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Replacing dietary fish oil by vegetable oils has little effect on lipogenesis, lipid transport and tissue lipid uptake in rainbow trout (Oncorhynchus mykiss)

Published online by Cambridge University Press:  08 March 2007

Nadège Richard ,
Sadasivam Kaushik ,
Laurence Larroquet ,
Stéphane Panserat  and
Geneviève Corraze
Nadège Richard
Affiliation:
UMR Nutrition Aquaculture Génomique, INRA Pôle Hydrobiologie, 64310 Saint Pée-sur-Nivelle, France
Sadasivam Kaushik
Affiliation:
UMR Nutrition Aquaculture Génomique, INRA Pôle Hydrobiologie, 64310 Saint Pée-sur-Nivelle, France
Laurence Larroquet
Affiliation:
UMR Nutrition Aquaculture Génomique, INRA Pôle Hydrobiologie, 64310 Saint Pée-sur-Nivelle, France
Stéphane Panserat
Affiliation:
UMR Nutrition Aquaculture Génomique, INRA Pôle Hydrobiologie, 64310 Saint Pée-sur-Nivelle, France
Geneviève Corraze*
Affiliation:
UMR Nutrition Aquaculture Génomique, INRA Pôle Hydrobiologie, 64310 Saint Pée-sur-Nivelle, France
*
*Corresponding author: Dr Geneviève Corraze, fax +33 5 59 54 51 52, email [email protected]
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Abstract

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In order to investigate the effects of dietary lipid sources on mechanisms involved in lipid deposition, two groups of rainbow trout were fed from first-feeding to the commercial size of 1kg (for 62 weeks) with two diets differing only by lipid source: 100% fish oil or 100% blend of vegetable oils (55% rapeseed oil, 30% palm oil, 15% linseed oil). The activities and levels of gene expression of lipogenic enzymes (fatty acid synthetase, glucose-6-phosphate dehydrogenase and malic enzyme) in liver and of lipoprotein lipase in perivisceral adipose tissue, white muscle and liver were determined. Transport of lipid was studied by determining lipid composition of plasma and lipoprotein classes. We also examined the clearance of LDL by assaying the level of LDL receptor gene expression in several tissues. Total replacement of dietary fish oil by the blend of vegetable oils did not affect growth of rainbow trout and did not modify muscle lipid content. Hepatic lipogenesis and lipid uptake in perivisceral adipose tissue, white muscle and liver were also not modified by dietary treatments. Diets containing the blend of vegetable oils induced a decrease in plasma cholesterol and LDL. In trout fed the vegetable oils diet, expression of LDL receptor gene in the liver was down-regulated.

Keywords

Lipid transportLipogenesisRainbow troutVegetable oils
Type
Research Article
Information
British Journal of Nutrition , Volume 96 , Issue 2 , August 2006 , pp. 299 - 309
Copyright
Copyright © The Nutrition Society 2006

References

Altschul, SF, Gish, W, Miller, W, Myers, EW, Lipman, DJ, Basic local alignment search tool. J Mol Biol (1990) 215 403–410.CrossRefGoogle ScholarPubMed
Alvarez, MJ, Diez, A, Lopez-Bote, C, Gallego, M, Bautista, JM, Short-term modulation of lipogenesis by macronutrients in rainbow trout (Oncorhynchus mykiss) hepatocytes. Br J Nutr (2000) 84 619–628.CrossRefGoogle ScholarPubMed
Amri, EZ, Teboul, L, Vannier, C, Grimaldi, PA, Ailhaud, G, Fatty acids regulate the expression of lipoprotein lipase gene and activity in preadipose and adipose cells. Biochem J (1996) 341 541–546.CrossRefGoogle Scholar
Armstrong, MJ, Carey, MC, Thermodynamic and molecular determinants of sterol solubilities in bile salt micelles. J Lipid Res (1987) 28 1144–1155.CrossRefGoogle ScholarPubMed
Babin, PJ, Vernier, JM, Plasma lipoproteins in fish. J Lipid Res (1989) 30 467–489.CrossRefGoogle ScholarPubMed
Baltzell, JK, Wooten, JT, Otto, DA, Lipoprotein lipase in rats fed fish oil: apparent relationship to plasma insulin levels. Lipids (1991) 26 289–294.CrossRefGoogle ScholarPubMed
Bautista, JM, Garrido-Pertierra, A, Soler, G, Glucose-6-phosphate dehydrogenase fromDicentrarchus labrax liver: kinetic mechanism and kinetics of NADPH inhibition. Biochim Biophys Acta (1998) 967 354–363.CrossRefGoogle Scholar
Bell, JG, McEvoy, J, Tocher, DR, McGhee, F, Campbell, PJ, Sargent, JR, Replacement of fish oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid compositions and hepatocyte fatty acid metabolism. J Nutr (2001) 131 1535–1543.CrossRefGoogle ScholarPubMed
Bell, JG, Henderson, RJ, Tocher, DR, McGhee, F, Dick, JR, Porter, A, Smullen, RP, Sargent, JR, Substituting fish oil with crude palm oil in the diet of Atlantic salmon (Salmo salar) affects muscle fatty acid composition and hepatic fatty acid metabolism. J Nutr (2002) 132 222–230.CrossRefGoogle ScholarPubMed
Bendiksen, EA, Berg, OK, Jobling, M, Arnesen, AM, Masoval, K, Digestibility, growth and nutrient utilisation of Atlantic salmon parr (Salmo salar L.) in relation to temperature, feed fat content and oil source. Aquaculture (2003) 224 283–299.CrossRefGoogle Scholar
Bengtsson-Olivecrona, G, Olivecrona, TAssay of lipoprotein lipase and hepatic lipase. In Lipoprotein Analysis PP. [Converse, C, Skinner, ER, editors]. Oxford: Oxford University Press (1992) 169–185.Google Scholar
Blake, WL, Clarke, SD, Suppression of rat hepatic fatty acid synthase and S14 gene transcription by dietary polyunsaturated fat. J Nutr (1990) 120 1727–1729.CrossRefGoogle ScholarPubMed
Bradford, MM, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem (1976) 72 248–254.CrossRefGoogle ScholarPubMed
Caballero, MJ, Obach, A, Rosenlund, G, Montero, D, Gisvold, M, Izquierdo, MS, Impact of different dietary lipid sources on growth, lipid digestibility, tissue fatty acid composition and histology of rainbow trout, Oncorhynchus mykiss. Aquaculture (2002) 214 253–271.CrossRefGoogle Scholar
Chang, NW, Wu, CT, Chen, FN, Huang, PC, High polyunsaturated and monounsaturated fatty acid to saturated fatty acid ratio increases plasma very low density lipoprotein lipids and reduces the hepatic hypertriglyceridemic effect of dietary cholesterol in rats. Nutr Res (2004) 24 73–83.CrossRefGoogle Scholar
Chapman, MJ, Goldstein, S, Mills, GL, Leger, C, Distribution and characterization of the serum lipoproteins and their apoproteins in the rainbow trout (Salmo gairdnerii). Biochemistry (1978) 17 4455–4464.CrossRefGoogle ScholarPubMed
Clarke, SD, Armstrong, MK, Jump, DB, Dietary polyunsaturated fats uniquely suppress rat liver fatty acid synthase and S14 mRNA content. J Nutr (1990) 120 225–231.CrossRefGoogle ScholarPubMed
Corraze, G, Kaushik, S, Lipids from marine and freshwater fish. Oléagineux Corps Gras Lipides (1999) 6 111–115.Google Scholar
Dias, J, Alvarez, MJ, Diez, A, Arzel, J, Corraze, G, Bautista, JM, Kaushik, SJ, Regulation of hepatic lipogenesis by dietary protein/energy in juvenile European seabass (Dicentrarchus labrax). Aquaculture (1998) 161 169–186.CrossRefGoogle Scholar
Dietschy, JM, Dietary fatty acids and the regulation of plasma low density lipoprotein cholesterol concentrations. J Nutr (1998) 128 444S–448S.CrossRefGoogle ScholarPubMed
Fernandez, ML, West, KL, Mechanisms by which dietary fatty acids modulate plasma lipids. J Nutr (2005) 135 2075–2078.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M, Sloane Stanley, GH, A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem (1957) 226 497–509.CrossRefGoogle ScholarPubMed
Fox, JC, McGill, HC jr, Carey, KD, Getz, GS, In vivo regulation of hepatic LDL receptor mRNA in the baboon. Differential effects of saturated and unsaturated fat. J Biol Chem (1987) 262 7014–7020.CrossRefGoogle ScholarPubMed
Gelineau, A, Corraze, G, Boujard, T, Larroquet, L, Kaushik, S, Relation between dietary lipid level and voluntary feed intake, growth, nutrient gain, lipid deposition and hepatic lipogenesis in rainbow trout. Reprod Nutr Dev (2001) 41 487–503.CrossRefGoogle ScholarPubMed
Gilman, CI, Leusch, FDL, Breckenridge, WC, MacLatchy, DL, Effects of a phytosterol mixture on male fish plasma lipoprotein fractions and testis P450scc activity. Gen Comparative Endocrinol (2003) 130 172–184.CrossRefGoogle ScholarPubMed
Gomez-Requeni, P, Mingarro, M, Kirchner, S, Calduch-Giner, JA, Medale, F, Corraze, G, Panserat, S, Martin, SAM, Houlihan, DF, Kaushik, SJ, Perez-Sanchez, J, Effects of dietary amino acid profile on growth performance, key metabolic enzymes and somatotropic axis responsiveness of gilthead sea bream (Sparus aurata). Aquaculture (2003) 220, 749–767.CrossRefGoogle Scholar
Greene, DHS, Selivonchick, DP, Effects of dietary vegetable, animal and marine lipids on muscle lipid and haematology of rainbow trout (Oncorhynchus mykiss). Aquaculture (1990) 89, 165–182.CrossRefGoogle Scholar
Grundy, SM, Denke, MA, Dietary influences on serum lipids and lipoproteins. J Lipid Res (1990) 31, 1149–1172.CrossRefGoogle ScholarPubMed
Guillou, A, Soucy, P, Khalil, M, Adambounou, L, Effects of dietary vegetable and marine lipid on growth, muscle fatty acid composition and organoleptic quality of flesh of brook charr (Salvelinus fontinalis). Aquaculture (1995) 136, 351–362.CrossRefGoogle Scholar
Higgins, DG, Sharp, PM, Fast and sensitive multiple sequence alignments on a microcomputer. Comput Appl Biosci (1998) 5 151–153.Google Scholar
Horton, JD, Cuthbert, JA, Spady, DK, Dietary fatty acids regulate hepatic low density lipoprotein (LDL) transport by altering LDL receptor protein and mRNA levels. J Clin Invest (1993) 92 743–749.CrossRefGoogle ScholarPubMed
Hsu, RY, Butterworth, PHW, Porter, JWPigeon liver fatty acid synthetase. inMethods of Enzymology, vol. 14, pp. (Lowenstein, JM,) New York: Academic Press. (1969 33–39.Google Scholar
Hung, SSO, Storebakken, T, Carbohydrate utilization by rainbow-trout is affected by feeding strategy. J Nutr (1994) 124 223–230.CrossRefGoogle ScholarPubMed
Izquierdo, MS, Obach, A, Arantzamendi, L, Montero, D, Robaina, L, Rosenlund, G, Dietary lipid sources for seabream and seabass: growth performance, tissue composition and flesh quality. Aquacult Nutr (2003) 9 397–407.CrossRefGoogle Scholar
Jeffery, NM, Yaqoob, P, Wiggins, D, Gibbons, GF, Newsholme, EA, Calder, PC, Characterization of lipoprotein composition in rats fed different dietary lipids and of the effects of lipoproteins upon lymphocyte proliferation. J Nutr Biochem (1996) 7 282–292.CrossRefGoogle Scholar
Kuo, P, Weinfeld, M, Loscalzo, J, Effect of membrane fatty acyl composition on LDL metabolism in Hep G2 hepatocytes. Biochemistry (1990) 29 6626–6632.CrossRefGoogle ScholarPubMed
Liang, XF, Ogata, HY, Oku, H, Effect of dietary fatty acids on lipoprotein lipase gene expression in the liver and visceral adipose tissue of fed and starved red sea bream Pagrus major. Comp Biochem Physiol A Mol Integr Physiol (2002 a) 132 913–919.CrossRefGoogle ScholarPubMed
Liang, XF, Ogata, HY, Oku, H, The effects of feeding condition and dietary lipid level on lipoprotein lipase gene expression in liver and visceral adipose tissue of red sea breamPagrus major. Comp Biochem Physiol A Mol Integr Physiol (2002 b) 131 335–342.CrossRefGoogle Scholar
Lie, O, Sandvin, A, Waagbo, R, Influence of dietary fatty acids on the lipid composition of lipoproteins in farmed Atlantic salmon (Salmo salar). Fish Physiol Biochem (1993) 12 249–260.CrossRefGoogle ScholarPubMed
Lin, H, Romsos, DR, Tack, PI, Leveille, GA, Influence of dietary lipid on lipogenic enzyme activities in coho salmon, Oncorhynchus kisutch (Walbaum). J Nutr (1977) 107 846–854.CrossRefGoogle ScholarPubMed
Lindberg, A, Olivecrona, G, Lipase evolution: trout, Xenopus and chicken have lipoprotein lipase and apolipoprotein C-II-like activity but lack hepatic lipase-like activity. Biochim Biophys Acta (1995) 1255 205–211.CrossRefGoogle ScholarPubMed
Matsuyama, H, Sato, K, Nakamura, Y, Suzuki, K & Akiba, YModulation of regulatory factors involved in cholesterol metabolism in response to feeding of pravastatin- or cholesterol-supplemented diet in chickens. Biochim Biophys Acta (2005) 1734, 136–142.CrossRefGoogle ScholarPubMed
Matvienko, OA, Lewis, DS, Swanson, M, Arndt, B, Rainwater, DL, Stewart, J & Alekel, DLA single daily dose of soybean phytosterols in ground beef decreases serum total cholesterol and LDL cholesterol in young, mildly hypercholesterolemic men. Am J Clin Nutr (2002) 76, 57–64.CrossRefGoogle ScholarPubMed
Menoyo, D, Lopez-Bote, CJ, Bautista, JM & Obach, AGrowth, digestibility and fatty acid utilization in large Atlantic salmon (Salmo salar) fed varying levels of n-3 and saturated fatty acids. Aquaculture (2003) 225, 295–307.CrossRefGoogle Scholar
Menoyo, D, Izquierdo, MS, Robaina, L, Gines, R, Lopez-Bote, CJ & Bautista, JMAdaptation of lipid metabolism, tissue composition and flesh quality in gilthead sea bream (Sparus aurata) to the replacement of dietary fish oil by linseed and soyabean oils. Br J Nutr (2004) 92, 41–52.CrossRefGoogle Scholar
Michaud, SE, Renier, GDirect regulatory effect of fatty acids on macrophage lipoprotein lipase: potential role of PPARs. Diabetes (2001) 50, 660–666.CrossRefGoogle ScholarPubMed
Moghadasian, MH & Frohlich, JJEffects of dietary phytosterols on cholesterol metabolism and atherosclerosis: clinical and experimental evidence. Am J Med (1999) 107, 588–594.CrossRefGoogle ScholarPubMed
Montalto, MB & Bensadoun, ALipoprotein lipase synthesis and secretion: effects of concentration and type of fatty acids in adipocyte cell culture. J Lipid Res (1993) 34, 397–407.CrossRefGoogle ScholarPubMed
Murphy, MC, Zampelas, A, Puddicombe, SM, Furlonger, NP, Morgan, LM & Williams, CMPretranslational regulation of the expression of the lipoprotein lipase (EC 3.1.1.34) gene by dietary fatty acids in the rat. Br J Nutr (1993) 70, 727–736.CrossRefGoogle ScholarPubMed
Mustad, VA, Ellsworth, JL, Cooper, AD, Kris-Etherton, PM & Etherton, TDDietary linoleic acid increases and palmitic acid decreases hepatic LDL receptor protein and mRNA abundance in young pigs. J Lipid Res (1996) 37, 2310–2323.CrossRefGoogle ScholarPubMed
National Research Council Nutrient Requirements of Fish. Washington, DC:. National Academy Press. (1993)Google Scholar
New, MB & Wijkstroem, UNUse of Fishmeal and Fish Oil in Aquafeeds. Futher Thoughts on the Fishmeal Trap. FAO Fisheries Circular no. Rome:. FAO 975,2002).Google Scholar
Normen, L, Dutta, P, Lia, A & Andersson, HSoy sterol esters and beta-sitostanol ester as inhibitors of cholesterol absorption in human small bowel. Am J Clin Nutr (2000) 71, 908–913.CrossRefGoogle ScholarPubMed
Ochoa, SMalic enzyme. In Methods of Enzymology, (Colowick, SP & Kaplan, NO, editors) New York:. Academic Press. (1955. vol11, pp 739–753.Google Scholar
Pfaffl, MW, Horgan, GW & Dempfle, LRelative expression software tool (REST ©)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res (2002) 30, 1–10.CrossRefGoogle Scholar
Phillips, KM, Ruggio, DM, Toivo, JI, Swank, MA & Simpkins, AHFree and esterified sterol composition of edible oils and fats. J Food Compost Anal (2002) 15, 123–142.CrossRefGoogle Scholar
Raclot, T, Groscolas, R, Langin, D & Ferre, PSite-specific regulation of gene expression by n-3 polyunsaturated fatty acids in rat white adipose tissues. J Lipid Res (1997) 38, 1963–1972.CrossRefGoogle ScholarPubMed
Regost, C, Arzel, J, Cardinal, M, Robin, J, Laroche, M & Kaushik, SJDietary lipid level, hepatic lipogenesis and flesh quality in turbot (Psetta maxima). Aquaculture (2001) 193, 291–309.CrossRefGoogle Scholar
Regost, C, Arzel, J, Robin, J, Rosenlund, G & Kaushik, SJTotal replacement of fish oil by soybean or linseed oil with a return to fish oil in turbot (Psetta maxima) –1. Growth performance, flesh fatty acid profile, and lipid metabolism. Aquaculture (2003) 217, 465–482.CrossRefGoogle Scholar
Rosenlund, G, Obach, A, Sandberg, MG, Standal, H & Tveit, KEffect of alternative lipid sources on long-term growth performance and quality of Atlantic salmon (Salmo salar L.). Aquacult Res (2001) 32, 323–328.CrossRefGoogle Scholar
Salati, LM & Amir-Ahmady, BDietary regulation of expression of glucose-6-phosphate dehydrogenase. Annu Rev Nutr (2001) 21, 121–140.CrossRefGoogle 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, 195–202.CrossRefGoogle ScholarPubMed
Shantha, NC, Ackman, RGNervonic acid versus tricosanoic acid as internal standards in quantitative gas chromatographic analyses of fish oil longer-chain n-3 polyunsaturated fatty acid methyl esters. J Chromatogr B Biomed Appl (1990) 533, 1–10.CrossRefGoogle ScholarPubMed
Sheridan, MALipid dynamics in fish: aspects of absorption, transportation, deposition and mobilization. Comp Biochem Physiol B Biochem Mol Biol (1988) 90, 679–690.CrossRefGoogle ScholarPubMed
Sorci-Thomas, M, Wilson, MD, Johnson, FL, Williams, DL & Rudel, LLStudies on the expression of genes encoding apolipoproteins B100 and B48 and the low density lipoprotein receptor in nonhuman primates. Comparison of dietary fat and cholesterol. J Biol Chem (1989) 264, 9039–9045.CrossRefGoogle ScholarPubMed
Spady, DK & Dietschy, JMInteraction of dietary cholesterol and triglycerides in the regulation of hepatic low density lipoprotein transport in the hamster. J Clin Invest (1988) 81, 300–309.CrossRefGoogle ScholarPubMed
Stabile, LP, Hodge, DL, Klautky, SA & Salati, LMPosttranscriptional regulation of glucose-6-phosphate dehydrogenase by dietary polyunsaturated fat. Arch Biochem Biophys (1996) 332, 269–279.CrossRefGoogle ScholarPubMed
Stabile, LP, Klautky, SA, Minor, SM & Salati, LMPolyunsaturated fatty acids inhibit the expression of the glucose-6-phosphate dehydrogenase gene in primary rat hepatocytes by a nuclear posttranscriptional mechanism. J Lipid Res (1998) 39, 1951–1963.CrossRefGoogle ScholarPubMed
Temme, EHM, Mensink, RP & Hornstra, GEffects of medium chain fatty acids (MCFA), myristic acid, and oleic acid on serum lipoproteins in healthy subjects. J Lipid Res (1997) 38, 1746–1754.CrossRefGoogle ScholarPubMed
Tocher, DRMetabolism and functions of lipids and fatty acids in teleost fish. Fish Sci (2003) 11, 107–184.Google Scholar
Torstensen, BE, Lie, O & Froyland, LLipid metabolism and tissue composition in Atlantic salmon (Salmo salar L.) – effects of capelin oil, palm oil, and oleic acid-enriched sunflower oil as dietary lipid sources. Lipids (2000) 35, 653–664.CrossRefGoogle ScholarPubMed
Torstensen, BE, Froyland, L & Lie, OReplacing dietary fish oil with increasing levels of rapeseed oil and olive oil –effects on Atlantic salmon (Salmo salar L.) tissue and lipoprotein lipid composition and lipogenic enzyme activities. Aquacult Nutr (2004) 10, 175–192.CrossRefGoogle Scholar
Vanstone, CA, Raeini-Sarjaz, M, Parsons, WE & Jones, PJUnesterified plant sterols and stanols lower LDL-cholesterol concentrations equivalently in hypercholesterolemic persons. Am J Clin Nutr (2002) 76, 1272–1278.CrossRefGoogle ScholarPubMed
Walzem, RL, Storebakken, T, Hung, SS & Hansen, RJRelationship between growth and selected liver enzyme activities of individual rainbow trout. J Nutr (1991) 121, 1090–1098.CrossRefGoogle ScholarPubMed
Watanabe, TLipid nutrition in fish. Comp Biochem Physiol B Biochem Mol Biol (1982) 273, 3–15.CrossRefGoogle Scholar
Zampelas, A, Murphy, M, Morgan, LM & Williams, CMPostprandial 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. Eur J Clin Nutr (1994) 48, 849–858.Google ScholarPubMed