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The use of genetic engineering techniques to improve the lipid composition in meat, milk and fish products: a review

Published online by Cambridge University Press:  12 December 2014

S. Świątkiewicz ,
M. Świątkiewicz ,
A. Arczewska-Włosek  and
D. Józefiak
S. Świątkiewicz*
Affiliation:
National Research Institute of Animal Production, ul. Krakowska 1, 32-083 Balice, Poland
M. Świątkiewicz
Affiliation:
National Research Institute of Animal Production, ul. Krakowska 1, 32-083 Balice, Poland
A. Arczewska-Włosek
Affiliation:
National Research Institute of Animal Production, ul. Krakowska 1, 32-083 Balice, Poland
D. Józefiak
Affiliation:
Department of Animal Nutrition and Feed Management Wolynska 33, Poznan University of Life Sciences, 60-637 Poznan, Poland
*
†E-mail: [email protected]
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Abstract

The health-promoting properties of dietary long-chain n-3 polyunsaturated fatty acids (n-3 LCPUFAs) for humans are well-known. Products of animal-origin enriched with n-3 LCPUFAs can be a good example of functional food, that is food that besides traditionally understood nutritional value may have a beneficial influence on the metabolism and health of consumers, thus reducing the risk of various lifestyle diseases such as atherosclerosis and coronary artery disease. The traditional method of enriching meat, milk or eggs with n-3 LCPUFA is the manipulation of the composition of animal diets. Huge progress in the development of genetic engineering techniques, for example transgenesis, has enabled the generation of many kinds of genetically modified animals. In recent years, one of the aims of animal transgenesis has been the modification of the lipid composition of meat and milk in order to improve the dietetic value of animal-origin products. This article reviews and discusses the data in the literature concerning studies where techniques of genetic engineering were used to create animal-origin products modified to contain health-promoting lipids. These studies are still at the laboratory stage, but their results have demonstrated that the transgenesis of pigs, cows, goats and fishes can be used in the future as efficient methods of production of healthy animal-origin food of high dietetic value. However, due to high costs and a low level of public acceptance, the introduction of this technology to commercial animal production and markets seems to be a distant prospect.

Keywords

genetic engineering techniquestransgenesisfood-producing animalsanimal-origin productsn-3 polyunsaturated fatty acids
Type
Research Article
Information
animal , Volume 9 , Issue 4 , April 2015 , pp. 696 - 706
Copyright
© The Animal Consortium 2014 

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References

Alimuddin, KV, Satoh, S, Takeuchi, T and Yoshizaki, G 2008. Cloning and over-expression of a masu salmon (Oncorhynchus masou) fatty acid elongase-like gene in zebra fish. Aquaculture 282, 13–18.Google Scholar
Alimuddin, YG, Kiron, V, Satoh, S and Takeuchi, T 2005. Enhancement of EPA and DHA biosynthesis by over-expression of masu salmon Δ6-desaturase-like gene in zebrafish. Transgenic Research 14, 159–165.CrossRefGoogle ScholarPubMed
Alimuddin, YG, Kiron, V, Satoh, S and Takeuchi, T 2007. Expression of masu salmon Δ6-desaturase-like gene elevated EPA and DHA biosynthesis in zebrafish. Marine Biotechnology 9, 92–100.Google Scholar
Alissa, EM and Ferns, GA 2012. Functional foods and nutraceuticals in the primary prevention of cardiovascular diseases. Journal of Nutrition and Metabolism, Article ID: 569486, 1–16, doi:10.1155/2012/569486.Google Scholar
Baldassarre, H, Hockley, DK, Olaniyan, B, Brochu, B, Zhao, X, Mustafa, A and Bordignon, V 2008. Milk composition studies in transgenic goats expressing recombinant human butyrylcholinesterase in the mammary gland. Transgenic Research 17, 863–872.CrossRefGoogle ScholarPubMed
Bell, JG, McEvoy, J, Tocher, DR, McGhee, F, Campbell, PJ and Sargent, JR 2001. Replacement of fish oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid compositions and hepatocyte fatty acid metabolism. Journal of Nutrition 131, 1535–1543.Google Scholar
Bellenger, J, Bellenger, S, Bataille, A, Massey, KA, Nicolaou, A, Rialland, M, Tessier, C, Kang, JX and Narce, M 2011. High pancreatic n-3 fatty acids prevent STZ-induced diabetes in fat-1 mice: inflammatory pathway inhibition. Diabetes 60, 1090–1099.Google Scholar
Benatti, P, Peluso, G, Nicolai, R and Calvani, M 2004. Polyunsaturated fatty acids: biochemical, nutritional and epigenetic properties. Journal of the American College of Nutrition 23, 281–302.CrossRefGoogle ScholarPubMed
Bernard, L, Leroux, C and Chilliard, Y 2008. Expression and nutritional regulation of lipogenic genes in the ruminant lactating mammary gland. In Bioactive components of milk, advances in experimental medicine and biology, vol. 606, (ed. Z Bosze), pp. 67–108. Springer, New York, USA.Google Scholar
Bilal, S, Haworth, O, Wu, L, Weylandt, KH, Levy, BD and Kang, JX 2011. Fat-1 transgenic mice with elevated omega-3 fatty acids are protected from allergic airway responses. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease 1812, 1164–1169.Google Scholar
Brenna, JT, Salem, N, Sinclair, AJ and Cunnane, SC 2009. α-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins, Leukotrienes and Essential Fatty Acids 80, 85–91.Google Scholar
Calder, PC 2006. n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. The American Journal of Clinical Nutrition 83, 1505S–1519S.Google Scholar
Chatakondi, N, Lovell, RT, Duncan, PL, Hayat, M, Chen, TT, Powers, DA, Weete, JD, Cummins, K and Dunham, RA 1995. Body composition of transgenic common carp (Cyprinus carpio), containing rainbow trout growth hormone gene. Aquaculture 138, 99–109.Google Scholar
Chen, Q, Liu, Q, Wu, ZF, Wang, ZY and Gou, KM 2009. Generation of fad2 transgenic mice that produce omega-6 fatty acids. Science in China Series C: Life Science 52, 1048–1054.Google Scholar
Chen, Y, Zhang, M and Gou, K 2010. SDD17 desaturase can convert arachidonic acid to eicosapentaenoic acid in mammalian cells. Biochemical and Biophysacal Research Communications 394, 158–162.CrossRefGoogle ScholarPubMed
Chen, Y, Mei, M, Zhang, P, Ma, K, Song, G, Ma, X, Zhao, T, Tang, B, Ouyang, H, Li, G and Li, Z 2013. The generation of transgenic mice with Fat1 and Fad2 genes that have their own polyunsaturated fatty acid biosynthetic pathway. Cellular Physiology and Biochemistry 32, 523–532.Google Scholar
Cook, JT, McNiven, MA, Richardson, GF and Sutterlin, AM 2000. Growth rate, body composition and feed digestibility/conversion of growth-enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture 188, 15–32.Google Scholar
Cooper, CA, Klobas, LCG, Maga, EA and Murray, JD 2013. Consuming transgenic goats’ milk containing the antimicrobial protein lysozyme helps resolve diarrhea in young pigs. PLoS One 8, e58409.CrossRefGoogle ScholarPubMed
Duran-Montge, P, Theil, PK, Lauridsen, C and Esteve-Garcia, E 2009. Dietary fat source affects metabolism of fatty acids in pigs as evaluated by altered expression of lipogenic genes in liver and adipose tissues. Animal 3, 535–542.Google Scholar
Dunham, RA, Chatakondi, N, Nichols, AJ, Kucuktas, H, Chen, TT, Powers, DA, Weete, JD, Cummins, K and Lovell, RT 2002. Effect of rainbow trout growth hormone complementary DNA on body shape, carcass yield, and carcass composition of F1 and F2 transgenic common carp (Cyprinus carpio). Marine Biotechnology 4, 604–611.CrossRefGoogle ScholarPubMed
Fan, J and Watanabe, T 2003. Transgenic rabbits as therapeutic protein bioreactors and human disease models. Pharmocology & Therapeutics 99, 261–282.CrossRefGoogle ScholarPubMed
Fan, J, Shimoyamada, H, Sun, H, Marcovina, S, Honda, K and Watanabe, T 2001. Transgenic rabbits expressing human apolipoprotein (a) develop more extensive atherosclerotic lesions in response to a cholesterol-rich diet. Arteriosclerosic, Thrombosis, and Vascular Biology 21, 88–94.Google Scholar
Fan, J, Wang, J, Bensadoun, A, Lauer, SL, Dang, Q, Mahley, RW and Taylor, JW 1997. Overexpression of hepatic lipase in transgenic rabbits leads to a marked reduction of plasma high density lipoproteins and intermediate density lipoproteins. Proceedings of the National Academy of Sciences of USA 91, 8724–8728.Google Scholar
Forabosco, F, Löhmus, M, Rydhmer, L and Sundström, LF 2013. Genetically modified farm animals and fish in agriculture: a review. Livestock Science 153, 1–9.Google Scholar
Gerster, H 1997. Can adults adequately convert alpha-linolenic acid (18:3n-3) to eicosapentaenoic acid (20:5 n-3) and docosahexaenoic acid (22:6 n-3)? International Journal for Vitamin and Nutrition Research 68, 159–173.Google Scholar
Givens, DI and Gibbs, RA 2008. Current intakes of EPA and DHA in European populations and the potential of animal-derived foods to increase them. Proceedings of the Nutrition Society 67, 273–280.Google Scholar
Goldburg, R and Naylor, R 2005. Future seascapes, fishing, and fish farming. Frontiers in Ecology and the Environment 3, 21–28.Google Scholar
Gravaghi, C, La Perle, KMD, Ogrodwski, P, Kang, JX, Quimby, F, Lipkin, M and Lamprecht, SS 2011. Cox-2 expression, PGE2 and cytokines production are inhibited by endogenously synthesized n-3 PUFA in inflamed colon of fat-1 mice. Journal of Nutritional Biochemistry 22, 360–365.Google Scholar
Greger, M 2011. Transgenesis in animal agriculture: addressing animal health and welfare concerns. Journal of Agricultural and Environmental Ethics 24, 451–472.Google Scholar
Griffitts, J, Saunders, D, Tesiram, YA, Reid, GE, Salih, A, Liu, S, Lydic, TA, Busik, JV, Kang, JX and Towner, RA 2010. Non-mammalian fat-1 gene prevents neoplasia when introduced to a mouse hepatocarcinogenesis model: omega-3 fatty acids prevent liver neoplasia. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids 1801, 1133–1144.Google Scholar
Grummer, RR 1991. Effect of feed on the composition of milk fat. Journal of Dairy Science 74, 3244–3257.Google Scholar
Hanson, M and Gluckman, P 2011. Developmental origins of noncommunicable disease: population and public health implications. The American Journal of Clinical Nutrition 94 (6 suppl.), 1754S–1758S.Google Scholar
Havel, RJ 1997. Milk fat consumption and human health: recent NIH and other American government recommendations. In Milk composition, production and biotechnology (ed. RAS Welch, DJW Burns, RS Davis, AI Popay and CJ Prosser), pp. 13–22. Wallingford, UK.Google Scholar
He, C, Qu, X, Cui, L, Wang, J and Kang, JX 2009. Improved spatial learning performance of fat-1 mice is associated with enhanced neurogenesis and neuritogenesis by docosahexaenoic acid. Proceedings of the National Academy of Sciences of USA 106, 11370–11375.Google Scholar
Hoeg, JM, Santamarina-Fojo, S, Berard, AM, Cornhill, JF, Herderick, EE, Feldman, SH, Haudenschild, CC, Vaisman, BL, Hoyt, RF Jr, Demosky, SJ Jr, Kauffman, RD, Hazel, CM, Marcovina, SM and Brewer, HB Jr 1996. Overepression of lecithin:cholesterol acyltransferase in transgenic rabbits prevents diet-induced atherosclerosis. Proceedings of the National Academy of Sciences of USA 93, 11448–11453.Google Scholar
Hu, FB, Manson, JE and Willett, WC 2001. Types of dietary fat and risk of coronary heart disease: a critical review. Journal of the American College of Nutrition 20, 5–19.Google Scholar
Hu, X, Zhang, F, Leak, RK, Zhang, W, Iwai, M, Stetler, RA, Dai, Y, Zhao, A, Gao, Y and Chen, J 2013. Transgenic overproduction of omega-3 polyunsaturated fatty acids provides neuroprotection and enhances endogenous neurogenesis after stroke. Current Molecular Medicine 13, 1465–1473.CrossRefGoogle ScholarPubMed
Hudert, CA, Weylandt, KH, Lu, Y, Wang, J, Hong, S, Dignass, A, Serhan, CN and Kang, JX 2006. Transgenic mice rich in endogenous omega-3 fatty acids are protected from colitis. Proceedings of the National Academy of Sciences of USA 103, 11276–11281.Google Scholar
Indo, Y, Tatemizo, A, Abe, Y, Suzuki, I, Matsumoto, K, Hosoi, Y, Kinoshita, M, Mikami, K, Murata, N, Iritani, A and Saeki, K 2009. Functional expression of a humanized gene for an omega-3 fatty acid desaturase from scarlet flax in transfected bovine adipocytes and bovine embryos cloned from the cells. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids 1791, 183–190.Google Scholar
James, MJ, Gibson, RA and Cleland, LG 2000. Dietary polyunsaturated fatty acids and inflammatory mediator production. The American Journal of Clinical Nutrition 71, 343s–348s.Google Scholar
Jang, HY, Lim, K, Lee, SM and Park, BH 2013. Effects of n-3 PUFA on the CD4+ type 2 helper T-cell-mediated immune responses in Fat-1 mice. Molecular Nutrition & Food Research 58, 365–375.Google Scholar
Jenkins, TC, Wallace, RJ, Moate, PJ and Mosley, EE 2008. Board-invited review: recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. Journal of Animal Science 86, 397–412.Google Scholar
Jia, Q, Lupton, JR, Smith, R, Weeks, BR, Callaway, E, Davidson, LA, Kim, W, Fan, YY, Yang, P, Newman, RA, Kang, JX, McMurray, DN and Chapkin, RS 2008. Reduced colitis-associated colon cancer in Fat-1 (n-3 fatty acid desaturase) transgenic mice. Cancer Research 68, 3985–3991.Google Scholar
Kabeya, N, Takeuchi, Y, Yamamoto, Y, Yazawa, R, Haga, Y, Satoh, S and Yoshizaki, G 2014. Modification of the n-3 HUFA biosynthetic pathway by transgenesis in a marine teleost, nibe croaker. Journal of Biotechnology 172, 46–54.Google Scholar
Kang, JX, Wang, J, Wu, L and Kang, ZB 2004. Transgenic mice: fat-1 mice convert n-6 to n-3. Nature 427, 504.CrossRefGoogle ScholarPubMed
Kao, BT, DePeters, EJ and Van Eenennaam, AL 2006a. Mice raised on milk transgenically enriched with n-3 PUFA have increased brain docosahexaenoic acid. Lipids 41, 543–549.CrossRefGoogle ScholarPubMed
Kao, BT, Lewis, KA, DePeters, EJ and Van Eenennaam, AL 2006b. Endogenous production and elevated levels of long-chain n-3 fatty acids in the milk of transgenic mice. Dairy Science 89, 3195–3201.Google Scholar
Kim, EH, Bae, JS, Hahm, KB and Cha, JY 2012. Endogenously synthesized n-3 polyunsaturated fatty acids in fat-1 mice ameliorate high-fat diet-induced non-alcoholic fatty liver disease. Biochemical Pharmacology 84, 1359–1365.Google Scholar
Kobayashi, T, Ito, T and Shiomi, M 2011. Roles of the WHHL rabbit in translational research on hypercholesterolemia and cardiovascular diseases. Journal of Biomedicine and Biotechnology, Article ID: 406473, 1–10, doi:10.1155/2011/406473.Google Scholar
Kromhout, D, Menotti, A, Kestleloot, H and Sans, S 2002. Prevention of coronary heart disease by diet and lifestyle: evidence from prospective cross-cultural, cohort, and interventional studies. Circulation 105, 893–898.Google Scholar
Lai, L, Kang, JX, Li, R, Wang, J, Wilt, WT, Yong, HY, Hao, Y, Wax, DM, Murphy, CN, Rieke, A, Samuel, M, Linville, ML, Corte, SW, Evans, RW, Starzi, TE, Prather, PS and Dai, Y 2006. Generation of cloned transgenic pigs rich in omega-3 fatty acids. Nature Biotechnology 24, 435–436.Google Scholar
Li, R, Lai, L, Wax, D, Hao, Y, Murphy, CN, Rieke, A, Samuel, M, Linville, ML, Korte, SW, Evans, RW, Turk, JR, Kang, JX, Witt, WT, Dai, Y and Prather, RS 2006. Cloned transgenic swine via in vitro production and cryopreservation. Biology of Reproduction 75, 226–230.Google Scholar
Lim, SN, Gladman, SJ, Dyall, SC, Patel, U, Virani, N, Kang, JX, Priestley, JV and Michael-Titus, AT 2013. Transgenic mice with high endogenous omega-3 fatty acids are protected from spinal cord injury. Neurobiology of Disease 51, 104–112.Google Scholar
Lu, D, Li, Q, Wu, Z, Shang, S, Liu, S, Wen, X, Li, Z, Wu, F and Li, N 2014. High-level recombinant human lysozyme expressed in milk of transgenic pigs can inhibit the growth of Escherichia coli in the duodenum and influence intestinal morphology of sucking pigs. PLoS One 9, e89130.Google Scholar
Ma, DWL, Ngo, V, Huot, PSP and Kang, JX 2006. N-3 polyunsaturated acids endogenously synthesized in Fat-1 mice are enriched in mammary gland. Lipids 41, 35–39.Google Scholar
Maga, EA and Murray, JD 1995. Mammary gland expression of transgenes and the potential for altering the properties of milk. Biotechnology 13, 1452–1457.Google Scholar
Mansbridge, RJ and Blake, JS 1997. Nutritional factors affecting the fatty acid composition of bovine milk. British Journal of Nutrition 78, S37–S47.Google Scholar
Marshall, AC, Kubena, KS, Hinton, KR, Hargis, PS and van Elswyk, ME 1994. n-3 fatty acid enriched table eggs: a survey of consumer acceptability. Poultry Science 73, 1334–1340.Google Scholar
Martínez, R, Arenal, A, Estrada, MP, Herrera, F, Huerta, V, Vázquez, J, Sanchez, T and de la Fuente, J 1999. Mendelian transmission, transgene dosage and growth phenotype in transgenic tilapia (Oreochromis hornorum) showing ectopic expression of homologous growth hormone. Aquaculture 173, 271–283.Google Scholar
Mori, TA 2014. Dietary n-3 PUFA and CVD: a review of the evidence. Proceedings of the Nutrition Society 73, 57–64.Google Scholar
Nair, H, Shu, XO, Volmink, J, Romieu, I and Spiegelman, D 2012. Cohort studies around the world: methodologies, research questions and integration to address the emerging global epidemic of chronic diseases. Public Health 126, 202–205.Google Scholar
National Research Council (NRC) 1988. Designing foods, animal product options in the market place. National Academy Press, Washington, DC.Google Scholar
Nowak, J, Weylandt, KH, Habbel, P, Wang, J, Dignass, A, Glickman, JN and Kang, JX 2007. Colitis-associated colon tumorigenesis is suppressed in transgenic mice rich in endogenous n-3 fatty acids. Carcinogenesis 28, 1991–1995.Google Scholar
Pan, DK, Zhang, L, Zhou, YR, Feng, C, Long, C, Liu, X, Wang, R, Zhang, J, Ling, AX, Dong, EQ, Wang, SC, Xu, HG and Chen, HX 2010. Efficient production of omega-3 fatty acid desaturase (sFat-1) – transgenic pigs by somatic cell nuclear transfer. Science China Life Sciences 53, 517–523.Google Scholar
Pisulewski, PM 2005. Health-related effects of nutritionally modified foods of animal origin. Journal of Animal and Feed Sciences 14 (suppl. 1), 303–315.Google Scholar
Pohlmeier, WE, Hovey, RC and van Eenennaam, AL 2011. Reproductive abnormalities in mice expressing omega-3 fatty acid desaturase in their mammary glands.p. Transgenic Research 20, 283–292.Google Scholar
Pursel, V and Solomon, M 1993. Alteration of carcass composition in transgenic swine. Food Reviews International 9, 423–439.CrossRefGoogle Scholar
Rahman, MM, Bhattacharya, A, Banu, J, Kang, JX and Fernandes, G 2009a. Endogenous n-3 fatty acids protect ovariectomy induced bone loss by attenuating osteoclastogenesis. Journal of Cellular and Molecular Medicine 13, 1833–1844.Google Scholar
Rahman, MM, Halade, GV, Bhattacharya, A and Fernandes, G 2009b. The fat-1 transgene in mice increases antioxidant potential, reduces pro-inflammatory cytokine levels, and enhances ppaRγ and sIRT-1 expression on a calorie restricted diet. Oxidative Medicine and Cellular Longevity 2, 307–316.Google Scholar
Rasmussen, RS and Morrissey, MT 2007. Biotechnology in aquaculture: transgenics and polyploidy. Comprehensive Reviews in Food Science and Food Safety 6, 2–16.Google Scholar
Reddy, R, Bayles, I and He, Q 2012. Expression of n-3 fatty acid desaturase suppresses tamoxifen-resistant breast cancer in vitro and in fat-1 transgenic mice. In Proceedings of the 11th Annual AACR International Conference on Frontiers in Cancer Prevention Research, Anaheim, 16 to 19 October 2012. Abstract B103 in AACR Cancer Prevention Research 5, doi:0.1158/1940-6207. PREV-12-B103.Google Scholar
Reh, WA, Maga, EA, Collette, NM, Moyer, A, Conrad-Brink, JS, Taylor, SJ, DePeters, EJ, Oppenheim, S, Rowe, JD, BonDurant, RH, Anderson, GD and Murray, JD 2004. Hot topic: using a stearoyl-CoA desaturase transgene to alter milk fatty acid composition. Journal of Dairy Science 87, 3510–3514.CrossRefGoogle ScholarPubMed
Ren, HY, Zheng, XM, Chen, HX and Li, K 2011. Transgenic pigs carrying a synthesized fatty acid desaturase gene yield high level of co-3 PUFAs. Agricultural Sciences in China 10, 1603–1608.Google Scholar
Richards, MP, Kathirvel, P, Gong, Y, Lopez-Hernandez, A, Walters, EM and Prather, RS 2011. Long chain omega-3 fatty acid levels in loin muscle from transgenic (fat-1 gene) pigs and effects on lipid oxidation during storage. Food Biotechnology 25, 103–114.Google Scholar
Riediger, ND, Othman, RA, Suh, M and Moghadasian, MH 2009. A systemic review of the roles of n-3 fatty acids in health and disease. Journal of the American Dietetic Association 109, 668–679.Google Scholar
Roche, HM, Noone, E and Gibney, AN 2001. Conjugated linoleic acid: a novel therapeutic nutrient? Nutrition Research Reviews 14, 173–188.Google Scholar
Romanatto, T, Fiamoncini, J, Wang, B, Curi, R and Kang, JX 2014. Elevated tissue omega-3 fatty acid status prevents age-related glucose intolerance in fat-1 transgenic mice. Biochimica et Biophysica Acta (BBA) – Molecular Basis of Disease 1842, 186–191.Google Scholar
Saeki, K, Matsumoto, K, Kinoshita, M, Suzuki, I, Tasaka, Y, Kano, K, Taguchi, Y, Mikami, K, Hirabayashi, M, Kashiwazaki, N, Hosoi, Y, Murata, N and Iritani, A 2004. Functional expression of a Delta12 fatty acid desaturase gene from spinach in transgenic pigs. Proceedings of the National Academy of Sciences of USA 101, 6361–6366.Google Scholar
Schmitz, G and Ecker, J 2008. The opposing effects of n-3 and n-fatty acids. Progress in Lipid Research 47, 147–155.Google Scholar
Simopoulos, AP 2004. Omega-6/omega-3 essential fatty acid ratio and chronic diseases. Food Reviews International 20, 77–90.Google Scholar
Simopoulos, AP 2008. The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Experimental Biology and Medicine 233, 674–688.Google Scholar
Simopoulos, AP 2011. Importance of the omega-6/omega-3 balance in health and disease: evolutionary aspects of diet. World Review of Nutrition and Dietetics 102, 10–21.Google Scholar
Solomon, MB, Pursel, VG, Campbell, RG and Steele, NC 1997. Biotechnology for porcine products and its effect on meat products. Food Chemistry 59, 499–504.Google Scholar
Sugiyama, M, Takenaga, F, Kitani, Y, Yamamoto, G, Okamoto, H, Masaoka, T, Araki, K, Nagoy, H and Mori, T 2012. Homozygous and heterozygous GH transgenesis alters fatty acid composition and content in the liver of Amago salmon (Oncorhynchus masou ishikawae). Biology Open 1, 1035–1042.Google Scholar
Sun, XH, Sun, XF, Ma, JM, Liu, HQ, Min, LJ, Pan, QJ, Qin, GQ, Shen, W and Li, L 2014. Anti-senescence effect of FatI gene in goat somatic cells. Biotechnology and Applied Biochemistry (in press), doi:10.1002/bab.1219.CrossRefGoogle Scholar
Taha, AY, Huot, PSP, Reza-Lopez, S, Prayitno, NR, Kang, JX, Burnham, W and Ma, DWL 2008. Seizure resistance in fat-1 transgenic mice endogenously synthesizing high level of omega-3 polyunsaturated fatty acids. Journal of Neurochemistry 105, 380–388.Google Scholar
Tang, MX, Zheng, XM, Hou, J, Qian, LL, Jiang, SW, Cui, WT and Li, K 2013. Horizontal gene transfer does not occur between sFat-1 transgenic pigs and nontransgenic pigs. Theriogenology 79, 667–672.CrossRefGoogle Scholar
Tang, MX, Zheng, XM, Cheng, W, Jin, E, Chen, H, Yang, S, Cui, WT and Li, K 2011. Safety assessment of sFat-1 transgenic pigs by detecting their co-habitant microbe in intestinal tract. Transgenic Research 20, 749–758.Google Scholar
Van Reenen, CG, Meuwissen, TH, Hopster, H, Oldenbroek, K, Kruip, TH and Blokhuis, HJ 2001. Transgenesis may affect farm animal welfare: a case for systematic risk assessment. Journal of Animal Science 79, 1763–1779.Google Scholar
Weylandt, KH, Nadolny, A, Kahlke, L, Köhnke, T, Schmöcker, C, Wang, J, Lauwers, GY, Glickman, JN and Kang, JX 2008. Reduction of inflammation and chronic tissue damage by omega-3 fatty acids in fat-1 transgenic mice with pancreatitis. Biochimica et Biophysica Acta (BBA) – Molecular Basis of Disease 1782, 634–641.Google Scholar
Weylandt, KH, Krause, LF, Gomolka, B, Chiu, CY, Bilal, S, Nadolny, A, Waechter, SF, Fischer, A, Rothe, M and Kang, JX 2011. Suppressed liver tumorigenesis in fat-1 mice with elevated omega-3 fatty acids is associated with increased omega-3 derived lipid mediators and reduced TNF-α. Carcinogenesis 32, 897–903.Google Scholar
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, QY, Chen, DY, Lai, L, Dai, Y and Li, GP 2012. Production of cloned transgenic cow expressing omega-3 fatty acids. Transgenic Research 21, 537–543.Google Scholar
Wu, Z, Li, D and Gou, K 2010. Overexpression of stearoyl-CoA desaturase-1 results in an increase of conjugated linoleic acid (CLA) and n-7 fatty acids in 293 cells. Biochemical and Biophysical Research Communications 398, 473–476.Google Scholar
Xia, S, Lu, Y, Wang, J, He, C, Hong, S, Serhan, CN and Kang, JX 2006. Melanoma growth is reduced in fat-1 transgenic mice: impact of omega-6/omega-3 essential fatty acids. Proceedings of the National Academy of Sciences of USA 103, 12499–12504.Google Scholar
Zdunczyk, Z and Jankowski, J 2013. Poultry meat as functional food: modification of the fatty acid profile – a review. Annals of Animal Science 13, 463–480.Google Scholar
Zhang, P, Zhang, Y, Dou, H, Yin, J, Chen, Y, Pang, X, Vajta, G, Bolund, L, Du, Y and Ma, RZ 2012. Handmade cloned transgenic piglets expressing the nematode fat-1 gene. Cellular Reprogramming 14, 258–266.Google Scholar
Zhou, Y, Lin, Y, Wu, X, Feng, C, Long, C, Xiong, F, Wang, F, Pan, D and Chen, H 2014. The high-level accumulation of n-3 polyunsaturated fatty acids in transgenic pigs harboring the n-3 fatty acid desaturase gene from Caenorhabditis briggsae . Transgenic Research 23, 89–97.Google Scholar
Zhu, G, Chen, H, Wu, X, Zhou, Y, Lu, J, Chen, H and Deng, J 2008. A modified n-3 fatty acid desaturase from Caenorhabditis briggsae produced high proportion of DHA and DPA in transgenic mice. Transgenic Research 17, 717–725.CrossRefGoogle ScholarPubMed
Zou, Z, Bellenger, S, Massey, KA, Nicolaou, A, Geissler, A, Bidu, C, Bonotte, B, Pierre, AS, Minville-Walz, M, Rialland, M, Seubert, J, Kang, JX, Lagrost, L, Narce, M and Bellenger, J 2013. Inhibition of the HER2 pathway by n-3 polyunsaturated fatty acids prevents breast cancer in fat-1 transgenic mice. Journal of Lipid Research 54, 3453–3463.Google Scholar