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Conjugated linoleic acid and betaine affect lipolysis in pig adipose tissue explants

Published online by Cambridge University Press:  31 May 2019

I. Fernández-Fígares*
Affiliation:
Departmento de Fisiología y Bioquímica de la Nutrición Animal, Estación Experimental del Zaidín, CSIC, Profesor Albareda 1, Granada 18008, Spain
M. Lachica
Affiliation:
Departmento de Fisiología y Bioquímica de la Nutrición Animal, Estación Experimental del Zaidín, CSIC, Profesor Albareda 1, Granada 18008, Spain
M. Martínez-Pérez
Affiliation:
Instituto de Ciencia Animal, Carretera Central San José de las Lajas, Mayabeque, Cuba
T. G. Ramsay
Affiliation:
Animal Biosciences and Biotechnology Laboratory, Beltsville Agricultural Research Center, USDA-ARS, 10300 Baltimore Avenue, BARC-East, Beltsville MD 20705, USA
*
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Abstract

Consumers’ demand of leaner meat products is a challenge. Although betaine and conjugated linoleic acid (CLA) have the potential to decrease porcine adipose tissue, their mode of action is poorly understood. The aim of the study was to determine the lipolytic effect of betaine and CLA in the adipose tissue of Iberian pigs. Adipose tissue explants from five pigs (38 kg BW) were prepared from dorsal subcutaneous adipose tissue samples and cultivated for 2 h (acute experiments) or 72 h (chronic experiments). Treatments included 100 µM linoleic acid (control), 100 µM trans-10, cis-12 CLA, 100 µM linoleic acid + 1 mM betaine and 100 µM trans-10, cis-12 CLA + 1 mM betaine (CLABET). To examine the ability of betaine or CLA to inhibit insulin’s suppression of isoproterenol-stimulated lipolysis, test medium was amended with 1 µM isoproterenol ±10 nM insulin. Media glycerol was measured at the end of the incubations. Acute lipolysis (2 h) was increased by CLA and CLABET (85% to 121%; P < 0.05) under basal conditions. When lipolysis was stimulated with isoproterenol (1090%), acute exposure to betaine tended to increase (13%; P = 0.071), while CLA and CLABET increased (14% to 18%; P < 0.05) isoproterenol-stimulated lipolysis compared with control. When insulin was added to isoproterenol-stimulated explants, lipolytic rate was decreased by 50% (P < 0.001). However, supplementation of betaine to the insulin + isoproterenol-containing medium tended to increase (P = 0.07), while CLABET increased (45%; P < 0.05) lipolysis, partly counteracting insulin inhibition. When culture was extended for 72 h, CLA decreased lipolysis under basal conditions (18%; P < 0.05) with no effect of betaine and CLABET (P > 0.10). When lipolysis was stimulated by isoproterenol (125% increase in rate compared with basal), CLA and CLABET decreased glycerol release (27%; P < 0.001) compared with control (isoproterenol alone). When insulin was added to isoproterenol-stimulated explants, isoproterenol stimulation of lipolysis was completely blunted and neither betaine nor CLA altered the inhibitory effect of insulin on lipolysis. Isoproterenol, and especially isoproterenol + insulin, stimulated leptin secretion compared with basal conditions (68% and 464%, respectively; P < 0.001), with no effect of CLA or betaine (P > 0.10). CLA decreased leptin release (25%; P < 0.001) when insulin was present in the media, partially inhibiting insulin stimulation of leptin release. In conclusion, betaine and CLA produced a biphasic response regarding lipolysis so that glycerol release was increased in acute conditions, while CLA decreased glycerol release and betaine had no effect in chronic conditions. Furthermore, CLA and CLABET indirectly increased lipolysis by reducing insulin-mediated inhibition of lipolysis during acute conditions.

Type
Research Article
Copyright
© The Animal Consortium 2019 

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References

Ahn, IS 2006. Isomer-specific effect of conjugated linoleic acid on inflammatory adipokines associated with fat accumulation in 3T3-L1 adipocytes. Journal of Medicinal Food 9, 307312.CrossRefGoogle ScholarPubMed
Albuquerque, A, Redondeiro, M, Laranjo, M, Felix, MR, Neves, J, Félix, MR, Freitas, A, Tirapicos, J and Martins, J 2017. Long term betaine supplementation regulates genes involved in lipid and cholesterol metabolism of two muscles from an obese pig breed. Meat Science 124, 2533.CrossRefGoogle ScholarPubMed
Boden, G, Chen, X, Kolaczynski, JW and Polansky, M 1997. Effects of prolonged hyperinsulinemia on serum leptin in normal human subjects. Journal of Clinical Investigation 100, 11071113.CrossRefGoogle ScholarPubMed
Chin, S, Liu, W, Storkson, J, Ha, Y and Pariza, M 1992. Dietary sources of conjugated dienoic isomers of linoleic acid, a newly recognized class of anticarcinogens. Journal of Food Composition and Analysis 5, 185197.CrossRefGoogle Scholar
Craig, SAS 2004. Betaine in human nutrition. The American Journal of Clinical Nutrition 80, 539549.CrossRefGoogle ScholarPubMed
Cusin, I, Sainsbury, A, Doyle, P, Rohner Jeanrenaud, F and Jeanrenaud, B 1995. The ob gene and insulin. A relationship leading to clues to the understanding of obesity. Diabetes 44, 14671470.CrossRefGoogle ScholarPubMed
Dietz, J and Schwartz, J 1991. Growth hormone alters lipolysis and hormone-sensitive lipase activity in 3T3-F442A adipocytes. Metabolism, Clinical and Experimental 40, 800806.CrossRefGoogle ScholarPubMed
Dugan, MER, Aalhus, JL, Schaefer, AL and Kramer, JKG 1997. The effect of conjugated linoleic acid on fat to lean repartitioning and feed conversion in pigs. Canadian Journal of Animal Science 77, 723725.CrossRefGoogle Scholar
Evans, M, Lin, X, Odle, J and McIntosh, M 2002. Trans-10, Cis-12 conjugated linoleic acid increases fatty acid oxidation in 3T3-L1 preadipocytes. Journal of Nutrition 132, 450455.CrossRefGoogle ScholarPubMed
Fernandez-Figares, I, Conde-Aguilera, JA, Nieto, R, Lachica, M and Aguilera, JF 2008. Synergistic effects of betaine and conjugated linoleic acid on the growth and carcass composition of growing Iberian pigs. Journal of Animal Science 86, 102111.CrossRefGoogle ScholarPubMed
Fernandez-Figares, I, Lachica, M, Martin, A, Nieto, R, Gonzalez-Valero, L, Rodriguez-Lopez, JM and Aguilera, JF 2012. Impact of dietary betaine and conjugated linoleic acid on insulin sensitivity, protein and fat metabolism of obese pigs. Animal 6, 10581067.CrossRefGoogle ScholarPubMed
Fernandez-Figares, I, Wray-Cahen, D, Steele, NC, Campbell, RG, Hall, DD, Virtanen, E and Caperna, TJ 2002. Effect of dietary betaine on nutrient utilization and partitioning in the young growing feed-restricted pig. Journal of Animal Science 80, 421428.CrossRefGoogle Scholar
Friedman, J and Halaas, J 1998. Leptin and the regulation of body weight in mammals. Nature 395, 763770.CrossRefGoogle ScholarPubMed
Fruhbeck, G, Martinez, JA, Martínez, JA, Frühbeck, G, Aguado, M and Martınez, JA 1997. In vitro lipolytic effect of leptin on mouse adipocytes: evidence for a possible autocrine/paracrine role of leptin. Biochemical and Biophysical Research Communications 240, 590594.CrossRefGoogle ScholarPubMed
Huang, QC, Xu, ZR, Han, XY and Li, WF 2006. Changes in hormones, growth factor and lipid metabolism in finishing pigs fed betaine. Livestock Science 105, 7885.CrossRefGoogle Scholar
Jang, A, Kim, D, Sung, KS, Jung, S, Kim, H and Jo, C 2014. The effect of dietary α-lipoic acid, betaine, l-carnitine, and swimming on the obesity of mice induced by a high-fat diet. Food and Function 5, 19661974.CrossRefGoogle ScholarPubMed
José, AAFBV, Gama, MAS and Lanna, DDP 2008. Effects of trans-10, cis-12 conjugated linoleic acid on gene expression and lipid metabolism of adipose tissue of growing pigs. Genetics and Molecular Research 7, 284294.CrossRefGoogle ScholarPubMed
Lee, MJ, Wang, YX, Ricci, MR, Sullivan, S, Russell, CD and Fried, SK 2007. Acute and chronic regulation of leptin synthesis, storage, and secretion by insulin and dexamethasone in human adipose tissue. American Journal of Physiology-Endocrinology and Metabolism 292, E858E864.CrossRefGoogle ScholarPubMed
Lin, J, Barb, CR, Matteri, RL, Kraeling, RR, Chen, X, Meinersmann, RJ and Rampacek, GB 2000. Long form leptin receptor mRNA expression in the brain, pituitary, and other tissues in the pig. Domestic Animal Endocrinology 19, 5361.CrossRefGoogle ScholarPubMed
Mersmann, HJ 1984. Specificity of β-adrenergic control of lipolysis in swine adipose tissue. Comparative Biochemistry and Physiology. C, Comparative Pharmacology 77, 3942.CrossRefGoogle ScholarPubMed
Mersmann, HJ 1989. The effect of insulin on porcine adipose tissue lipogenesis. Comparative Biochemistry and Physiology. B. Comparative Biochemistry 94, 709713.CrossRefGoogle ScholarPubMed
Mueller, W, Gregoire, F, Stanhope, K, Mobbs, C, Mizuno, T, Warden, C, Stern, J and Havel, P 1998. Evidence that glucose metabolism regulates leptin secretion from cultured rat adipocytes. Endocrinology 139, 551558.CrossRefGoogle ScholarPubMed
Neilands, JB. (1955). Lactic dehydrogenase of heart muscle. Methods in Enzymology 1, 449454.CrossRefGoogle Scholar
Park, Y, Storkson, J, Albright, K, Liu, W and Pariza, M 1999. Evidence that trans-10, cis-12 isomer of conjugated linoleic acid induces body composition changes in mice. Lipids 34, 235241.CrossRefGoogle ScholarPubMed
Ramsay, TG 2001. Porcine leptin alters insulin inhibition of lipolysis in porcine adipocytes in vitro. Journal of Animal Science 79, 653657.CrossRefGoogle ScholarPubMed
Ramsay, TG 2004. Porcine leptin alters isolated adipocyte glucose and fatty acid metabolism. Domestic Animal Endocrinology 26, 1121.CrossRefGoogle ScholarPubMed
Ramsay, TG and Richards, MP 2004. Hormonal regulation of leptin and leptin receptor expression in porcine subcutaneous adipose tissue. Journal of Animal Science 82, 34863492.CrossRefGoogle ScholarPubMed
Ramsay, TG and White, ME 2000. Insulin regulation of leptin expression in streptozotocin diabetic pigs. Journal of Animal Science 78, 14971503.CrossRefGoogle ScholarPubMed
Ricci, M, Lee, MJ, Russell, C, Wang, Y, Sullivan, S, Schneider, S, Brolin, R and Fried, S 2005. Isoproterenol decreases leptin release from rat and human adipose tissue through posttranscriptional mechanisms. American Journal of Physiology: Endocrinology and Metabolism 288, E798E804.Google ScholarPubMed
Rojas-Cano, M, Lachica, M, Lara, L, Haro, A and Fernandez-Figares, I 2017. Portal-drained viscera heat production in Iberian pigs fed betaine- and conjugated linoleic acid-supplemented diets. Journal of the Science of Food and Agriculture 97, 679685.CrossRefGoogle ScholarPubMed
Rojas-Cano, ML, Lara, L, Lachica, M, Aguilera, JF and Fernandez-Figares, I 2011. Influence of betaine and conjugated linoleic acid on development of carcass cuts of Iberian pigs growing from 20 to 50 kg body weight. Meat Science 88, 525530.CrossRefGoogle ScholarPubMed
Svedberg, J, Bjorntorp, P, Smith, U and Lonnroth, P 1990. Free fatty-acid inhibition of insulin binding, degradation, and action in isolated rat hepatocytes. Diabetes 39, 570574.CrossRefGoogle ScholarPubMed
Wang, Z, Pini, M, Yao, T, Zhou, Z, Sun, C, Fantuzzi, G and Song, Z 2011. Homocysteine suppresses lipolysis in adipocytes by activating the AMPK pathway. American Journal of Physiology: Endocrinology and Metabolism 301, E703E712.Google ScholarPubMed
Yeganeh, A, Taylor, CG, Tworek, L, Poole, J and Zahradka, P 2016. Trans-10, cis-12 conjugated linoleic acid (CLA) interferes with lipid droplet accumulation during 3T3-L1 preadipocyte differentiation. The International Journal of Biochemistry & Cell Biology 76, 3950.CrossRefGoogle ScholarPubMed
Zhou, X, Li, D, Yin, J, Ni, J, Dong, B, Zhang, J and Du, M 2007. CLA differently regulates adipogenesis in stromal vascular cells from porcine subcutaneous adipose and skeletal muscle. Journal of Lipid Research 48, 17011709.CrossRefGoogle ScholarPubMed