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Developments in genetic modification of cattle and implications for regulation, safety and traceability |
Jan Pieter VAN DER BERG1( ), Gijs A. KLETER1, Evy BATTAGLIA1, Martien A. M. GROENEN2, Esther J. KOK1 |
1. Wageningen Food Safety Research, Wageningen University and Research, 6700 AE Wageningen, the Netherlands 2. Animal Breeding and Genomics, Wageningen University and Research, 6700 AH Wageningen, the Netherlands |
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Abstract Genetic modification techniques, in particular novel gene editing technologies, hold the yet unfulfilled promise of altering genetic traits in farm animals more efficiently than by crossbreeding, allowing for a more rapid development of new cattle breeds with distinct traits. Gene editing technologies allow for the directed alteration of specific traits and thereby have the potential to enhance, for instance, disease resilience, production yield and the production of desired substances in milk. The potential implications of these technological advancements, which are often combined with animal cloning methods, are discussed both for animal health and for consumer safety, also with consideration of available methods for the detection and identification of the related products in the food supply chain. Finally, an overview is provided of current regulatory approaches in the European Union (EU) and major countries exporting beef to the EU, for products from animals bred through established practices as well as modern biotechnologies.
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Keywords
cattle
food safety
gene editing
genetic modification
GMO detection
regulation
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Corresponding Author(s):
Jan Pieter VAN DER BERG
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Just Accepted Date: 19 January 2020
Online First Date: 16 March 2020
Issue Date: 28 April 2020
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1 |
C Tait-Burkard, A Doeschl-Wilson, M J McGrew, A L Archibald, H M Sang, R D Houston, C B Whitelaw, M Watson. Livestock 2.0—genome editing for fitter, healthier, and more productive farmed animals. Genome Biology, 2018, 19(1): 204
https://doi.org/10.1186/s13059-018-1583-1
pmid: 30477539
|
2 |
U.S. Food and Drug Administration (FDA). AquAdvantage Salmon Approval Letter and Appendix (NADA 141–454). Available at FDA website on September 1, 2019
|
3 |
F Miglior, A Fleming, F Malchiodi, L F Brito, P Martin, C F A Baes. A 100-year review: identification and genetic selection of economically important traits in dairy cattle. Journal of Dairy Science, 2017, 100(12): 10251–10271
https://doi.org/10.3168/jds.2017-12968
pmid: 29153164
|
4 |
W Haires. What is an EBV and how can it help you? Available at The Cattle Site on September 1, 2019
|
5 |
R Mrode, J M K Ojango, A M Okeyo, J M Mwacharo. Genomic selection and use of molecular tools in breeding programs for indigenous and crossbred cattle in developing countries: current status and future prospects. Frontiers in Genetics, 2019, 9: 694
https://doi.org/10.3389/fgene.2018.00694
pmid: 30687382
|
6 |
B J Hayes, H A Lewin, M E Goddard. The future of livestock breeding: genomic selection for efficiency, reduced emissions intensity, and adaptation. Trends in Genetics, 2013, 29(4): 206–214
https://doi.org/10.1016/j.tig.2012.11.009
pmid: 23261029
|
7 |
S G Moore, J F A Hasler. A 100-year review: reproductive technologies in dairy science. Journal of Dairy Science, 2017, 100(12): 10314–10331
https://doi.org/10.3168/jds.2017-13138
pmid: 29153167
|
8 |
M Mikkola. Superovulation and embryo transfer in dairy cattle —effect of management factors with emphasis on sex-sorted semen (Academic Dissertation). Finland: University of Helsinki, 2017
|
9 |
G E Seidel, S Moore Seidel. Training Manual for Embryo Transfer in Cattle (FAO Animal Production and Health Paper 77). Rome: Food and Agriculture Organization of the United Nations, 1991
|
10 |
K C S Tavares, I S Carneiro, D B Rios, C Feltrin, A K C Ribeiro, S Gaudêncio-Neto, L T Martins, L H Aguiar, C R Lazzarotto, C E M Calderón, F E M Lopes, L P R Teixeira, M Bertolini, L R Bertolini. A fast and simple method for the polymerase chain reaction-based sexing of livestock embryos. Genetics and Molecular Research, 2016, 15(1): gmr7476
https://doi.org/10.4238/gmr.15017476
pmid: 27050974
|
11 |
X Wu, H Ouyang, B Duan, D Pang, L Zhang, T Yuan, L Xue, D Ni, L Cheng, S Dong, Z Wei, L Li, M Yu, Q Y Sun, D Y Chen, L Lai, Y Dai, G P Li. Production of cloned transgenic cow expressing omega-3 fatty acids. Transgenic Research, 2012, 21(3): 537–543
https://doi.org/10.1007/s11248-011-9554-2
pmid: 21918821
|
12 |
S Yu, J Luo, Z Song, F Ding, Y Dai, N Li. Highly efficient modification of beta-lactoglobulin (BLG) gene via zinc-finger nucleases in cattle. Cell Research, 2011, 21(11): 1638–1640
https://doi.org/10.1038/cr.2011.153
pmid: 21912434
|
13 |
Y Gao, H Wu, Y Wang, X Liu, L Chen, Q Li, C Cui, X Liu, J Zhang, Y Zhang. Single Cas9 nickase induced generation of NRAMP1 knockin cattle with reduced off-target effects. Genome Biology, 2017, 18(1): 13
https://doi.org/10.1186/s13059-016-1144-4
pmid: 28143571
|
14 |
C Proudfoot, D F Carlson, R Huddart, C R Long, J H Pryor, T J King, S G Lillico, A J Mileham, D G McLaren, C B A Whitelaw, S C Fahrenkrug. Genome edited sheep and cattle. Transgenic Research, 2015, 24(1): 147–153
https://doi.org/10.1007/s11248-014-9832-x
pmid: 25204701
|
15 |
P Krimpenfort, A Rademakers, W Eyestone, A van der Schans, S van den Broek, P Kooiman, E Kootwijk, G Platenburg, F Pieper, R Strijker, H de Boer. Generation of transgenic dairy cattle using ‘in vitro’ embryo production. Nature Biotechnology, 1991, 9(9): 844–847
https://doi.org/10.1038/nbt0991-844
pmid: 1367358
|
16 |
J Wang, P Yang, B Tang, X Sun, R Zhang, C Guo, G Gong, Y Liu, R Li, L Zhang, Y Dai, N Li. Expression and characterization of bioactive recombinant human α-lactalbumin in the milk of transgenic cloned cows. Journal of Dairy Science, 2008, 91(12): 4466–4476
https://doi.org/10.3168/jds.2008-1189
pmid: 19038921
|
17 |
W H Eyestone. 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
pmid: 10729109
|
18 |
S H Chen, T D Vaught, J A Monahan, J Boone, E Emslie, P M Jobst, A E Lamborn, A Schnieke, L Robertson, A Colman, Y Dai, I A Polejaeva, D L Ayares. Efficient production of transgenic cloned calves using preimplantation screening. Biology of Reproduction, 2002, 67(5): 1488–1492
https://doi.org/10.1095/biolreprod.102.006981
pmid: 12390880
|
19 |
Y Kuroiwa, P Kasinathan, Y J Choi, R Naeem, K Tomizuka, E J Sullivan, J G Knott, A Duteau, R A Goldsby, B A Osborne, I Ishida, J M Robl. Cloned transchromosomic calves producing human immunoglobulin. Nature Biotechnology, 2002, 20(9): 889–894
https://doi.org/10.1038/nbt727
pmid: 12172556
|
20 |
L Grosse-Hovest, S Müller, R Minoia, E Wolf, V Zakhartchenko, H Wenigerkind, C Lassnig, U Besenfelder, M Müller, S D Lytton, G Jung, G Brem. Cloned transgenic farm animals produce a bispecific antibody for T cell-mediated tumor cell killing. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(18): 6858–6863
https://doi.org/10.1073/pnas.0308487101
pmid: 15105446
|
21 |
B Brophy, G Smolenski, T Wheeler, D Wells, P L’Huillier, G Laible. Cloned transgenic cattle produce milk with higher levels of β-casein and k-casein. Nature Biotechnology, 2003, 21(2): 157–162
https://doi.org/10.1038/nbt783
pmid: 12548290
|
22 |
B Yang, J Wang, B Tang, Y Liu, C Guo, P Yang, T Yu, R Li, J Zhao, L Zhang, Y Dai, N Li. Characterization of bioactive recombinant human lysozyme expressed in milk of cloned transgenic cattle. PLoS One, 2011, 6(3): e17593
https://doi.org/10.1371/journal.pone.0017593
pmid: 21436886
|
23 |
Y Yu, Y Wang, Q Tong, X Liu, F Su, F Quan, Z Guo, Y Zhang. A site-specific recombinase-based method to produce antibiotic selectable marker free transgenic cattle. PLoS One, 2013, 8(5): e62457
https://doi.org/10.1371/journal.pone.0062457
pmid: 23658729
|
24 |
X Su, S Wang, G Su, Z Zheng, J Zhang, Y Ma, Z Liu, H Zhou, Y Zhang, L Zhang. Production of microhomologous-mediated site-specific integrated LacS gene cow using TALENs. Theriogenology, 2018, 119: 282–288
https://doi.org/10.1016/j.theriogenology.2018.07.011
pmid: 30075414
|
25 |
R J Wall, A M Powell, M J Paape, D E Kerr, D D Bannerman, V G Pursel, K D Wells, N Talbot, H W Hawk. Genetically enhanced cows resist intramammary Staphylococcus aureus infection. Nature Biotechnology, 2005, 23(4): 445–451
https://doi.org/10.1038/nbt1078
pmid: 15806099
|
26 |
J A Richt, P Kasinathan, A N Hamir, J Castilla, T Sathiyaseelan, F Vargas, J Sathiyaseelan, H Wu, H Matsushita, J Koster, S Kato, I Ishida, C Soto, J M Robl, Y Kuroiwa. Production of cattle lacking prion protein. Nature Biotechnology, 2007, 25(1): 132–138
https://doi.org/10.1038/nbt1271
pmid: 17195841
|
27 |
S Shanthalingam, A Tibary, J E Beever, P Kasinathan, W C Brown, S Srikumaran. Precise gene editing paves the way for derivation of Mannheimia haemolytica leukotoxin-resistant cattle. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(46): 13186–13190
https://doi.org/10.1073/pnas.1613428113
pmid: 27799556
|
28 |
H Wu, Y Wang, Y Zhang, M Yang, J Lv, J Liu, Y Zhang. TALE nickase-mediated SP110 knockin endows cattle with increased resistance to tuberculosis. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(13): E1530–E1539
https://doi.org/10.1073/pnas.1421587112
pmid: 25733846
|
29 |
D F Carlson, C A Lancto, B Zang, E S Kim, M Walton, D Oldeschulte, C Seabury, T S Sonstegard, S C Fahrenkrug. Production of hornless dairy cattle from genome-edited cell lines. Nature Biotechnology, 2016, 34(5): 479–481
https://doi.org/10.1038/nbt.3560
pmid: 27153274
|
30 |
J Bellini. This gene-edited calf could transform Brazil’s beef industry. Available at The Wall Street Journal website on October 1, 2018
|
31 |
H J Huson, E S Kim, R W Godfrey, T A Olson, M C McClure, C C Chase, R Rizzi, A M P O’Brien, C P Van Tassell, J F Garcia, T S Sonstegard. Genome-wide association study and ancestral origins of the slick-hair coat in tropically adapted cattle. Frontiers in Genetics, 2014, 5: 101
https://doi.org/10.3389/fgene.2014.00101
pmid: 24808908
|
32 |
A W S Chan, E J Homan, L U Ballou, J C Burns, R D Bremel. Transgenic cattle produced by reverse-transcribed gene transfer in oocytes. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95(24): 14028–14033
https://doi.org/10.1073/pnas.95.24.14028
pmid: 9826647
|
33 |
J B Cibelli, S L Stice, P J Golueke, J J Kane, J Jerry, C Blackwell, F A Ponce de León, J M Robl. Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science, 1998, 280(5367): 1256–1258
https://doi.org/10.1126/science.280.5367.1256
pmid: 9596577
|
34 |
A Hofmann, V Zakhartchenko, M Weppert, H Sebald, H Wenigerkind, G Brem, E Wolf, A Pfeifer. Generation of transgenic cattle by lentiviral gene transfer into oocytes. Biology of Reproduction, 2004, 71(2): 405–409
https://doi.org/10.1095/biolreprod.104.028472
pmid: 15044266
|
35 |
S Y Yum, S J Lee, H M Kim, W J Choi, J H Park, W W Lee, H S Kim, H J Kim, S H Bae, J H Lee, J Y Moon, J H Lee, C I Lee, B J Son, S H Song, S M Ji, S J Kim, G Jang. Efficient generation of transgenic cattle using the DNA transposon and their analysis by next-generation sequencing. Scientific Reports, 2016, 6(1): 27185
https://doi.org/10.1038/srep27185
pmid: 27324781
|
36 |
M Wang, Z Sun, Z Zou, F Ding, L Li, H Wang, C Zhao, N Li, Y Dai. Efficient targeted integration into the bovine Rosa26 locus using TALENs. Scientific Reports, 2018, 8(1): 10385
https://doi.org/10.1038/s41598-018-28502-x
pmid: 29991797
|
37 |
W H Eyestone. Challenges and progress in the production of transgenic cattle. Reproduction, Fertility, and Development, 1994, 6(5): 647–652
https://doi.org/10.1071/RD9940647
pmid: 7569045
|
38 |
R J Wall, D E Kerr, K R Bondioli. Transgenic dairy cattle: genetic engineering on a large scale. Journal of Dairy Science, 1997, 80(9): 2213–2224
https://doi.org/10.3168/jds.S0022-0302(97)76170-8
pmid: 9313167
|
39 |
R L Krisher, J R Gibbons, R S Canseco, J L Johnson, C G Russell, D R Notter, W H Velander, F C Gwazdauskas. Influence of time of gene microinjection on development and DNA detection frequency in bovine embryos. Transgenic Research, 1994, 3(4): 226–231
https://doi.org/10.1007/BF02336775
pmid: 7920738
|
40 |
M Gagné, F Pothier, M A Sirard. Effect of microinjection time during postfertilization S-phase on bovine embryonic development. Molecular Reproduction and Development, 1995, 41(2): 184–194
https://doi.org/10.1002/mrd.1080410209
pmid: 7654372
|
41 |
C Galli, I Lagutina, A Perota, S Colleoni, R Duchi, F Lucchini, G Lazzari. Somatic cell nuclear transfer and transgenesis in large animals: current and future insights. Reproduction in Domestic Animals, 2012, 47(Suppl 3): 2–11
https://doi.org/10.1111/j.1439-0531.2012.02045.x
pmid: 22681293
|
42 |
C A Hodges, S L Stice. Generation of bovine transgenics using somatic cell nuclear transfer. Reproductive Biology and Endocrinology, 2003, 1(1): 81
https://doi.org/10.1186/1477-7827-1-81
pmid: 14613543
|
43 |
S Dikmen, F A Khan, H J Huson, T S Sonstegard, J I Moss, G E Dahl, P J Hansen. The SLICK hair locus derived from Senepol cattle confers thermotolerance to intensively managed lactating Holstein cows. Journal of Dairy Science, 2014, 97(9): 5508–5520
https://doi.org/10.3168/jds.2014-8087
pmid: 24996281
|
44 |
A L Norris, S S Lee, K J Greenlees, D A Tadesse, M F Miller, H Lombardi. Template plasmid integration in germline genome-edited cattle. bioRxiv 2019 [Preprint]
https://doi.org/10.1101/715482
|
45 |
A E Young, T A Mansour, B R McNabb, J R Owen, J F Trott, C T Brown, A L Van Eenennaam. Genomic and phenotypic analyses of six offspring of a genome-edited hornless bull. Nature Biotechnology, 2019 [Published Online]
https://doi.org/10.1038/s41587-019-0266-0
pmid: 31591551
|
46 |
United States Department of Agriculture, Foreign Agricultural Service (USDA FAS). Brazil—Agricultural Biotechnology Annual, BR 1818. Washington DC: USDA FAS, 2018
|
47 |
M Drost. Complications during gestation in the cow. Theriogenology, 2007, 68(3): 487–491
https://doi.org/10.1016/j.theriogenology.2007.04.023
pmid: 17531308
|
48 |
A Schurmann, D N Wells, B Oback. Early zygotes are suitable recipients for bovine somatic nuclear transfer and result in cloned offspring. Reproduction, 2006, 132(6): 839–848
https://doi.org/10.1530/REP-06-0054
pmid: 17127744
|
49 |
D Miao, M I Giassetti, M Ciccarelli, B Lopez-Biladeau, J M Oatley. Simplified pipelines for genetic engineering of mammalian embryos by CRISPR-Cas9 electroporation. Biology of Reproduction, 2019, 101(1): 177–187
https://doi.org/10.1093/biolre/ioz075
pmid: 31095680
|
50 |
J Ryu, R S Prather, K Lee. Use of gene-editing technology to introduce targeted modifications in pigs. Journal of Animal Science and Biotechnology, 2018, 9(1): 5
https://doi.org/10.1186/s40104-017-0228-7
pmid: 29423214
|
51 |
J P van der Berg, G A Kleter, E J Kok. Regulation and safety considerations of somatic cell nuclear transfer-cloned farm animals and their offspring used for food production. Theriogenology, 2019, 135: 85–93
https://doi.org/10.1016/j.theriogenology.2019.06.001
pmid: 31203092
|
52 |
United States Department of Agriculture, Foreign Agricultural Service (USDA FAS). EU-28—Agricultural Biotechnology Annual FR1827. Washington DC: USDA FAS, 2018
|
53 |
U.S. Food and Drug Administration (FDA). Animal Cloning—Risk Management Plan for Clones and Their Progeny. Available at FDA website on August 10, 2019
|
54 |
U.S. Food and Drug Administration (FDA). Guidance for Industry—Use of Animal Clones and Clone Progeny for Human Food and Animal Feed. Available at FDA website on August 10, 2019
|
55 |
U.S. Food and Drug Administration (FDA). Guidance for Industry #187 Regulation of Intentionally Altered Genomic DNA in Animals—Draft Guidance. Available at FDA website on August 10, 2019
|
56 |
Health Canada. Food Directorate Interim Policy on Foods from Cloned Animals. Ontario: Health Canada, 2003
|
57 |
Canada Food Inspection Agency (CFIA). Animals and Animal Products Derived Through Modern Biotechnology. Available at CFIA website on August 10, 2019
|
58 |
United States Department of Agriculture, Foreign Agricultural Service (USDA FAS). Argentina—Agricultural Biotechnology Annual. Washington DC: USDA FAS, 2019
|
59 |
United States Department of Agriculture, Foreign Agricultural Service (USDA FAS). Australia—Agricultural Biotechnology Annual AS1826. Washington DC: USDA FAS, 2018
|
60 |
Office of the Gene Technology Regulator (OGTR). Technical Review of the Gene Technology Regulations 2001—Decision Regulation Impact Statement. Available at the OGTR website on August 10, 2019
|
61 |
United States Department of Agriculture, Foreign Agricultural Service (USDA FAS). Uruguay Annual Biotechnology Report 2012. Washington DC: USDA FAS, 2012
|
62 |
Government of Argentina. Argentina presented to the WTO the Declaration on Gene Edition Techniques of the Southern Agricultural Council. Available at Government of Argentina website on August 9, 2019 (in Spanish)
|
63 |
European Commission (EC). EU Meat Market Observatory—Beef and veal. Available at EC website (Beef Statistics) on August 9, 2019
|
64 |
Enropean Group on Ethics in Science and New Technologies (EGE). Ethical aspects of animal cloning for food supply. Luxembourg: Office for Official Publications of the European Communities, 2008
|
65 |
European Parliament (EP). Cloning of animals kept and reproduced for farming purposes. Brussels, Belgium: European Parliament, 2015
|
66 |
European Food Safety Authority (EFSA). Food safety, animal health and welfare and environmental impact of animals derived from cloning by somatic cell nucleus transfer (SCNT) and their offspring and products obtained from those animals. EFSA Journal, 2008, 767: 1–49
|
67 |
International Embryo Transfer Society (IETS). Health assessment and care for animals involved in the cloning process. Champaign: International Embryo Technology Society, 2008
|
68 |
S Mallapaty. Australian gene-editing rules adopt ‘middle ground’. Nature, 2019 [Published Online] doi: 10.1038/d41586-019-01282-8
|
69 |
Ministry of Livestock, Agriculture and Fisheries (MGAP), Government of Uruguay. Regulations and Documents—Legislation. Available at MGAP website on August 6, 2019 (in Spanish)
|
70 |
World Trade Organization (WTO). Ministerial declaration of the southern agricultural council (CAS) on gene editing techniques—Communication from Argentina. Geneva, Switzerland: WTO, 2019
|
71 |
C Alimentarius. Guideline for the Conduct of Food Safety Assessment of Foods Produced using Recombinant-DNA Animals (CAC/GL 68–2008). Rome: FAO/WHO Joint Publications, 2008
|
72 |
European Food Safety Authority (EFSA). Guidance on the risk assessment of food and feed from genetically modified animals and on animal health and welfare aspects. EFSA Journal, 2012, 10(1): 2501
https://doi.org/10.2903/j.efsa.2012.2501
|
73 |
Food and Agriculture Organization of the United Nations (FAO). Development of integrated multipurpose animal recording systems. Rome: FAO, 2016
|
74 |
European Commission (EC). Study on the labelling of products from cloned animals and their offspring. Luxembourg: European Commission, 2015
|
75 |
J Huffman. Special Skretting feed key to RAS salmon grower’s ‘non-GMO’ label. Available at Undercurrent News website on December 19, 2019
|
76 |
Eurofins Gene Scan Technologies GmbH. A New Kit for the Detection of Genetically Modified Salmon in Food and Feed. Available at the Eurofins website on December 19, 2019
|
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