Skip to main content

Novel GM animal technologies and their governance

Abstract

Scientific advances in methods of producing genetically modified (GM) animals continue, yet few such animals have reached commercial production. Existing regulations designed for early techniques of genetic modification pose formidable barriers to commercial applications. Radically improved techniques for producing GM animals invite a re-examination of current regulatory regimes. We critically examine current GM animal regulations, with a particular focus on the European Union, through a framework that recognises the importance of interactions among regulatory regimes, innovation outcomes and industry sectors. The current focus on the regulation of risk is necessary but is unable to discriminate among applications and tends to close down broad areas of application rather than facilitate innovation and positive industry interactions. Furthermore, the fields of innovative animal biosciences appear to lack networks of organisations with co-ordinated future oriented actions. Such networks could drive coherent programmes of innovation towards particular visions and contribute actively to the development of regulatory systems for GM animals. The analysis presented makes the case for regulatory consideration of each animal bioscience related innovation on the basis of the nature of the product itself and not the process by which it was developed.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. AFAA (2004) Biotechnology and animal production. AgriFood Awareness Australia

  2. Alexandratos N, Bruinsma J (2012) World Agriculture Trends 2030/2050. The 2012 Revision. ESA working paper no. 12-03. Food and Agriculture Organization of the United Nations. http://www.fao.org/docrep/016/ap106e/ap106e.pdf. Accessed 27 May 2013

  3. Bronzwaer S (2008) EFSA scientific forum ‘from safe foods to healthy diets’. EU risk assessment—past, present and future. Trends Food Sci Technol 19:52–58

    Article  Google Scholar 

  4. Brown N, Rappert B, Webster A, Cabello C, Sans-Menendez L, Markx F, van de Meulen B (2001) Final Report of the FORMAKIN Project, TSER Programme, Stage 2, Work Package 5/6, Jan, 2001. http://www.york.ac.uk/media/satsu/documents-papers/Brown-Rappert-2001-formakin.PDF. Accessed 9 April 2013

  5. Buck EH (2011) Genetically Engineered Fish and Seafood: Environmental Concerns. Congressional Research Service. Report for Congress

  6. Capecchi, MR (1989) Altering the genome by homologous recombination. Science 244:1288–1292 PMID2660260

    Google Scholar 

  7. Carlson DF, Wenfang Tan W, Lillico SG, Stverakovad D, Proudfoot C, Michelle Christiana M, Voytasa DF, Longf CR, Whitelaw CBA, Fahrenkrug SC (2012) Efficient TALEN-mediated gene knockout in livestock. PNAS 109(43):17382–17387

    PubMed  Article  CAS  Google Scholar 

  8. CAST (2009) Animal productivity and genetic diversity. Part 8, IP43

  9. Clark J, Whitelaw B (2003) A future for transgenic livestock. Nat Rev 4:825–833

    CAS  Google Scholar 

  10. Chataway J, Tait J, Wield D (2004) Understanding company R&D strategies in agro-biotechnology: trajectories and Blindspots. Res Policy 33(6–7):1041–1057

    Article  Google Scholar 

  11. Codex Alimentarius (2008) Guideline for the conduct of food safety assessment of foods derived from recombinant DNA animals. http://www.codexalimentarius.org/codex-home/en/. Accessed 4 April 2013

  12. COGEM (2011) Genetically modified animals: a wanted and unwanted reality. COGEM Topic Report (CGM/120111-01) Independent scientific advice and information for the Dutch Government

  13. DeFrancesco L (2011) Move over ZFNs. Nat Biotechnol 29(7):681–684

    Google Scholar 

  14. Dove A (2000) Milking the genome for profit. Nat Biotechnol 18(10):1045–1047

    PubMed  Article  CAS  Google Scholar 

  15. Durai S, Mani M, Kandavelou K, Wu J, Porteus MH, Chandrasegaran S (2005) Zinc finger nucleases: custom designed molecular scissors for genome engineering of plant and mammalian cells. Nucleic Acids Res 33(18):5978–5990

    PubMed  Article  CAS  Google Scholar 

  16. EFSA Panels on GMO and AHAW (2012) Guidance on the risk assessment of food and feed from genetically modified animals and on animal health and welfare aspects. EFSA J 10(1):2501–2544

    Google Scholar 

  17. EFSA (2013) Guidance on the environmental risk assessment of genetically modified animals. EFSA J 11(5):3200 http://www.efsa.europa.eu/en/efsajournal/pub/3200.htm?utm_source=feedly. Accessed 25 May 2013

    Google Scholar 

  18. Ekser B, Edwin Klein E, Jing H, Stolz DB, Echeverri GJ, Long C, Lin CC, Mohamed E, Hidetaka H, Veroux M, Ayares D, Cooper DKC, Gridelli B (2012) Genetically engineered pig to baboon liver xenotransplantation: histopathology of xenografts and native organs. PLoS ONE 7(1):e29720

    PubMed  Article  CAS  Google Scholar 

  19. Fahrenkrug SC, Blake A, Carlson DF, Doran T, Van Eenennaam A, Faber D, Galli C, Gao Q, Hackett PB, Li N, Maga EA, Muir WM, Murray JD, Shi D, Stotish R, Sullivan E, Taylor JF, Walton M, Wheeler M, Whitelaw B, Glenn BP (2010) Precision genetics for complex objectives in animal agriculture. J Anim Sci 88:2530–2539

    PubMed  Article  CAS  Google Scholar 

  20. FAO (2009) The state of food and agriculture—livestock in the balance. Food and Agriculture Orgainzation of the United Nations, Rome

    Google Scholar 

  21. FDA (2009) The Regulation of Genetically Engineered Animals containing Heritable Recombinant DNA constructs. Final Guidance

  22. FDA (2011) Advancing regulatory science at FDA: a strategic plan. August 2011. http://www.fda.gov/ScienceResearch/SpecialTopics/RegulatoryScience/ucm267719.htm. Accessed 17 March 2013

  23. FDA (2012) AquAdvantage salmon preliminary finding. Prepared by the Center for Veterinary Medicine, United States Food and Drug Administration Department of Health and Human Services. 4 May 2012 http://www.fda.gov/AnimalVeterinary/DevelopmentApprovalProcess/GeneticEngineering/GeneticallyEngineeredAnimals/ucm280853.htm. Accessed 31 May 2013

  24. Fernandez M, Schook L (2005) Introduction. In A Future for Animal Biotechnology. Proceedings from a forum hosted by the University of Illinois and the Pew Initiative on Food and Biotechnology, Chicago, Illinois, Dec. 2005, pp 5–6 http://www.pewtrusts.org/uploadedFiles/wwwpewtrustsorg/Summaries_-_reports_and_pubs/PIFB_Future_for_Animal_Biotech_Workshop_Proceedings.pdf. Accessed 17 March 2013

  25. Foresight. The Future of Food and Farming (2011) Final Project Report. The Government Office for Science, London

  26. GAIN (2011) China—People’s Republic of, GE plants and animals. Annual 2010. GAIN report number CH11002. USDA Global Agricultural Information Network. http://gain.fas.usda.gov/Recent%20GAIN%20Publications/Biotechnology%20-%20GE%20Plants%20and%20Animals_Beijing_China%20-%20Peoples%20Republic%20of_3-15-2011.pdf. Accessed 31 May 2013

  27. Garnett T (2009) Livestock-related greenhouse gas emissions: impacts and options for policy makers. Environ Sci Policy 12:491–503

    Article  CAS  Google Scholar 

  28. Gaskell G, Allansdottir A, Allum N, Castro P, Esmer Y, Fischler C, Jackson J, Kronberger N, Hampel J, Mejlgaard N, Quintanvilha A, Rammer A, Revuelta G, Stares S, Torgersen H, Wager W (2011) The 2010 Eurobarometer on the life sciences. Nat Biotechnol 29(2):113–114

    PubMed  Article  CAS  Google Scholar 

  29. Golovan SP, Meidinger RG, Ajakaiye A, Cottrill M, Wiederkehr M, Barney D, Plante C, Pollard J, Fan MZ, Hayes MA, Laursen J, Hjorth JP, Hacker RR, Phillips JP, Forsberg CW (2001) Pigs expressing salivary phytase and acid phosphatase activities. Can J Microbiol 46:59–71

    Google Scholar 

  30. Gordon JW, Scangos GA, Plotkin DJ, Barbosa JA, Ruddle FH (1980) Genetic transformation of mouse embryos by microinjection of purified DNA. Proc Natl Acad Sci USA 77:7380–7384

    PubMed  Article  CAS  Google Scholar 

  31. Geurts AM, Cost GJ, Freyvert Y, Zeitler B, Miller JC, Choi VM, Jenkins SS, Wood A (2009) Knockout rats via embryo microinjection of zinc-finger nucleases. Science 325(5939):433

    PubMed  Article  CAS  Google Scholar 

  32. Health Canada (2011) The Regulation of genetically modified food. http://www.hc-sc.gc.ca/sr-sr/pubs/biotech/reg_gen_mod-eng.php. Accessed 4 March 2013

  33. Houdebine L-M (2009) Production of pharmaceutical proteins by transgenic animals. Comp Immunol Microbiol Infect Dis 32(2):107–121

    PubMed  Article  Google Scholar 

  34. Huang J, Wang Q (2002) Agricultural biotechnology development and policy in China. AgBioForum 5(4):122–131

    Google Scholar 

  35. Hume DA, Whitelaw CBA, Archibald AL (2011) The future of animal production; improving productivity and sustainability. J Agric Sci 149:9–16

    Article  Google Scholar 

  36. Ittner LM, Gotz J (2007) Pronuclear injection for the production of transgenic mice. Nat Protoc 2:1206–1215

    PubMed  Article  CAS  Google Scholar 

  37. Jabed A, Wagner S, McCraken J, Wells DW, Laible G (2012) Targeted microRNA expression in dairy cattle directs production of β-lactoglobulin-free high-casein milk. Proc Nat Acad Sci USA 109(42):16811–16816

    PubMed  Article  CAS  Google Scholar 

  38. Kaneko T, Moisyadi S, Suganuma R, Hohn B, Yanagimachi R, Pelczar P (2005) Recombinase-mediated mouse transgenesis by intracytoplasmic sperm injection. Theriogenology 64:1704–1715

    PubMed  Article  CAS  Google Scholar 

  39. Kleter GA, Kok EJ (2010) Safety assessment of biotechnology used in animal production, including Genetically Modified (GM) feed and GM animals—a review. Animal Sci Pap Rep 28(2):105–114

    Google Scholar 

  40. Lazaris A, Arcidiacono S, Huang Y, Zhou J-F, Duguay F, Chretien N, Welsh EA, Soareas W, Karatzas CN (2002) Spider silk fibers spun from soluble recombinant silk produced in mammalian cells. Science 295:472–476

    PubMed  Article  CAS  Google Scholar 

  41. Le Provost F, Lillico S, Passet B, Young R, Whitelaw B, Vilotte J-L (2009) Zinc finger nuclease technology heralds a new era in mammalian transgenesis. Trends Biotechnol 28(3):134–141

    PubMed  Article  Google Scholar 

  42. Lusser M, Davies HV (2013) Comparative regulatory approaches for groups of new plant breeding techniques. New Biotechnol (in press) http://dx.doi.org/10.1016/j.nbt.2013.02.004

  43. Lyall J, Irvine RA, Sherman A, McKinley TJ, Nunez A, Purdie A, Outtrim L, Brown IH, Rolleston-Smith G, Sang H, Tiley L (2011) Suppression of avian influenza transmission in genetically modified chickens. Science 33:223–226

    Article  Google Scholar 

  44. Maga EA, Murray JD (2010) Welfare applications of genetically engineered animals for use in agriculture. J Anim Sci 88:1588–1591

    PubMed  Article  CAS  Google Scholar 

  45. Mandel GN (2004) Gaps, inexperience, inconsistencies and overlaps: crisis in the regulation of genetically modified plants and animals. William Mary Law Rev 45:2167–2260

    Google Scholar 

  46. Marshall KM, Hurley WL, Shanks RD, Wheeler MB (2006) Effects of suckling intensity on milk yield and piglet growth from lactation-enhanced gilts. J Anim Sci 84:2346–2351

    PubMed  Article  CAS  Google Scholar 

  47. Martineau B (2001) First Fruit. The creation of the Flavr Savr™ tomato and the birth of biotech food. McGraw-Hill, New York

  48. Mastroeni M, Tait J, Rosiello A (2013) Regional innovation policies in a globally connected environment. Sci Public Policy 40(1):8–16

    Article  Google Scholar 

  49. Mastroeni M, Mittra J, Tait J (2012) Methodology for the Analysis of Life Science Innovation Systems (ALSIS) and its Application to Three Case Studies. TSB Regenerative Medicine Programme: Value Systems and Business Models. REALISE Project. Innogen Centre Report to Technology Strategy Board. 29th May, 2012. http://www.genomicsnetwork.ac.uk/media/REALISE%20Case%20Study%20Report%20-%20Innogen.pdf. Accessed 4 April 2013

  50. McGrew MJ, Sherman A, Ellard FM, Lillico SG, Gilhooley HJ, Kingsman AJ, Mitrophanous KA, Sang H (2004) Efficient production of germline transgenic chickens using lentiviral vectors. EMBO Rep 5:728–733

    PubMed  Article  CAS  Google Scholar 

  51. Mendon A-Hagler L, Souza L, Aleixo L, Oda L (2008) Trends in biotechnology and biosafety in Brazil. Environ Biosafety Res 7:115–121

    Article  Google Scholar 

  52. Mittra J, Tait J, Wield D (2011) From maturity to value-added innovation: lessons from the pharmaceutical and agro-biotechnology industries. Trends Biotechnol 29(3):105–109

    PubMed  Article  CAS  Google Scholar 

  53. Milne CP, Tait J (2009) Evolution along the government-governance continuum: FDA’S orphan products and fast track programs as exemplars of “what works” for innovation and regulation. Food and Drug Law J 64(4):733–753

    Google Scholar 

  54. Mittra J, Tait J (2012) Analysing stratified medicine business models and value systems: innovation-regulation interactions. New Biotechnol 29(6):709–719

    Article  CAS  Google Scholar 

  55. Murray JD, Maga EA (2010) Is there a risk from not using GE animals? Transgenic Res 19:357–361

    PubMed  Article  CAS  Google Scholar 

  56. Murray JD, Mohamad-Fauzi N, Cooper CA, Maga EA (2010) Current status of transgenic animal research for human health applications. Acta Sci Vet 38(2):627–632

    Google Scholar 

  57. Niemann H, Kues W, Carnwath JW (2009) Transgenic farm animals: present and future. Rev Sci Tech 24:285–298

    Google Scholar 

  58. Noyes H, Brass A, Obara I, Anderson S, Archibald AL, Bradley DG, Fisher P, Freeman A, Gibson J, Gicheru M, Hall L, Hanotte O, Hulme H, McKeever D, Murray C, Oh SJ, Tate C, Smith K, Tapio M, Wambugo J, Williams DJ, Agaba M, Kemp SJ (2011) Genetic and expression analysis of cattle identifies candidate gene in pathways responding to Trypanosoma congolense infection. Proc Natl Acad Sci 108(22):9304–9309

    PubMed  Article  CAS  Google Scholar 

  59. Novosleva TA, Meuwissen MPM, Huirne RBM (2007) Adoption of GM technology in livestock production chains: an integrating framework. Trends Food Sci Technol 18:175–188

    Article  Google Scholar 

  60. Palmiter RD, Brinster RL, Hammer RE, Trumbauer ME, Rosenfeld MG, Birnberg NC, Evans RM (1982) Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion genes. Nature 300:611–615

    PubMed  Article  CAS  Google Scholar 

  61. Park F (2007) Lentiviral vectors; are they the future of animal transgenesis? Physiol Genomics 31:159–173

    PubMed  Article  CAS  Google Scholar 

  62. Pig Progress (2012) Enviropig project halted as Ontario Pork pulls the plug. http://www.pigprogress.net/Health-Diseases/Research/2012/4/Enviropig-project-halted-as-Ontario-Pork-pulls-the-plug-PP008578W/. Accessed 4 April 2012

  63. Pray L (2008) Recombinant DNA technology and transgenic animals. Nature Education 1(1)

  64. Regaldo A (2010) Building a Better Goat. MIT Technology Review. http://www.technologyreview.com/news/421268/building-a-better-goat/. Accessed 10 March 2013

  65. Ridley M (2013) Editing our Genes, One Letter at a Time. The Wall Street Journal, Mind and Matter. January 11th

  66. Salamone D, Barañao L, Santos C, Bussmann L, Artuso J, Werning C, Prync A, Carbonetto C, Dabsys S, Munar C, Salaberry R, Berra G, Berra I, Fernández N, Papouchado M, Foti M, Judewicz N, Mujica I, Muñoz L, Alvarez SF, González E, Zimmermann J, Criscuolo M, Melo C (2006) High level expression of bioactive recombinant hormone growth hormone in the milk of transgenic cows. J Biotechnol 124(2):46–72

    Article  Google Scholar 

  67. Schnieke AE, Kind AJ, Ritchie WA, Mycock K, Scott AR, Ritchie M, Wilmut I, Colman A, Campbell KH (1997) Human factor IX transgenic sheep produced by transfer of nuclei from transfected fetal fibroblasts. Science 278:2130–2133

    PubMed  Article  CAS  Google Scholar 

  68. Service F (2002) Mammalian cells spin a spidery new yarn. Science 295(5554):419–421

    Article  Google Scholar 

  69. Subramanian V (2012) Driving forces in global agriculture. Rice Today—International Rice Research Institute. 11(2):40–41

  70. Suk J, Bruce A, Gertz R, Whitelaw CBA, Braun A, Oram C, Rodriguez-Cerezo E, Papatryfon I (2007) Dolly for dinner? Assessing commercial and regulatory trends in cloned livestock. Nat Biotechnol 25(1):47–53

    PubMed  Article  CAS  Google Scholar 

  71. Tait J (2007) Systemic interactions in life science innovation. Technol Anal Strateg Manag 19(3):257–277

    Article  Google Scholar 

  72. Tait J (2008) Risk governance of genetically modified crops: European and American perspectives. In: Renn O, Walker K (eds) Global risk governance: concept and practice using the IRGC framework. Springer Science and Business Media, Dordrecht, pp 133–153

    Chapter  Google Scholar 

  73. Tait J, Barker G (2011) Global food security and the governance of modern biotechnologies: opportunities and challenges for Europe. EMBO Rep 12:763–768

    PubMed  Article  CAS  Google Scholar 

  74. Tait J, Levidow L (1992) Proactive and reactive approaches to risk regulation: the case of biotechnology. Futures 24(3):219–231

    Article  Google Scholar 

  75. Tait J, with Wield D, Chataway J, Bruce A (2008) Health Biotechnology to 2030. Report to OECD International Futures Project, “The Bio-Economy to 2030: Designing a Policy Agenda”, OECD, Paris, pp 51; http://www.oecd.org/dataoecd/12/10/40922867.pdf. Accessed 4 April 2013

  76. Tomley FM, Shirley MW (2009) Livestock infectious diseases and zoonoses. Philos Trans R Soc B 364:2637–2642

    Article  Google Scholar 

  77. Van Eenennaam AL, Muir WM (2011) Transgenic salmon: a final leap to the grocery shelf. Nat Biotechnol 29(8):706–7011

    PubMed  Article  Google Scholar 

  78. Vàzquez-Salat N, Salter B, Smets G (2010) International Multi-level Governance of Genetically Modified Organisms: EU, USA and India. Work Package 6: Activity 6.1. PEGASUS

  79. Vàzquez-Salat N, Houdebine LM (2013) Will GM animals follow the GM plant fate? Transgenic Res 22:5–13

    PubMed  Article  Google Scholar 

  80. Vàzquez-Salat N, Salter B, Smets G, Houdebine LM (2012) The current state of GMO governance: are we ready for GM animals? Biotechnol Adv 30:1336–1343

    PubMed  Article  Google Scholar 

  81. Waigmann E, Paoletti C, Davies H, Perry J, Kärenlampi S, Kuiper H (2012) Risk assessment of genetically modified organisms (GMOs). EFSA J 10(10) s1008:1–7 http://www.efsa.europa.eu/en/efsajournal/pub/s1008.htm . Accessed 31 May 2013

    Google Scholar 

  82. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/cas-mediated genome engineering. Cell 153(4):910–918

    PubMed  Article  CAS  Google Scholar 

  83. World Trade Organization (WTO) (2010) European communities—measures affecting the approval and marketing of biotech products. http://www.wto.org/english/tratop_e/dispu_e/cases_e/ds291_e.htm. Accessed 27 May 2013

  84. Yang W (2003) Regulation of genetically modified organisms in China. RECIEL 12(1):99–108

    Google Scholar 

  85. Yang B, Wang J, Tang B, Liu Y, Guo C, Yang P, Yu T, Li R, Zhao J, Zhang L, Dai Y, Li N (2011) Characterisation of bioactive recombinant human lysozyme expressed in milk of transgenic cattle. PLoS ONE 6(3):1–10

    Google Scholar 

Download references

Acknowledgments

The research forming the basis of this paper was supported by the Economic and Social Research Council (grant RES-000-22-3737) and formed part of the research programme at the ESRC Innogen Centre at the University of Edinburgh. CBAW is supported by a BBSRC ISP Grant. We are very grateful for thoughtful comments from four anonymous reviewers.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ann Bruce.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bruce, A., Castle, D., Gibbs, C. et al. Novel GM animal technologies and their governance. Transgenic Res 22, 681–695 (2013). https://doi.org/10.1007/s11248-013-9724-5

Download citation

Keywords

  • GM animals
  • Biotechnology
  • Livestock
  • Company strategies
  • Regulatory science
  • Governance