Diet × genotype interactions in hepatic cholesterol and lipoprotein metabolism in Atlantic salmon (Salmo salar) in response to replacement of dietary fish oil with vegetable oil

British Journal of Nutrition

Volumn 106, Issue 10, 2011, Pages 1457-1469

  Morais, Sofia ^a   Pratoomyot, Jarunan ^a   Torstensen, Bente E ^b   Taggart, John B ^a   Guy, Derrick R ^c   Gordon Bell, J ^a   Tocher, Douglas R ^a  

^a UNIVERSITY OF STIRLING   (United Kingdom)

^b INSTITUTE OF MARINE RESEARCH   (Norway)

^c Landcatch Natural Selection   (United Kingdom)

Author keywords

Aquaculture alternative diets; Family genetic selection; Fish diets; Liver transcriptome

Indexed keywords

7 DEHYDROCHOLESTEROL REDUCTASE; ABC TRANSPORTER A1; ACYL COENZYME A OXIDASE; APOLIPOPROTEIN A1; APOLIPOPROTEIN B; APOLIPOPROTEIN C2; CARNITINE PALMITOYLTRANSFERASE I; CHOLESTEROL; ENDOTHELIAL LIPASE; FISH OIL; HIGH DENSITY LIPOPROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; ISOPENTENYL DIPHOSPHATE DELTA ISOMERASE; LIPOPROTEIN; LIPOPROTEIN LIPASE; LIPOPROTEIN LIPASE A; LIPOPROTEIN LIPASE B; LIPOPROTEIN LIPASE C; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MEVALONATE KINASE; OXIDOREDUCTASE; SCAVENGER RECEPTOR BI; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; VEGETABLE OIL; VERY LOW DENSITY LIPOPROTEIN; EDIBLE OIL; PRIMER DNA;

7 DEHYDROCHOLESTEROL REDUCTASE GENE; ACYL COENZYME A OXIDASE GENE; ANIMAL EXPERIMENT; ANIMAL FOOD; ANIMAL TISSUE; APOLIPOPROTEIN A1 GENE; APOLIPOPROTEIN C2 GENE; ARTICLE; ATLANTIC SALMON; ATP BINDING CASSETTE TRANSPORTER A1 GENE; CARNITINE PALMITOYLTRANSFERASE I GENE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIAL LIPASE GENE; FAT INTAKE; FATTY ACID OXIDATION; GENE; GENE EXPRESSION; GENE INTERACTION; GENOTYPE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE GENE; ISOPENTENYL DIPHOSPHATE DELTA ISOMERASE GENE; LEAN BODY WEIGHT; LIPOPROTEIN LIPASE A GENE; LIPOPROTEIN LIPASE B GENE; LIPOPROTEIN LIPASE C GENE; LIPOPROTEIN METABOLISM; MEVALONATE KINASE GENE; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; SCAVENGER RECEPTOR BI GENE; STEROL REGULATORY ELEMENT BINDING PROTEIN 2 GENE; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; ANIMAL; DIET; GENE EXPRESSION PROFILING; LIVER; METABOLISM; NUCLEIC ACID HYBRIDIZATION;

MAMMALIA; SALMO SALAR;

ANIMALS; BASE SEQUENCE; CHOLESTEROL; DIET; DIETARY FATS, UNSATURATED; DNA PRIMERS; FISH OILS; GENE EXPRESSION PROFILING; GENOTYPE; LIPOPROTEINS; LIVER; NUCLEIC ACID HYBRIDIZATION; PLANT OILS; REAL-TIME POLYMERASE CHAIN REACTION; SALMO SALAR;

EID: 80755185118     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114511001954     Document Type: Article

References (52)

1. Tacon AGJ & Metian M (2008) Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 285, 146-158.
2. Bell JG, McEvoy J, Tocher DR, et al. (2001) 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 131, 1535-1543. (Pubitemid 32422979)
3. Torstensen BE, Bell JG, Rosenlund G, et al. (2005) Tailoring of Atlantic salmon (Salmo salar L.) flesh lipid composition and sensory quality by replacing fish oil with a vegetable oil blend. J Agric Food Chem 53, 10166-10178. (Pubitemid 43081232)
4. Richard N, Kaushik S, Larroquet L, et al. (2006) Replacing dietary fish oil by vegetable oils has little effect on lipogenesis, lipid transport and tissue lipid uptake in rainbow trout (Oncorhynchus mykiss). Br J Nutr 96, 299-309. (Pubitemid 46485235)
5. Leaver MJ, Taggart JB, Villeneuve L, et al. (2011) Heritability and mechanisms of n-3 long chain polyunsaturated fatty acid deposition in the flesh of Atlantic salmon. Comp Biochem Physiol Part D Genomics Proteomics 6, 62-69.
6. Bell JG, McVicar AH, Park MT, et al. (1991) High dietary linoleic acid affects the fatty acid compositions of individual phospholipids from tissues of Atlantic salmon (Salmo salar): association with stress susceptibility and cardiac lesion. J Nutr 121, 1163-1172.
7. Bell JG, Dick JR, McVicar AH, et al. (1993) Dietary sunflower, linseed and fish oils affect phospholipid fatty acid composition, development of cardiac lesions, phospholipase activity and eicosanoid production in Atlantic salmon (Salmo salar). Prostaglandins Leukot Essent Fatty Acids 49, 665-673. (Pubitemid 23278509)
8. Seierstad SL, Poppe TT, Koppang EO, et al. (2005) Influence of dietary lipid composition on cardiac pathology in farmed Atlantic salmon, Salmo salar L. J Fish Dis 28, 677-690.
9. Acton S, Osgood D, Donoghue M, et al. (1999) Association of polymorphisms at the SR-BI gene locus with plasma lipid levels and body mass index in a white population. Arterioscler Thromb Vasc Biol 19, 1734-1743. (Pubitemid 29323833)
10. Dansky HM, Charlton SA, Sikes JL, et al. (1999) Genetic background determines the extent of atherosclerosis in apoE-deficient mice. Arterioscler Thromb Vasc Biol 19, 1960-1968. (Pubitemid 29379929)
11. Zhu M, Ji G, Jin G, et al. (2009) Different responsiveness to a high-fat/cholesterol diet in two inbred mice and underlying genetic factors: a whole genome microarray analysis. Nutr Metab 6, 43.
12. Liu X, Li Y, Lu X, et al. (2010) Interactions among genetic variants from SREBP2 activating-related pathway on risk of coronary heart disease in Chinese Han population. Atherosclerosis 208, 421-426.
13. Bell JG, Pratoomyot J, Strachan F, et al. (2010) Growth, flesh adiposity and fatty acid composition of Atlantic salmon (Salmo salar) families with contrasting flesh adiposity: effects of replacement of dietary fish oil with vegetable oils. Aquaculture 306, 225-232.
14. Taggart JB, Bron JE, Martin SAM, et al. (2008) A description of the origins, designs and performance of the TRAITS-SGP Atlantic salmon Salmo salar L. cDNA microarray. J Fish Biol 72, 2071-2094. (Pubitemid 351814263)
15. Brazma A, Hingamp P, Quackenbush J, et al. (2001) Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 29, 365-371. (Pubitemid 34326681)
16. Leaver MJ, Villeneuve LA, Obach A, et al. (2008) Functional genomics reveals increases in cholesterol biosynthetic genes and highly unsaturated fatty acid biosynthesis after dietary substitution of fish oil with vegetable oils in Atlantic salmon (Salmo salar). BMC Genomics 9, 299.
17. Pfaffl MW, Horgan GW & Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in realtime PCR. Nucleic Acids Res 30, e36.
18. Havel RJ, Eder HA & Bragdon JH (1955) The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J Clin Invest 34, 1345-1353.
19. Aviram M (1983) Plasma lipoprotein separation by discontinuous density gradient ultracentrifugation in hyperlipoproteinemic patients. Biochem Med 30, 111-118. (Pubitemid 13041720)
20. Lie Ø, Sandvin A & Waagbø R (1994) Transport of alphatocopherol in Atlantic salmon (Salmo salar) during vitellogenesis. Fish Physiol Biochem 13, 241-247. (Pubitemid 2130062)
21. Warnick GR, Cheung MC & Albers JJ (1979) Comparison of current methods for high-density lipoprotein cholesterol quantitation. Clin Chem 25, 596-604. (Pubitemid 9166999)
22. Folch J, Lees M & Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497-509.
23. Henderson RJ & Tocher DR (1992) Thin-layer chromatography. In Lipid Analysis: A Practical Approach, pp. 65-111 [RJ Hamilton and S Hamilton, editors]. Oxford: Oxford University Press.
24. Gilman CI, Leusch FD, Breckenridge WC, et al. (2003) Effects of a phytosterol mixture on male fish plasma lipoprotein fractions and testis P450scc activity. Gen Comp Endocrinol 130, 172-184. (Pubitemid 36268771)
25. Ostlund RE Jr (2002) Phytosterols in human nutrition. Annu Rev Nutr 22, 533-549. (Pubitemid 35221472)
26. Sakakura Y, Shimano H, Sone H, et al. (2001) Sterol regulatory element-binding proteins induce an entire pathway of cholesterol synthesis. Biochem Biophys Res Commun 286, 176-183. (Pubitemid 32917666)
27. Oram JF & Vaughan AM (2006) ATP-binding cassette cholesterol transporters and cardiovascular disease. Circ Res 99, 1031-1043. (Pubitemid 44729927)
28. Zeng L, Liao H, Liu Y, et al. (2004) Sterol-responsive elementbinding protein (SREBP) 2 down-regulates ATP-binding cassette transporter A1 in vascular endothelial cells: a novel role of SREBP in regulating cholesterol metabolism. J Biol Chem 279, 48801-48807. (Pubitemid 39625759)
29. Jordal A-EO, Lie Ø & Torstensen BE (2007) Complete replacement of dietary fish oil with a vegetable oil blend affect liver lipid and plasma lipoproteins levels in Atlantic salmon (Salmo salar L.). Aquacult Nutr 13, 114-130. (Pubitemid 46340725)
30. Sundaram M & Yao Z (2010) Recent progress in understanding protein and lipid factors affecting hepatic VLDL assembly and secretion. Nutr Metab 7, 35.
31. Chapman MJ (1980) Animal lipoproteins: chemistry, structure, and comparative aspects. J Lipid Res 21, 789-853. (Pubitemid 11230305)
32. Babin PJ & Vernier JM (1989) Plasma lipoproteins in fish. J Lipid Res 30, 467-489. (Pubitemid 19107735)
33. Jump DB, Clarke SD, Thelen A, et al. (1996) Dietary polyunsaturated fatty acid regulation of gene transcription. Prog Lipid Res 35, 227-241. (Pubitemid 27092443)
34. Clarke SD (2001) Polyunsaturated fatty acid regulation of gene transcription: a molecular mechanism to improve the metabolic syndrome. J Nutr 131, 1129-1132. (Pubitemid 32275088)
35. Davidson MH (2006) Mechanisms for the hypotriglyceridemic effect of marine omega-3 fatty acids. Am J Cardiol 98, 27i-33i.
36. Kjær MA, Vegusdal A, Gjøen T, et al. (2008) Effect of rapeseed oil and dietary n-3 fatty acids on triacylglycerol synthesis and secretion in Atlantic salmon hepatocytes. Biochim Biophys Acta 1781, 112-122.
37. Steinberg GR & Kemp BE (2009) AMPK in health and disease. Physiol Rev 89, 1025-1078.
38. Liang XF, Oku H & Ogata HY (2002) The effects of feeding condition and dietary lipid level on lipoprotein lipase gene expression in liver and visceral adipose tissue of red sea bream Pagrus major. Comp Biochem Physiol A Mol Integr Physiol 131, 335-342. (Pubitemid 34127734)
39. Mead JR, Irvine SA & Ramji DP (2002) Lipoprotein lipase: structure, function, regulation, and role in disease. J Mol Med 80, 753-769. (Pubitemid 35478124)
40. Saera-Vila A, Calduch-Giner JA, Gómez-Requeni P, et al. (2005) Molecular characterization of gilthead sea bream (Sparus aurata) lipoprotein lipase. Transcriptional regulation by season and nutritional condition in skeletal muscle and fat storage tissues. Comp Biochem Physiol B Biochem Mol Biol 142, 224-232. (Pubitemid 41262562)
41. Oku H, Koizumi N, Okumura T, et al. (2006) Molecular characterization of lipoprotein lipase, hepatic lipase and pancreatic lipase genes: effects of fasting and refeeding on their gene expression in red sea bream Pagrus major. Comp Biochem Physiol B Biochem Mol Biol 145, 168-178. (Pubitemid 44428210)
42. Lichtenstein L, Berbée JF, van Dijk SJ, et al. (2007) Angptl4 upregulates cholesterol synthesis in liver via inhibition of LPL-and HL-dependent hepatic cholesterol uptake. Arterioscler Thromb Vasc Biol 27, 2420-2427. (Pubitemid 350203959)
43. Cohen JC (2003) Endothelial lipase: direct evidence for a role in HDL metabolism. J Clin Invest 111, 318-321. (Pubitemid 36182207)
44. Broedl UC, Maugeais C, Millar JS, et al. (2004) Endothelial lipase promotes the catabolism of apoB-containing lipoproteins. Circ Res 94, 1554-1561. (Pubitemid 38856962)
45. Chung S, Timmins JM, Duong M, et al. (2010) Targeted deletion of hepatocyte ABCA1 leads to very low density lipoprotein triglyceride overproduction and low density lipoprotein hypercatabolism. J Biol Chem 285, 12197-12209.
46. Wang N, Arai T, Ji Y, et al. (1998) Liver-specific overexpression of scavenger receptor BI decreases levels of very low density lipoprotein apoB, low density lipoprotein apoB, and high density lipoprotein in transgenic mice. J Biol Chem 273, 32920-32926. (Pubitemid 28557684)
47. Wiersma H, Nijstad N, Gautier T, et al. (2010) Scavenger receptor BI facilitates hepatic very low density lipoprotein production in mice. J Lipid Res 51, 544-553.
48. Joyce CW, Amar MJ, Lambert G, et al. (2002) The ATP binding cassette transporter A1 (ABCA1) modulates the development of aortic atherosclerosis in C57BL/6 and apoE-knockout mice. Proc Natl Acad Sci USA 99, 407-412. (Pubitemid 34060374)
49. Trigatti BL, Krieger M & Rigotti A (2003) Influence of the HDL receptor SR-BI on lipoprotein metabolism and atherosclerosis. Arterioscler Thromb Vasc Biol 23, 1732-1738. (Pubitemid 37254855)
50. Kleveland EJ, Ruyter B, Vegusdal A, et al. (2006) Effects of 3-thia fatty acids on expression of some lipid related genes in Atlantic salmon (Salmo salar L.). Comp Biochem Physiol B Biochem Mol Biol 145, 239-248. (Pubitemid 44428217)
51. Liang XF, Ogata HY & Oku H (2002) 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 132, 913-919. (Pubitemid 34722593)
52. Allendorf FW & Thorgaard GH (1984) Tetraploidy and the evolution of salmonid fishes. In Evolutionary Genetics of Fishes, pp. 55-93 [BJ Turner, editor]. New York: Plenum Press.