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Uptake of triacylglycerol-rich lipoproteins of differing triacylglycerol molecular species and unsaponifiable content by liver cells

Published online by Cambridge University Press:  08 March 2007

Javier S. Perona ,
Michael Avella ,
Kathleen M. Botham  and
Valentina Ruiz-Gutierrez
Javier S. Perona
Affiliation:
Instituto de la Grasa (CSIC)Av. Padre Garcia Tejero4.41012 Seville, Spain.
Michael Avella
Affiliation:
Royal Veterinary CollegeRoyal College StreetLondon, NW1 0TU UK
Kathleen M. Botham
Affiliation:
Royal Veterinary CollegeRoyal College StreetLondon, NW1 0TU UK
Valentina Ruiz-Gutierrez*
Affiliation:
Instituto de la Grasa (CSIC)Av. Padre Garcia Tejero4.41012 Seville, Spain.
*
*Corresponding author: Dr Valentina Ruiz-Gutierrez, fax +34 95461679, email valruiz@ig.csic.es
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Abstract

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The fatty acid composition of dietary oils can modulate the incorporation of triacylglycerol-rich lipoproteins (TRL) into hepatocytes, thus affecting the atherogenicity of these particles. However, nothing is known about the effect of the unsaponifiable fraction of the oils. In the present study, we evaluated the influence of these components on the uptake of TRL by rat primary hepatocytes. TRL were isolated from human serum after the intake of meals enriched in high-oleic sunflower oil (HOSO), virgin olive oil (VOO) or VOO enriched in its own unsaponifiable fraction (EVO). HOSO and HOSO-TRL differed from VOO and EVO and their corresponding TRL in the composition of triacylglycerol molecular species and of the unsaponifiable fraction. Furthermore, the increase in the unsaponifiable fraction of VOO led to changes in the triacylglycerol molecular species in the EVO-TRL. On incubation with hepatocytes, HOSO-TRL were taken up at a faster rate than VOO-TRL or EVO-TRL. In addition, in comparison to VOO-TRL, HOSO-TRL increased the expression of mRNA for the LDL receptor-related protein receptor, which plays an important role in the internalisation of remnant lipoproteins. EVO-TRL also increased LDL receptor-related protein mRNA expression in comparison with VOO-TRL, but this change was not accompanied by a rise in the uptake rate, suggesting that the unsaponifiable fraction of VOO may inhibit LDL receptor-related protein expression or activity post-transcriptionally. In conclusion, TRL from dietary oils with differing triacylglycerol molecular species and unsaponifiable fraction content are taken up by liver cells at different rates, and this may be important in the atherogenicity of these particles.

Keywords

LiverOlive oilTriacylglycerolTriacylglycerol-rich lipoproteinUptake
Type
Research Article
Information
British Journal of Nutrition , Volume 95 , Issue 5 , May 2006 , pp. 889 - 897
Copyright
Copyright © The Nutrition Society 2006

References

Abia, RPacheco, YMPerona, JSMontero, EMuriana, FJ&Ruiz-Gutierrez, VThe metabolic availability of dietary triacylglycerols from two high oleic oils during the postprandial period does not depend on the amount of oleic acid ingested by healthy men J Nutr 2001 131 59–65CrossRefGoogle Scholar
Abia, RPerona, JSPacheco, YMMontero, EMuriana, FJ &Ruiz-Gutierrez, VPostprandial triacylglycerols from dietary virgin olive oil are selectively cleared in humans. J Nutr 1999 129 2184–2191CrossRefGoogle ScholarPubMed
Batt, KVPatel, LBotham, KM&Suckling, KEChylomicron remnants and oxidised low density lipoprotein have differential effects on the expression of mRNA for genes involved in human macrophage foam cell formation. J Mol Med 2004 82 449–458CrossRefGoogle ScholarPubMed
Borensztajn, J&Kotlar, TJPhospholipids as modulators of hepatic recognition of chylomicron remnants. Observations with emulsified lipoprotein lipids Biochem J 1990 269 539–542CrossRefGoogle ScholarPubMed
Botham, KMAvella, MCantafora, A&Bravo, EThe lipolysis of chylomicrons derived from different dietary fats by lipoprotein lipase in vitro Biochim Biophys Acta 1997 1349 257–263CrossRefGoogle ScholarPubMed
Bravo, EOrtu, GCantafora, ALambert, MSAvella, MMayes, PA &Botham, KMComparison of the hepatic uptake and processing of cholesterol from chylomicrons of different fatty acid composition in the rat in vivo. Biochim Biophys Acta 1995 1258 328–336CrossRefGoogle ScholarPubMed
Cooper, ADHepatic uptake of chylomicron remnants. J Lipid Res. 1997 38 2173–2192CrossRefGoogle ScholarPubMed
Crawford, SE&Borensztajn, JPlasma clearance and liver uptake of chylomicron remnants generated by hepatic lipase lipolysis: evidence for a lactoferrin-sensitive and apolipoprotein E-independent pathway. J Lipid Res 1999 40 797–805CrossRefGoogle ScholarPubMed
de la Puerta, R&Martinez-Dominguez, ERuiz-Gutierrez, VEffect of minor components of virgin olive oil on topical antiinflammatory assays. Z Naturforsch 2000 55 814–819CrossRefGoogle ScholarPubMed
Dietschy, JMDietary fatty acids and the regulation of plasma low density lipoprotein cholesterol concentrations. J Nutr 1998 128 444S–448SCrossRefGoogle ScholarPubMed
Folch, JLess, M&Sloan Stanley, GHA simple method for the isolation and purification of total lipids from the animal tissues. J Biol Chem 1957 33 497–509CrossRefGoogle Scholar
Ford, RPBotham, KMSuckling, RP&Boyd, GSCharacterisation of rat hepatocyte monolayers for investigation of the metabolism of bile salts. Biochim Biophys Acta 1985 836 185–191CrossRefGoogle Scholar
Friedewald, WTLevy, RI&Fredrickson, DSEstimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge Clin Chem 1972 18 499–502CrossRefGoogle ScholarPubMed
Grieve, DJAvella, MABotham, KM&Elliott, JChylomicron remnants potentiate phenylephrine-induced contractions of rat aorta by an endothelium-dependent mechanism. Atherosclerosis 2000 151 471–480CrossRefGoogle ScholarPubMed
Grieve, DJAvella, MAElliott, J&Botham, KMThe influence of chylomicron remnants on endothelial cell function in the isolated perfused rat aorta Atherosclerosis 1998 139 273–281CrossRefGoogle ScholarPubMed
Isusi, EAspicheta, PLiza, MHernandez, MLDiaz, CMartinez, MJ &Ochoa, BShort and long term effects of atrovastatin, lovastatin and simvastatin on the cellular metabolism of cholesteryl esters and VLDL secretion in rat hepatocytes. Atherosclerosi 2000 153 283–294CrossRefGoogle Scholar
Jansen, H&Hulsmann, WCEnzymology and physiological role of hepatic lipase Biochem Soc Trans 1985 13 24–26CrossRefGoogle ScholarPubMed
Ji, Z-SFazio, SLee, YL&Mahley, RWSecretion-capture role for apolipoprotein E in remnant lipoprotein metabolism involving cell surface heparan sulfate proteoglycans J Biol Chem 1993 269 2764–2772.CrossRefGoogle Scholar
Keys, A, Menotti, A, Karvonen, MJet al.. The diet and 15-year death rate in the seven countries study. Am J Epidemiol 1986 124 903915.CrossRefGoogle ScholarPubMed
Lambert, MS, Avella, MA, Berhane, Y, Shervill, E & Botham, KMThe fatty acid composition of chylomicron remnants influences their binding and internalization by isolated hepatocytes. Eur J Biochem 2001 268, 3983 – 3992.CrossRefGoogle ScholarPubMed
Lambert, MS, Botham, KM & Mayes, PAVariations in composition of dietary fats affect hepatic uptake and metabolism of chylomicron remnants. Biochem J 1995 310, 845 – 852.CrossRefGoogle ScholarPubMed
Mamo, JC & Wheeler, JRChylomicrons or their remnants penetrate rabbit thoracic aorta as efficiently as do smaller macromolecules, including low-density lipoprotein, high-density lipoprotein, and albumin. Coron Artery Dis 1994 5, 695 – 705.CrossRefGoogle ScholarPubMed
Napolitano, M, Avella, M, Botham, KM & Bravo, EChylomicron remnant induction of lipid accumulation in J774 macrophages is associated with up-regulation of triacylglycerol synthesis which is not dependent on oxidation of the particles. Biochim Biophys Acta 2003 1631, 255 – 264.CrossRefGoogle Scholar
Nicolosi, RJDietary fat saturation effects on low-density-lipoprotein concentrations and metabolism in various animal models. Am J Clin Nutr 1997 65, Suppl., 1617S – 1627S.CrossRefGoogle ScholarPubMed
Ochoa, JJ, Quiles, JL, Ramirez-Tortosa, MC, Mataix, J, & Huertas, JRDietary oils high in oleic acid but with different unsaponifiable fraction contents have different effects in fatty acid composition and peroxidation in rabbit LDL. Nutrition 2002 18, 60 – 65.CrossRefGoogle ScholarPubMed
Pal, S, Thomson, AM, Bottema, CD & Roach, PDAlpha-tocopherol modulates the low density lipoprotein receptor of human HepG2 cells. Nutr J 2003 2, 3CrossRefGoogle ScholarPubMed
Pedersen, A, Baumstark, MW, Marckmann, P, Gylling, H, & Sandstrom, B\ An olive oil-rich diet results in higher concentrations of LDL cholesterol and a higher number of LDL subfraction particles than rapeseed oil and sunflower oil diets. J Lipid Res 2000 41, 1901 – 1911.CrossRefGoogle Scholar
Perona, JS, Martinez-Gonzalez, J, Sanchez-Dominguez, JM, Badimon, L & Ruiz-Gutierrez, VThe unsaponifiable fraction of virgin olive oil in chylomicrons from men improves the balance between vasoprotective and prothrombotic factors released by endothelial cells. J Nutr 2004 134, 3284 – 3289.CrossRefGoogle ScholarPubMed
Perona, JS & Ruiz-Gutiérrez, VCharacterization of the triacylglycerol molecular species of fish oil by reversed-phase high-performance liquid chromatography. J Liquid Chromatogr 1999 22, 1699 – 1714.CrossRefGoogle Scholar
Perona, JS & Ruiz-Gutierrez, VQuantification of major lipid classes in human triacylglycerol-rich lipoproteins by high-performance liquid chromatography with evaporative light-scattering detection. J Sep Sci 2004 27, 653 – 659.CrossRefGoogle ScholarPubMed
Redgrave, TG, Kodali, DR & Small, DMThe effect of triacylsn-glycerol structure on the metabolism of chylomicrons and triacylglycerol emulsions in the rat. J Biol Chem 1988 263, 5118 – 5123.CrossRefGoogle Scholar
Relas, H, Gylling, H & Miettinen, TADietary squalene increases cholesterol synthesis measured with serum non-cholesterol sterols after a single oral dose in humans. Atherosclerosis 2000 152, 377 – 383.CrossRefGoogle ScholarPubMed
Rohlmann, A, Gotthardt, M, Hammer, RE & Herz, JInducible inactivation of hepatic LRP gene by cre-mediated recombination confirms role of LRP in clearance of chylomicron remnants. J Clin Invest 1998 101, 689 – 695.CrossRefGoogle ScholarPubMed
Sato, K, Takahashi, T, Takahashi, Y, Shiono, H & Akiba, YPreparation of chylomicron and VLDL with monoacid-rich triacylglycerol and characterization of kinetic parameters in lipoprotein lipase-mediated hydrolysis in chickens. J Nutr 1999 129, 126 – 131.CrossRefGoogle ScholarPubMed
Sato, K, Takahashi, Y, Takahashi, T, Katoh, N & Akiba, YIdentification of factors regulating lipoprotein lipase catalyzed hydrolysis in rats with the aid of monoacid-rich lipoprotein preparations. J Nutr Biochem 2002 13, 528 – 538.CrossRefGoogle ScholarPubMed
Spady, DK, Horton, JD & Cuthbert, JARegulatory effects of n-3 polyunsaturated fatty acids on hepatic LDL uptake in the hamster and rat. J Lipid Res 1995 3636, 1009 – 1020.CrossRefGoogle Scholar
Vasandani, C, Kafrouni, AI, Caronna, A, Bashmakov, Y, Gotthardt, M, Horton, JD & Spady, DKUpregulation of hepatic LDL transport by n-3 fatty acids in LDL receptor knockout mice. J Lipid Res 2002 43, 772 – 784.CrossRefGoogle ScholarPubMed
Wang, CS, Hartsuck, J & McConathy, WJStructure and functional properties of lipoprotein lipase. Biochim Biophys Acta 1992 1123, 1 – 17.CrossRefGoogle ScholarPubMed
Wilhelm, MG, Cooper, ADInduction of atherosclerosis by human chylomicron remnants: a hypothesis. J Atheroscler Thromb 2003 10, 132 – 139.CrossRefGoogle ScholarPubMed
Zeng, BJ, Mortimer, BC, Martins, IJ, Seydel, U & Redgrave, TGChylomicron remnant uptake is regulated by the expression and function of heparan sulfate proteoglycan in hepatocytes. J Lipid Res 1998 39, 845 – 860.CrossRefGoogle ScholarPubMed
Zheng, X, Rivabene, R, Cavallari, CNapolitano, M, Avella, M, Bravo, E, & Botham, KMThe effects of chylomicron remnants enriched in n-3 or n-6 polyunsaturated fatty acids on the transcription of genes regulating their uptake and metabolism by the liver: influence of cellular oxidative state. Free Radic Biol Med 2002 32, 1123 – 1131.CrossRefGoogle ScholarPubMed