Skip to main content
SpringerLink
Log in

Genome Editing: Current State of Research and Application to Animal Husbandry

  • PROBLEMS AND PROSPECTS
  • Published:
Applied Biochemistry and Microbiology Aims and scope Submit manuscript

Abstract

The creation and development of genome editing (GE) technologies bring new opportunities for the genetic engineering of farm mammals and poultry. The present review characterizes GE systems based on ZFN, TALEN, and CRISPR/Cas9 and directions for their improvement in relation to farm animals. The fields for the application of GE technologies in animal husbandry and poultry farming and the objectives and prospects for their further development are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. 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 

  2. 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.

    Article  CAS  PubMed  Google Scholar 

  3. Zinovieva, N.A., Volkova, N.A., Bagirov, V.A., and Brem, G., Transgenic farm animals: current state of research and prospects, Ekol. Genet., 2015, vol. 13, no. 2, pp. 58–76.

    Google Scholar 

  4. Serov, O.L., Transgenic animals: fundamental and applied aspects, Vavilov. Zh. Genet. Selekts., 2013, vol. 17, nos. 4/2, pp. 1055–1064.

  5. Singina, G.N., Volkova, N.A., Bagirov, V.A., and Zinov’eva, N.A., Cryobanks of somatic cells as a promising way of preserving animal genetic resources, S.-Kh. Biol., 2014, no. 6, pp. 3–14. https://doi.org/10.15389/agrobiology.2014.6.3rus

  6. 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. https://doi.org/10.1007/s00018-015-1842-1

    Article  CAS  PubMed  Google Scholar 

  7. 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. S13.

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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  Google Scholar 

  9. 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 

  10. 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 

  11. Kues, W.A. and Niemann, H., Advances in farm animal transgenesis, Prev. Vet. Med., 2011, vol. 102, pp. 146–156. https://doi.org/10.1016/j.prevetmed.2011.04.009

    Article  PubMed  Google Scholar 

  12. Kim, Y.G., Cha, J., and Chandrasegaran, S., Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain, Proc. Natl. Acad. Sci. U. S. A., 1996, vol. 93, pp. 1156–1160.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Christian, M., Cermak, T., Doyle, E.L., et al., Targeting DNA double-strand breaks with TAL effector nucleases, Genetics, 2010, vol. 186, no. 2, pp. 757–761. https://doi.org/10.1534/genetics.110.120717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Fu, Y., Sander, J.D., Reyon, D., et al., Improving CRISPR-Cas nuclease specificity using truncated guide RNAs, Nat. Biotechnol., 2014, vol. 32, no. 3, pp. 279–284. https://doi.org/10.1038/nbt.2808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hsu, P.D., Scott, D.A., Weinstein, J.A., et al., DNA targeting specificity of RNA-guided Cas9 nucleases, Nat. Biotechnol., 2013, vol. 31, no. 9, pp. 827–832. https://doi.org/10.1038/nbt.2647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Jinek, M., Chylinski, K., Fonfara, I., et al., A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity, Science, 2012, vol. 337, no. 6096, pp. 816–821. https://doi.org/10.1126/science.1225829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Galli, A. and Schiestl, R.H., Effects of DNA double-strand and single-strand breaks on intrachromosomal recombination events in cell-cycle-arrested yeast cells, Genetics, 1998, vol. 149, pp. 1235–1250.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Storici, F., Durham, C.L., Gordenin, D.A., and Resnick, M.A., Chromosomal site-specific double-strand breaks are efficiently targeted for repair by oligonucleotides in yeast, Proc. Natl. Acad. Sci. U. S. A., 2003, vol. 100, pp. 14994–14999. https://doi.org/10.1073/pnas.2036296100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  20. 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. https://doi.org/10.1038/nbt.1755

    Article  CAS  PubMed  Google Scholar 

  21. Hauschild, J., Petersen, B., Santiago, Y., et al., Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases, Proc. Natl. Acad. Sci. U. S. A., 2001, vol. 108, pp. 12013–12017.

    Article  Google Scholar 

  22. Xin, J., Yang, H., Fan, N., et al., Highly efficient generation of GGTA1 biallelic knockout inbred mini-pigs with TALENs, PLoS One, 2013, vol. 8, no. 12. e84250. https://doi.org/10.1371/journal.pone.0084250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. 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. https://doi.org/10.1126/science.1231143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mali, P., Yang, L., Esvelt, K.M., et al., RNA-guided human genome engineering via Cas9, Science, 2013, vol. 339, no. 6121, pp. 823–826. https://doi.org/10.1126/science.1232033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Salsman, J. and Dellaire, G., Precision genome editing in the CRISPR era, Biochem. Cell Biol., 2017, vol. 95, no. 2, pp. 87–201. https://doi.org/10.1139/bcb-2016-0137

    Article  CAS  Google Scholar 

  26. Wiedenheft, B., Sternberg, S.H., and Doudna, J.A., RNA-guided genetic silencing systems in bacteria and archaea, Nature, 2012, vol. 482, no. 7385, pp. 331–338. https://doi.org/10.1038/nature10886

    Article  CAS  PubMed  Google Scholar 

  27. Wang, Y., Zhao, S., Bai, L., et al., Expression systems and species used for transgenic animal bioreactors, BioMed. Res. Int., 2013, vol. 2013, article ID 580463. https://doi.org/10.1155/2013/580463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. 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, no. 4, pp. 535–541. https://doi.org/10.1016/j.theriogenology.2009.04.009

    Article  CAS  PubMed  Google Scholar 

  29. 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. https://doi.org/10.1101/gad.248252.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Nemudryi, A.A., Valetdinova, K.R., Medvedev, S.P., and Zakiyan, S.M., Genome editing systems TALEN and CRISPR/Cas—instruments of discoveries, Acta Naturae, 2014, vol. 6, no. 3, pp. 20–42.

    Article  Google Scholar 

  31. Lee, B.R., Choi, H.J., Jung, K.M., and Han, J.Y., Recent progress toward precise genome editing in animals, J. Anim. Breed. Genomics, 2017, vol. 1, no. 2, pp. 85–101. https://doi.org/10.12972/jabng.20170010

    Article  Google Scholar 

  32. Lieber, M.R., The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway, Ann. Rev. Biochem., 2010, vol. 79, pp. 181–211.https://doi.org/10.1146/annurev.biochem.052308.093131

    Article  CAS  PubMed  Google Scholar 

  33. Burkard, C., Lillico, S.G., Reid, E., et 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 Pathogens, 2017, vol. 13, no. 2. e1006206. https://doi.org/10.1371/journal.ppat.1006206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Pattanayak, V., Lin, S., Guilinger, J.P., et al., High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity, Nat. Biotechnol., 2013, vol. 31, pp. 839–843.https://doi.org/10.1038/nbt.2673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Cho, S.W., Kim, S., Kim, Y., et al., Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases, Genome Res., 2014, vol. 24, pp. 132–141.https://doi.org/10.1101/gr.162339.113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Gao, Y., Wu, H., Wang, Y., Liu, X., et al., Single Cas9 nickase induced generation of NRAMP1 knock-in cattle with reduced off-target effects, Genome Biol., 2017, vol. 18, p. 13. https://doi.org/10.1186/s13059-016-1144-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Richardson, C.D., Ray, G.J., Bray, N.L., and Corn, J.E., Non-homologous DNA increases gene disruption efficiency by altering DNA repair outcomes, Nat. Commun., 2016, vol. 7, p. 12463. https://doi.org/10.1038/ncomms12463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Hess, G.T., Tycko, J., Yao, D., and Bassik, M.C., Methods and applications of CRISPR-Mediated base editing in eukaryotic genomes, Mol. Cell, 2017, vol. 68, no. 1, pp. 26–43. https://doi.org/10.1016/j.molcel.2017.09.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Conticello, S.G., The AID/APOBEC family of nucleic acid mutators, Genome Biol, 2008, vol. 9, no. 6, p. 229. https://doi.org/10.1186/gb-2008-9-6-229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ran, F.A., Hsu, P.D., Lin, C.Y., et al., Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity, Cell, 2013, vol. 154, no. 6, pp. 1380–1389. https://doi.org/10.1016/j.cell.2013.08.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Komor, A.C., Kim, Y.B., Packer, M.S., et al., Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage, Nature, 2016, vol. 533, no. 7603, pp. 420–424. https://doi.org/10.1038/nature17946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Ma, Y., Zhang, J., Yin, W., et al., Targeted AID-mediated mutagenesis (TAM) enables efficient genomic diversification in mammalian cells, Nat. Methods, 2016, vol. 13, no. 12, pp. 1029–1035. https://doi.org/10.1038/nmeth.4027

    Article  CAS  PubMed  Google Scholar 

  43. Gould, F., Broadening the application of evolutionarily based genetic pest management, Evolution, 2008, vol. 62, no. 2, pp. 500–510.

    Article  PubMed  Google Scholar 

  44. Burt, A. and Trivers, R., Genes in Conflict: the Biology of Selfish Genetic Elements, Cambridge: Belknap Press, 2006.

    Book  Google Scholar 

  45. https://nplus1.ru/material/2017/06/09/genedrive/. Accessed March 15, 2018.

  46. Clark, J.B. and Kidwell, M.G., A phylogenetic perspective on P transposable element evolution in Drosophila,Proc. Natl. Acad. Sci. U. S. A., 1997, vol. 94, no. 21, pp. 11428–11433.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Burt, A., Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc. Soc. Biol. Sci., 2003, vol. 270, no. 1518, pp. 921–928.

    Article  CAS  Google Scholar 

  48. Gantz, V.M. and Bier, E., The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations, Science, 2015, vol. 348, no. 6233, pp. 442–444. https://doi.org/10.1126/science.aaa5945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. 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. https://doi.org/10.1038/srep04513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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, no. 3, pp. 372–375. https://doi.org/10.1038/cr.2014.11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 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. https://doi.org/10.1095/biolreprod.114.121723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Kuroiwa, Y., Kasinathan, P., Matsushita, H., et al., Sequential targeting of the genes encoding immunoglobulin-mu and prion protein in cattle, Nat. Genet., 2004, vol. 36, no. 7, pp. 775–780.

    Article  CAS  PubMed  Google Scholar 

  53. Sendai, Y., Sawada, T., Urakawa, M., et al., Alpha1,3-Galactosyltransferasegene knockout in cattle using a single targeting vector with loxP sequences and cre-expressing adenovirus, Transplantation, 2006, vol. 81, no. 5, pp. 760–766.

    Article  CAS  PubMed  Google Scholar 

  54. Richt, J.A., Kasinathan, P., Hamir, A.N., et al., Production of cattle lacking prion protein, Nat. Biotechnol., 2007, vol. 25, no. 1, pp. 132–138.

    Article  CAS  PubMed  Google Scholar 

  55. Robl, J.M., Wang, Z., Kasinathan, P., and Kuroiwa, Y., Transgenic animal production and animal biotechnology, Theriogenology, 2007, vol. 67, no. 1, pp. 127–133.

    Article  CAS  PubMed  Google Scholar 

  56. Wang, S., Zhang, K., Ding, F., et al., A novel promoterless gene targeting vector to efficiently disrupt PRNP gene in cattle, J. Biotechnol., 2013, vol. 163, no. 4, pp. 377–385. https://doi.org/10.1016/j.jbiotec.2012.10.018

    Article  CAS  PubMed  Google Scholar 

  57. Matsushita, H., Sano, A., Wu, H., et al., Triple immunoglobulin gene knockout transchromosomic cattle: bovine lambda cluster deletion and its effect on fully human polyclonal antibody production, PLoS One, 2014, vol. 9, no. 3. e90383. https://doi.org/10.1371/journal.pone.0090383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Heo, Y.T., Quan, X.Y., Xu, Y.N., et al., CRISPR/Cas9 nuclease-mediated gene knock-in in bovine-induced pluripotent cells, Stem. Cells Dev., 2015, vol. 24, no. 3, pp. 393–402. https://doi.org/10.1089/scd.2014.0278

    Article  CAS  PubMed  Google Scholar 

  59. Aponte, P.M., Spermatogonial stem cells: Current biotechnological advances in reproduction and regenerative medicine, World J. Stem. Cells, 2015, vol. 7, no. 4, pp. 669–680. https://doi.org/10.4252/wjsc.v7.i4.669

    Article  PubMed  PubMed Central  Google Scholar 

  60. Cai, H. and Wu, J.Y., An X.L., et al. Enrichment and culture of spermatogonia from cryopreserved adult bovine testis tissue, Anim. Reprod. Sci., 2016, vol. 166, pp. 109–115. https://doi.org/10.1016/j.anireprosci.2016.01.009

    Article  PubMed  Google Scholar 

  61. Lee, Y.A., Kim, Y.H., Ha, S.J., et al., Cryopreservation of porcine spermatogonial stem cells by slow-freezing testis tissue in trehalose, J. Anim. Sci., 2014, vol. 92, no. 3, pp. 984–995. https://doi.org/10.2527/jas.2013-6843

    Article  CAS  PubMed  Google Scholar 

  62. Costa, G.M.J., Avelar, G.F., Lacerda, S.M.S.N., et al., Horse spermatogonial stem cell cryopreservation: feasible protocols and potential biotechnological applications, Cell Tissue Res., 2017, vol. 370, no. 3, pp. 489–500. https://doi.org/10.1007/s00441-017-2673-1

    Article  CAS  PubMed  Google Scholar 

  63. Oatley, J.M. and Griswold, M.D., Application of spermatogonial transplantation in agricultural animals, in The Biology of Mammalian Spermatogonia, Springer Science + Business Media LL, 2017, pp. 343–378.

  64. Park, K.E., Kaucher, A.V., Powell, A., et al., Generation of germline ablated male pigs by CRISPR/Cas9 editing of the NANOS2 gene, Sci. Rep., 2017, vol. 7, pp. 40176. https://doi.org/10.1038/srep40176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Carroll, D. and Charo, R.A., The societal opportunities and challenges of genome editing, Genome Biol., 2015, vol. 16, p. 242. https://doi.org/10.1186/s13059-015-0812-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Gonen, S., Jenko, J., Gorjanc, G., et al., Potential of gene drives with genome editing to increase genetic gain in livestock breeding programs, Genet. Sel. Evol., 2017, vol. 49, p. 3. https://doi.org/10.1186/s12711-016-0280-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Luo, J., Song, Z., Yu, S., et al., Efficient generation of myostatin (MSTN) biallelic mutations in cattle using zinc finger nucleases, PLoS One, 2014, vol. 9, no. 4. e95225. https://doi.org/10.1371/journal.pone.0095225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Proudfoot, C., Carlson, D.F., Huddart, R., et al., Genome edited sheep and cattle, Transgenic Res., 2014, vol. 24, no. 1, pp. 147–153. https://doi.org/10.1007/s11248-014-9832-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Qian, L., Tang, M., Yang, J., et al., Targeted mutations in myostatin by zinc-finger nucleases result in double-muscled phenotype in Meishan pigs, Sci. Rep., 2015, vol. 5, p. 14435. https://doi.org/10.1038/srep14435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Cai, C., Qian, L., Jiang, S., et al., Loss-of-function myostatin mutation increases insulin sensitivity and browning of white fat in Meishan pigs, Oncotarget, 2017, vol. 8, no. 21, pp. 34911–34922. https://doi.org/10.18632/oncotarget.16822

    Article  PubMed  PubMed Central  Google Scholar 

  71. Cui, C., Song, Y., Liu, J., et al., Gene targeting by TALEN-induced homologous recombination in goats directs production of β-lactoglobulin-free, high-human lactoferrin milk, Sci. Rep., vol. 5, p. 10482. https://doi.org/10.1038/srep10482

  72. 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. https://doi.org/10.1073/pnas.1310478110

    Article  PubMed  PubMed Central  Google Scholar 

  73. Zinov'eva, N.A., Gladyr’, E.A., and Korkina, E., DNA markers of sheep fertility, Ovtsy Kozy Sherst.Delo, 2006, vol. 3, pp. 30–38.

    Google Scholar 

  74. Demars, J., Fabre, S., Sarry, J., et al., Genome-wide association studies identify two novel BMP15 mutations responsible for an atypical hyperprolificacy phenotype in sheep, PLoS Genet., 2013, vol. 9, no. 4. e1003482. https://doi.org/10.1371/journal.pgen.1003482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Jenko, J., Gorjanc, G., Cleveland, M.A., et al., Potential of promotion of alleles by genome editing to improve quantitative traits in livestock breeding programs, Genet. Sel. Evol., 2015, vol. 47, p. 55. https://doi.org/10.1186/s12711-015-0135-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. 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 

  77. Lassnig, C. and Mueller, M., Disease-resistant transgenic animals, in Sustainable Food Production, Christou, P., et al., Eds., New York: Springer Science+Business Media, 2013, pp. 747–760. https://doi.org/10.1007/978-1-4614-5797-8

  78. Ikeda, M., Matsuyama, S., Akagi, S., et al., Correction of a disease mutation using CRISPR/Cas9-assisted genome editing in Japanese Black cattle, Sci. Rep., 2017, vol. 7, p. 17827. https://doi.org/10.1038/s41598-017-17968-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Liu, X., Wang, Y., Guo, W., et al., Zinc-finger nickase-mediated insertion of the lysostaphin gene into the beta-casein locus in cloned cows, Nat. Commun., 2013, vol. 4, p. 2565. https://doi.org/10.1038/ncomms3565

    Article  CAS  PubMed  Google Scholar 

  80. Liu, X., Wang, Y., Tian, Y., et al., Generation of mastitis resistance in cows by targeting human lysozyme gene to beta-casein locus using zinc-finger nucleases, Proc. Biol. Sci., 2014, vol. 281, p. 20133368. https://doi.org/10.1098/rspb.2013.3368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Whitworth, K.M., Rowland, R.R.R., Ewen, C.L., et al., Gene-edited pigs are protected from porcine reproductive and respiratory syndrome virus, Nat. Biotechnol., 2016, vol. 34, no. 1, pp. 20–22. https://doi.org/10.1038/nbt.3434

    Article  CAS  PubMed  Google Scholar 

  82. Lillico, S.G., Proudfoot, C., King, T.J., et al., Mammalian interspecies substitution of immune modulatory alleles by genome editing, Sci. Rep., 2016, vol. 6, p. 21645. https://doi.org/10.1038/srep21645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Houdebine, L., Production of pharmaceutical proteins by transgenic animals. Comparative Immunology, Microbiology and Infectious Diseases, 2009, vol. 32, no. 2, pp. 107–121. https://doi.org/10.1016/j.cimid.2007.11.005

    Article  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  85. Jim, K., First US approval for a transgenic animal drug, Nat. Biotechnol., 2009, vol. 27, no. 4, pp. 302–304. https://doi.org/10.1038/nbt0409-302

    Article  CAS  Google Scholar 

  86. 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. e89631. https://doi.org/10.1371/journal.pone.0089631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Luo, Y., Lin, L., Bolund, L., et al., Genetically modified pigs for biomedical research, J. Inherit. Metab. Dis., 2012, vol. 35, no. 4, pp. 695–713. https://doi.org/10.1007/s10545-012-9475-0

    Article  CAS  PubMed  Google Scholar 

  88. Zinov’eva, N.A., Melerzanov, A.V., Petersen, E.V., et al., The use of transgenic GAL-KO pigs in xenotransplantology: problems and prospects, S.-Kh. Biol., 2014, no. 2, pp. 42–49. https://doi.org/10.15389/agrobiology.2014.2.42rus

  89. 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 

  90. 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 

  91. Weiner, J., Yamada, K., Ishikawa, Y., et al., Prolonged survival of GalT-KO swine skin on baboons, Xenotransplantation, 2010, vol. 17, no. 2, pp. 147–152. https://doi.org/10.1111/j.1399-3089.2010.00576.x

    Article  PubMed  PubMed Central  Google Scholar 

  92. Iwase, H., Liu, H., Wijkstrom, M., et al., Pig kidney graft survival in a baboon for 136 days: longest life-supporting organ graft survival to date, Xenotransplantation, 2015, vol. 22, no. 4, pp. 302–309. https://doi.org/10.1111/xen.12174

    Article  PubMed  PubMed Central  Google Scholar 

  93. Gustafsson, K.T. and Sachs, D.H., α(1,3)galactosyltransferase negative porcine cells, US Patent no. 6153428A, 1994.

  94. Hauschild, J., Petersen, B., Santiago, Y., et al., Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases, Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, no. 29, pp. 12013–12017. https://doi.org/10.1073/pnas.1106422108

    Article  PubMed  PubMed Central  Google Scholar 

  95. Lutz, A.J., Li, P., Estrada, J.L., et al., Double knockout pigs deficient in N-glycolylneuraminic acid and galactose alpha-1,3-galactose reduce the humoral barrier to xenotransplantation, Xenotransplantation, 2013, vol. 20, no. 1, pp. 2–35. https://doi.org/10.1111/xen.12019

    Article  Google Scholar 

  96. Xin, J., Yang, H., Fan, N., et al., Highly efficient generation of GGTA1 biallelic knockout inbred mini-pigs with TALENs, PLoS One, 2013, vol. 8, no. 12. e84250. https://doi.org/10.1371/journal.pone.0084250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Kang, J.T., Kwon, D.K., Park, A.R., et al., Production of α1,3-galactosyltransferase targeted pigs using transcription activator-like effector nuclease-mediated genome editing technology, J. Vet. Sci., 2016, vol. 17, no. 1, pp. 89–96. https://doi.org/10.4142/jvs.2016.17.1.89

    Article  PubMed  PubMed Central  Google Scholar 

  98. Petersen, B., Frenzel, A., Lucas-Hahn, A., et al., Efficient production of biallelic GGTA1 knockout pigs by cytoplasmic microinjection of CRISPR/Cas9 into zygotes, Xenotransplantation, 2016, vol. 23, no. 5, pp. 338–346. https://doi.org/10.1111/xen.12258

    Article  PubMed  Google Scholar 

  99. Niu, D., Wei, H.J., Lin, L., et al., Inactivation of porcine endogenous retrovirus in pigs using CRISPR-Cas9, Science, 2017, vol. 357, no. 6357, pp. 1303–1307. https://doi.org/10.1126/science.aan4187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Wang, Z.Y., Burlak, C., Estrada, J.L., et al., Erythrocytes from GGTA1/CMAH knockout pigs: implications for xenotransfusion and testing in non-human primates, Xenotransplantation, 2014, vol. 21, no. 4, pp. 376–384. https://doi.org/10.1111/xen.12106

    Article  PubMed  PubMed Central  Google Scholar 

  101. Mohiuddin, M.M., Singh, A.K., Corcoran, P.C., et al., Chimeric 2C10R4 anti-CD40 antibody therapy is critical for long-term survival of GTKO.hCD46.hTBM pig-to-primate cardiac xenograft, Nat. Commun., 2016, vol. 7, p. 11138. https://doi.org/10.1038/ncomms11138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Liu, Z., Hu, W., He, T., et al., Pig-to-primate islet xenotransplantation: past, present, and future, Cell Transplant., 2017, vol. 26, no. 6, pp. 925–947. https://doi.org/10.3727/096368917X694859

    Article  PubMed  PubMed Central  Google Scholar 

  103. Aigner, B., Renner, S., Kessler, B., et al., Transgenic pigs as models for translational biomedical research, J. Mol. Med., 2010, vol. 88, no. 7, pp. 653–664. https://doi.org/10.1007/s00109-010-0610-9

    Article  PubMed  Google Scholar 

  104. 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, no. 5897, pp. 1837–1841. https://doi.org/10.1126/science.1163600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Wine, J.J., The development of lung disease in cystic fibrosis pigs, Sci. Transl. Med., 2010, vol. 2, no. 29, p. 29ps20. https://doi.org/10.1126/scitranslmed.3001130

    Article  PubMed  Google Scholar 

  106. Renner, S., Fehlings, C., Herbach, N., et al., Glucose intolerance and reduced proliferation of pancreatic beta-cells in transgenic pigs with impaired glucose-dependent insulinotropic polypeptide function, Diabete, 2010, vol. 59, no. 5, pp. 1228–1238. https://doi.org/10.2337/db09-0519

    Article  CAS  Google Scholar 

  107. 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. https://doi.org/10.1136/bjophthalmol-2011-300417

    Article  PubMed  Google Scholar 

  108. Klymiuk, N., Bocker, W., Schonitzer, V., et al., First inducible transgene expression in porcine large animal models, FASEB J., 2012, vol. 26, no. 3, pp. 1086–1099. https://doi.org/10.1096/fj.11-185041

    Article  CAS  PubMed  Google Scholar 

  109. Perez Saez, J.M., Bussmann, L.E., Baranao, J.L., and Bussmann, U.A., Improvement of chicken primordial germ cell maintenance in vitro by blockade of the aryl hydrocarbon receptor endogenous activity, Cell Reprogram., 2016, vol. 18, no. 3, pp. 154–161. https://doi.org/10.1089/cell.2016.0015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Volkova, N.A., Bagirov, V.A., Tomgorova, E.K., Vetokh, A.N., Volkova, L.A., and Zinovieva, N.A., Isolation, cultivation, and characterization of quail primordial germ cells, S.-Kh. Biol., 2017, vol. 52, no. 2, pp. 261–267. https://doi.org/10.15389/agrobiology.2017.2.261eng

    Article  Google Scholar 

  111. Yakhkeshi, S., Rahimi, S., Sharafi, M., et al., In vitro improvement of quail primordial germ cell expansion through activation of TGF-beta signaling pathway, J. Cell Biochem., 2017. https://doi.org/10.1002/jcb.26618

    Article  CAS  PubMed  Google Scholar 

  112. Choi, J.W., Kim, S., Kim, T.M., et al., Basic fibroblast growth factor activates MEK/ERK cell signaling pathway and stimulates the proliferation of chicken primordial germ cells, PLoS One, 2010, vol. 5, no. 9. e12968. https://doi.org/10.1371/journal.pone.0012968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Volkova, N.A., Korzhikova, S.V., Kotova, T.O., et al., Isolation, cultivation,a nd characterization of cock spermatogonia, S.-Kh.Biol., 2016, vol. 51, no. 4, pp. 450–458. https://doi.org/10.15389/agrobiology.2016.4.450eng

    Article  Google Scholar 

  114. Pramod, R.K., Lee, B.R., Kim, Y.M., et al., Isolation, characterization, and in vitro culturing of spermatogonial stem cells in Japanese quail (Coturnix japonica), Stem. Cells Dev., 2017, vol. 26, no. 1, pp. 60–70. https://doi.org/10.1089/scd.2016.0129

    Article  CAS  PubMed  Google Scholar 

  115. Macdonald, J., Glover, J.D., Taylor, L., et al., Characterisation and germline transmission of cultured avian primordial germ cells, PLoS One, 2010, vol. 5, no. 11. e15518. doihttps://doi.org/10.1371/journal.pone.0015518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Song, Y., Duraisamy, S., Ali, J., et al., Characteristics of long-term cultures of avian primordial germ cells and gonocytes, Biol. Reprod., 2014, vol. 90, no. 1, p. 15. https://doi.org/10.1095/biolreprod.113.113381

    Article  CAS  PubMed  Google Scholar 

  117. Tonus, C., Cloquette, K., Ectors, F., et al., Long term-cultured and cryopreserved primordial germ cells from various chicken breeds retain high proliferative potential and gonadal colonisation competency, Reprod. Fertil. Dev., 2016, vol. 28, no. 5, pp. 628–639. https://doi.org/10.1071/RD14194

    Article  CAS  PubMed  Google Scholar 

  118. Volkova, N.A., Vetokh, A.N., Kotova, T.O., et al., Recovery of spermatogenesis in male chickens by transplantation of donor spermatogonia, Reprod. Domest. Anim., 2017, vol. 52, no. S3, pp. 141–142.

    Google Scholar 

  119. Park, T.S., Lee, H.J., Kim, K.H., et al., Targeted gene knockout in chickens mediated by TALENs, Proc. Natl. Acad. Sci. U. S. A., 2014, vol. 111, no. 35, pp. 12716–12721. https://doi.org/10.1073/pnas.1410555111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Taylor, L., Carlson, D.F., Nandi, S., et al., Efficient TALEN-mediated gene targeting of chicken primordial germ cells, Development, 2017, vol. 144, p. 928934. https://doi.org/10.1242/dev.145367

    Article  CAS  Google Scholar 

  121. Dimitrov, L., Pedersen, D., Ching, K.H., et al., Germline gene editing in chickens by efficient CRISPR-mediated homologous recombination in primordial germ cells, PLoS One, 2016, vol. 11, no. 4, pp. 1–10. https://doi.org/10.1371/journal.pone.0154303

    Article  CAS  Google Scholar 

  122. Oishi, I., Yoshii, K., Miyahara, D., et al., Targeted mutagenesis in chicken using CRISPR/Cas9 system, Sci. Rep., 2016, vol. 6, p. 23980. https://doi.org/10.1038/srep23980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Cooper, C.A., Challagulla, A., Jenkins, K.A., et al., Generation of gene edited birds in one generation using sperm transfection assisted gene editing (STAGE), Transgen. Res., 2016, vol. 26, no. 3, p. 331347. https://doi.org/10.1007/s11248-016-0003-0

    Article  CAS  Google Scholar 

  124. Bai, Y., He, L., Li, P., et al., Efficient genome editing in chicken DF-1 cells using the CRISPR/Cas9 system, G3 (Bethesda), 2016, vol. 6, no. 4, pp. 917–923. https://doi.org/10.1534/g3.116.027706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Yamamoto, T., Juneja, L.R., Hatta, H., and Kim, M., Hen Eggs: Their Basic and Applied Science, Boca Raton, FL: CRC Press, 1997.

    Google Scholar 

  126. Sheridan, C., FDA approves ‘farmaceutical’ drug from transgenic chickens, Nat. Biotechnol., 2016, vol. 34, no. 2, pp. 117–119. https://doi.org/10.1038/nbt0216-117

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The material in the article was prepared within the framework of the task from the Federal Agency of Research Organizations (FANO), no. АААА-А18-118021590132-9.

Author information

Authors and Affiliations

  1. Ernst Federal Science Center for Animal Husbandry, 142132, Dubrovitsy village, Moscow oblast, Russia

    N. A. Zinovieva, N. A. Volkova & V. A. Bagirov

Authors
  1. N. A. Zinovieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. A. Volkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. A. Bagirov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. A. Zinovieva.

Ethics declarations

The authors declare that they have no conflicts of interest.

This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by I. Gordon

Abbreviations: Cas9—CRISPR-associated protein 9; Cas9n—Cas9 nickase; CRISPR—clustered regularly interspaced short palindromic repeats; DSB—double-stranded break(s); FDA—Food and Drug Administration (USA); GD—gene drive; GE—genome editing; GGTA1—α-1,3-galactosyl transferase; HDR—homologous repair; HR—homologous recombination; indel(s)—insertion/deletion(s); iPSC—induced pluripotent stem cells; LGB—lactoglobulin-beta; MCR—mutagenic chain reaction; MSTN—myostatin; NE—nucleotide editing; NHEJ—non-homologous end joining; off-target effect—nontargeted impact; OV—ovalbumin; OVM—ovomucoid; PAGE—promotion of alleles by genome editing; PERV—porcine endogenic retrovirus; PRRS—porcine reproductive-respiratory syndrome; SCNT—somatic cell nuclear transfer; Sg—spermatogonia; TALEN—transcription activation-like effector nucleases; ZFN—zinc finger nuclease.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zinovieva, N.A., Volkova, N.A. & Bagirov, V.A. Genome Editing: Current State of Research and Application to Animal Husbandry. Appl Biochem Microbiol 55, 711–721 (2019). https://doi.org/10.1134/S000368381907007X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S000368381907007X

Keywords:

Search

Navigation