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Regulation of glucose and protein metabolism in growing steers by long-chain n-3 fatty acids in muscle membrane phospholipids is dose-dependent

Published online by Cambridge University Press:  05 October 2009

M. Fortin
Affiliation:
Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, G1V 0A6, Canada Institut des nutraceutiques et des aliments fonctionnels, Université Laval, Québec, G1V 0A6, Canada
P. Julien
Affiliation:
Lipid Research Center, Laval University Hospital Center (CHUL), Québec, QC, G1V 4G2, Canada
Y. Couture
Affiliation:
Faculté de médecine vétérinaire, Université de Montréal, St-Hyacinthe, QC, J2S 7C6, Canada
P. Dubreuil
Affiliation:
Faculté de médecine vétérinaire, Université de Montréal, St-Hyacinthe, QC, J2S 7C6, Canada
P. Y. Chouinard
Affiliation:
Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, G1V 0A6, Canada Institut des nutraceutiques et des aliments fonctionnels, Université Laval, Québec, G1V 0A6, Canada
C. Latulippe
Affiliation:
Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, G1V 0A6, Canada Institut des nutraceutiques et des aliments fonctionnels, Université Laval, Québec, G1V 0A6, Canada
T. A. Davis
Affiliation:
USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas, 77030, USA
M. C. Thivierge*
Affiliation:
Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, G1V 0A6, Canada Institut des nutraceutiques et des aliments fonctionnels, Université Laval, Québec, G1V 0A6, Canada Rowett Institute of Nutrition and Health, University of Aberdeen, Aberdeen, AB21 9SB, UK
*
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Abstract

A previous study showed that long-chain n-3 polyunsaturated fatty acids (LCn-3PUFA; >18 carbons n-3) exert an anabolic effect on protein metabolism through the upregulation of insulin sensitivity and activation of the insulin signaling pathway. This study further delineates for the first time whether the anabolic effect of LCn-3PUFA on metabolism is dose responsive. Six steers were used to test three graded amounts of menhaden oil rich in LCn-3PUFA (0%, 2% and 4%; enteral infusions) according to a double 3 × 3 Latin square design. Treatment comparisons were made using iso-energetic substitutions of control oil for menhaden oil and using 6-week experimental periods. The LCn-3PUFA in muscle total membrane phospholipids increased from 8%, 14% to 20% as dietary menhaden oil increased. Feeding graded amounts of menhaden oil linearly decreased plasma insulin concentration (49, 35 and 25 μU/ml, P = 0.01). The insulin-stimulated amino acid disposal rates as assessed using hyperinsulinemic–euglycemic–euaminoacidemic clamps (20, 40 and 80 mU/kg per h) were linearly increased by the incremental administrations of menhaden oil from 169, 238 to 375 μmol/kg per h (P = 0.005) during the 40 mU/kg per h clamp, and from 295, 360 and 590 μmol/kg per h (P = 0.02) during the 80 mU/kg per h clamp. Glucose disposal rate responded according to a quadratic relationship with the incremental menhaden oil amounts (P < 0.05). A regression analysis showed that 47% of the amino acid disposal rates elicited during the hyperinsulinemic clamp was related to muscle membrane LCn-3PUFA content (P = 0.003). These results show for the first time that both protein and glucose metabolism respond in a dose-dependent manner to menhaden oil and to muscle membrane LCn-3PUFA.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2009

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References

Abel, S, Gelderblom, WCA, Smuts, CM, Kruger, M 1997. Thresholds and kinetics of fatty acid replacement in different cellular compartments in rat liver as a function of dietary n-6/n-3 fatty acid content. Prostaglandins, Leukotrienes and Essential Fatty Acids 56, 2939.Google Scholar
Adams, HR 2001. Veterinary pharmacology and therapeutics. Iowa State University Press, Ames, IA, USA.Google Scholar
Association of Official Analytical Chemists 1990. Official Methods of Analysis. AOAC, Arlington, VA, USA.Google Scholar
Bergeron, K, Julien, P, Davis, TA, Myre, A, Thivierge, MC 2007. Long-chain n-3 fatty acids enhance neonatal insulin-regulated protein metabolism in piglets by differentially altering muscle lipid composition. Journal of Lipid Research 48, 23962410.Google Scholar
Black, AL, Anand, RS, Bruss, ML, Brown, CA, Nakagiri, JA 1990. Partitioning of amino acids in lactating cows: Oxidation to carbon dioxide. The Journal of Nutrition 120, 700710.CrossRefGoogle ScholarPubMed
Canadian Council on Animal Care 1993. Guide to care and used of experimental animals, vol. 1, 2nd edition. Bradda Printing Services, Ottawa, ON, Canada.Google Scholar
Cao, H, Gerhold, K, Mayers, JR, Wiest, MM, Watkins, SM, Hotamisligil, GS 2008. Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell 134, 933944.Google Scholar
Chapman, RA, Mackay, K 1949. The estimation of peroxides in fats and oils by the ferric thiocyanate method. Journal of American Oil Chemists Society 26, 321325.CrossRefGoogle Scholar
Chouinard, PY, Corneau, L, Barbano, DM, Metzger, LE, Bauman, DE 1999. Conjugated linoleic acids alter milk fatty acid composition and inhibit milk fat secretion in dairy cows. The Journal of Nutrition 129, 15791584.CrossRefGoogle ScholarPubMed
Combaret, L, Dardevet, D, Rieu, I, Pouch, M-N, Bechet, D, Taillandier, D, Grizard, J, Attaix, D 2005. A leucine-supplemented diet restores the defective postprandial inhibition of proteasome-dependent proteolysis in aged rat skeletal muscle. The Journal of Physiology 569, 489499.CrossRefGoogle ScholarPubMed
Counil, E, Julien, P, Lamarche, B, Chateau-Degat, M-L, Ferland, A, Dewailly, E 2009. Association between trans-fatty acids in erythrocytes and pro-atherogenic lipid profiles among Canadian Inuit of Nunavik: possible influences of sex and age. The British Journal of Nutrition 102, 766776.Google Scholar
Daveloose, D, Linard, A, Asfi, T, Viret, J, Christon, R 1993. Simultaneous changes in lipid composition, fluidity and enzyme activity in piglet intestinal brush border membrane as affected by dietary polyunsaturated fatty acid deficiency. Biochimica Biophysica Acta 1166, 229237.CrossRefGoogle ScholarPubMed
Davis, TA, Burrin, DG, Fiorotto, ML, Reeds, PJ, Jahoor, F 1998. Roles of insulin and amino acids in the regulation of protein synthesis in the neonate. The Journal of Nutrition 128, 347S350S.CrossRefGoogle ScholarPubMed
Davis, TA, Suryawan, A, Bush, JA, O’Connor, PMJ, Thivierge, MC 2003. Interaction of amino acids and hormones in the regulation of protein metabolism in growing animals. Canadian Journal of Animal Science 83, 353364.CrossRefGoogle Scholar
Dudouet, C 1999. La croissance et le développement. In La production des bovins allaitants (ed. Dudouet C), p. 39. Groupe France Agricole, France.Google Scholar
Eisemann, JH, Huntington, GB, Catherman, DR 1997. Insulin sensitivity and responsiveness of portal-drained viscera, liver, hindquarters, and whole body of beef steers weighing 275 or 490 kilograms. Journal of Animal Science 75, 20842091.Google Scholar
Else, PL, Hulbert, AJ 2003. Membranes as metabolic pacemakers. Clinical Experimental Pharmacology & Physiology 30, 559564.CrossRefGoogle ScholarPubMed
Fink, RI, Kolterman, OG, Griffin, J, Olefsky, JM 1983. Mechanisms of insulin resistance in aging. The Journal of Clinical Investigation 71, 12351523.CrossRefGoogle ScholarPubMed
Fox, DG, Sniffen, CJ, O’Connor, JD, Russell, JB, Soest, PJV 1992. A net carbohydrate and protein system for evaluating cattle diets: III. Cattle requirements and diet adequacy. Journal of Animal Science 70, 35783596.CrossRefGoogle ScholarPubMed
Gelfand, RA, Glickman, MG, Castellino, P, Louard, RJ, DeFronzo, RA 1988. Measurement of L-[1-14C]leucine kinetics in splanchnic and leg tissues in humans. Diabetes 37, 13651372.CrossRefGoogle ScholarPubMed
Gingras, AA, White, PJ, Chouinard, PY, Julien, P, Davis, TA, Dombroski, L, Couture, Y, Dubreuil, P, Myre, A, Bergeron, K, Marette, A, Thivierge, MC 2007. Long-chain omega-3 fatty acids regulate whole-body protein metabolism by promoting muscle insulin signaling to the Akt-mTOR-S6K1 pathway and insulin sensitivity. The Journal of Physiology 579, 269284.Google Scholar
Harris, PM, Skene, PA, Buchan, V, Milne, E, Calder, AG, Anderson, SE, Connell, A, Lobley, GE 1992. Effect of food intake on hind-limb and whole-body protein metabolism in young growing sheep: chronic studies based on arterio-venous techniques. The British Journal of Nutrition 68, 389407.CrossRefGoogle ScholarPubMed
Innis, SM, Clandinin, MT 1981. Dynamic modulation of mitochondrial inner-membrane lipids in rat heart by dietary fat. The Biochemical Journal 193, 155167.Google Scholar
Jobgen, WS, Fried, SK, FU, WJ, Meininger, CJ, Wu, G 2006. Regulatory role for the arginine-nitric oxide pathway in metabolism of energy substrate. Journal of Nutritional Biochemistry 17, 571588.CrossRefGoogle Scholar
Jones, PJH, Toy, BR, Cha, MC 1995. Differential fatty acid accretion in hearth, liver, and adipose tissues of rats fed beef tallow, fish oil, olive oil and safflower oil at three levels of energy intake. The Journal of Nutrition 125, 11751182.Google Scholar
Li, P, Kim, SW, Li, X, Datta, S, Pound, WG, Wu, G 2008a. Dietary supplementation with cholesterol and docosahexaenoic acid affects concentrations of amino acids in tissues of young pigs. Amino Acids doi:10.1007/s00726-008-0196-5, Published Online by Springer Wien 30 October 2008.Google Scholar
Li, P, Sung, WK, Li, X, Datta, S, Pond, WG, Wu, G 2008b. Dietary supplementation with cholesterol and docosahexaenoic acid increases the activity of the arginine-nitric oxide pathway in tissues of young pigs. Nitric Oxide 19, 259265.Google Scholar
Liu, S, Baracos, VE, Quinney, HA, Clandinin, MT 1994. Dietary omega-3 and polyunsaturated fatty acids modify fatty acyl composition and insulin binding in skeletal-muscle sarcolemma. The Biochemical Journal 299, 831837.Google Scholar
MacDonald, JIS, Sprecher, H 1991. Phospholipid fatty acid remodeling in mammalian cells. Biochemica Biophysica Acta 1084, 105121.Google Scholar
National Research Council 2000. Nutrient Requirements of Beef Cattle. Last updated. National Academy of Science, Washington, DC.Google Scholar
Olefsky, JM 2008. Fat talks, liver and muscle listen. Cell 134, 914916.Google Scholar
Palmquist, DL 2009. Omega-3 fatty acids in metabolism, health, and nutrition and for modified animal product foods. The Professional Animal Scientist 25, 207249.CrossRefGoogle Scholar
Pan, DA, Lillioja, S, Milner, MR, Kriketos, AD, Baur, LA, Bogardus, C, Storlien, LH 1995. Skeletal muscle membrane lipid composition is related to adiposity and insulin action. The Journal of Clinical Investigation 96, 28022808.CrossRefGoogle ScholarPubMed
Pires, JAA, Pescara, JB, Brickner, AE, Silvia del Rio, N, Cunha, AP, Grummer, RR 2007. Effects of abomasal infusion of linseed oil on responses to glucose and insulin in Holstein cows. Journal of Dairy Science 91, 13781390.CrossRefGoogle Scholar
Rieu, I, Balage, M, Sornet, C, Giraudet, C, Pujos, E, Grizard, J, Mosoni, L, Dardevet, D 2006. Leucine supplementation improves muscle protein synthesis in elderly men independently of hyperaminoacidaemia. Journal of Physiology 575, 305315.CrossRefGoogle ScholarPubMed
SAS Institute Inc., 2000. Statistical Analysis System. SAS Institute Inc., Cary, NC, USA.Google Scholar
Simopoulos, AP 1991. Omega-3 fatty acids in health and disease and in growth and development. American The Journal of Clinical Nutrition 54, 438463.Google Scholar
Storlien, LH, Jenkins, AB, Chishlom, DJ, Pascoe, WS, Khouri, S, Kraegen, EW 1991. Influence of dietary fat composition on development of insulin resistance in rats. Relationship to muscle triglycerides and omega-3 fatty acids in muscle phospholipids. Diabetes 40, 280289.Google Scholar
Storlien, LH, Kraegen, EW, Chishlom, DJ, Ford, GL, Bruce, DG, Pascoe, WS 1987. Fish oil prevents insulin resistance induced by high-fat feeding in rats. Science 237, 885888.Google Scholar
Stubbs, CD, Smith, AD 1984. The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochemica et Biophysica Acta 779, 89137.Google Scholar
Taouis, M, Dagou, C, Ster, C, Durand, G, Pinault, M, Delarue, J 2002. N-3 polyunsaturated fatty acids prevent the defect of insulin receptor signaling in muscle. American Journal of Physiology. Endocrinology and Metabolism 282, E664E671.Google Scholar
Thivierge, MC, Bernier, JF, Dubreuil, P, Lapierre, H 2002. The effect of jugular or abomasal infusion of amino acids on milk yield in lactating cows fed a protein deficient diet. Reproduction, Nutrition and Development 42, 113.CrossRefGoogle ScholarPubMed
Thivierge, MC, Bush, JA, Suryawan, A, Nguyen, HV, Orellana, RA, Burrin, DG, Jahoor, F, Davis, TA 2005. Whole body and hindlimb protein breakdown are differentially altered by feeding in neonatal piglets. The Journal of Nutrition 135, 14301435.Google Scholar
Voelker, DR 1991. Organelle biogenesis and intracellular lipid transport in eukaryotes. Microbiology Review 55, 543560.Google Scholar
Volpi, E, Ferrando, A, Yeckel, CW, Tipton, KD, Wolfe, RR 1998. Exogenous amino acids stimulates net muscle protein synthesis in the elderly. The Journal of Clinical Investigation 101, 20002007.Google Scholar
Wray-Cahen, D, Beckett, PR, Nguyen, HV, Davis, TA 1997. Insulin-stimulated amino acid utilization during glucose and amino acids clamps decreases with development. American Journal of Physiology Endocrinology and Metabolism 273, E305E314.Google Scholar
Yang, X, Yang, C, Farberman, A, Rideout, TC, de Lange, CFM, France, J, Fan, MZ 2008. The mammalian target of rapamycin-signaling pathway in regulating metabolism and growth. Journal of Animal Science 86, E36E50.Google Scholar