Journal of Veterinary Science

The Korean Society of Veterinary Science (대한수의학회)
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Outlook on genome editing application to cattle

  • Received : 2023.05.15
  • Accepted : 2023.08.20
  • Published : 2024.01.31
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Abstract

In livestock industry, there is growing interest in methods to increase the production efficiency of livestock to address food shortages, given the increasing global population. With the advancements in gene engineering technology, it is a valuable tool and has been intensively utilized in research specifically focused on human disease. In historically, this technology has been used with livestock to create human disease models or to produce recombinant proteins from their byproducts. However, in recent years, utilizing gene editing technology, cattle with identified genes related to productivity can be edited, thereby enhancing productivity in response to climate change or specific disease instead of producing recombinant proteins. Furthermore, with the advancement in the efficiency of gene editing, it has become possible to edit multiple genes simultaneously. This cattle breed improvement has been achieved by discovering the genes through the comprehensive analysis of the entire genome of cattle. The cattle industry has been able to address gene bottlenecks that were previously impossible through conventional breeding systems. This review concludes that gene editing is necessary to expand the cattle industry, improving productivity in the future. Additionally, the enhancement of cattle through gene editing is expected to contribute to addressing environmental challenges associated with the cattle industry. Further research and development in gene editing, coupled with genomic analysis technologies, will significantly contribute to solving issues that conventional breeding systems have not been able to address.

Keywords

Acknowledgement

This study was financially supported by NRF-2021R1A5A1 033157 for SRC program: 382 Comparative medicine Disease Research Center, the Research Institute of Veterinary Science, the BK21 Four for Future Veterinary Medicine Leading Education and Research Center, and a Seoul National University (SNU) grant (#550-20220044).

References

  1. Yum SY, Youn KY, Choi WJ, Jang G. Development of genome engineering technologies in cattle: from random to specific. J Anim Sci Biotechnol. 2018;9:16.
  2. Salamone D, Baranao L, Santos C, Bussmann L, Artuso J, Werning C, et al. High level expression of bioactive recombinant human growth hormone in the milk of a cloned transgenic cow. J Biotechnol. 2006;124(2):469-472. https://doi.org/10.1016/j.jbiotec.2006.01.005
  3. Johnson TE, Nelson GA. Caenorhabditis elegans: a model system for space biology studies. Exp Gerontol. 1991;26(2-3):299-309. https://doi.org/10.1016/0531-5565(91)90024-G
  4. Wall RJ, Powell AM, Paape MJ, Kerr DE, Bannerman DD, Pursel VG, et al. Genetically enhanced cows resist intramammary Staphylococcus aureus infection. Nat Biotechnol. 2005;23(4):445-451. https://doi.org/10.1038/nbt1078
  5. Richt JA, Kasinathan P, Hamir AN, Castilla J, Sathiyaseelan T, Vargas F, et al. Production of cattle lacking prion protein. Nat Biotechnol. 2007;25(1):132-138. https://doi.org/10.1038/nbt1271
  6. Carlson DF, Lancto CA, Zang B, Kim ES, Walton M, Oldeschulte D, et al. Production of hornless dairy cattle from genome-edited cell lines. Nat Biotechnol. 2016;34(5):479-481. https://doi.org/10.1038/nbt.3560
  7. de Almeida Camargo LS, Pereira JF. Genome-editing opportunities to enhance cattle productivity in the tropics. CABI Agric Biosci. 2022;3(1):8.
  8. Krimpenfort P, Rademakers A, Eyestone W, van der Schans A, van den Broek S, Kooiman P, et al. Generation of transgenic dairy cattle using 'in vitro' embryo production. Biotechnology (N Y) 1991;9(9):844-847. https://doi.org/10.1038/nbt0991-844
  9. Hyttinen JM, Peura T, Tolvanen M, Aalto J, Alhonen L, Sinervirta R, et al. Generation of transgenic dairy cattle from transgene-analyzed and sexed embryos produced in vitro. Biotechnology (N Y) 1994;12(6):606-608. https://doi.org/10.1038/nbt0694-606
  10. Eyestone WH. Production and breeding of transgenic cattle using in vitro embryo production technology. Theriogenology. 1999;51(2):509-517. https://doi.org/10.1016/S0093-691X(98)00244-1
  11. Kubota C, Yamakuchi H, Todoroki J, Mizoshita K, Tabara N, Barber M, et al. Six cloned calves produced from adult fibroblast cells after long-term culture. Proc Natl Acad Sci U S A. 2000;97(3):990-995. https://doi.org/10.1073/pnas.97.3.990
  12. Zhao J, Hao Y, Ross JW, Spate LD, Walters EM, Samuel MS, et al. Histone deacetylase inhibitors improve in vitro and in vivo developmental competence of somatic cell nuclear transfer porcine embryos. Cell Reprogram. 2010;12(1):75-83. https://doi.org/10.1089/cell.2009.0038
  13. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, McCormack MP, Wulffraat N, Leboulch P, et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science. 2003;302(5644):415-419. https://doi.org/10.1126/science.1088547
  14. Bushman F, Lewinski M, Ciuffi A, Barr S, Leipzig J, Hannenhalli S, et al. Genome-wide analysis of retroviral DNA integration. Nat Rev Microbiol. 2005;3(11):848-858. https://doi.org/10.1038/nrmicro1263
  15. Wyman C, Kanaar R. DNA double-strand break repair: all's well that ends well. Annu Rev Genet. 2006;40:363-383. https://doi.org/10.1146/annurev.genet.40.110405.090451
  16. Rouet P, Smih F, Jasin M. Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. Proc Natl Acad Sci U S A. 1994;91(13):6064-6068. https://doi.org/10.1073/pnas.91.13.6064
  17. Pabo CO, Peisach E, Grant RA. Design and selection of novel Cys2His2 zinc finger proteins. Annu Rev Biochem. 2001;70(1):313-340. https://doi.org/10.1146/annurev.biochem.70.1.313
  18. Pavletich NP, Pabo CO. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science. 1991;252(5007):809-817. https://doi.org/10.1126/science.2028256
  19. Orlando SJ, Santiago Y, DeKelver RC, Freyvert Y, Boydston EA, Moehle EA, et al. Zinc-finger nuclease-driven targeted integration into mammalian genomes using donors with limited chromosomal homology. Nucleic Acids Res. 2010;38(15):e152.
  20. Yu S, Luo J, Song Z, Ding F, Dai Y, Li N. Highly efficient modification of beta-lactoglobulin (BLG) gene via zinc-finger nucleases in cattle. Cell Res. 2011;21(11):1638-1640. https://doi.org/10.1038/cr.2011.153
  21. Sun Z, Wang M, Han S, Ma S, Zou Z, Ding F, et al. Production of hypoallergenic milk from DNA-free beta-lactoglobulin (BLG) gene knockout cow using zinc-finger nucleases mRNA. Sci Rep. 2018;8(1):15430.
  22. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, et al. Breaking the code of DNA binding specificity of TAL-type III effectors. Science. 2009;326(5959):1509-1512. https://doi.org/10.1126/science.1178811
  23. Moscou MJ, Bogdanove AJ. A simple cipher governs DNA recognition by TAL effectors. Science. 2009;326(5959):1501.
  24. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, et al. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol. 2011;29(2):143-148. https://doi.org/10.1038/nbt.1755
  25. Mahfouz MM, Li L, Shamimuzzaman M, Wibowo A, Fang X, Zhu JK. De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc Natl Acad Sci U S A. 2011;108(6):2623-2628. https://doi.org/10.1073/pnas.1019533108
  26. Litos IK, Ioannou PC, Christopoulos TK, Tzetis M, Kanavakis E, Traeger-Synodinos J. Quadruple-allele dipstick test for simultaneous visual genotyping of A896G (Asp299Gly) and C1196T (Thr399Ile) polymorphisms in the toll-like receptor-4 gene. Clin Chim Acta. 2011;412(21-22):1968-1972. https://doi.org/10.1016/j.cca.2011.07.001
  27. Move over ZFNs. Nat Biotechnol. 2011;29(8):681-684. https://doi.org/10.1038/nbt.1935
  28. Khan SH. Genome-editing technologies: concept, pros, and cons of various genome-editing techniques and bioethical concerns for clinical application. Mol Ther Nucleic Acids. 2019;16:326-334. https://doi.org/10.1016/j.omtn.2019.02.027
  29. Proudfoot C, Carlson DF, Huddart R, Long CR, Pryor JH, King TJ, et al. Genome edited sheep and cattle. Transgenic Res. 2015;24(1):147-153. https://doi.org/10.1007/s11248-014-9832-x
  30. Carlson DF, Tan W, Lillico SG, Stverakova D, Proudfoot C, Christian M, et al. Efficient TALEN-mediated gene knockout in livestock. Proc Natl Acad Sci U S A. 2012;109(43):17382-17387. https://doi.org/10.1073/pnas.1211446109
  31. Young AE, Mansour TA, McNabb BR, Owen JR, Trott JF, Brown CT, et al. Genomic and phenotypic analyses of six offspring of a genome-edited hornless bull. Nat Biotechnol. 2020;38(2):225-232. https://doi.org/10.1038/s41587-019-0266-0
  32. Wiedenheft B, Sternberg SH, Doudna JA. RNA-guided genetic silencing systems in bacteria and archaea. Nature. 2012;482(7385):331-338. https://doi.org/10.1038/nature10886
  33. Mojica FJM, Diez-Villasenor C, Garcia-Martinez J, Soria E. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol. 2005;60(2):174-182. https://doi.org/10.1007/s00239-004-0046-3
  34. Jansen R, Embden JD, Gaastra W, Schouls LM. Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol. 2002;43(6):1565-1575. https://doi.org/10.1046/j.1365-2958.2002.02839.x
  35. Doudna JA, Charpentier E. Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science. 2014;346(6213):1258096.
  36. Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J. RNA-programmed genome editing in human cells. Elife. 2013;2:e00471.
  37. 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(3):372-375. https://doi.org/10.1038/cr.2014.11
  38. Meng X, Noyes MB, Zhu LJ, Lawson ND, Wolfe SA. Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat Biotechnol. 2008;26(6):695-701. https://doi.org/10.1038/nbt1398
  39. Doyon Y, McCammon JM, Miller JC, Faraji F, Ngo C, Katibah GE, et al. Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat Biotechnol. 2008;26(6):702-708. https://doi.org/10.1038/nbt1409
  40. Geurts AM, Cost GJ, Freyvert Y, Zeitler B, Miller JC, Choi VM, et al. Knockout rats via embryo microinjection of zinc-finger nucleases. Science. 2009;325(5939):433.
  41. Cui X, Ji D, Fisher DA, Wu Y, Briner DM, Weinstein EJ. Targeted integration in rat and mouse embryos with zinc-finger nucleases. Nat Biotechnol. 2011;29(1):64-67. https://doi.org/10.1038/nbt.1731
  42. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell. 2013;153(4):910-918. https://doi.org/10.1016/j.cell.2013.04.025
  43. Meyer M, de Angelis MH, Wurst W, Kuhn R. Gene targeting by homologous recombination in mouse zygotes mediated by zinc-finger nucleases. Proc Natl Acad Sci U S A. 2010;107(34):15022-15026. https://doi.org/10.1073/pnas.1009424107
  44. Kurome M, Geistlinger L, Kessler B, Zakhartchenko V, Klymiuk N, Wuensch A, et al. 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.
  45. Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, et al. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics. 2010;186(2):757-761. https://doi.org/10.1534/genetics.110.120717
  46. Flisikowska T, Thorey IS, Offner S, Ros F, Lifke V, Zeitler B, et al. Efficient immunoglobulin gene disruption and targeted replacement in rabbit using zinc finger nucleases. PLoS One. 2011;6(6):e21045.
  47. Yang H, Wang H, Shivalila CS, Cheng AW, Shi L, Jaenisch R. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell. 2013;154(6):1370-1379. https://doi.org/10.1016/j.cell.2013.08.022
  48. Whitworth KM, Lee K, Benne JA, Beaton BP, Spate LD, Murphy SL, et al. Use of the CRISPR/Cas9 system to produce genetically engineered pigs from in vitro-derived oocytes and embryos. Biol Reprod. 2014;91(3):78.
  49. Lillico SG, Proudfoot C, Carlson DF, Stverakova D, Neil C, Blain C, et al. Live pigs produced from genome edited zygotes. Sci Rep. 2013;3:2847.
  50. Sander JD, Joung JK. CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol. 2014;32(4):347-355. https://doi.org/10.1038/nbt.2842
  51. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819-823. https://doi.org/10.1126/science.1231143
  52. Zhang JP, Li XL, Li GH, Chen W, Arakaki C, Botimer GD, et al. Efficient precise knockin with a double cut HDR donor after CRISPR/Cas9-mediated double-stranded DNA cleavage. Genome Biol. 2017;18(1):35.
  53. Davis L, Maizels N. Homology-directed repair of DNA nicks via pathways distinct from canonical doublestrand break repair. Proc Natl Acad Sci U S A. 2014;111(10):E924-E932. https://doi.org/10.1073/pnas.1400236111
  54. Chu VT, Weber T, Wefers B, Wurst W, Sander S, Rajewsky K, et al. Increasing the efficiency of homologydirected repair for CRISPR-Cas9-induced precise gene editing in mammalian cells. Nat Biotechnol. 2015;33(5):543-548. https://doi.org/10.1038/nbt.3198
  55. Byrne SM, Ortiz L, Mali P, Aach J, Church GM. Multi-kilobase homozygous targeted gene replacement in human induced pluripotent stem cells. Nucleic Acids Res. 2015;43(3):e21.
  56. Quadros RM, Miura H, Harms DW, Akatsuka H, Sato T, Aida T, et al. Easi-CRISPR: a robust method for one-step generation of mice carrying conditional and insertion alleles using long ssDNA donors and CRISPR ribonucleoproteins. Genome Biol. 2017;18(1):92.
  57. Suzuki K, Izpisua Belmonte JC. In vivo genome editing via the HITI method as a tool for gene therapy. J Hum Genet. 2018;63(2):157-164. https://doi.org/10.1038/s10038-017-0352-4
  58. Auer TO, Duroure K, De Cian A, Concordet JP, Del Bene F. Highly efficient CRISPR/Cas9-mediated knock-in in zebrafish by homology-independent DNA repair. Genome Res. 2014;24(1):142-153. https://doi.org/10.1101/gr.161638.113
  59. Yao X, Wang X, Hu X, Liu Z, Liu J, Zhou H, et al. Homology-mediated end joining-based targeted integration using CRISPR/Cas9. Cell Res. 2017;27(6):801-814. https://doi.org/10.1038/cr.2017.76
  60. Nakade S, Tsubota T, Sakane Y, Kume S, Sakamoto N, Obara M, et al. Microhomology-mediated end-joining-dependent integration of donor DNA in cells and animals using TALENs and CRISPR/Cas9. Nat Commun. 2014;5:5560.
  61. Yao X, Zhang M, Wang X, Ying W, Hu X, Dai P, et al. Tild-CRISPR allows for efficient and precise gene knockin in mouse and human cells. Dev Cell. 2018;45(4):526-536.e5. https://doi.org/10.1016/j.devcel.2018.04.021
  62. Gim GM, Kwon DH, Eom KH, Moon J, Park JH, Lee WW, et al. Production of MSTN-mutated cattle without exogenous gene integration using CRISPR-Cas9. Biotechnol J. 2022;17(7):e2100198.
  63. Gim GM, Uhm KH, Kwon DH, Kim MJ, Jung DJ, Kim DH, et al. Germline transmission of MSTN knockout cattle via CRISPR-Cas9. Theriogenology. 2022;192:22-27. https://doi.org/10.1016/j.theriogenology.2022.08.021
  64. Owen JR, Hennig SL, McNabb BR, Mansour TA, Smith JM, Lin JC, et al. One-step generation of a targeted knock-in calf using the CRISPR-Cas9 system in bovine zygotes. BMC Genomics. 2021;22(1):118.
  65. Chan AW, Homan EJ, Ballou LU, Burns JC, Bremel RD. Transgenic cattle produced by reverse-transcribed gene transfer in oocytes. Proc Natl Acad Sci U S A. 1998;95(24):14028-14033. https://doi.org/10.1073/pnas.95.24.14028
  66. van Berkel PH, Welling MM, Geerts M, van Veen HA, Ravensbergen B, Salaheddine M, et al. Large scale production of recombinant human lactoferrin in the milk of transgenic cows. Nat Biotechnol. 2002;20(5):484-487. https://doi.org/10.1038/nbt0502-484
  67. Brophy B, Smolenski G, Wheeler T, Wells D, L'Huillier P, Laible G. Cloned transgenic cattle produce milk with higher levels of beta-casein and kappa-casein. Nat Biotechnol. 2003;21(2):157-162. https://doi.org/10.1038/nbt783
  68. Hofmann A, Zakhartchenko V, Weppert M, Sebald H, Wenigerkind H, Brem G, et al. Generation of transgenic cattle by lentiviral gene transfer into oocytes. Biol Reprod. 2004;71(2):405-409. https://doi.org/10.1095/biolreprod.104.028472
  69. Grosse-Hovest L, Muller S, Minoia R, Wolf E, Zakhartchenko V, Wenigerkind H, et al. Cloned transgenic farm animals produce a bispecific antibody for T cell-mediated tumor cell killing. Proc Natl Acad Sci U S A. 2004;101(18):6858-6863. https://doi.org/10.1073/pnas.0308487101
  70. Yang P, Wang J, Gong G, Sun X, Zhang R, Du Z, et al. Cattle mammary bioreactor generated by a novel procedure of transgenic cloning for large-scale production of functional human lactoferrin. PLoS One. 2008;3(10):e3453.
  71. Echelard Y, Williams JL, Destrempes MM, Koster JA, Overton SA, Pollock DP, et al. Production of recombinant albumin by a herd of cloned transgenic cattle. Transgenic Res. 2009;18(3):361-376. https://doi.org/10.1007/s11248-008-9229-9
  72. Kuroiwa Y, Kasinathan P, Sathiyaseelan T, Jiao JA, Matsushita H, Sathiyaseelan J, et al. Antigen-specific human polyclonal antibodies from hyperimmunized cattle. Nat Biotechnol. 2009;27(2):173-181. https://doi.org/10.1038/nbt.1521
  73. Wongsrikeao P, Sutou S, Kunishi M, Dong YJ, Bai X, Otoi T. Combination of the somatic cell nuclear transfer method and RNAi technology for the production of a prion gene-knockdown calf using plasmid vectors harboring the U6 or tRNA promoter. Prion. 2011;5(1):39-46. https://doi.org/10.4161/pri.5.1.14075
  74. Jabed A, Wagner S, McCracken J, Wells DN, Laible G. Targeted microRNA expression in dairy cattle directs production of β-lactoglobulin-free, high-casein milk. Proc Natl Acad Sci U S A. 2012;109(42):16811-16816. https://doi.org/10.1073/pnas.1210057109
  75. Garrels W, Talluri TR, Apfelbaum R, Carratala YP, Bosch P, Potzsch K, et al. One-step multiplex transgenesis via sleeping beauty transposition in cattle. Sci Rep. 2016;6:21953.
  76. Su F, Wang Y, Liu G, Ru K, Liu X, Yu Y, et al. Generation of transgenic cattle expressing human β-defensin 3 as an approach to reducing susceptibility to Mycobacterium bovis infection. FEBS J. 2016;283(5):776-790. https://doi.org/10.1111/febs.13641
  77. Yum SY, Lee SJ, Kim HM, Choi WJ, Park JH, Lee WW, et al. Efficient generation of transgenic cattle using the DNA transposon and their analysis by next-generation sequencing. Sci Rep. 2016;6:27185.
  78. Wang Y, Ding F, Wang T, Liu W, Lindquist S, Hernell O, et al. Purification and characterization of recombinant human bile salt-stimulated lipase expressed in milk of transgenic cloned cows. PLoS One. 2017;12(5):e0176864.
  79. Wang M, Sun Z, Yu T, Ding F, Li L, Wang X, et al. Large-scale production of recombinant human lactoferrin from high-expression, marker-free transgenic cloned cows. Sci Rep. 2017;7(1):10733.
  80. Liu X, Wang Y, Tian Y, Yu Y, Gao M, Hu G, et al. Generation of mastitis resistance in cows by targeting human lysozyme gene to β-casein locus using zinc-finger nucleases. Proc Biol Sci. 2014;281(1780):20133368.
  81. Luo J, Song Z, Yu S, Cui D, Wang B, Ding F, et al. Efficient generation of myostatin (MSTN) biallelic mutations in cattle using zinc finger nucleases. PLoS One. 2014;9(4):e95225.
  82. Wu H, Wang Y, Zhang Y, Yang M, Lv J, Liu J, et al. TALE nickase-mediated SP110 knockin endows cattle with increased resistance to tuberculosis. Proc Natl Acad Sci U S A. 2015;112(13):E1530-E1539. https://doi.org/10.1073/pnas.1421587112
  83. Wei J, Wagner S, Maclean P, Brophy B, Cole S, Smolenski G, et al. Cattle with a precise, zygote-mediated deletion safely eliminate the major milk allergen beta-lactoglobulin. Sci Rep. 2018;8(1):7661.
  84. Petersen B, Niemann H. Molecular scissors and their application in genetically modified farm animals. Transgenic Res. 2015;24(3):381-396. https://doi.org/10.1007/s11248-015-9862-z
  85. Ikeda M, Matsuyama S, Akagi S, Ohkoshi K, Nakamura S, Minabe S, et al. Correction of a disease mutation using CRISPR/Cas9-assisted genome editing in Japanese black cattle. Sci Rep. 2017;7(1):17827.