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The differential hepatic uptake of chylomicron remnants of different fatty acid composition is not mediated by hepatic lipase

Published online by Cambridge University Press:  09 March 2007

Marc S. Lambert
Affiliation:
Department of Veterinary Basic Sciences, The Royal Veterinary College, Royal College St, London NW1 0TU, UK
Michael A. Avell
Affiliation:
Department of Veterinary Basic Sciences, The Royal Veterinary College, Royal College St, London NW1 0TU, UK
Yoel Berhane
Affiliation:
Department of Veterinary Basic Sciences, The Royal Veterinary College, Royal College St, London NW1 0TU, UK
Elaine Shervill
Affiliation:
Department of Veterinary Basic Sciences, The Royal Veterinary College, Royal College St, London NW1 0TU, UK
Kathleen M. Botham*
Affiliation:
Department of Veterinary Basic Sciences, The Royal Veterinary College, Royal College St, London NW1 0TU, UK
*
*Corresponding author: Dr Kathleen M. Botham, fax +44 (0) 207 388 1027, email kbotham@rvc.ac.uk
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Abstract

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The hypothesis that hepatic lipase mediates the differential hepatic uptake of chylomicron remnants of different fatty acid composition, demonstrated in previous work from our laboratory, was tested by investigating the effect of antibodies to the enzyme on the uptake of remnants enriched with saturated or n-3 polyunsaturated fatty acids by the perfused rat liver. After perfusion of rat livers with polyclonal antibodies to rat hepatic lipase raised in rabbits or with rabbit non-immune serum for 15 min, [3H]oleate-labelled chylomicron remnants, derived from chylomicrons of rats given a bolus of either palm (rich in saturated fatty acids) oil or fish (rich in n-3 polyunsaturated fatty acids) oil, were added. The disappearance of radioactivity from the perfusate during 120 min and its recovery in the liver at the end of the experiments were then measured. Although the rabbit anti-rat hepatic lipase antiserum was shown to inhibit hepatic lipase activity by up to 90 %, and to bind extensively to hepatic sinusoidal surfaces when added to the perfusate, radioactivity from remnants of chylomicrons from rats given a bolus of fish oil as compared with palm oil disappeared from the perfusate and appeared in the liver more rapidly in the presence both the antiserum and the non-immune serum, and the differences between the uptake of the two types of remnants were similar. We conclude, therefore, that differential interaction with hepatic lipase is not responsible for the differences in the rate of removal of chylomicron remnants of different fatty acid composition from the blood.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2001

References

Amar, MJ, Dugi, KA, Haudenschild, CC, Shamburek, RD, Chase, M, Bensadoun, A, Hoyt, RF, Brewer, HB & Santamarina-Fojo, S (1998) Hepatic lipase facilitates the selective uptake of cholesteryl esters from remnant lipoproteins in apoE-deficient mice. Journal of Lipid Research 39, 24362442.CrossRefGoogle ScholarPubMed
Borensztajn, J, Getz, GS & Kotlar, TJ (1988) Uptake of chylomicron remnants by the liver: further evidence for the modulating role of phospholipids.Journal of Lipid Research 29, 10871096.CrossRefGoogle ScholarPubMed
Botham, KM, Mayes, PA, Avella, M, Cantafora, A & Bravo, E (1995) Comparison of the lipolysis of chylomicron remnants derived from corn oil and olive oil by hepatic lipase. Biochemical Society Transactions 23, 284S.CrossRefGoogle ScholarPubMed
Botham, KM, Mayes, PA, Avella, M, Cantafora, A & Bravo, E (1997) The lipolysis of chylomicrons derived from different dietary fats by lipoprotein lipase in vitro Biochimica et Biophysica Acta 1349, 257263.CrossRefGoogle ScholarPubMed
Brasaemle, DL, Cornely-Moss, K & Bensadoun, A (1993) Hepatic lipase treatment of chylomicron remnants increases exposure of apolipoprotein E. Journal of Lipid Research 34, 455465.CrossRefGoogle ScholarPubMed
Bravo, E, Ortu, G, Cantafora, A, Lambert, MS, Avella, M, Mayes, PA & Botham, KM (1995) Comparison of the hepatic uptake and processing of cholesterol from chylomicrons of different fatty acid composition in the rat in vivo Biochimica et Biophysica Acta 1258, 328336.CrossRefGoogle ScholarPubMed
Breedveld, B, Schoonderwoerd, K, Verhoeven, AJ, Willemsen, R & Jansen, H (1997) Hepatic lipase is localized at the parenchymal cell microvilli in rat liver. Biochemical Journal 321, 425430.CrossRefGoogle ScholarPubMed
Brouwer, CB, De Bruin, TW, Jansen, H & Erkelens, DW (1993) Different clearance of intravenously administered olive oil and soybean oil emulsions: role of hepatic lipase. American Journal of Clinical Nutrition 57, 533539.CrossRefGoogle ScholarPubMed
Chappell, DA & Medh, JD (1998) Receptor-mediated mechanisms of lipoprotein remnant uptake. Progress in Lipid Research 37, 393422.CrossRefGoogle Scholar
Connelly, PW, Maguire, GF, Lee, M & Little, JA (1990) Plasma lipoproteins in familial hepatic lipase deficiency. Arteriosclerosis 10, 4048.CrossRefGoogle ScholarPubMed
Cooper, AD (1997) Hepatic uptake of chylomicron remnants. Journal of Lipid Research 38, 21732192.CrossRefGoogle ScholarPubMed
Crawford, SE & Borensztajn, J (1999) Plasma clearance and liver uptake of chylomicron remnants generated by hepatic lipase lipolysis: evidence for a lactoferrin-sensitive and apolipoprotein E-independent pathway. Journal of Lipid Research 40, 797805.CrossRefGoogle ScholarPubMed
Daggy, BP & Bensadoun, A (1986) Enrichment of apolipoprotein-B48 in the low density lipoprotein density class following in vivo inhibition with hepatic lipase. Biochimica et Biophysica Acta 877, 252261.CrossRefGoogle ScholarPubMed
Derewenda, ZS & Cambillau, C (1991) Effects of gene mutations in lipoprotein and hepatic lipase as interpreted by a molecular model of the pancreatic triglyceride lipase. Journal of Biological Chemistry 266, 2311223119.CrossRefGoogle ScholarPubMed
Diard, P, Malewiak, M-I, Lagrange, D & Griglio, S (1994) Hepatic lipase may act as a ligand in the uptake of artificial chylomicron remnant-like particles by isolated rat hepatocytes. Biochemical Journal 299, 889894.CrossRefGoogle ScholarPubMed
Fan, J & Watanabe, T (1998) Hepatic lipase. Journal of Atherosclerosis and Thrombosis 5, 4145.CrossRefGoogle ScholarPubMed
Grieve, DJ, Avella, MA, Botham, KM & Elliott, J (1998 a) Effects of chylomicrons and chylomicron remnants on endothelium-dependent relaxation of rat aorta. European Journal of Pharmacology 348, 181190.CrossRefGoogle ScholarPubMed
Grieve, DJ, Avella, MA, Elliott, J & Botham, KM (1998 b) Influence of chylomicron remnants on endothelial cell function in the isolated perfused rat aorta. Atherosclerosis 139, 273281.CrossRefGoogle ScholarPubMed
Grieve, DJ, Avella, MA, Elliott, J & Botham, KM (2000) The interaction between oxidised chylomicron remnants and the aorta of rats fed a normocholesterolaemic or hypercholesterolaemic diet. Journal of Vascular Research 37, 265275.CrossRefGoogle ScholarPubMed
Goldstein, JL, Ho, YK, Brown, MS, Innerarity, TL & Mahley, RW (1980) Cholesteryl ester accumulation in macrophages resulting from receptor-mediated uptake and degradation of hypercholesterolemic canine β-very low density lipoproteins. Journal of Biological Chemistry 255, 18391848.CrossRefGoogle ScholarPubMed
Harris, WS (1989) Fish oils and plasma lipids and lipoprotein metabolism in humans: a critical review. Journal of Lipid Research 30, 785807.CrossRefGoogle ScholarPubMed
Ji, Z-S, Lauer, SJ, Fazio, S, Bensadoun, A, Taylor, JM & Mahley, RW (1994) Enhanced binding and uptake of remnant lipoproteins by hepatic lipase-secreting hepatoma cells in culture. Journal of Biological Chemistry 269, 1342913436.CrossRefGoogle ScholarPubMed
Ji, Z-S, Sanan, DA & Mahley, RW (1995) Intravenous heparinase inhibits remnant lipoprotein clearance from the plasma and uptake by the liver: in vivo role of heparan sulfate proteoglycans. Journal of Lipid Research 36, 583592.CrossRefGoogle ScholarPubMed
Kirchgessner, TG, Chuat, J-C, Heinzmann, C, Etienne, J, Guilhot, S, Svenson, K, Ameis, D, Pilon, C, D'Auriol, L, Andalibi, A, Schotz, MC, Galibert, F & Lusis, AJ (1989) Organisation of the human lipoprotein lipase gene family and evolution of the lipase gene family. Proceedings of the National Academy of Sciences USA 86, 96479651.CrossRefGoogle ScholarPubMed
Lambert, MS, Avella, MA, Berhane, Y, Shervill, E & Botham, KM (1999) The fatty acid composition of chylomicron remnants can alter their interaction with receptors on isolated hepatocytes. Atherosclerosis 144(Suppl. 1), 111112.CrossRefGoogle Scholar
Lambert, MS, Botham, KM & Mayes, PA (1995) Variations in composition of dietary fats affect hepatic uptake and metabolism of chylomicron remnants. Biochemical Journal 310, 845852.CrossRefGoogle ScholarPubMed
Lambert, MS, Botham, KM & Mayes, PA (1996) Modification of the composition of dietary oils and fats upon incorporation into chylomicron remnants. British Journal of Nutrition 76, 435445.CrossRefGoogle ScholarPubMed
Mahley, RW, Innerarity, TL, Brown, MS, Ho, YK & Goldstein, JL (1980) Cholesteryl ester synthesis in macrophages: stimulation by β-very low density lipoproteins from cholesterol-fed animals of several species. Journal of Lipid Research 21, 970980.CrossRefGoogle ScholarPubMed
Mamo, JCL (1995) Atherosclerosis is a post-prandial disease. Endocrinology and Metabolism 2, 229244.Google Scholar
Mattson, FH & Grundy, SM (1985) Comparison of the effects of saturated, monounsaturated and polyunsaturated fatty acids on plasma lipids and lipoproteins in man. Journal of Lipid Research 26, 684689.CrossRefGoogle ScholarPubMed
Patsch, JR, Miesenbock, G, Hopferwieser, V, Knapp, E, Dunn, JK, Gotto, AM & Patsch, W (1992) The relationship of triglyceride metabolism and coronary artery disease. Studies in the postprandial state. Arteriosclerosis and Thrombosis 12, 13361345.CrossRefGoogle Scholar
Proctor, SD & Mamo, JC (1998) Retention of fluorescent-labelled chylomicron remnants within the intima of the arterial wall – evidence that plaque cholesterol may be derived from post prandial lipoproteins. European Journal of Clinical Investigation 28, 379384.CrossRefGoogle ScholarPubMed
Redgrave, TG (1983) Formation and metabolism of chylomicrons. International Review of Physiology 28, 103129.Google ScholarPubMed
Rohlmann, A, Gotthardt, M, Hammer, RE & Herz, J (1998) Inducible inactivation of hepatic LRP by Cre-mediated recombination confirms role of LRP in clearance of chylomicron remnants. Journal of Clinical Invesigation 101, 689695.CrossRefGoogle ScholarPubMed
Shafi, S, Brady, SE, Bensadoun, A & Havel, JR (1994) Role of hepatic lipase in the uptake and processing of chylomicron remnants in rat liver. Journal of Lipid Research 35, 709720.CrossRefGoogle ScholarPubMed
Sultan, F, Lagrange, D, Jansen, H & Griglio, S (1990) Inhibition of hepatic lipase impairs chylomicron remnant-removal in rats. Biochimica et Biophysica Acta 1042, 150152.CrossRefGoogle ScholarPubMed
Truswell, AS (1985) Reducing the risk of coronary heart disease. British Medical Journal 291, 3437.CrossRefGoogle ScholarPubMed
van Lenten, BJ, Fogelman, AM, Jackson, RL, Shapiro, S, Haberland, ME & Edwards, PA (1985) Receptor-mediated uptake of remnant lipoproteins by cholesterol-laden human monocyte-macrophages. Journal of Biological Chemistry 260, 8783–8788.Google Scholar