Genetically modified farm animals and fish in agriculture: A review

Livestock Science

Volumn 153, Issue 1-3, 2013, Pages 1-9

  Forabosco, F ^a   Lohmus M ^a   Rydhmer, L ^a   Sundstrom L F ^b  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Economical traits; Environment; Fish; Food; Genetically modified animal

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); BOS; CYPRINIDAE; GALLUS GALLUS; OVIS ARIES; SUIDAE; SUS; TILAPIA;

EID: 84875814132     PISSN: 18711413     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.livsci.2013.01.002     Document Type: Review

References (92)

1. Amsterdam A., Lin S., Moss L.G., Hopkins N. Requirements for green fluorescent protein detection in transgenic zebrafish embryos. Gene 1996, 173:99-103.
2. Anderson E.D., Mourich D.V., Fahrenkrug S.C., LaPatra S., Shepherd J., Leong J.A. Genetic immunization of rainbow trout (Oncorhynchus mykiss) against infectious hematopoietic necrosis virus. Mol. Mar. Biol. Biotechnol. 1996, 5:114-122.
3. Blasco A. The role of genetic engineering in livestock production. Livest. Sci. 2008, 113:191-201.
4. Bleck G.T., White B.R., Miller D.J., Wheeler M.B. Production of bovine alpha-lactalbumin in the milk of transgenic pigs. J. Anim. Sci. 1998, 76:3072-3078.
5. 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, 21:157-161.
6. Butler T.M., Fletcher G.L. Promoter analysis of a growth hormone transgene in Atlantic salmon. Theriogenology 2009, 72:62-71.
7. Chen W.Y., Wight D.C., Wagner T.E., Kopchick J.J. Expression of a mutated bovine growth hormone gene suppresses growth of transgenic mice. Proc. Natl. Acad. Sci. USA 1990, 87:5061-5065.
8. Clements J.E., Wall R.J., Narayan O., Hauer D., Schoborg R., Sheffer D., Powell A., Carruth L.M., Zink M.C., Rexroad C.E. Development of transgenic sheep that express the visna virus envelope gene. Virology (New York) 1994, 200:370-380.
9. Cundiff L.V., Bishop M.C., Johnson R.K. Challenges and opportunities for integrating genetically modified animals into traditional animal breeding plans. J. Anim. Sci. 1993, 71:20-25.
10. Damak S., Su H., Jay N.P., Bullock D.W., Su H.Y. Improved wool production in transgenic sheep expressing insulin-like growth factor 1. Biotechnology 1996, 14:185-188.
11. Denning C., Burl S., Ainslie A., Bracken J., Dinnyes A., Fletcher J., King T., Ritchie M., Ritchie W.A., Rollo M., Sousa P.D., Travers A., Wilmut I., Clark A.J., de Sousa P. Deletion of the alpha(1,3)galactosyl transferase (GGTA1) gene and the prion protein (PrP) gene in sheep. Nat. Biotechnol. 2001, 19:559-562.
12. Devlin R.H., Yesaki T.Y., Biagi C.A., Donaldson E.M., Swanson P., Chan W.K. Extraordinary salmon growth. Nature 1994, 371:209-210.
13. Devlin R.H., Biagi C.A., Yesaki T.Y., Smailus D.E., Byatt J.C. Growth of domesticated transgenic fish. Nature (London) 2001, 409:781-782.
14. Du S.J., Gong Z., Fletcher G.L., Shears M.A., King M.J., Idler D.R., Hew C.L. Growth enhancement in transgenic Atlantic salmon by the use of an "all fish" chimeric growth hormone gene construct. Nat. Biotechnol. 1992, 10:176-181.
15. Dunham R.A., Warr G.W., Nichols A., Duncan P.L., Argue B., Middleton D., Kucuktas H. Enhanced bacterial disease resistance of transgenic channel catfish Ictalurus punctatus possessing cecropin genes. Mar. Biotechnol. 2002, 4:338-344.
16. Dybvig T., Facci M., Gerdts V., Wilson H.L. Biological roles of host defense peptides: lessons from transgenic animals and bioengineered tissues. Cell Tissue Res. 2011, 343:213-225.
17. El-Zaeem S.Y., Ahmed M.M.M., Salama M.E.-S., El-Maremie H.A.-R. Production of salinity tolerant Nile tilapia, Oreochromis niloticus through traditional and modern breeding methods: II. Application of genetically modified breeding by introducing foreign DNA into fish gonads. Afr. J. Biotechnol. 2011, 10:684-695.
18. European Food Safety Authority. Guidance on the environmental risk assessment of genetically modified animals. EFSA Panel on Genetically Modified Organisms (GMO). EFSA Journal, 175, in press.
19. Fahrenkrug S.C., Blake A., Carlson D.F., Doran T., Eenennaam A.V., Faber D., Galli C., Gao Q., Hackett P.B., Li N., Maga E.A., Muir W.M., Murray J.D., Shi D., Stotish R., Sullivan E., Taylor J.F., Walton M., Wheeler M., Whitelaw B., Glenn B.P., van Eenennaam A. Precision genetics for complex objectives in animal agriculture. J. Anim. Sci. 2010, 88:2530-2539.
20. FAO, 2012. GMOs in the pipeline: looking to the next five years in the crop, forestry, livestock, aquaculture and agro-industry sectors in developing countries. In: Proceedings of the 18th FAO Biotechnology Forum Conference, p. 128.
21. Fletcher G.L., Shears M.A., Yaskowiak E.S., King M.J., Goddard S.V. Gene transfer: potential to enhance the genome of Atlantic salmon for aquaculture. Aust. J. Exp. Agric. 2004, 44:1095-1100.
22. Fletcher G.L., Hobbs R.S., Evans R.P., Shears M.A., Hahn A.L., Hew C.L. Lysozyme transgenic Atlantic salmon (Salmo salar L.). Aquac. Res. 2011, 42:427-440.
23. Forabosco F., Rydhmer L. The current status and future prospects of genetically modified farm animals in Europe. Genomics Quant. Genet. 2012, 5:1-4.
24. Forsberg C.W., Meidinger R.G., Ajakaiye A., Verschoor C., Golovan S.P., Murray D.A., Phillips J.P., Fan M.Z., Hayes T., Walters S., Kelly J.M., Hacker R.R. The Enviropig (TM): phosphorus nutrition, physiology and tissue composition. Transgenic Res. 2006, 15:116-117.
25. Gama L.T., Smith C., Gibson J.P. Transgene effects, introgression strategies and testing schemes in pigs. Anim. Prod. 1992, 54:427-440.
26. Golovan S.P., Meidinger R.G., Ajakaiye A., Cottrill M., Wiederkehr M.Z., Barney D.J., Plante C., Pollard J.W., Fan M.Z., Hayes M.A., Laursen J., Hjorth J.P., Hacker R.R., Phillips J.P., Forsberg C.W. Pigs expressing salivary phytase produce low-phosphorus manure. Nat. Biotechnol. 2001, 19:741.
27. Greger M. Transgenesis in animal agriculture: addressing animal health and welfare concerns. J. Agric. Environ. Ethics 2011, 24:451-472.
28. Hammer R.E., Pursel V.G., Rexroad C.E., Wall R.J., Bolt D.J., Ebert K.M., Palmiter R.D., Brinster R.L. Production of transgenic rabbits, sheep and pigs by microinjection. Nature (UK) 1985, 315:680-683.
29. Hew C., Poon R., Xiong F., Gauthier S., Shears M., King M., Davies P., Fletcher G. Liver-specific and seasonal expression of transgenic Atlantic salmon harboring the winter flounder antifreeze protein gene. Transgenic Res. 1999, 8:405-414.
30. Houdebine L.M. Production of pharmaceutical proteins by transgenic animals. Comp. Immunol., Microbiol. Infect. Dis. 2009, 32:107-121.
31. Huang X., Zhou L., Gong Z. Liver tumor models in transgenic zebrafish: an alternative in vivo approach to study hepatocarcinogenes. Future Oncol. 2012, 8:21-28.
32. Kinsella J.E., Lokesh B., Stone R.A. Dietary n-3 polyunsaturated fatty acids and amelioration of cardiovascular disease: possible mechanisms. Am. J. Clin. Nutr. 1990, 52:1-28.
33. Konishi K., Yonai M., Kaneyama K., Ito S., Matsuda H., Yoshioka H., Nagai T., Imai K. Relationships of survival time, productivity and cause of death with telomere lengths of cows produced by somatic cell nuclear transfer. J. Reprod. Dev. 2011, 57:572-578.
34. Krasnov A., Pitkänen T.I., Mölsä H. Gene transfer for targeted modification of salmonid fish metabolism. Genet. Anal.: Biomol. Eng. 1999, 15:115-119.
35. Krasnov A., Pitkänen T.I., Reinisalo M., Mölsä H. Expression of human glucose transporter type 1 and rat hexokinase type II complementary DNAs in rainbow trout embryos: effects on glucose metabolism. Mar. Biotechnol. 1999, 1:25-32.
36. Kues W.A., Niemann H. The contribution of farm animals to human health. Trends Biotechnol. 2004, 22:286-294.
37. Kues W.A., Niemann H. Advances in farm animal transgenesis. Prev. Vet. Med. 2011, 102:146-156.
38. Lai L., Kang J.X., Li R., Wang J., Witt W.T., Yong H.Y., Hao Y., Wax D.M., Murphy C.N., Rieke A., Samuel M., Linville M.L., Korte S.W., Evans R.W., Starzl T.E., Prather R.S., Dai Y. Generation of cloned transgenic pigs rich in omega-3 fatty acids. Nat. Biotechnol. 2006, 24:435-436.
39. Lo D., Pursel V., Linton P.J., Sandgren E., Behringer R., Rexroad C., Palmiter R.D., Brinster R.L. Expression of mouse IgA by transgenic mice, pigs and sheep. Eur. J. Immunol. 1991, 21:1001-1006.
40. Lyall J., Irvine R.M., Sherman A., McKinley T.J., Nunez A., Purdie A., Outtrim L., Brown I.H., Rolleston-Smith G., Sang H., Tiley L. Suppression of avian influenza transmission in genetically modified chickens. Science (Washington) 2011, 331:223-226.
41. Mao W., Wang Y., Wang W., Wu B., Feng J., Zhu Z. Enhanced resistance to Aeromonas hydrophila infection and enhanced phagocytic activities in human lactoferrin-transgenic grass carp (Ctenopharyngodon idellus). Aquaculture 2004, 242:93-103.
42. Martinez R., Estrada M.P., Berlanga J., Guillen I., Hernandez O., Cabrera E., Pimentel R., Morales R., Herrera F., Morales A., Pina J.C., Abad Z., Sanchez V., Melamed P., Lleonart R., De L.F.J. Growth enhancement in transgenic tilapia by ectopic expression of tilapia growth hormone. Mol. Mar. Biol. Biotechnol. 1996, 5:62-70.
43. Maxmen A. Politics holds back animal engineers. Nature 2012, 490:318-319.
44. Medeiros E., Phelps M., Fuentes F., Bradley T. Overexpression of follistatin in trout stimulates increased muscling. Am. J. Physiol.-Regul., Integrative Comp. Physiol. 2009, 297:R235-R242.
45. Mozdziak P.E., Pophal S., Borwornpinyo S., Petitte J.N. Transgenic chickens expressing beta-galactosidase hydrolyze lactose in the intestine. J. Nutr. 2003, 133:3076-3079.
46. Mueller M., Brenig B., Winnacker E.-L., Brem G. Transgenic pigs carry cDNA copies encoding the murine Mx1 protein which confers resistance to influenza virus infection. Gene (Amsterdam) 1992, 121:263-270.
47. Nam Y.K., Noh J.K., Cho Y.S., Cho H.J., Cho K.N., Kim C.G., Kim D.S. Dramatically accelerated growth and extraordinary gigantism of transgenic mud loach Misgurnus mizolepis. Transgenic Res. 2001, 10:353-362.
48. Nam Y.K., Maclean N., Hwang G., Kim D.S. Autotransgenic and allotransgenic manipulation of growth traits in fish for aquaculture: a review. J. Fish Biol. 2008, 72:1-26.
49. Niemann H., Kues W.A. Transgenic farm animals: an update. Reprod., Fertil. Dev. 2007, 19:762-770.
50. Niemann H., Kuhla B., Flachowsky G. Perspectives for feed-efficient animal production. J. Anim. Sci. 2011, 89:4344-4363.
51. Noble M.S., Rodriguez-Zas S., Cook J.B., Bleck G.T., Hurley W.L., Wheeler M.B. Lactational performance of first-parity transgenic gilts expressing bovine alpha-lactalbumin in their milk. J. Anim. Sci. 2002, 80:1090-1096.
52. Nottle M.B., Nagashima H., Verma P.J., et al. Meeting on the Application of Transgenic Animals for Use in Production AgricultureLocation: TAHOE CITY, CA. Transgenic Animals in Agriculture 1999, 145-156. J.D. Murray, G.B. Anderson, A.M. Oberbauer (Eds.).
53. Panarace M., Aguero J.I., Garrote M., Jauregui G., Segovia A., Cane L., Gutierrez J., Marfil M., Rigali F., Pugliese M., Young S., Lagioia J., Garnil C., Pontes J.E.F., Junio J.C.E., Mower S., Medina M. How healthy are clones and their progeny: 5 years of field experience. Theriogenology 2007, 67:142-151.
54. Peng X. Production of transgenic rabbit models for human diseases. J. Am. Assoc. Lab. Anim. Sci. 2011, 50:817-818.
55. Phillips, J.P., Golovan, S.P., Meidinger, R.G., Forsberg, C.W., 2006. Transgenic enhancement of nutrient cycling: moving toward an environmentally sustainable animal agriculture. In: Proceedings of the 8th World Congress on Genetics Applied to Livestock Production. Belo Horizonte, Minas Gerais, Brazil, 13-18 August, 2006. Instituto Prociencia, Minas Gerais, pp. 19-02.
56. Pitkänen T.I., Krasnov A., Reinisalo M., Mölsä H. Transfer and expression of glucose transporter and hexokinase genes in salmonid fish. Aquaculture 1999, 173:319-332.
57. Pohajdak B., Mansour M., Hrytsenko O., Conlon J.M., Dymond L.C., Wright J.R. Production of transgenic tilapia with Brockmann bodies secreting [desThrB30] human insulin. Transgenic Res. 2004, 13:313-323.
58. Pursel V.G., Bolt D.J., Miller K.F., Pinkert C.A., Hammer R.E., Palmiter R.D., Brinster R.L. Expression and performance in transgenic pigs. J. Reprod. Fertil. 1990, 235-245.
59. Pursel V.G., Sutrave P., Wall R.J., Kelly A.M., Hughes S.H. Transfer of C-Ski gene into swine to enhance muscle development. Theriogenology 1992, 37:278.
60. Pursel, V.G., Wall, R.J., Mitchell, A.D., Elsasser, T.H., Solomon, M.B., Coleman, M.E., DeMayo, F., Schwartz, R.J., 1999. Expression of insulin-like growth factor-I in skeletal muscle of transgenic swine.
61. Raven P.A., Devlin R.H., Higgs D.A. Influence of dietary digestible energy content on growth, protein and energy utilization and body composition of growth hormone transgenic and non-transgenic coho salmon (Oncorhynchus kisutch). Aquaculture 2006, 254:730-747.
62. Reh W.A., Maga E.A., Collette N.M., Moyer A., Conrad-Brink J.S., Taylor S.J., DePeters E.J., Oppenheim S., Rowe J.D., BonDurant R.H., Anderson G.B., Murray J.D. Hot topic: using a stearoyl-CoA desaturase transgene to alter milk fatty acid composition. J. Dairy Sci. 2004, 87:3510-3514.
63. Renard J.P., Chastant S., Chesne P., Richard C., Marchal J., Cordonnier N., Chavatte P., Vignon X. Lymphoid hypoplasia and somatic cloning. Lancet 1999, 353:1489-1491.
64. Rhind S.M., King T.J., Harkness L.M., Bellamy C., Wallace W., DeSousa P., Wilmut I. Cloned lambs-lessons from pathology. Nat. Biotechnol. 2003, 21:744-745.
65. Richt J.A., Hall S.M. BSE case associated with prion protein gene mutation. PLoS Pathog. 2008, 4:e1000156.
66. Richt J.A., Kasinathan P., Hamir A.N., Castilla J., Sathiyaseelan T., Vargas F., Sathiyaseelan J., Wu H., Matsushita H., Koster J., Kato S., Ishida I., Soto C., Robl J.M., Kuroiwa Y. Production of cattle lacking prion protein. Nat. Biotechnol. 2007, 25:132-138.
67. Rogers G.E. Improvement of wool production through genetic engineering. Trends Biotechnol. 1990, 8:6-11.
68. Rollin B.E. The Frankenstein Syndrome: Ethical and Social Issues in the Genetic Engineering of Animals 1995, Cambridge University Press, Cambridge, New York.
69. Saeki K., Matsumoto K., Kinoshita M., Suzuki I., Tasaka Y., Kano K., Taguchi Y., Mikami K., Hirabayashi M., Kashiwazaki N., Hosoi Y., Murata N., Iritani A. Functional expression of a Delta12 fatty acid desaturase gene from spinach in transgenic pigs. Proc. Natl. Acad. Sci. USA 2004, 101:6361-6366.
70. Salter D.W., Crittenden L.B. Artificial insertion of a dominant gene for resistance to avian leukosis virus into the germ line of the chicken. Theor. Appl. Genet. 1989, 77:457-461.
71. Saunders R.L., Fletcher G.L., Hew C.L. Smolt development in growth hormone transgenic Atlantic salmon. Aquaculture 1998, 168:177-193.
72. Schaeffer E.L., Figueiro M., Gattaz W.F. Insights into Alzheimer disease pathogenesis from studies in transgenic animal models. Clinics (Sao Paulo) 2011, 66(Suppl. 1):S45-S54.
73. Scharfen E.C., Mills D.A., Maga E.A. Use of human lysozyme transgenic goat milk in cheese making: effects on lactic acid bacteria performance. J. Dairy Sci. 2007, 90:4084-4091.
74. Seegers H., Fourichon C., Beaudeau F. Production effects related to mastitis and mastitis economics in dairy cattle herds. Vet. Res. 2003, 34:475-491.
75. Semaan M., Kaulitz D., Petersen B., Niemann H., Denner J. Long-term effects of PERV-specific RNA interference in transgenic pigs. Xenotransplantation 2012, 19:112-121.
76. Soleimani M., Fonouni H., Esmaeilzadeh M., Kashfi A., Fani Yazdi S.H., Golriz M., Hafezi M., Rahbari N.N., Schmidt J., Mehrabi A. Appropriate donor size for porcine liver xenotransplant. Exp. Clin. Transplant. 2012, 10:148-153.
77. Su H.Y., Jay N.P., Gourley T.S., Kay G.W., Damak S. Wool production in transgenic sheep: results from first-generation adults and second-generation lambs. Anim. Biotechnol. 1998, 9:135-147.
78. Thresher R.E. Autocidal technology for the control of invasive fish. Fisheries (Bethesda) 2008, 33:114-121.
79. Tong J., Wei H., Liu X., Hu W., Bi M., Wang Y., Li Q., Li N., Tong J., Wei H.X., Liu X.F., Hu W.P., Bi M.J., Wang Y.Y., Li Q.Y., Li N. Production of recombinant human lysozyme in the milk of transgenic pigs. Transgenic Res. 2011, 20:417-419.
80. Valdez M.R.W.D., Nimmo D., Betz J., Gong H., James A.A., Alphey L., Black W.C.I., de Valdez M.R.W., Gong H.F. Genetic elimination of dengue vector mosquitoes. Proc. Natl. Acad. Sci. USA 2011, 108:4772-4775.
81. Valfrè F., Renieri C. Veterinary medicine and livestock production related to climate modifications-presentation and reasons. Vet. Res. Commun. 2006, 30:65-67.
82. Van Eenennaam A.L., Muir W.M. Transgenic salmon: a final leap to the grocery shelf?. Nat. Biotechnol. 2011, 29:706-710.
83. Vazquez-Salat, N., Houdebine, L.M., 2012. Will GM animals follow the GM plant fate? Transgenic Res. 2013 22(1):5-13. Epub 2012 Sep 18. http://dx.doi.org/10.1007/s11248-012-9648-5.
84. Venugopal T., Anathy V., Kirankumar S., Pandian T.J. Growth enhancement and food conversion efficiency of transgenic fish Labeo rohita. J. Exp. Zool. Pt. A: Comp. Exp. Biol. 2004, 301A:477-490.
85. Wall R.J., Powell A.M., Paape M.J., Kerr D.E., Bannerman D.D., Pursel V.G., Wells K.D., Talbot N., Hawk H.W. Genetically enhanced cows resist intramammary Staphylococcus aureus infection. Nat. Biotechnol. 2005, 23:445-451.
86. Wells, D.J., 2010. Genetically modified animals and pharmacological research. In: Cunningham, F., Elliott, J., Lees, P. (Eds.), Comparative and Veterinary Pharmacology, Handb Exp Pharmacol. 2010;(199):213-26. http://dx.doi.org/10.1007/978-3-642-10324-7_9.
87. Wheeler M.B., Bleck G.T., Donovan S.M. Transgenic alteration of sow milk to improve piglet growth and health. Control of Pig Reproduction VI: Proceedings of the Sixth International Conference on Pig Reproduction held at the University of Missouri-Columbia, USA in June 2001 2001, 313-324. Society for Reproduction and Fertility, Cambridge. R.D. Geisert, H. Niemann, C. Doberska (Eds.).
88. Wright G., Carver A., Cottom D., Reeves D., Scott A., Simons P., Wilmut I., Garner I., Colman A. High-level expression of active human alpha-1-antitrypsin in the milk of the transgenic sheep. BioTechnology 1991, 9:830-834.
89. Wu X., Ouyang H., Duan B., Pang D., Zhang L., Yuan T., Xue L., Ni D., Cheng L., Dong S., Wei Z., Li L., Yu M., Sun Q., Chen D., Lai L., Dai Y., Li G., Wu X., Ouyang H.S., Duan B., Pang D.X., Zhang L., Yuan T., Xue L., Ni D.B., Cheng L., Dong S.H., Wei Z.Y., Li L., Yu M., Sun Q.Y., Chen D.Y., Lai L.X., Dai Y.F., Li G.P. Production of cloned transgenic cow expressing omega-3 fatty acids. Transgenic Res. 2012, 21:537-543.
90. Yang B., Wang J., Tang B., Liu Y., Guo C., Yang P., Yu T., Li R., Zhao J., Zhang L., Dai Y., Li N., Yang B., Wang J.W., Tang B., Liu Y.F., Guo C.D., Yang P.H., Yu T., Li R., Zhao J.M., Zhang L., Dai Y.P., Li N. Characterization of bioactive recombinant human lysozyme expressed in milk of cloned transgenic cattle. PLoS One 2011, 6(3). e17593. 10.1371/journal.pone.0017593.
91. Zhang P., Hayat M., Joyce C., Gonzalez-Villaseñor L.I., Lin C.M., Dunham R.A., Chen T.T., Powers D.A. Gene transfer, expression and inheritance of PRSV-rainbow trout-GH cDNA in the common carp, Cyprinus carpio (Linnaeus). Mol. Reprod. Dev. 1990, 25:3-13.
92. Zhong J., Wang Y., Zhu Z. Introduction of the human lactoferrin gene into grass carp (Ctenopharyngodon idellus) to increase resistance against GCH virus. Aquaculture 2002, 214:93-101.