Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-17T16:01:30.508Z Has data issue: false hasContentIssue false

Acute-on-chronic effects of fatty acids on intestinal triacylglycerol-rich lipoprotein metabolism

Published online by Cambridge University Press:  09 March 2007

Irene L. Black
Affiliation:
Unit of Nutrition, Department of Clinical Medicine, Trinity Health Sciences Centre, St. James's Hospital, Dublin 8, Ireland
Helen M. Roche*
Affiliation:
Unit of Nutrition, Department of Clinical Medicine, Trinity Health Sciences Centre, St. James's Hospital, Dublin 8, Ireland
Anne-Marie Tully
Affiliation:
Unit of Nutrition, Department of Clinical Medicine, Trinity Health Sciences Centre, St. James's Hospital, Dublin 8, Ireland
Michael J. Gibney
Affiliation:
Unit of Nutrition, Department of Clinical Medicine, Trinity Health Sciences Centre, St. James's Hospital, Dublin 8, Ireland
*
*Corresponding author: Dr Helen M. Roche, fax +353 1 4542043, 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.

Postprandial triacylglycerol (TAG) metabolism is an important metabolic state that has been associated with cardiovascular disease. The magnitude of the postprandial TAG response is determined by dietary fat composition, which alters intestinal and hepatic TAG-rich lipoprotein (TRL) metabolism. Caco-2 cell monolayers are morphologically and physiologically similar to the human intestinal enterocytes, hence they are a good model to study intestinal lipoprotein metabolism. To date only the acute effect of fatty acid composition on intestinal TRL metabolism in Caco-2 cells has been investigated. Little is known of the effect of habitual, or chronic, dietary fat composition on intestinal TRL metabolism. Using the Caco-2 cell model, the present study investigated the acute-on-chronic effect of fatty acid composition on TRL metabolism. Caco-2 cells were grown in the presence of 0·05 mM-PALMITIC ACID (PA; 16 : 0), -OLEIC ACID (OA; 18 : 1N-9),-EICOSAPENTAENOIC ACID (EPA; 20 : 5N-3) OR NO FATTY ACID (CONTROL) FOR 19 D, THEN ONE OF FOUR ACUTE TREATMENTS (CONTROL (BOVINE SERUM ALBUMIN (BSA; 5 G/L)) OR BSA (5 G/L) PLUS 0·5 Mm-PA, -OA or -EPA) were administered for 22 h. Significant acute×chronic interactions for the effect of fatty acid composition on cellular TAG:secreted de novo TAG, and cellular de novo TAG:de novo phospholipid were observed. Thus the effect of a fatty acid was determined by the duration of exposure to the fatty acid intervention. Acute PA treatment increased de novo TAG synthesis, but chronic PA supplementation did not. Acute and chronic OA treatments increased de novo TAG secretion. For EPA, chronic supplementation had the greatest effect on TAG synthesis and secretion. The acute-on-chronic effects of fatty acids on apolipoprotein B metabolism were relatively minor compared with the changes noted for TRL lipid composition. The present study shows that the Caco-2 cell model is valuable for studying intestinal TRL metabolism and that fatty acids modulate this process, the nature of which can be determined by the length of exposure of the cell to the fatty acid.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2002

References

Arrol, S, Mackness, MI & Durrington, PN (2000) The effects of fatty acids on apolipoprotein B secretion by human hepatoma cells (HepG2). Atherosclerosis 150, 255264.CrossRefGoogle Scholar
Field, FJ, Albright, E & Mathur, SN (1988) Regulation of triglyceride-rich lipoprotein secretion by fatty acids in Caco-2 cells. Journal of Lipid Research 29, 14271437.CrossRefGoogle ScholarPubMed
Gibney, MJ & Daly, E (1994) The incorporation of n-3 polyunsaturated fatty acids into plasma lipid and lipoprotein fractions in the postprandial phase in healthy volunteers. European Journal of Clinical Nutrition 48, 866872.Google ScholarPubMed
Harris, WS, Connor, WE, Illingworth, DR, Rothrock, DW & Foster, DM (1990) Effects of fish oil on VLDL kinetics in humans. Journal of Lipid Research 31, 15491558.CrossRefGoogle ScholarPubMed
Karpe, F, Olivecrona, T, Hamsten, A & Hultin, M (1997) Chylomicron remnant turnover in humans: evidence for margination of chylomicrons and poor conversion of larger to smaller chylomicron remnants. Journal of Lipid Research 38, 949961.CrossRefGoogle ScholarPubMed
Karpe, F, Steiner, G, Uffelman, K, Olivercrona, T & Hamsten, A (1994) Postprandial lipoproteins and progression of coronary atherosclerosis. Atherosclerosis 106, 8397.CrossRefGoogle ScholarPubMed
Levy, E, Mehran, M & Seidman, E (1995) Caco-2 cells as a model for intestinal lipoprotein synthesis and secretion. FASEB Journal 9 626635.CrossRefGoogle Scholar
Moberly, JB, Cole, TG, Alpers, DH & Schonfeld, G (1990) Oleic acid stimulation of apolipoprotein B secretion from HepG2 and Caco-2 cells occurs post-transcriptional. Biochimica et Biophysica Acta 1042, 7080.CrossRefGoogle Scholar
Murthy, S, Albright, E, Mathur, SN & Field, FJ (1990) Effect of eicosapentaenoic acid on triacylglycerol transport in Caco-2 cells. Biochimica et Biophysica Acta 1045, 147155.CrossRefGoogle ScholarPubMed
Murthy, S, Born, E, Mathur, S & Field, FJ (1998) 13-Hydroxy octadecadienoic acid (13-HODE) inhibits triacylglycerol-rich lipoprotein secretion by Caco-2 cells. Journal of Lipid Research 39, 12541262.CrossRefGoogle ScholarPubMed
Patsch, JR, Miesenbock, G, Hopferwieser, T, Muhlberger, V, Knapp, E, Dunn, JK, Gotto, AM & Patsch, W (1992) Relation of triglyceride metabolism and coronary artery disease. Arteriosclerosis and Thrombosis 12, 13361345.CrossRefGoogle ScholarPubMed
Ranheim, T, Gedde-Dahl, A, Rustan, AC & Drevon, CA (1992) Influence of eicosapentaenoic acid (20:5, n-3) on secretion of lipoproteins in Caco-2 cells. Journal of Lipid Research 33, 12811293.CrossRefGoogle Scholar
Roche, HM & Gibney, MJ (1995) Postprandial triacylglycerolaemia – Nutritional Implications. Progress in Lipid Research 34, 249266.CrossRefGoogle ScholarPubMed
Roche, HM & Gibney, MJ (1996) Postprandial triacylglycerolaemia: The effect of a low-fat diet with and without fish oil supplementation. European Journal of Clinical Nutrition 50, 617624.Google ScholarPubMed
Roche, HM & Gibney, MJ (1997) Postprandial coagulation factor VII activity: the effect of monounsaturated fatty acids. British Journal of Nutrition 77, 537549.CrossRefGoogle ScholarPubMed
Roche, HM & Gibney, MJ (2000) The effect of long-chain n-3 PUFA on fasting and postprandial triacylglycerol metabolism. American Journal of Clinical Nutrition 71, 232237.CrossRefGoogle ScholarPubMed
Roche, HM, Terres, AM, Black, IL, Gibney, MJ & Kelleher, D (2001) Fatty acids and epithelial permeability: effect of conjugated linoleic acid in Caco-2 cells. Gut 48, 797802.CrossRefGoogle ScholarPubMed
Roche, HM, Zampelas, A, Jackson, KG, Williams, CM & Gibney, MJ (1998) The effect of test meal monounsaturated fatty acid:saturated fatty acid ratio on postprandial lipid metabolism. British Journal of Nutrition 79, 419424.CrossRefGoogle ScholarPubMed
Shishehbor, F, Roche, HM & Gibney, MJ (1998) The effect of acute carbohydrate load on the monophasic or biphasic nature of the postprandial lipaemic response of acute fat ingestion in human subjects. British Journal of Nutrition 80, 411418.CrossRefGoogle ScholarPubMed
Trotter, PJ & Storch, J (1993) Fatty acid esterification during differentiation of the human intestinal cell line Caco-2. Journal of Biological Chemistry 268, 1001710023.CrossRefGoogle ScholarPubMed
Van Greevenbroek, MMJ, Erkelens, DW & de Bruin, TWA (2000) Caco-2 cells secrete two independent classes of lipoproteins with distinct density: effect of the ratio of unsaturated to saturated fatty acid. Atherosclerosis 149, 2531.CrossRefGoogle ScholarPubMed
Van Greevenbroek, MMJ, Robertus-Tenissen, MG, Erkelens, DW & de Bruin, TWA (1998) Participation of the microsomal triglyceride transfer protein in lipoprotein assembly in Caco-2 cells: interaction with saturated and unsaturated dietary fatty acids. Journal of Lipid Research 39, 173185.CrossRefGoogle ScholarPubMed
Van Greevenbroek, MMJ, Van Meer, G, Erkelens, DW & de Bruin, TWA (1996) Effects of saturated, mono-, and polyunsaturated fatty acids on the secretion of apoB containing lipoproteins by Caco-2 cells. Atherosclerosis 121, 139150.CrossRefGoogle ScholarPubMed
Van Greevenbroek, MMJ, Voorhout, WF, Erkelens, DW, Van Meer, G & de Bruin, TWA (1995) Palmitic acid and linoleic acid metabolism in Caco-2 cells: different triglyceride synthesis and lipoprotein secretion. Journal of Lipid Research 36, 1324.CrossRefGoogle ScholarPubMed
Weintraub, MS, Grosskopf, I, Rassin, T, Miller, H, Charach, G, Rotmensch, HH, Liron, M, Rubinstein, A & Iaina, A (1996) Clearance of chylomicron remnants in normolipidemic patients with coronary artery disease: case control study over three years. British Medical Journal 312 936939.CrossRefGoogle Scholar
Zampelas, A, Murphy, M, Morgan, LM & Williams, CM (1994) Postprandial lipoprotein lipase, insulin and gastric inhibitory polypeptide responses to test meals of different fatty acid composition: comparison of saturated, n-6 and n-3 polyunsaturated fatty acids. European Journal of Clinical Nutrition 48, 849858.Google ScholarPubMed
Zampelas, A, Roche, H, Kapsokefalou, M, Knapper, JME, Jackson, KG, Pentaris, E, Tornatis, M, Hatzis, C, Gibney, MJ, Kafatos, A, Gould, BJ, Wright, J & Williams, CM (1998) Differences in postprandial lipaemic response between Northern and Southern Europeans. Atherosclerosis 139, 8393.CrossRefGoogle ScholarPubMed