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Transgenic farm animals: the status of research and prospects

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Russian Journal of Genetics: Applied Research

Abstract

The production of transgenic animals is of great interest for current basic and applied research. This article is a review of methods for the production of transgenic farm animals and their advantages and disadvantages. The advances in various fields of genetic engineering of domestic animals are discussed, including the creation of animals with altered metabolism for higher quality and productivity, animals genetically resistant to infectious diseases, producers of biologically active recombinant proteins, donors of organs for human transplantation (xenotransplantation), and animal models.

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References

  • Aigner, B., Renner, S., Kessler, B., Klymiuk, N., Kurome, M., Wünsch, A., and Wolf, E., Transgenic pigs as models for translational biomedical research, J. Mol. Med., 2010, vol. 88, no. 7, pp. 653–664. doi 10.1007/s00109-010-0610-9.

    Article  PubMed  Google Scholar 

  • Bagle, T.R., Kunkulol, R.R., Baig, M.S., and More, S.Y., Transgenic animals and their application in medicine, Int. J. Med. Res. Health Sci., 2013, vol. 2, no. 1, pp. 107–116.

    Google Scholar 

  • Bosch, P., Forcato, D.O., Alustiza, F.E., et al., Exogenous enzymes upgrade transgenesis and genetic engineering of farm animals, Cell. Mol. Life Sci., 2015, vol. 72, pp. 1907–1929.

    Article  CAS  PubMed  Google Scholar 

  • Brackett, B.G., Baranska, W., Sawikki, W., and Korpowski, H., Uptake of heterologous genome by mammalian spermatozoa and itstransfer to ova through fertilization, Proc. Natl. Acad. Sci., 1971, vol. 68, pp. 353–357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brem, G., Brenig, B., Goodman, H.M., et al., Production of transgenic mice, rabbits and pig by microinjection into pronuclei, Zuchtkunde, 1985, vol. 20, pp. 251–252.

    Google Scholar 

  • Brinster, R. and Nagano, M., Spermatogonial stem cell transplantation, cryopreservation and culture, Semin. Cell. Dev. Biol., 1998, vol. 9, no. 4, pp. 401–409.

    Article  CAS  Google Scholar 

  • Byun, S.J., Kim, S.W., Kim, K.W., et al., Oviduct specific enhanced green fluorescent protein expression in transgenic chickens, Biosci. Biotechnol. Biochem., 2011, vol. 75, no. 4, pp. 646–649.

    Article  CAS  PubMed  Google Scholar 

  • Campbell, K.H., McWhir, J., Ritchie, W.A., and Wilmut, I., Sheep cloned by nuclear transfer from a cultured cell line, Nature, 1996, vol. 380, pp. 64–66.

    Article  CAS  PubMed  Google Scholar 

  • Carlson, D.F., Tan, W., Lillico, S.G., et al., Efficient TALEN-mediated gene knockout in livestock, Proc. Natl. Acad. Sci. U.S.A., 2012, vol. 109, no. 43, pp. 17382–17387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan, A., Homan, E., Ballou, L., et al., Transgenic cattle produced by reverse-transcribed gene transfer in oocytes, Proc. Natl. Acad. Sci. U.S.A., 1998, vol. 95, pp. 14028–14033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang, K., Qian, J., Jiang, M., et al., Effective generation of transgenic pigs and mice by linker based sperm-mediated gene transfer, BMC Biotechnol., 2002, vol. 2, p. 5. doi 10.1186/1472-6750-2.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chapman, S.C., Lawson, A., Macarthur, W.C., et al., Ubiquitous GFP expression in transgenic chickens using a lentivira vector, Development, 2005, vol. 132, pp. 935–940.

    Article  CAS  PubMed  Google Scholar 

  • Cibelli, J.B., Campbell, K.H., Seidel, G.E., et al., The health profile of cloned animals, Nat. Biotechnol., 2002, vol. 20, pp. 13–14.

    Article  CAS  PubMed  Google Scholar 

  • Clark, K.J., Carlson, D.F., and Fahrenkrug, S.C., Pigs taking wings with transposons and recombinases, Genome Biol., 2007, vol. 8., suppl. 1, p. 13.

    Article  Google Scholar 

  • Cong, L., Ran, F.A., Cox, D., et al., Multiplex genome engineering using CRISPR/Cas system, Science, 2013, vol. 339, no. 6121, pp. 819–823.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • d’Apice, A.J. and Cowan, P.J., Xenotransplantation: The next generation of engineered animals, Transpl. Immunol., 2009, vol. 21, pp. 111–115.

    Article  PubMed  Google Scholar 

  • Dai, Y., Vaught, T.D., Boone, J., et al., Targeted disruption of the alpha1,3-galactosyltransferase gene in cloned pigs, Nat. Biotechnol., 2002, vol. 20, pp. 251–255.

    Article  CAS  PubMed  Google Scholar 

  • de Koning, D.J., Archibald, A., and Haley, C.S., Livestock genomics: Bridging the gap between mice and men, Trends Biotechnol., 2007, vol. 25, pp. 483–489.

    Article  PubMed  CAS  Google Scholar 

  • Delacote, F., Perez, C., Guyot, V., et al., High frequency targeted mutagenesis using engineered endonucleases and DNA-end processing enzymes, PloS One, 2013, vol. 8, no. 1, p. e53217.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dougherty, D.C. and Sanders, M.M., Estrogen action: Revitalization of the chick oviduct model, Trends Endocrinol. Metab., 2005, vol. 16, pp. 414–419.

    Article  CAS  PubMed  Google Scholar 

  • Dyck, M.K., Lacroix, D., Pothier, F., and Sirard, M.A., Making recombinant proteins in animals–different systems, different applications, Trends Biotechnol., 2003, vol. 21, no. 9, pp. 394–409.

    Article  CAS  PubMed  Google Scholar 

  • Ebert, K.M., Low, M.J., Overstrom, E.W., et al., Moloney MLV-rat somatotropin fusion gene produces biologically active somatotropin in a transgenic pig, Mol. Endocrinol., 1988, vol. 2, no. 3, pp. 277–283.

    Article  CAS  PubMed  Google Scholar 

  • Ernst, L.K. and Zinovieva, N.A., Biologicheskie problemy zhivotnovodstva v XXI veke (Biological Problems of Livestock in the 21st Century), Moscow: Ross. Akad. S-kh. Nauk, 2008.

    Google Scholar 

  • Ernst, L.K., Volkova, N.A., and Zinovieva, N.A., Fenotipicheskii effekt ekspressii rekombinantnykh genov v organizme transgennykh zhivotnykh raznykh vidov (Phenotypic Effects of Expression of Recombinant Genes in an Organism of Transgenic Animals of Various Species), Moscow: Ross. Akad. S-kh. Nauk, 2008.

  • Furlan-Magaril, M., Rebollar, E., Guerrero, G., et al., An insulator embedded in the chicken ß-globin locus regulates chromatin domain configuration and differential gene expression, Nucleic Acid Res., 2011, vol. 39, no. 1, pp. 89–103.

    Article  CAS  PubMed  Google Scholar 

  • Gandolfi, F., Lavitrano, M., Camaioni, A., et al., The use of sperm-mediated gene transfer for the generation of transgenic pigs, J. Reprod. Fertil., 1989, vol. 81, pp. 23–28.

    Article  Google Scholar 

  • Gandolfi, F., Spermatozoa, DNA binding and transgenic animals, Trans. Res., 1998, vol. 7, pp. 147–155.

    CAS  Google Scholar 

  • Garrels, W., Mates, L., Holler, S., et al., Generation of transgenic pigs by the sleeping beauty transposition in zygotes, Reprod. Dom. Anim., 2010, vol. 45, p. 65.

    Google Scholar 

  • Ghazizadeh, S., Harington, R., and Taichmann, L., In vivo transduction of mouse epidermis with recombinant retroviral vectors: Implications for cutaneous gene therapy, Gene Ther., 1999, vol. 7, pp. 1267–1275.

    Article  CAS  Google Scholar 

  • Gordon, J.W., Scangos, D.J., Plotkin, J.A., et al., Genetic transformation of mouse embryos by microinjection of purified DNA, Proc. Natl. Acad. Sci. U.S.A., 1980, vol. 77, pp. 7380–7384.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grosse-Hovest, L., Hartlapp, I., Marwan, W., et al., A recombinant bispecific single-chain antibody induces targeted, supra-agonistic CD28-stimulation and tumor cell killing, Eur. J. Immunol., 2003, vol. 33, no. 5, pp. 1334–1340.

    Article  CAS  PubMed  Google Scholar 

  • Grosse-Hovest, L., Müller, S., Minoia, R., et al., Cloned transgenic farm animals produce a bispecific antibody for t cell-mediated tumor cell killing, Proc. Natl. Acad. Sci., 2004, vol. 101, no. 18, pp. 6858–6863.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grosse-Hovest, L., Wick, W., Minoia, R., et al., Supraagonistic, bispecific single-chain antibody purified from the serum of cloned, transgenic cows induces T-cell-mediated killing of glioblastoma cells in vitro and in vivo, Int. J. Cancer, 2005, vol. 117, no. 6, pp. 1060–1064.

    CAS  PubMed  Google Scholar 

  • Hai, T., Teng, F., Guo, R., et al., One-step generation of knockout pigs by zygote injection of Crispr/Cas system, Cell Res., 2014, vol. 24, pp. 372–375.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammer, R., Pursel, V., Rexroad, J., et al., Production of trans-genie rabbits, sheep and pigs by microinjection, Nature, 1985, vol. 315, pp. 680–683.

    CAS  PubMed  Google Scholar 

  • Harrison, M.M., Jenkins, B.V., O’Connor-Giles, K.M., and Wildonger, J.A., CRISPR view of development, Genes & Dev., 2014, vol. 28, pp. 1859–1872. doi 10.1101/gad.248252..

    Article  CAS  Google Scholar 

  • Harvey, A.J. Speksnijder, Baugh, L.R., et al., Expression of exogenous protein in the egg white of transgenic chickens, Nat. Biotechnol., 2002, vol. 20, pp. 396–399.

    Article  CAS  PubMed  Google Scholar 

  • Haskell, R. and Bowen, R., Efficient production of transgenic cattle by retroviral infection of early embryos, Mol. Reprod. Dev., 1995, vol. 40, no. 3, pp. 386–390.

    Article  CAS  PubMed  Google Scholar 

  • Hauschild, J., Petersen, B., Santiago, Y., et al., Efficient generation of a biallelic knockout in pigs using zincfinger nucleases, Proc. Natl. Acad. Sci., 2011, vol. 108, pp. 12013–12017.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heo, Y., Quan, X., Xu, Y., et al., CRISPR/Cas9 nucleasemediated gene knock-in in bovine pluripotent stem cells and embryos, Stem Cells Dev. doi 10.1089/scd.2014..

  • Hofmann, A., Kessler, B., Ewerling, S., et al., Efficient transgenesis in farm animals by lentiviral vectors, EMBO Rep., 2003, vol. 4, no. 11, pp. 1054–1060. doi 10.1038/sj.embor..

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hofmann, A., Kessler, B., Ewerling, S., et al., Epigenetic regulation of lentiviral transgene vectors in a large animal model, MolTher, 2006, vol. 13, pp. 59–66.

    CAS  Google Scholar 

  • Hofmann, A., Zakhartchenko, V., Weppert, M., et al., Generation of transgenic cattle by lentiviral gene transfer into oocytes, Biol. Reprod., 2004, vol. 71, no. 2, pp. 405–409.

    Article  CAS  PubMed  Google Scholar 

  • Horii, T., Arai, Y., Yamazaki, M., et al., Validation of microinjection methods for generating knockout mice by CRISPR/Cas-mediated genome engineering, Sci. Rep., 2014, vol. 4, p. 4513. doi 10.1038/srep.

    Article  PubMed  CAS  Google Scholar 

  • Houdebine, L., Production of pharmaceutical proteins by transgenic animals, Comp. Immunol., Microbiol. Infect. Dis., 2009, vol. 32, pp. 107–121.

    Article  Google Scholar 

  • Iqbal, K., Barg-Kues, B., Broll, S., et al., Cytoplasmic injection of circular plasmids allows targeted expression in mammalian embryos, BioTechniques, 2009, vol. 47, pp. 959–968.

    Article  PubMed  CAS  Google Scholar 

  • Ivarie, R., Aviantransgenesis: Progress towards the promise, Trends Biotechnol., 2003, vol. 21, pp. 14–19.

    Article  CAS  PubMed  Google Scholar 

  • Ivics, Z., Hackett, P.B., Plasterk, R.H., and Izsvák, Z., Molecular reconstruction of sleeping beauty, a Tc1-616 like transposon from fish, and its transposition in human cells, Cell, 1997, vol. 91, pp. 501–510.

    CAS  PubMed  Google Scholar 

  • Jacobsen, J.C., Bawden, C.S., Rudiger, S.R., et al., An ovine transgenic Huntington’s disease model, Hum. Mol. Genet., 2010, vol. 19, pp. 1873–1882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jahner, D. and Jaenisch, R., Retorvirus-induced de novo methylation of flanking host sequences correlates with gene inactivity, Nature, 1985, vol. 315, pp. 594–597.

    Article  CAS  PubMed  Google Scholar 

  • Jim, K., First USapproval for a transgenic animal drug, Nat. Biotechnol., 2009, vol. 27, no. 4, pp. 302–304.

  • Kamihira, M., Ono, K., Esaka, K., et al., High-level expression of single-chain fv-fc fusion protein in serum and egg white of genetically manipulated chickens by using a retroviral vector, J. Virol., 2005, vol. 79, no. 17, pp. 10864–10874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klymiuk, N., Böcker, W., Schönitzer, V., et al., First inducible transgene expression in porcine large animal models, FASEB J., 2012, vol. 26, no. 3, pp. 1086–1099.

    Article  CAS  PubMed  Google Scholar 

  • Kodama, D., Nishimiya, D., Nishijima, K., et al., Chicken oviduct-specific expression of transgene by a hybrid ovalbumin enhancer and the Tet expression system, J. Biosci. Bioeng., 2012, vol. 113, no. 2, pp. 146–153.

    Article  CAS  PubMed  Google Scholar 

  • Kolber-Simonds, D., Lai, L., Watt, S.R., et al., Production of alpha-1,3-galactosyltransferase null pigs by means of nuclear transfer with fibroblasts bearing loss of heterozygosity mutations, Proc. Natl. Acad. Sci. U.S.A., 2004, vol. 101, no. 19, pp. 7335–7340.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kues, W.A. and Niemann, H., Advances in farm animal transgenesis, Prev. Vet. Med., 2011, vol. 102, pp. 146–156.

    Article  PubMed  Google Scholar 

  • Kues, W.A., Garrels, W., Mates, L., et al., Production of transgenic pigs by the Sleeping Beauty transposon system, Transgenic Res., 2010, vol. 19, p. 336.

    Google Scholar 

  • Kuroiwa, Y., Kasinathan, P., Choi, Y.J., et al., Cloned transchromosomic calves producing human immunoglobulin, Nat. Biotechnol., 2002, vol. 20, pp. 889–894.

    Article  CAS  PubMed  Google Scholar 

  • Kwon, M.S., Koo, B.C., Choi, B.R., et al., Generation of transgenic chickens that produce bioactive human granulocyte- colony stimulating factor, Mol. Reprod. Dev., 2008, vol. 75, pp. 1120–1126.

    Article  CAS  PubMed  Google Scholar 

  • Kwon, S.C., Choi, J.W., Jang, H.J., et al., Production of biofunctional recombinant human interleukin 1 receptor antagonist (rhIL1RN) from transgenic quail egg white, Biol. Reprod., 2010, vol. 82, pp. 1057–1064.

    Article  CAS  PubMed  Google Scholar 

  • Lai, L., Kolber-Simonds, D., Park, K.W., et al., Production of alpha-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning, Science, 2002, vol. 295, no. 5557, pp. 1089–1092.

    Article  CAS  PubMed  Google Scholar 

  • Lassnig, C. and Mueller, M., Disease-resistant transgenic animals, in Sustainable Food Production, Christou, P. et al., Eds., Springer Science + Business Media New York, 2013, pp. 747–760. doi 10.1007/978-1-4614-5797-.

    Chapter  Google Scholar 

  • Lee, S., Park, H., Kong, I., and Wang, Z., 30 a transcription activatorlike effector nuclease (Talen)-mediated universal gene knock-in strategy for mammary glandsspecific expression of recombinant proteins in dairy cattle, Reprod. Fertil. Dev., 2013, vol. 26, p. 129.

    Article  Google Scholar 

  • Lillico, S.G., Sherman, A., Mcgrew, M.J., et al., Oviductspecific expression of two therapeutic proteins in transgenic hens, Proc. Natl. Acad. Sci. U.S.A., 2007, vol. 104, no. 6, pp. 1771–1776.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo, Y., Lin, L., Bolund, L., Jensen, T.G., and Sørensen, C.B., Genetically modified pigs for biomedical research, J. Inherit. Metab. Dis., 2012, vol. 35, no. 4, pp. 695–713.

    Article  CAS  PubMed  Google Scholar 

  • Maione, B., Lavitrano, M., Spadatora, C., and Kiessling, A.A., Sperm-mediated gene transfer in mice, Mol. Reprod. Dev., 1998, vol. 50, pp. 406–409.

    Article  CAS  PubMed  Google Scholar 

  • Mali, P., Yang, L., Esvelt, K.M., et al., RNA-guided human genome engineering via Cas9, Science, 2013, vol. 339, pp. 823–826.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCreath, K.J., Howcroft, J., Campbell, K.H., et al., Production of gene-targeted sheep by nuclear transfer from cultured somatic cells, Nature, 2000, vol. 405, pp. 1066–1069.

    Article  CAS  PubMed  Google Scholar 

  • McGrew, M.J., Sherman, A., Ellard, F.M., et al., Efficient production of germline transgenic chickens using lentiviral vectors, EMBO Rep., 2004, vol. 5, pp. 728–733.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melo, E.O., Canavessi, A.M., Franco, M.M., and Rumpf, R., Animal transgenesis: State of the art and applications, J. Appl. Genet., 2007, vol. 48, no. 1, pp. 47–61.

    Article  PubMed  Google Scholar 

  • Miller, J.C., Tan, S., Qiao, G., et al., A TALE nuclease architecture for efficient genome editing, Nat. Biotechnol., 2011, vol. 29, no. 2, pp. 143–148.

    Article  CAS  PubMed  Google Scholar 

  • Miyahara, D., Mori, T., Makino, R., et al., Culture conditions for maintain propagation, long-term survival and germline transmission of chicken primordial germ cell-like cells, J. Poult. Sci., 2014, vol. 51, pp. 87–95.

    Article  CAS  Google Scholar 

  • Moghaddassi, S., Eyestone, W., and Bishop, C.E., TALEN-mediated modification of the bovine genome for large-scale production of human serum albumin, PLoS One, 2014, vol. 9, no. 2, p. e89631.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mozdziak, P.E. and Petitte, J.N., Status of transgenic chicken models for developmental biology, Dev. Dyn., 2004, vol. 229, pp. 414–421.

    Article  CAS  PubMed  Google Scholar 

  • Mozdziak, P.E., Borwornpinyo, S., McCoy, D.W., and Petitte, J.N., Development of transgenic chickens expressing bacterial betagalactosidase, Dev. Dyn., 2003, vol. 226, pp. 439–445.

    Article  CAS  PubMed  Google Scholar 

  • Muramatsu, T., Mizutani, Y., Ohmori, Y., and Okumura, J., Comparison of three nonviral transfection methods for foreign gene expression in early chicken embryos in ovo, Biochem. Biophys. Res. Commun., 1997, vol. 230, pp. 376–380.

    Article  CAS  PubMed  Google Scholar 

  • Nakamura, Y., Kagami, H., and Tagami, T., Development, differentiation and manipulation of chickengerm cells, Dev. Growth Differ., 2013, vol. 55, pp. 20–40.

    Article  PubMed  Google Scholar 

  • Nemudryi, A.A., Valetdinova, K.R., and Medvedev, S.P., et al., Genome editing systems TALEN and CRISPR/Cas as tools of discovery, Acta Nat., 2014, vol. 6, no. 3 (22), pp. 20–42.

    Google Scholar 

  • Ni, W., Qiao, J., Hu, S., et al., Efficient gene knockout in goats using CRISPR/Cas9 system, PLoS One, 2014, vol. 9, no. 9, p. e106718. doi 10.1371/journal.pone..

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Palmiter, R., Sandgren, E., Avarbock, M., et al., Heterologous introns can enhance expression of transgenes in mice, Proc. Natl. Acad. Sci. U.S.A., 1991, vol. 88, pp. 478–482.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmiter, R.D., Brinster, R.L., Hammer, R.E., et al., Dramatic growth of mice that develop from eggs micro-injected with metallothionein-growth hormone fusion gene, Nature, 1982, vol. 300, pp. 611–615.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perry, A.C., Rothman, A., Heras de las, J.I., et al., Efficient metaphase II transgenesis with different transgene archetypes, Nat. Biotechnol., 2001, vol. 19, pp. 1071–1073.

    Article  CAS  PubMed  Google Scholar 

  • Perry, A.C.F., Wakayama, T., Kishikawa, H., et al., Mammalian transgenesis by intracytoplasmic sperm injection, Science, 1999, vol. 284, pp. 1180–1183.

    Article  CAS  PubMed  Google Scholar 

  • Phelps, C.J., Koike, C., Vaught, T.D., et al., Production of alpha 1,3-galactosyltransferase-deficient pigs, Science, 2003, vol. 299, no. 5605, pp. 411–414.

    Article  CAS  PubMed  Google Scholar 

  • Porteus, M.H. and Carroll, D., Gene targeting using zinc finger nucleases, Nat. Biotech, 2005, vol. 23, pp. 967–973.

    Article  CAS  Google Scholar 

  • Pursel, V.G., Hammer, R.E., Bolt, D.J., et al., Integration, expression and germ-line transmission of growth-related genes in pigs, J. Reprod. Fertil., 1990, vol. 41, suppl., pp. 77–87.

    CAS  Google Scholar 

  • Raju, T.S., Briggs, J.B., Borge, S.M., and Jones, A.J., Species-specific variation in glycosylation of IgG: Evidence for the species-specific sialylation and branch-specific galactosylation and importance for engineering recombinant glycoprotein therapeutics, Glycobiology, 2000, vol. 10, pp. 477–486.

    Article  CAS  PubMed  Google Scholar 

  • Rapp, J.C., Harvey, A.J., Speksnijder, G.L., et al., Biologically active human interferon a-2b produced in the egg white of transgenic hens, Transgenic Res., 2003, vol. 12, pp. 569–575.

    Article  CAS  PubMed  Google Scholar 

  • Renner, S., Fehlings, C., Herbach, N., et al., Glucose intolerance and reduced proliferation of pancreatic betacells in transgenic pigs with impaired glucose-dependent insulinotropic polypeptide function, Diabetes, 2010, vol. 59, pp. 1228–1238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rexroad, C.E., Hammer, R.E., Behringer, R.R., et al., Insertion, expression and physiology of growth-regulating genes in ruminants, J. Reprod. Fertil., 1990, vol. 41, suppl., pp. 119–124.

    CAS  Google Scholar 

  • Rexroad, C.E., Hammer, R.E., Bolt, D.J., et al., Production of transgenic sheep with growth-regulating genes, Mol. Reprod. Dev., 1989, vol. 1, no. 3, pp. 164–169.

    Article  CAS  PubMed  Google Scholar 

  • Richt, J.A., Kasinathan, P., Hamir, A.N., et al., Production of cattle lacking prion protein, Nat. Biotechnol., 2007, vol. 25, pp. 132–138.

    Article  CAS  PubMed  Google Scholar 

  • Ritchie, W.A., King, T., Neil, C., et al., Transgenic sheep designed for transplantation studies, Mol. Reprod. Dev., 2009, vol. 76, pp. 61–64.

    Article  CAS  PubMed  Google Scholar 

  • Rogers, C.S., Stoltz, D.A., Meyerholz, D.K., et al., Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs, Science, 2008, vol. 321, pp. 1837–1841.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savchenkova, I.P., Zinovieva N.A., Bulla I., and Brem, G., Embryonic stem cells, their genetic modification by homologous recombination and the use in the production of transgenic animals, Usp. Sovrem. Biol., 1996, vol. 116, no. 1, pp. 78–91.

    Google Scholar 

  • Schellander, K., Peli, J., Small, F., and Brem, G., Artificial insemination in cattle with DNA-treated sperm, Anim. Biotechnol., 1995, vol. 6, pp. 41–50.

    Article  Google Scholar 

  • Schnieke, A., Kind, A., Ritchie, W., et al., Human factor IX transgenic sheep produced by transfer of nuclei from transfected fetal fibroblasts, Science, 1997, vol. 278, pp. 2130–2133.

    Article  CAS  PubMed  Google Scholar 

  • Scott, B.B. and Lois, C., Generation of tissue-specific transgenic birds with lentiviral vectors, Proc. Natl. Acad. Sci. U.S.A., 2005, vol. 102, no. 45, pp. 16443–16447.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scott, B.B., Velho, T.A., Sim, S., and Lois, C., Applications of avian transgenesis, ILAR J., 2010, vol. 51, no. 4, pp. 353–61.

    Article  CAS  PubMed  Google Scholar 

  • Serov, O.L., Transgenic animals: Fundamental and applied aspects, Russ. J. Genet., Appl. Res., 2014, vol. 4, no. 3, pp. 200–207.

    Article  Google Scholar 

  • Shimizu, M., Losos, J.K., and Gibbins, A.M., Analysis of an approach to oviduct-specific expression of modified chicken lysozyme genes, Biochem. Cell Biol., 2005, vol. 83, no. 1, pp. 49–60.

    Article  CAS  PubMed  Google Scholar 

  • Shumakov, V. and Tonevitskii, A., Xenotransplantation: Scientific and ethical problems, Chelovek, 1999, no. 6. http://vivovoco.astronet.ru/VV/PAPERS/MEN/TRANSPLANT. HTM. Cited April 14, 2015.

  • Simons, J., Wilmut, I., Clark, A., et al., Gene transfer into sheep, Bio/Technol., 1988, vol. 6, pp. 179–183.

    Article  CAS  Google Scholar 

  • Singina, G.N., Lopukhov, A.V., Zinovieva, N.A., et al., Optimization of parameters of enucleation and fusion of the oocyte and somatic cell upon receipt of cloned mammalian embryos, S. Biol., 2013, no. 2, pp. 46–51.

    Google Scholar 

  • Singina, G.N., Volkova, N.A., Bagirov, V.A., and Zinovieva, N.A., Cryobanks of somatic cells as a promising way to preserve animal genetic resources, S-kh. Biol., 2014, no. 6, pp. 3–14.

    Google Scholar 

  • Smith, C.A., Roeszler, K.N., and Sinclair, A.H., Robust and ubiquitous GFP expression in a single generation of chicken embryos using the avian retroviral vector, RCASBP, Differentiation, 2009, vol. 77, no. 5, pp. 473–82.

    Article  CAS  PubMed  Google Scholar 

  • Sommer, J.R., Estrada, J.L., Collins, E.B., et al., Production of ELOVL4 transgenic pigs: A large animal model for Stargardt-like macular degeneration, Br. J. Ophthalmol., 2011, vol. 95, no. 12, pp. 1749–1754.

    Article  PubMed  Google Scholar 

  • Sperandio, S., Lulli, V., Bacci, M., et al., Sperm mediated DNA transfer in bovine and swine species, Anim. Biotechnol., 1996, vol. 7, pp. 59–77.

    Article  CAS  Google Scholar 

  • Tan, W., Carlson, D.F., Lancto, C.A., et al., Efficient nonmeiotic allele introgression in livestock using custom endonucleases, Proc. Natl. Acad. Sci. U.S.A., 2013, vol. 110, no. 41, pp. 16526–16531.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tyack, S.G., Jenkins, K.A., O’Neil, T.E., et al., A new method for producing transgenic birds via direct in vivo transfection of primordial germ cells, Transgenic Res., 2013, vol. 22, pp. 1257–1264.

    Article  CAS  PubMed  Google Scholar 

  • Volkova, N.A., Volkova, L.A., and Fomin, I.K., et al., Integration and expression of marker genes in chicken embryos using retrovirus expressing vectors), S-kh. Biol., 2013, no. 2, pp. 58–61.

    Google Scholar 

  • Volkova, N.A., Volkova, L.A., and Fomin, I.K., et al., Optimization of conditions for introduction of recombinant DNA in spermatogenic cells of the testes of cocks in vivo), S-kh. Biol., 2012, no. 6, pp. 56–61.

    Google Scholar 

  • Wang, S., Sun, X., Ding, F., et al., Removal of selectable marker gene from fibroblast cells in transgenic cloned cattle by transient expression of Cre recombinase and subsequent effects on recloned embryo development, Theriogenology, 2009, vol. 72, pp. 535–541.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Zhao, S., Bai, L., et al., Expression systems and species used for transgenic animal bioreactors, BioMed Res. Int., 2013, vol. 2013. doi doi 10.1155/2013/.

  • Ward, K.A., Nancarrow, C.D., Murray, J.D., et al., The physiological consequences of growth hormone fusion gene expression in transgenic sheep, J. Cell Biochem., 1989, vol. 13, p. 164.

    Google Scholar 

  • Weiss, E.H., Lilienfeld, B.G., Muller, S., et al., HLA-E/human beta2-microglobulin transgenic pigs: Protection against xenogeneic human anti-pig natural killer cell cytotoxicity, Transplantation, 2009, vol. 87, pp. 35–43.

    Article  CAS  PubMed  Google Scholar 

  • Whitelaw, C.B., Radcliffe, P.A., Ritchie, W.A., et al., Efficient generation of transgenic pigs using equine infectious anaemia virus (EIAV) derived vector, FEBS Lett., 2004, vol. 571, pp. 233–236.

    Article  CAS  PubMed  Google Scholar 

  • Whitworth, K.M., Lee, K., Benne, J.A., et al., Use of the CRISPR/Cas9 system to produce genetically engineered pigs from in vitro-derived oocytes and embryos, Biol. Reprod., 2014, vol. 91, no. 3, pp. 78–90.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wiedenheft, B., Sternberg, S.H., and Doudna, J.A., RNAguided genetic silencing systems in bacteria and archaea, Nature, 2012, vol. 482, pp. 331–338.

    Article  CAS  PubMed  Google Scholar 

  • Wieghart, M., Hoover, J.L., McGrane, M.M., et al., Production of transgenic pigs harbouring a rat phosphoenolpyruvate carboxykinase-bovine growth hormone fusion gene, J. Reprod. Fertil., 1990, vol. 41, suppl., pp. 89–96.

    CAS  Google Scholar 

  • Wine, J.J., The development of lung disease in cystic fibrosis pigs, Sci. Transl. Med., 2010, vol. 2, no. 29, p. 29ps20.

    Article  Google Scholar 

  • Xin, J., Yang, H., Fan, N., et al., Highly efficient generation of GGTA1 biallelic knockout inbred minipigs with TALENs, PLoS One, 2013, vol. 8, no. 12, p. e84250.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zinovieva, N.A. and Ernst, L.K., Problemy biotekhnologii i selektsii sel’skokhozyaistvennykh zhivotnykh (Problems of Biotechnology and Breeding of Farm Animals), Dubrovitsy: VIZh, 2006, 2nd. ed.

    Google Scholar 

  • Zinovieva, N.A., Melerzanov, A.V. and Petersen, E.V., et al., The use of transgenic GAL-KO pigs in xenotransplantation: Problems and prospects, S-kh. Biol., 2014, no. 2, pp. 42–49.

    Google Scholar 

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Original Russian Text © N.A. Zinovieva, N.A. Volkova, V.A. Bagirov, G. Brem, 2015, published in Ecologicheskaya Genetika, 2015, Vol. 13, No. 2, pp. 58–76.

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Zinovieva, N.A., Volkova, N.A., Bagirov, V.A. et al. Transgenic farm animals: the status of research and prospects. Russ J Genet Appl Res 6, 657–668 (2016). https://doi.org/10.1134/S2079059716060101

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  • DOI: https://doi.org/10.1134/S2079059716060101

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