Prather RS. Production of alpha-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning. Science. 2002;295:1089–92.

    CAS 
    PubMed 

    Google Scholar
     

  • 39.

    Huai G, Qi P, Yang H, Wang Y. Characteristics of alpha-gal epitope, anti-gal antibody, alpha1,3 galactosyltransferase and its clinical exploitation (review). Int J Mol Med. 2016;37:11–20.

    CAS 
    PubMed 

    Google Scholar
     

  • 40.

    Milland J, Christiansen D, Lazarus BD, Taylor SG, Xing PX, Sandrin MS. The molecular basis for galalpha(1,3) gal expression in animals with a deletion of the alpha1,3galactosyltransferase gene. J Immunol. 2006;176:2448–54.

    CAS 
    PubMed 

    Google Scholar
     

  • 41.

    Butler JR, Skill NJ, Priestman DL, Platt FM, Li P, Estrada JL, Martens GR, Ladowski JM, Tector M, Tector AJ. Silencing the porcine iGb3s gene does not affect Galalpha3Gal levels or measures of anticipated pig-to-human and pig-to-primate acute rejection. Xenotransplantation. 2016;23:106–16.

    PubMed 

    Google Scholar
     

  • 42.

    Hai T, Teng F, Guo R, Li W, Zhou Q. One-step generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Res. 2014;24:372–5.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 43.

    Burkard C, Lillico SG, Reid E, Jackson B, Mileham AJ, Ait-Ali T, Whitelaw CB, Archibald AL. Precision engineering for PRRSV resistance in pigs: macrophages from genome edited pigs lacking CD163 SRCR5 domain are fully resistant to both PRRSV genotypes while maintaining biological function. PLoS Pathog. 2017;13:e1006206.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 44.

    Hirata M, Tanihara F, Wittayarat M, Hirano T, Nguyen NT, Le QA, Namula Z, Nii M, Otoi T. Genome mutation after introduction of the gene editing by electroporation of Cas9 protein (GEEP) system in matured oocytes and putative zygotes. Vitro Cell Dev Biol Anim. 2019;55:237–42.

    CAS 

    Google Scholar
     

  • 45.

    Su X, Chen W, Cai Q, Liang P, Chen Y, Cong P, Huang J. Production of non-mosaic genome edited porcine embryos by injection of CRISPR/Cas9 into germinal vesicle oocytes. J Genet Genomics. 2019;46:335–42.

    PubMed 

    Google Scholar
     

  • 46.

    Onuma A, Fujii W, Sugiura K, Naito K. Efficient mutagenesis by CRISPR/Cas system during meiotic maturation of porcine oocytes. J Reprod Dev. 2017;63:45–50.

    CAS 
    PubMed 

    Google Scholar
     

  • 47.

    Byrne G, Ahmad-Villiers S, Du Z, McGregor C. B4GALNT2 and xenotransplantation: a newly appreciated xenogeneic antigen. Xenotransplantation. 2018;25:e12394.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 48.

    Nguyen DH, Tangvoranuntakul P, Varki A. Effects of natural human antibodies against a nonhuman sialic acid that metabolically incorporates into activated and malignant immune cells. J Immunol. 2005;175:228–36.

    CAS 
    PubMed 

    Google Scholar
     

  • 49.

    Hurh S, Kang B, Choi I, Cho B, Lee EM, Kim H, Kim YJ, Chung YS, Jeong JC, Hwang JI, Kim JY, Lee BC, Surh CD, Yang J, Ahn C. Human antibody reactivity against xenogeneic N-glycolylneuraminic acid and galactose-alpha-1,3-galactose antigen. Xenotransplantation. 2016;23:279–92.

    PubMed 

    Google Scholar
     

  • 50.

    Martens GR, Reyes LM, Li P, Butler JR, Ladowski JM, Estrada JL, Sidner RA, Eckhoff DE, Tector M, Tector AJ. Humoral reactivity of renal transplant-waitlisted patients to cells from GGTA1/CMAH/B4GalNT2, and SLA class I knockout pigs. Transplantation. 2017;101:e86–92.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 51.

    Estrada JL, Martens G, Li P, Adams A, Newell KA, Ford ML, Butler JR, Sidner R, Tector M, Tector J. Evaluation of human and non-human primate antibody binding to pig cells lacking GGTA1/CMAH/beta4GalNT2 genes. Xenotransplantation. 2015;22:194–202.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 52.

    Fischer K, Rieblinger B, Hein R, Sfriso R, Zuber J, Fischer A, Klinger B, Liang W, Flisikowski K, Kurome M, Zakhartchenko V, Kessler B, Wolf E, Rieben R, Schwinzer R, Kind A, Schnieke A. Viable pigs after simultaneous inactivation of porcine MHC class I and three xenoreactive antigen genes GGTA1, CMAH and B4GALNT2. Xenotransplantation. 2019:e12560.

  • 53.

    Zhang R, Wang Y, Chen L, Wang R, Li C, Li X, Fang B, Ren X, Ruan M, Liu J, Xiong Q, Zhang L, Jin Y, Zhang M, Liu X, Li L, Chen Q, Pan D, Li R, Cooper DKC, Yang H, Dai Y. Reducing immunoreactivity of porcine bioprosthetic heart valves by genetically-deleting three major glycan antigens, GGTA1/beta4GalNT2/CMAH. Acta Biomater. 2018;72:196–205.

    CAS 
    PubMed 

    Google Scholar
     

  • 54.

    Liu F, Liu J, Yuan Z, Qing Y, Li H, Xu K, Zhu W, Zhao H, Jia B, Pan W, Guo J, Zhang X, Cheng W, Wang W, Zhao HY, Wei HJ. Generation of GTKO Diannan miniature pig expressing human complementary regulator proteins hCD55 and hCD59 via T2A peptide-based Bicistronic vectors and SCNT. Mol Biotechnol. 2018;60:550–62.

    CAS 
    PubMed 

    Google Scholar
     

  • 55.

    Cho B, Koo OJ, Hwang JI, Kim H, Lee EM, Hurh S, Park SJ, Ro H, Yang J, Surh CD, D’Apice AJ, Lee BC, Ahn C. Generation of soluble human tumor necrosis factor-alpha receptor 1-fc transgenic pig. Transplantation. 2011;92:139–47.

    CAS 
    PubMed 

    Google Scholar
     

  • 56.

    Kim GA, Lee EM, Cho B, Alam Z, Kim SJ, Lee S, Oh HJ, Hwang JI, Ahn C, Lee BC. Generation by somatic cell nuclear transfer of GGTA1 knockout pigs expressing soluble human TNFRI-fc and human HO-1. Transgenic Res. 2019;28:91–102.

    CAS 
    PubMed 

    Google Scholar
     

  • 57.

    Park SJ, Cho B, Koo OJ, Kim H, Kang JT, Hurh S, Kim SJ, Yeom HJ, Moon J, Lee EM, Choi JY, Hong JH, Jang G, Hwang JI, Yang J, Lee BC, Ahn C. Production and characterization of soluble human TNFRI-fc and human HO-1(HMOX1) transgenic pigs by using the F2A peptide. Transgenic Res. 2014;23:407–19.

    CAS 
    PubMed 

    Google Scholar
     

  • 58.

    Zhang J, Xie C, Lu Y, Zhou M, Qu Z, Yao D, Qiu C, Xu J, Pan D, Dai Y, Hara H, Cooper DKC, Ma S, Li M, Cai Z, Mou L. Potential antigens involved in delayed Xenograft rejection in a Ggta1/Cmah Dko pig-to-monkey model. Sci Rep. 2017;7:10024.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 59.

    Watanabe H, Sahara H, Nomura S, Tanabe T, Ekanayake-Alper DK, Boyd LK, Louras NJ, Asfour A, Danton MA, Ho SH, Arn SJ, Hawley RJ, Shimizu A, Nagayasu T, Ayares D, Lorber MI, Sykes M, Sachs DH, Yamada K. GalT-KO pig lungs are highly susceptible to acute vascular rejection in baboons, which may be mitigated by transgenic expression of hCD47 on porcine blood vessels. Xenotransplantation. 2018;25:e12391.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 60.

    Meier RPH, Muller YD, Balaphas A, Morel P, Pascual M, Seebach JD, Buhler LH. Xenotransplantation: back to the future? Transpl Int. 2018;31:465–77.

    PubMed 

    Google Scholar
     

  • 61.

    Nguyen TV, Tanihara F, Do L, Sato Y, Taniguchi M, Takagi M, Van Nguyen T, Otoi T. Chlorogenic acid supplementation during in vitro maturation improves maturation, fertilization and developmental competence of porcine oocytes. Reprod Domest Anim. 2017;52:969–75.

    CAS 
    PubMed 

    Google Scholar
     

  • 62.

    Naito Y, Hino K, Bono H, Ui-Tei K. CRISPRdirect: software for designing CRISPR/Cas guide RNA with reduced off-target sites. Bioinformatics. 2015;31:1120–3.

    CAS 
    PubMed 

    Google Scholar
     

  • 63.

    Cradick TJ, Qiu P, Lee CM, Fine EJ, Bao G. COSMID: a web-based tool for identifying and validating CRISPR/Cas off-target sites. Mol Ther Nucleic Acids. 2014;3:e214.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 64.

    Onishi A, Iwamoto M, Akita T, Mikawa S, Takeda K, Awata T, Hanada H, Perry AC. Pig cloning by microinjection of fetal fibroblast nuclei. Science. 2000;289:1188–90.

    CAS 
    PubMed 

    Google Scholar
     

  • 65.

    Bennett GL, Leymaster KA. Integration of ovulation rate, potential embryonic viability and uterine capacity into a model of litter size in swine. J Anim Sci. 1989;67:1230–41.

    CAS 
    PubMed 

    Google Scholar
     

  • 66.

    Bolet G, Botte FM, Locatelli A, Gruand J, Terqui M, Berthelot F. Components of prolificacy in hyperprolific large white sows compared with the Meishan and large white breeds. Genet Sel Evol. 1986;18:333–42.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 67.

    Machaty Z, Day BN, Prather RS. Development of early porcine embryos in vitro and in vivo. Biol Reprod. 1998;59:451–5.

    CAS 
    PubMed 

    Google Scholar
     

  • 68.

    Pinello L, Canver MC, Hoban MD, Orkin SH, Kohn DB, Bauer DE, Yuan GC. Analyzing CRISPR genome-editing experiments with CRISPResso. Nat Biotechnol. 2016;34:695–7.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     



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