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Gender-related response of lipid metabolism to dietary fatty acids in the hamster

Published online by Cambridge University Press:  08 March 2007

Anne Morise
Affiliation:
Laboratoire d'Endocrinologie de la Nutrition, Université Paris Sud, 91405 Orsay Cedex, France
Jacques Mourot
Affiliation:
INRA, SENAH, Saint-Gilles, 35590 L'Hermitage, France
Carole Boué
Affiliation:
3ITERG-Nutrition, 35405 Talence, France
Nicole Combe
Affiliation:
3ITERG-Nutrition, 35405 Talence, France
Ghislaine Amsler
Affiliation:
Laboratoire d'Endocrinologie de la Nutrition, Université Paris Sud, 91405 Orsay Cedex, France
Daniel Gripois
Affiliation:
Laboratoire d'Endocrinologie de la Nutrition, Université Paris Sud, 91405 Orsay Cedex, France
Annie Quignard-Boulangé
Affiliation:
INSERM 465, 75005 Paris, France
Laurent Yvan-Charvet
Affiliation:
INSERM 465, 75005 Paris, France
Evelyne Fénart
Affiliation:
ONIDOL, 75008 Paris, France
Pierre Weill
Affiliation:
La Messayais, 35210 Combourtillé, France
Dominique Hermier*
Affiliation:
UMR Physiologie de la Nutrition et du Comportement Alimentaire, INRA-INA-PG, 16 rue Claude Bernard, 75231 Paris Cedex 05, France
*
*Corresponding author: Dr Dominique Hermier, fax +33 1 44 08 72 46, email [email protected]
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Abstract

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Gender and dietary fatty acids are involved in the regulation of lipid metabolism, disturbances of which can lead to pathologies such as metabolic syndrome or CVD. Possible interactions between these factors were investigated in male and female hamsters fed diets rich in either saturated fatty acids (‘butter’ diet) or in α-linolenic acid (‘linseed oil’ diet). Gender effect predominated over the diet effect on cholesterol (CH) metabolism; compared to males, females exhibited lower concentrations of plasma total CH (−20%, P<0·001), LDL-CH (−40%, P<0·001) and HDL-CH (−16%, P<0·001), together with higher LDL receptor (+40%) and lower HDL receptor (−60%) hepatic content. Triacylglycerol (TG) metabolism was affected by diet above all: compared to animals fed the ‘butter’ diet, those fed the ‘linseed oil’ diet exhibited lower plasma (−23%, P=0·046) and liver TG (−20%, P=0·026) concentration which may result from both an increased β-oxidation (P<0·001), without any change in PPARα mRNA, and a decreased hepatic lipogenesis (P=0·023), without increased sterol response element binding protein 1c (SREBP1c) mRNA. The response to diet was much more pronounced in males than in females, without gender effect on the transcription level of PPARα and SREBP1c. Finally, the ‘linseed oil’ diet decreased the insulin resistance index (−80%, P<0·001) with a more marked effect in males, in relation to their higher hepatic PPARγ expression (+90%, P=0·012). In conclusion, in our model, the response of either TG or CH to dietary fatty acids is modulated differently by gender. The possible relevance of these interactions to dietary practice should be taken into account in man.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2006

References

Abraham, S, Hillyard, LA, Hansen, FN & Lin, CYTissue specificity for theeffect of estrogen on lipogenic activity in male and female rats. Biochim Biophys Acta (2002) 620, 167171.CrossRefGoogle Scholar
Acton, S, Rigotti, A, Landschulz, KTXu, SHobbs, HH & Krieger, MIdentification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science (1996) 271, 518520.CrossRefGoogle ScholarPubMed
Ascherio, A, Rimm, EBGiovannucci, EL,Spiegelman, D, Stampfer, M & Willett, WCDietary fat and risk of coronary heart diseasein men: cohort follow up study in the United States. Br Med J (1996) 313 8490.CrossRefGoogle Scholar
Bieber, LL, Abraham, T & Helmrath, TA rapid spectrophotometric assay for carnitine palmitoyltransferase. Anal Biochem (1972) 50, 509518.CrossRefGoogle ScholarPubMed
Boehler, N, Riottot, MFerezou, J, Souidi, M, Milliat, F, Serougne, C, Smith, JL & Lutton, CAntilithiasic effect of beta-cyclodextrin in LPN hamster: comparison with cholestyramine. J Lipid Res (1999) 40 726734.CrossRefGoogle ScholarPubMed
Bonithon-Kopp, C, Scarabin, PY, Darne, B, Malmejac, A & Guize, LMenopause-related changes in lipoproteins and some other cardiovascular risk factors. Int J Epidemiol (1990) 19, 4248.CrossRefGoogle ScholarPubMed
Boué, C, Combe, N, Billeaud, C, Mignerot, C, Entressangles, B, Thery, G, Geoffrion, H, Brun, JL, Dallay, D & Leng, JJTrans fatty acids in adipose tissue of French women in relation to their dietary sources. Lipids (2000) 35, 561566.CrossRefGoogle ScholarPubMed
Burdge, GC & Wootton, SAConversion of alpha-linolenic acid to eicosapentaenoic, docosapentaenoic and docosahexaenoicacids in young women Br J Nutr (2002) 88, 411420.CrossRefGoogle ScholarPubMed
Carlson, LA & Ericsson, MQuantitative and qualitative serum lipoprotein analysis. Part 1. Studies in healthy men andwomen. Atherosclerosis (1975) 21, 417 & 433.CrossRefGoogle Scholar
Chakrabarty, K & Leveille, GAAcetylCoA carboxylase and fatty acid synthetase activities in liver and adipose tissue of meal-fed rats. Proc Soc Exp Biol Med (1969) 131,10511054.CrossRefGoogle Scholar
Chang, HC, Seidman, I, Teebor, G & Lane, MDLiver acetyl CoAcarboxylase and fatty acid synthetase: relative activities in the normal state and in hereditary obesity. Biochem Biophys Res Commun (1967) 28, 682686.CrossRefGoogle Scholar
Chomczynski, P, Qasba, P & Topper, YJTranscriptional and post-transcriptional roles of glucocorticoid in the expression of the rat 25,000 molecular weight casein gene. Biochem Biophys Res Commun (1986) 134, 812818.CrossRefGoogle ScholarPubMed
Cobb, M, Greenspan, J, Timmons, M & Teitelbaum, HGender differences in lipoprotein responses to diet. G.Ann Nutr Metab (1993) 37, 225236.CrossRefGoogle ScholarPubMed
Couillard, C, Bergeron, N, Prud'homme, D,Bergeron, J,Tremblay, A, Bouchard, C, Mauriege, P & Despres, JPGender difference in postprandial lipemia: importance of visceral adipose tissue accumulation. Arterioscler Thromb Vasc Biol (1999) 19 24482455.CrossRefGoogle ScholarPubMed
De Caterina, R & Zampolli, An-3 Fatty acids: antiatherosclerotic effects. Lipids (2001) 36 S69S78CrossRefGoogle ScholarPubMed
Djousse, L, Hunt, SC, Arnett, DK, Province, MA, Eckfeldt, JH & Ellison, RCDietary linolenic acid is inversely associated with plasma triacylglycerol: the National Heart, Lung, and Blood Institute Family Heart Study. Am J Clin Nutr (2003) 78 10981102CrossRefGoogle ScholarPubMed
Ferezou, J, Riottot, M, Serougne, Cet al.. Hypocholesterolemic action of beta-cyclodextrin and its effects on cholesterol metabolism in pigs fed a cholesterol-enriched diet. J Lipid Res (1997) 38 86100CrossRefGoogle ScholarPubMed
Fernandez, MLDietary fat saturation and gender/hormonal status modulate plasma lipids and lipoprotein composition J Nutr Biochem (2001) 12 703710Google Scholar
Fitch, WM, Hill, R & Chaikoff, ILThe effect of fructose feeding on glycolytic enzyme activities of the normal rat liver. J BiolChem (1959) 234 10481051Google ScholarPubMed
Folch, J, Lees, M & Sloane-Stanley, GHA simple method for the isolation and purification of total lipids from animal tissues. J Biol Biochem (1957) 226 497509Google ScholarPubMed
Fossati, P & Prencipe, LSerum triglycerides determined colorimetrically with an enzyme that produces hydrogen peroxide. Clin Chem (1982) 28 20772080CrossRefGoogle ScholarPubMed
Gandemer, G, Pascal, G & Durand, GLipogenic capacity and relative contribution of the different tissues and organs to lipid synthesis in male rat. Reprod Nutr Dev (1983) 23 575586CrossRefGoogle ScholarPubMed
Ghafoorunissa, I, brahim, A & Natarajan, SSubstituting dietary linoleic acid with alpha-linolenic acid improves insulin sensitivity in sucrose fed rats. Biochim Biophys Acta (2005) 1733 6775CrossRefGoogle ScholarPubMed
Goulinet, S & Chapman, MJPlasma lipoproteins in the golden Syrian hamster (Mesocricetus auratus): heterogeneity of apoB- and apoA-I-containing particles. J Lipid Res (1993) 34 943959CrossRefGoogle ScholarPubMed
Gower, BA, Nagy, TR, Blaylock, ML, Wang, C & Nyman, LEstradiol may limit lipid oxidation via Cpt 1 expression and hormonal mechanisms. Obes Res (2002) 10 167172CrossRefGoogle ScholarPubMed
Hsu, RY & Lardy, HAMalic enzyme. In Methods in Enzymology. [Lowenstein, JM] New YorkAcademic Press (1969) 13 230235Google Scholar
Hu, FB, Stampfer, MJ, Manson, JE, Rimm, E, Colditz, GA, Rosner, BA, Hennekens, CH & Willett, WCDietary fat intake and the risk of coronary heart disease in women. N Engl J Med (1997) 337 14911499CrossRefGoogle ScholarPubMed
Kersten, S, Seydoux, J, Peters, JM, Gonzalez, FJ, Desvergne, B & Wahli, WPeroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting. J Clin Invest (1999) 103 14891498CrossRefGoogle ScholarPubMed
Lapenna, D, Ciofani, G,Pierdomenico, SD, Giamberardino, MA & Cuccurullo, FReaction conditions affecting the relationship between thiobarbituric acid reactivity and lipid peroxides in human plasma. Free Radic Biol Med (2001) 31 331335CrossRefGoogle ScholarPubMed
Lavau, M, Bazin, R, Karaoghlanian, Z & Guichard, CEvidence for a high fatty acid synthesis activity in interscapular brown adipose tissue of genetically obese Zucker rats. Biochem J (1982) 204 503507CrossRefGoogle ScholarPubMed
Lazarow, PB & De Duve, CA fatty acyl-CoA oxidizing system in rat liver peroxisomes; enhancement by clofibrate, a hypolipidemic drug. Proc Natl Acad Sci USA (1976) 73 20432046CrossRefGoogle ScholarPubMed
Li, Z, Otvos, JD, Lamon-Fava, S, Carrasco, WV, Lichtenstein, AH, McNamara, JR, Ordovas, JM & Schaefer, EJMen and women differ in lipoprotein response to dietary saturated fat and cholesterol restriction. J Nutr (2003) 133 34283433CrossRefGoogle ScholarPubMed
Lloyd-Jones, DM, Larson, MG, Beiser, A & Levy, DLifetime risk of developing coronary heart disease. Lancet (1999) 353 8992CrossRefGoogle ScholarPubMed
Loison, C, Mendy, F, Serougne, C & Lutton, CDietary myristic acid modifies the HDL-cholesterol concentration and liver scavenger receptor BI expression in the hamster. Br J Nutr (2002) 87 199210CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL & Randal, RJProtein measurement with the Folin phenol reagent. J Biol Chem (1951) 193 265275CrossRefGoogle ScholarPubMed
Manco, M, Calvani, M & Mingrone, GEffects of dietary fatty acids on insulin sensitivity and secretion. Diabetes Obes Metab (2004) 6 402413CrossRefGoogle ScholarPubMed
Matthews, DR, Hosker, JP, Rudenski, AS, Naylor, BA, Treacher, DF & Turner, RCHomeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia (1985) 28 412419CrossRefGoogle ScholarPubMed
Matthews, KA, Meilahn, E, Kuller, LH, Kelsey, SF, Caggiula, AW & Wing, RRMenopause and risk factors for coronary heart disease. N Engl J Med (1989) 321 641646CrossRefGoogle ScholarPubMed
Menke, T, Niklowitz, P, Adam, S, Weber, M, Schluter, B & Andler, WSimultaneous detection of ubiquinol-10, ubiquinone-10, and tocopherols in human plasma microsamples and macrosamples as a marker of oxidative damage in neonates and infants. Anal Biochem (2000) 282 209217CrossRefGoogle ScholarPubMed
Milliat, F, Gripois, D, Blouquit, ME, Ferezou, J, Serougne, C, Fidge, NH & Lutton, CShort and long-term effects of streptozotocin on dietary cholesterol absorption, plasma lipoproteins and liver lipoprotein receptors in RICO rats. Exp Clin Endocrinol Diabetes (2000) 108 436446CrossRefGoogle Scholar
Morise, A, Combe, N, Boué, C, Legrand, P, Catheline, D, Delplanque, B, Fénart, E, Weill, P & Hermier, DDose effect of alpha-linolenic acid on PUFA conversion, bioavailability and storage in the hamster. Lipids (2004 a) 39 325334CrossRefGoogle ScholarPubMed
Morise, A, Mourot, J, Riottot, M, Weill, P, Fenart, E & Hermier, DDose effect of alpha-linolenic acid on lipid metabolism in the hamster. Reprod Nutr Dev (2005) 45 405418CrossRefGoogle ScholarPubMed
Morise, A, Sérougne, C, Gripois, D, Blouquit, MF, Lutton, C & Hermier, DEffects of dietary alpha linolenic acid on cholesterol metabolism in male and female hamsters of the LPN strain. J Nutr Biochem (2004 b) 15 5161CrossRefGoogle ScholarPubMed
Morisson, W & Smith, LPreparation of fatty acid methyl esters and dimetylacetals from lipids with boron fluoride methanol. J Lipid Res (1964) 5 600608CrossRefGoogle Scholar
Mourot, J, Guy, G,Lagarrigue, S, Peiniau, P & Hermier, DRole of hepatic lipogenesis in the susceptibility to fatty liver in the goose (Anser anser). Comp Biochem Physiol B Biochem Mol Biol (2000) 126 8187CrossRefGoogle ScholarPubMed
Noonan, WT & Banks, RORenal function and glucose transport in male and female mice with diet-induced type II diabetes mellitus. Proc Soc Exp Biol Med (2000) 225 221230Google ScholarPubMed
Pawlosky, RJ, Hibbeln, JR, Novotny, JA & Salem, N JrPhysiological compartmental analysis of alpha-linolenic acid metabolism in adult humans. J Lipid Res (2001) 42 12571265CrossRefGoogle ScholarPubMed
Philipp, BW & Shapiro, DJImproved methods for the assay and activation of 3-hydroxy-3-methylglutaryl coenzyme A reductase. J Lipid Res (1979) 20 588593CrossRefGoogle ScholarPubMed
Quintao, E, Grundy, SM & Ahrens, EH JrAn evaluation of four methods for measuring cholesterol absorption by the intestine in man. J Lipid Res (1971) 12 221232CrossRefGoogle ScholarPubMed
Richmond, WPreparation and properties of a cholesterol oxidase from Nocardia sp. and its application to the enzymatic assay of total cholesterol in serum. Clin Chem (1973) 19 13501356CrossRefGoogle ScholarPubMed
Salter, AM, Mangiapane, EH, Bennett, AJ, Bruce, JS, Billett, MA & Anderton, KL, Marenah, CB, Lawson, N & White, DAThe effect of different dietary fatty acids on lipoprotein metabolism: concentration-dependent effects of diets enriched in oleic, myristic, palmitic and stearic acids. Br J Nutr (1998) 79 195202CrossRefGoogle ScholarPubMed
Saltiel, AR & Olefsky, JMThiazolidinediones in the treatment of insulin resistance and type II diabetes Diabetes (1996) 45 16611669CrossRefGoogle ScholarPubMed
Souidi, M, Parquet, M, Ferezou, J & Lutton, CModulation of cholesterol 7alpha-hydroxylase and sterol 27-hydroxylase activities by steroids and physiological conditions in hamster. Life Sci (1999) 64 15851593CrossRefGoogle ScholarPubMed
Spady, DK, Kearney, DM & Hobbs, HHPolyunsaturated fatty acids up-regulate hepatic scavenger receptor B1 (SR-BI) expression and HDL cholesteryl ester uptake in the hamster. J Lipid Res (1999) 40 13841394CrossRefGoogle ScholarPubMed
Stampfer, MJ, Colditz, GA, Willett, WC, Manson, JE, Rosner, B, Speizer, FE & Hennekens, CHPostmenopausal estrogen therapy and cardiovascular disease. Ten-year follow-up from the nurses' health study. N Engl J Med (1991) 325 756762CrossRefGoogle ScholarPubMed
Surette, ME, Whelan, J, Lu, GP, Broughton, KS & Kinsella, JEDependence on dietary cholesterol for n-3 polyunsaturated fatty acid-induced changes in plasma cholesterol in the Syrian hamster. J Lipid Res (1992) 33 263271CrossRefGoogle ScholarPubMed
Takada, R, Saitoh, M & Mori, TDietary gamma-linolenic acidenriched oil reduces body fat content and induces liver enzyme activities relating to fatty acid beta-oxidation in rats. J Nutr (1994) 124 469474CrossRefGoogle ScholarPubMed
Takayama, M, Itoh, S, Nagasaki, T & Tanimizu, IA new enzymatic method for determination of serum choline-containing phospholipids. Clin Chim Acta (1977) 79 9398Google ScholarPubMed
Trinder, PDetermination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann Clin Biochem (1969) 6 2427CrossRefGoogle Scholar
Turley, SD & Dietschy, JMRe-evaluation of the 3 alphahydroxysteroid dehydrogenase assay for total bile acids in bile. J Lipid Res (1978) 19 924928CrossRefGoogle ScholarPubMed
van Beek, AP, de Ruijter-Heijstek, FC, Erkelens, DW & de Bruin, TWMenopause is associated with reduced protection from postprandial lipemia. Arterioscler Thromb Vasc Biol (1999) 19 27372741CrossRefGoogle ScholarPubMed
Weinstein, I, Cook, GA & Heimberg, MRegulation by oestrogen of carnitine palmitoyltransferase in hepatic mitochondria. Biochem J (1986) 237 593596CrossRefGoogle ScholarPubMed
Wilkinson, P, Leach, C, Ah-Sing, EE, Hussain, N, Miller, GJ, Millward, DJ & Griffin, BAInfluence of alpha-linolenic acid and fish-oil on markers of cardiovascular risk in subjects with an atherogenic lipoprotein phenotype. Atherosclerosis (2005) 181 115124CrossRefGoogle ScholarPubMed
Wilson, TA, Nicolosi, RJ, Lawton, CW & Babiak, JGender differences in response to a hypercholesterolemic diet in hamsters:effects on plasma lipoprotein cholesterol concentrations and early aortic atherosclerosis. Atherosclerosis (1999) 146 8391CrossRefGoogle ScholarPubMed
Xu, HE, Lambert, MH & Montana, VGet al.. Molecular recognition of fatty acids by peroxisome proliferator-activated receptors. Mol Cell (1999) 3 397403CrossRefGoogle ScholarPubMed
Xu, J, Cho, H, O'Malley, S, Park, JH & Clarke, SDDietary polyunsaturated fats regulate rat liver sterol regulatory element binding proteins-1 and -2 in three distinct stages and by different mechanisms. J Nutr (2002) 132 33333339CrossRefGoogle ScholarPubMed
Zuckerman, SH & Evans, GFCholesteryl ester transfer protein inhibition in hypercholesterolemic hamsters: kinetics of apoprotein changes. Lipids (1995) 30 307311CrossRefGoogle ScholarPubMed