Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-26T13:25:50.812Z Has data issue: false hasContentIssue false

trans-10, cis-12 Conjugated linoleic acid inhibits lipoprotein lipase but increases the activity of lipogenic enzymes in adipose tissue from hamsters fed an atherogenic diet

Published online by Cambridge University Press:  08 March 2007

Amaia Zabala
Affiliation:
Department of Nutrition and Food ScienceUniversity of País VascoPaseo de la Universidad 701006 VitoriaSpain
Itziar Churruca
Affiliation:
Department of Nutrition and Food ScienceUniversity of País VascoPaseo de la Universidad 701006 VitoriaSpain
Alfredo Fernández-Quintela
Affiliation:
Department of Nutrition and Food ScienceUniversity of País VascoPaseo de la Universidad 701006 VitoriaSpain
Víctor M. Rodríguez
Affiliation:
Department of Nutrition and Food ScienceUniversity of País VascoPaseo de la Universidad 701006 VitoriaSpain
M. Teresa Macarulla
Affiliation:
Department of Nutrition and Food ScienceUniversity of País VascoPaseo de la Universidad 701006 VitoriaSpain
J. Alfredo Martínez
Affiliation:
Department of Physiology and NutritionUniversity of Navarrac/Irunlarrea s/n31008 PamplonaSpain
María P. Portillo*
Affiliation:
Department of Nutrition and Food ScienceUniversity of País VascoPaseo de la Universidad 701006 VitoriaSpain
*
*Corresponding author: Dr Maráa P. Portillo, fax +34 945 013014, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The aim of the present work was to investigate the effects of trans-10,cis-12conjugated linoleic acid (CLA) on the activity and expression of lipogenic enzymes and lipoprotein lipase (LPL), as well as on the expression of transcriptional factors controlling these enzymes, in adipose tissue from hamsters, and to evaluate the involvement of these changes in the body fat-reducing effect of this CLA isomer. Thirty male hamsters were divided into three groups and fed atherogenic diets supplemented with 0 (linoleic group), 5 or 10g trans-10,cis-12CLA/kg diet, for 6 weeks. Body and adipose tissue weights, food intake and serum insulin were measured. Total and heparin-releasable LPL and lipogenic enzyme activities (acetyl-CoA carboxylase (ACC); fatty acid synthase (FAS); glucose-6-phosphate dehydrogenase (G6PDH); and malic enzyme (ME)) were assessed. ACC, FAS, LPL, sterolregulatory element-binding proteins (SREBP-1a), SREBP-1c and PPARγ mRNA levels were alsodetermined by real-time PCR. CLA did not modify food intake, body weight and serum insulin level. CLA feeding reduced adipose tissue weight, LPL activity and expression, and increased lipogenic enzyme activities, despite a significant reduction in ACC and FAS mRNA levels. The expression of the three transcriptional factors analysed (SREBP-1a, SREBP-1c and PPARγ) wasalso reduced. These results appear to provide a framework for partially understanding the reduction in body fat induced by CLA. Inhibition of LPL activity seems to be an important mechanism underlying body fat reduction in hamsters. Further research is needed to better characterizethe effects of CLA on lipogenesis and the role of these effects in CLA action.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2006

References

Azain, MJ, Hausman, DB, Sisk, MB, Flatt, WP & Jewell, DEDietary conjugated linoleic acid reduces rat adipose tissue cell size rather than cell number. J Nutr 2000 130, 15481554.CrossRefGoogle ScholarPubMed
Belfrage, P & Vaughan, MSimple liquid–liquid partition system for isolation of labeled oleic acid from mixtures with glycerides. J Lipid Res 1969 10, 341344.CrossRefGoogle ScholarPubMed
Belury, MDietary conjugated linoleic acid in health: physiological mechanisms of action. Annu Rev Nutr 2002 22, 505531.CrossRefGoogle ScholarPubMed
Bradford, MMA rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976 72, 248254.CrossRefGoogle ScholarPubMed
Brodie, AE, Manning, VA, Ferguson, KR, Jewell, DE & Hu, CYConjugated linoleic acid inhibits differentiation of pre- and postconfluent 3T3-L1 preadipocytes but inhibits cell proliferation only in preconfluent cells.. J Nutr 1999, 602606.CrossRefGoogle Scholar
Brown, JM, Boysen, MS, Jensen, SS, Morrison, RF, Storkson, J, Lea-Currie, RPariza, M, Mandrup, S & McIntosh, MKIsomer-specific regulation of metabolism and PPARg signalling by CLA in human preadipocytes. J Lipid Res 2003 44, 12871300.CrossRefGoogle Scholar
Choi, Y, Kim, YC, Han, YB, Park, Y, Pariza, MW, Ntambi, JMThe trans-10, cis-12 isomer of conjugated linoleic acid downregulates stearoyl-CoA desaturase 1 gene expression in 3T3-L1 adipocytes. J Nutr 2000 130, 1901924.CrossRefGoogle ScholarPubMed
Clement, L, Poirier, H, Niot, I, Bocher, V, Guerre-Millo, M, Krief, S, Staels, B & Besnard, PDietary trans-10, cis-12 conjugated linoleic acid induces hyperinsulinemia and fatty liver in the mouse. J Lipid Res 2002 43, 14001409.CrossRefGoogle ScholarPubMed
Corino, C, Mourot, J, Magni, S, Pastorelli, G & Rosi, FInfluence of dietary conjugated linoleic acid on growth, meat quality, lipogenesis, plasma leptin and physiological variables of lipid metabolism in rabbits. J Anim Sci 2002 80, 10201028.CrossRefGoogle ScholarPubMed
Ealey, KN, El-Sohemy, A & Archer, MCEffects of dietary conjugated linoleic acid on the expression of uncoupling proteins in mice and rats. Lipids 2002 37, 853861.CrossRefGoogle ScholarPubMed
Evans, M, Brown, J & McIntosh, MIsomer-specific effect of conjugated linoleic acid (CLA) on adiposity and lipid metabolism. J Nutr Biochem 2002 13, 508516.CrossRefGoogle ScholarPubMed
Evans, M, Park, Y, Pariza, M, Curtis, L, Kuebler, B & McIntosh, Mtrans-10, cis-12 Conjugated linoleic acid reduces triglyceride content while differentially affecting peroxisome proliferator activated receptor g2 and P2 expression in 3T3-L1 preadipocytes. Lipids 2001 36, 12231232.CrossRefGoogle Scholar
Faulconnier, Y, Arnal, MA, Patureau, Mirand P, Chardigny, JM & Chilliard, YIsomers of conjugated linoleic acid decrease plasma lipids and stimulate adipose tissue lipogenesis without changing adipose weight in post-prandial adult sedentary or trained Wistar rat. J Nutr Biochem 2004 15, 741748.CrossRefGoogle ScholarPubMed
Field, FJ, Born, E & Mathur, SNFatty acid flux suppress fatty acid synthesis in hamster intestine independently of SREBP-1 expression. J Lipid Res 2003 44, 11991208.CrossRefGoogle ScholarPubMed
Fielding, BA & Frayn, KNLipoprotein lipase and the disposition of dietary fatty acids. Br J Nutr 1998 80, 495502.CrossRefGoogle ScholarPubMed
Grandlund,, L, Juvet, LK, Pedersen, JI & Nebb, HITrans10,-cis12-conjugated linoleic acid prevents triacylglycerol accumulation in adipocytes by acting as a PPARgamma modulator. J Lipid Res 2003 44, 14411452.CrossRefGoogle Scholar
Horton, JD, Goldstein, JL & Brown, MSSREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 2002 109, 11251131.CrossRefGoogle ScholarPubMed
Kang, K, Liu, W, Albright, KJ, Park, Y & Pariza, MW 2003) Trans–10,cis–12 CLA inhibits differentiation of 3T3-L1 adipocytes and decreases PPARgamma expression. Biochem Biophys Res Commun 303, 795799.CrossRefGoogle Scholar
Kang, K, Miyazaki, M, Ntambi, JM & Pariza, MWMEvidence that the anti-obesity effect of conjugated linoleic acid is independent of effects on stearoyl-CoA desaturase 1 expression and enzyme activity. Biochem Biophys Res Commun 2004 315, 532537.CrossRefGoogle Scholar
Kersten, SPeroxisome proliferator activated receptors and obesity. Eur J Pharmacol 2002 440, 223234.CrossRefGoogle ScholarPubMed
Khan, SA & Vanden, Heuvel JPRole of nuclear receptors in the regulation of gene expression by dietary fatty acids (review). J Nutr Biochem 2003 14, 554567.CrossRefGoogle ScholarPubMed
Kim, MR, Park, Y, Albright, KJ & Pariza, MDifferential responses of hamsters and rats fed high-fat or low-fat supplemented with conjugated linoleic acid. Nutr Res 2002 22, 715722.CrossRefGoogle Scholar
Lin, Y, Kreeft, A, Schuurbiers, JA & Draijer, RDifferent effects of conjugated linoleic acid isomers on lipoprotein lipase activity in 3T3-L1 adipocytes. J Nutr Biochem 2001 12, 183189.CrossRefGoogle ScholarPubMed
Livak, KJ & Schmittgen, TDAnalysis of relative gene expression data using real-time quantitative PCR and the 2(2DeltaDelta C(T)) method. Methods 2001 25, 402408.CrossRefGoogle Scholar
Macarulla, MT, Fernandez-Quintela, A, Zabala, A, Navarro, V, Echevarría,, E, Churruca, I, Rodrýguez, VM & Portillo, MPThe effects of conjugated linoleic acid on liver composition and fatty acid oxidation are isomer dependent in hamster. Nutrition 2005 21, 512519.CrossRefGoogle ScholarPubMed
Martin, JC, Grégoire, S, Siess, MH, Genty, M, Chardingy, JM, Berdeaux, O, Juanéda, P & Sébédio, JLEffects of conjugated linoleic acid isomers on lipid-mobilizing enzymes in male rats. Lipids 2000 35, 9198.CrossRefGoogle Scholar
Martin, JC & Valeille, KConjugated linoleic acid: all the same or to everyone its own function?. Reprod Nutr Dev 2002 42, 525536.CrossRefGoogle ScholarPubMed
Mourot, J, Peiniau, P & Mounier, A (1994) Effets de l’acide linoléique alimentaire sur l’activitédes enzymes de la lipogenése dans les tissus adipeux chez le porc. Reprod Nutr Dev 34, 213220.CrossRefGoogle Scholar
Navarro, V, Zabala, A, Macarulla, MTFern´ndez-Quintela, ARodríguez, VM, Simón, EPortillo, MPEffects of conjugated linoleic acid on body fat accumulation and serum lipids in hamsters fed an atherogenic diet. J Physiol Biochem 2003 59, 193199.CrossRefGoogle ScholarPubMed
Nilsson-Ehle, P & Schotz, MCA stable radioactive substrate emulsion for assay of lipoprotein lipase. J Lipid Res 1976 17, 536541.CrossRefGoogle ScholarPubMed
Pal, S, Takechi, R & Ho, SSConjugated linoleic acid suppresses the secretion of atherogenic lipoproteins from human HepG2 liver cells. Clin Chem Lab Med 2005 43, 269274.CrossRefGoogle ScholarPubMed
Pariza, MW, Park, Y & Cook, MEMechanism of action of conjugated linoleic acid: evidence and speculation. Proc Soc Exp Biol Med 2000 223, 813.Google ScholarPubMed
Pariza, MWPark, Y & Cook, METhe biologically active isomers of conjugated linoleic acid. Prog Lipid Res 2001 40, 283298.CrossRefGoogle ScholarPubMed
Park, Y, Albright, KJ, Liu, WStorkson, JM, Cook, ME & Pariza, MWEffects of conjugated linoleic acid on body composition in mice. Lipids 1997 32, 853858.CrossRefGoogle ScholarPubMed
Park, Y & Pariza, MWThe effects of dietary conjugated nonadecadienoic acid on body composition in mice. Biochim Biophys Acta 2001 1533, 171174.CrossRefGoogle ScholarPubMed
Park, Y, Storkson, JM, Albright, KJ, Liu, W & Pariza, MWEvidence that the trans–10,cis–12 isomer of conjugated linoleic acid induces body composition changes in mice. Lipids 1999 34, 235241.CrossRefGoogle ScholarPubMed
Park, Y, Storkson, JM, Liu, W, Albright, KJ, Cook, ME, & Pariza, MWStructure–activity relationship of conjugated linoleic acid and its cognates in inhibiting heparin–releasable lipoprotein lipase and glycerol release from fully differentiated 3T3–L1 adipocytes. J Nutr Biochem 2004 15, 561569.CrossRefGoogle ScholarPubMed
Reeves, PG, Nielsen, FH & Fahey, GC Jr AIN–93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN–76 rodent diet. J Nutr 1993 123, 19391951.CrossRefGoogle Scholar
Roche, HM, Noone, E, Nugent, A & Gibney, MJConjugated linoleic acid: a novel therapeutic nutrient?. Nutr Res Rev 2001 173187.CrossRefGoogle ScholarPubMed
Roche, HM, Noone, E, Sewter, C, McBennett, S, Savage, D, Gibney, MJ, O’Rahilly, S & Vidal-Puig, AJIsomer-dependent metabolic effects of conjugated linoleic acid: insights from molecular markers sterol regulatory element–binding protein-1c and LXRalpha.. Diabetes 2002 51, 20372044.CrossRefGoogle ScholarPubMed
Sauer, LA, Dauchy, RT, Blask, DE, Krause, JA, Davidson, LK, Dauchy, EM, Welham, KJ & Coupland, KConjugated linoleic acid isomers and trans fatty acids inhibit fatty acid transport in hepatoma 7288CTC and inguinal fat pads in Buffalo rats. J Nutr 2004 134, 19891997.CrossRefGoogle ScholarPubMed
Simón, E, Macarulla, MT, Fernéndez-Quintela, A, Rodrýguez, VM & Portillo, MPBody fat-lowering effect of conjugated linoleic acid is not due to increased lipolysis.. J Physiol Biochem 2005 61, 363370.CrossRefGoogle Scholar
Storkson,, JM, Park, Y, Cook, ME & Pariza, MWEffects of trans–10,cis–12 conjugated linoleic acid and cognates on apolipoprotein B secretion in HepG2 cells. Nutr Res 2005 25, 387399.CrossRefGoogle Scholar
Takahashi,, Y, Kushiro, M, Shinohara, K & Ide, TDietary conjugated linoleic acid reduces body fat mass and affects gene expression of proteins regulating energy metabolism in mice. Comp Biochem Physiol B Biochem Mol Biol 2002 133, 395404.CrossRefGoogle ScholarPubMed
Tsuboyama-Kasaoka, N, Takahashi, M, Tanemura, K, Kim, HJ, Tange, T, Okuyama, H, Kasai, M, Ikemoto, S & Ezaki, OConjugated linoleic acid supplementation reduces adipose tissue by apoptosis and develops lipodystrophy in mice. Diabetes 2000 49, 15341542.CrossRefGoogle ScholarPubMed
Waterman, RA, Romsos, DR, Tsai, AC, Miller, ER & Leveille, GAInfluence of dietary safflower oil and tallow on growth, plasma lipids and lipogenesis in rats, pig and chicks. Proc Soc Exp Biol Med 1975 150, 347351.CrossRefGoogle ScholarPubMed
West, DB, Blohm, FY, Truett, AA & DeLany, JPConjugated linoleic acid persistently increases total energy expenditure in AKR/J mice without increasing uncoupling protein gene expression. J Nutr 2000 130, 24712477.CrossRefGoogle ScholarPubMed
Xu, X, Storkson, J, Kim, S, Sugimoto, KPark, Y & Pariza, MW (2003) Short-term intake of conjugated linoleic acid inhibits lipoprotein lipase and glucose metabolism but does not enhance lipolysis in mouse adipose tissue. J Nutr 133, 663667.CrossRefGoogle Scholar
Yotsumoto, H, Hara, E, Naka, S, Adlof, RO, Emken, EA & Yanagita, T10trans, 12cis–Linoleic acid reduced apolipoprotein B secretion in HepG2 cells. Food Res Int 1999 31, 403409.CrossRefGoogle Scholar
Zabala, A, Fernández-Quintela, A, Macarulla, MT, Simón, E, Rodríguez, VM, Navarro, V & Portillo, MPEffects of conjugated linoleic acid on skeletal muscle triacylglycerol metabolism in hamsters. Nutrition 2006 (In the Press).CrossRefGoogle ScholarPubMed
Zabala, A, Churruca, I, Macarulla, MT, Rodrýguez, VM, Fernández-Quintela, A, Martínez, JA & Portillo, MPThe trans–10,cis–12 isomer of conjugated linoleic acid reduces hepatic triacylglycerol content without affecting lipogenic enzymes in hamsters.. Br J Nutr 2004 92, 383389.CrossRefGoogle ScholarPubMed