Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: A liver transcriptomic analysis

BMC Genomics

Volumn 12, Issue , 2011, Pages

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

^a UNIVERSITY OF STIRLING   (United Kingdom)

^b Landcatch Natural Selection Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1 ACYLGLYCEROPHOSPHOCHOLINE ACYLTRANSFERASE; FAS ANTIGEN; FATTY ACID SYNTHASE; FISH OIL; GLYCEROPHOSPHOLIPID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; POLYUNSATURATED FATTY ACID; TRANSCRIPTOME; VEGETABLE OIL; EDIBLE OIL; FATTY ACID;

AQUACULTURE; ARTICLE; ATLANTIC SALMON; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; DIETARY INTAKE; DOWN REGULATION; FAT INTAKE; FATTY ACID SYNTHESIS; GENE EXPRESSION; GENOTYPE; IMMUNE RESPONSE; LIPID COMPOSITION; LIPID METABOLISM; LIVER METABOLISM; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; UNINDEXED SEQUENCE; UPREGULATION; ANIMAL; DNA MICROARRAY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENETIC SELECTION; GENETICS; LIVER; METABOLISM; MOLECULAR EVOLUTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

SALMO SALAR;

ANIMALS; DIETARY FATS, UNSATURATED; EVOLUTION, MOLECULAR; FATTY ACIDS; FISH OILS; GENE EXPRESSION PROFILING; GENOTYPE; LIPID METABOLISM; LIVER; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT OILS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALMO SALAR; SELECTION, GENETIC;

EID: 79956198111     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-255     Document Type: Article

References (68)

1. Calder PC, Yaqoob P. Omega-3 polyunsaturated fatty acids and human health outcomes. BioFactors 2009, 35:266-272. 10.1002/biof.42, 19391122.
2. FAO The State of World Fisheries and Aquaculture 2008 2009, Rome: Food and Agriculture Organization of the United Nations, FAO.
3. Tacon AGJ, Metian M. Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: Trends and future prospects. Aquaculture 2008, 285:146-158.
4. Rosenlund G, Corraze G, Izquierdo M, Torstensen BE. The effects of fish oil replacement on nutritional and organoleptic qualities of farmed fish. Fish Oil Replacement and Alternative Lipid Sources in Aquaculture Feeds 2010, 487-522. Boca Raton: CRC Press, Turchini GM, Ng WK, Tocher DR.
5. Gjedrem T, Baranski M. Selective Breeding in Aquaculture: an Introduction 2009, 10. London: Springer Science + Business Media B.V, Series: Reviews: Methods and Technologies in Fish Biology and Fisheries.
6. Leaver MJ, Taggart JB, Villeneuve L, Bron JE, Guy DR, Bishop SC, Houston RD, Matika O, Tocher DR. 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 2011, 6:62-69. 10.1016/j.cbd.2010.04.002, 20451480.
7. Kolditz CI, Paboeuf G, Borthaire M, Esquerré D, SanCristobal M, Lefèvre F, Médale F. Changes induced by dietary energy intake and divergent selection for muscle fat content in rainbow trout (Oncorhynchus mykiss), assessed by transcriptome and proteome analysis of the liver. BMC Genomics 2008, 9:506. 10.1186/1471-2164-9-506, 2612026, 18959775.
8. Kolditz C, Borthaire M, Richard N, Corraze G, Panserat S, Vachot C, Lefèvre F, Médale F. Liver and muscle metabolic changes induced by dietary energy content and genetic selection in rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol 2008, 294:R1154-1164. 10.1152/ajpregu.00766.2007, 18234747.
9. Jordal AE, Torstensen BE, Tsoi S, Tocher DR, Lall SP, Douglas SE. Dietary rapeseed oil affects the expression of genes involved in hepatic lipid metabolism in Atlantic salmon (Salmo salar L.). J Nutr 2005, 135:2355-2361.
10. Taggart JB, Bron JE, Martin SAM, Seear PJ, Høyheim B, Talbot R, Carmichael SN, Villeneuve LAN, Sweeney GE, Houlihan DF, Secombes CJ, Tocher DR, Teale AJ. A description of the origins, designs and performance of the TRAITS-SGP Atlantic salmon Salmo salar L. cDNA microarray. J Fish Biol 2008, 72:2071-2094. 10.1111/j.1095-8649.2008.01876.x, 2610384, 19125201.
11. Panserat S, Hortopan GA, Plagnes-Juan E, Kolditz C, Lansard M, Skiba-Cassy S, Esquerre D, Geurden I, Médale F, Kaushik S, Corraze G. Differential gene expression after total replacement of dietary fish meal and fish oil by plant products in rainbow trout (Oncorhynchus mykiss) liver. Aquaculture 2009, 294:123-131.
12. Morais S, Pratoomyot J, Torstensen BE, Taggart JB, Guy DR, Bell JG, Tocher DR. 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. Br J Nutr
13. Allendorf FW, Thorgaard GH. Tetraploidy and the evolution of salmonid fishes. Evolutionary Genetics of Fishes 1984, 55-93. New York: Plenum Press, Turner BJ.
14. Leaver MJ, Villeneuve LA, Obach A, Jensen L, Bron JE, Tocher DR, Taggart JB. 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 2008, 9:299. 10.1186/1471-2164-9-299, 2459193, 18577222.
15. Morais S, Monroig O, Zheng X, Leaver MJ, Tocher DR. Highly unsaturated fatty acid synthesis in Atlantic salmon: characterization of ELOVL5- and ELOVL2-like elongases. Mar Biotechnol 2009, 1:627-639.
16. Zheng X, Tocher DR, Dickson CA, Bell JG, Teale AJ. Effects of diets containing vegetable oil on expression of genes involved in highly unsaturated fatty acid biosynthesis in liver of Atlantic salmon (Salmo salar). Aquaculture 2004, 236:467-483.
17. Zheng X, Torstensen BE, Tocher DR, Dick JR, Henderson RJ, Bell JG. Environmental and dietary influences on highly unsaturated fatty acid biosynthesis and expression of fatty acyl desaturase and elongase genes in liver of Atlantic salmon (Salmo salar). Biochim Biophys Acta 2005, 1734:13-24.
18. Davidson MH. Mechanisms for the hypotriglyceridemic effect of marine omega-3 fatty acids. Am J Cardiol 2006, 98:27i-33i.
19. Kim H, Choi S, Lee HJ, Lee JH, Choi H. Suppression of fatty acid synthase by dietary polyunsaturated fatty acids is mediated by fat itself, not by peroxidative mechanism. J Biochem Mol Biol 2003, 36:258-264. 10.5483/BMBRep.2003.36.3.258, 12787479.
20. Alvarez MJ, Díez A, López-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.
21. Torstensen BE, Frøyland L, Lie T. Replacing 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.
22. Richard N, Kaushik S, Larroquet L, Panserat S, Corraze G. 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 2006, 96:299-309. 10.1079/BJN20061821, 16923224.
23. Minghetti M, Leaver MJ, Tocher DR. Transcriptional control mechanisms of genes of lipid and fatty acid metabolism in the Atlantic salmon (Salmo salar L.) established cell line, SHK-1. Biochim Biophys Acta Molecular and Cell Biology of Lipids 2011, 1811:194-202.
24. Boukouvala E, Antonopoulou E, Favre-Krey L, Diez A, Bautista JM, Leaver MJ, Tocher DR, Krey G. Molecular characterization of three peroxisome proliferator-activated receptors from the sea bass (Dicentrarchus labrax). Lipids 2004, 39:1085-1092. 10.1007/s11745-004-1334-z, 15726823.
25. Leaver MJ, Boukouvala E, Antonopoulou E, Diez A, Favre-Krey L, Ezaz MT, Bautista JM, Tocher DR, Krey G. Three peroxisome proliferator-activated receptor isotypes from each of two species of marine fish. Endocrinology 2005, 146:3150-3162. 10.1210/en.2004-1638, 15790725.
26. Kondo H, Misaki R, Gelman L, Watabe S. Ligand-dependent transcriptional activities of four torafugu pufferfish Takifugu rubripes peroxisome proliferator-activated receptors. Gen Comp Endocrinol 2007, 154:120-127. 10.1016/j.ygcen.2007.05.034, 17632107.
27. Kjær MA, Todorcević M, Torstensen BE, Vegusdal A, Ruyter B. Dietary n-3 HUFA affects mitochondrial fatty acid beta-oxidation capacity and susceptibility to oxidative stress in Atlantic salmon. Lipids 2008, 43:813-827. 10.1007/s11745-008-3208-z, 18615261.
28. Jordal A-EO, Lie T, Torstensen BE. 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 2007, 13:114-130.
29. Jump DB, Clarke SD, Thelen A, Liimatta M, Ren B, Badin M. Dietary polyunsaturated fatty acid regulation of gene transcription. Prog Lipid Res 1996, 35:227-241. 10.1016/S0163-7827(96)00007-0, 9082451.
30. Clarke SD. Polyunsaturated fatty acid regulation of gene transcription: a molecular mechanism to improve the metabolic syndrome. J Nutr 2001, 131:1129-1132.
31. Nakamura MT, Nara TY. Gene regulation of mammalian desaturases. Biochem Soc Trans 2002, 30:1076-1079.
32. Wang Y, Botolin D, Christian B, Busik J, Xu J, Jump DB. Tissue-specific, nutritional, and developmental regulation of rat fatty acid elongases. J Lipid Res 2005, 46:706-715. 10.1194/jlr.M400335-JLR200, 2430181, 15654130.
33. Tang C, Cho HP, Nakamura MT, Clarke SD. Regulation of human Δ-6 desaturase gene transcription: identification of a functional direct repeat-1 element. J Lipid Res 2003, 44:686-695. 10.1194/jlr.M200195-JLR200, 12562861.
34. Zheng X, Leaver MJ, Tocher DR. Long-chain polyunsaturated fatty acid synthesis in fish: Comparative analysis of Atlantic salmon (Salmo salar L.) and Atlantic cod (Gadus morhua L.) Δ6 fatty acyl desaturase gene promoters. Comp Biochem Physiol B Biochem Mol Biol 2009, 154:255-263. 10.1016/j.cbpb.2009.06.010, 19563904.
35. Paine MJI, Scrutton NS, Munro AW, Gutierrez A, Roberts GCK, Wolf CR. Electron transfer partners of cytochrome P450. Cytochrome P450: structure, mechanism and biochemistry 2005, 115-148. NY: Kluwer Academic/Plenum Publishers, Ortiz de Montellano PR, 3.
36. Moon TW. Glucose intolerance in teleost fish: fact or fiction?. Comp Biochem Physiol 2001, 129B:243-249.
37. Hemre GI, Mommsen TP, Krogdahl T. Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 2002, 8:175-194.
38. Menoyo D, Diez A, Lopez-Bote CJ, Casado S, Obach A, Bautista JM. Dietary fat type affects lipid metabolism in Atlantic salmon (Salmo salar L.) and differentially regulates glucose transporter GLUT4 expression in muscle. Aquaculture 2006, 261:294-304.
39. Sriram G, Rahib L, He JS, Campos AE, Parr LS, Liao JC, Dipple KM. Global metabolic effects of glycerol kinase overexpression in rat hepatoma cells. Mol Genet Metab 2008, 93:145-159. 10.1016/j.ymgme.2007.09.008, 2702542, 18029214.
40. McMahon RJ. Biotin in metabolism and molecular biology. Annu Rev Nutr 2002, 22:221-239. 10.1146/annurev.nutr.22.121101.112819, 12055344.
41. Shepherd PR, Withers DJ, Siddle K. Phosphoinositide 3-kinase: the key switch mechanism in insulin signalling. Biochem J 1998, 333:471-490. 1219607, 9677303.
42. Delcommenne M, Tan C, Gray V, Rue L, Woodgett J, Dedhar S. Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc Natl Acad Sci USA 1998, 95:11211-11216. 10.1073/pnas.95.19.11211, 21621, 9736715.
43. Yost C, Farr GH, Pierce SB, Ferkey DM, Chen MM, Kimelman D. GBP, an inhibitor of GSK-3, is implicated in Xenopus development and oncogenesis. Cell 1998, 93:1031-1041. 10.1016/S0092-8674(00)81208-8, 9635432.
44. Takahashi M, Tsuboyama-Kasaoka N, Nakatani T, Ishii M, Tsutsumi S, Aburatani H, Ezaki O. Fish oil feeding alters liver gene expressions to defend against PPARα activation and ROS production. Am J Physiol Gastrointest Liver Physiol 2002, 282:G338-348.
45. Saera-Vila A, Benedito-Palos L, Sitjà-Bobadilla A, Nàcher-Mestre J, Serrano R, Kaushik S, Pérez-Sánchez J. Assessment of the health and antioxidant trade-off of gilthead sea bream (Sparus aurata) fed alternative diets with low levels of contaminants. Aquaculture 2009, 296:87-95.
46. Finne EF, Olsvik PA, Berntssen MH, Hylland K, Tollefsen KE. The partial pressure of oxygen affects biomarkers of oxidative stress in cultured rainbow trout (Oncorhynchus mykiss) hepatocytes. Toxicol In Vitro 2008, 22:1657-1661. 10.1016/j.tiv.2008.05.011, 18603400.
47. Leaver MJ, George SG. A piscine glutathione S-transferase which efficiently conjugates the end-products of lipid peroxidation. Mar Environ Res 1998, 46:71-74.
48. Barnes CJ, Cameron IL, Puleo-Scheppke B, Lee M. Age alters expression and inducibility of heme oxygenase isozymes in mice. Age 1998, 21:123-128.
49. Wagener FA, Volk HD, Willis D, Abraham NG, Soares MP, Adema GJ, Figdor CG. Different faces of the heme-heme oxygenase system in inflammation. Pharmacol Rev 2003, 55:551-571. 10.1124/pr.55.3.5, 12869663.
50. Calder PC. n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 2006, 83(6 Suppl):1505S-1519S.
51. Estensoro I, Benedito-Palos L, Palenzuela O, Kaushik S, Sitjà-Bobadilla A, Pérez-Sánchez J. The nutritional background of the host alters the disease course in a fish-myxosporean system. Vet Parasitol 2011, 175:141-150. 10.1016/j.vetpar.2010.09.015, 20947256.
52. Oxley A, Jolly C, Eide T, Jordal AE, Svardal A, Olsen RE. The combined impact of plant-derived dietary ingredients and acute stress on the intestinal arachidonic acid cascade in Atlantic salmon (Salmo salar). Br J Nutr 2010, 103:851-861. 10.1017/S0007114509992467, 19943982.
53. Boggs JM, Koo CH, Goetzl EJ. Down-regulation of receptor antigen in leukotriene B4-induced chemotactic deactivation of human polymorphonuclear leucocytes. Immunology 1991, 73:212-216. 1384467, 1649125.
54. Lawrence RH, Sorrell TC. Eicosapentaenoic acid modulates neutrophil leukotriene B4 receptor expression in cystic fibrosis. Clin Exp Immunol 1994, 98:12-16. 1534176, 7923869.
55. Valitutti S, Müller S, Salio M, Lanzavecchia A. Degradation of T cell receptor (TCR)-CD3-ζ complexes after antigenic stimulation. J Exp Med 1997, 185:1859-1864. 10.1084/jem.185.10.1859, 2196323, 9151711.
56. Dircks L, Sul HS. Acyltransferases of de novo glycerophospholipid biosynthesis. Prog Lipid Res 1999, 38:461-479. 10.1016/S0163-7827(99)00012-0, 10793891.
57. Jasinska R, Zhang QX, Pilquil C, Singh I, Xu J, Dewald J, Dillon DA, Berthiaume LG, Carman GM, Waggoner DW, Brindley DN. Lipid phosphate phosphohydrolase-1 degrades exogenous glycerolipid and sphingolipid phosphate esters. Biochem J 1999, 340:677-686. 10.1042/0264-6021:3400677, 1220298, 10359651.
58. Tsai ML, Chen HY, Tseng MC, Chang RC. Cloning of peroxisome proliferators activated receptors in the cobia (Rachycentron canadum) and their expression at different life-cycle stages under cage aquaculture. Gene 2008, 425:69-78. 10.1016/j.gene.2008.08.004, 18762234.
59. Collin A, Swennen Q, Skiba-Cassy S, Buyse J, Chartrin P, Le Bihan-Duval E, Crochet S, Duclos MJ, Joubert R, Decuypere E, Tesseraud S. Regulation of fatty acid oxidation in chicken (Gallus gallus): interactions between genotype and diet composition. Comp Biochem Physiol B Biochem Mol Biol 2009, 153:171-177. 10.1016/j.cbpb.2009.02.012, 19258045.
60. Bell JG, Pratoomyot J, Strachan F, Henderson RJ, Fontanillas R, Hebard A, Guy DR, Hunter D, Tocher DR. 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 2010, 306:225-232.
61. National Research Council (NRC) Nutrient Requirements of Fish 1993, Washington D.C.: National Academy Press, National Research Council (NRC).
62. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, Aach J, Ansorge W, Ball CA, Causton HC, Gaasterland T, Glenisson P, Holstege FC, Kim IF, Markowitz V, Matese JC, Parkinson H, Robinson A, Sarkans U, Schulze-Kremer S, Stewart J, Taylor R, Vilo J, Vingron M. Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 2001, 29:365-371. 10.1038/ng1201-365, 11726920.
63. Folch J, Lees M, Sloane-Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957, 226:497-509.
64. Christie WW. Lipid analysis 2003, Bridgewater: The Oily Press.
65. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36. 10.1093/nar/30.9.e36, 113859, 11972351.
66. Zheng X, Tocher DR, Dickson CA, Bell JG, Teale AJ. Highly unsaturated fatty acid synthesis in vertebrates: new insights with the cloning and characterization of a Δ6 desaturase of Atlantic salmon. Lipids 2005, 40:13-24. 10.1007/s11745-005-1355-7, 15825826.
67. Kleveland EJ, Ruyter B, Vegusdal A, Sundvold H, Berge RK, Gjøen T. 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 2006, 145:239-248. 10.1016/j.cbpb.2006.07.012, 16971150.
68. Olsvik PA, Torstensen BE, Berntssen MHG. Effects of complete replacement of fish oil with plant oil on gastrointestinal cell death, proliferation and transcription of eight genes' encoding proteins responding to cellular stress in Atlantic salmon Salmo salar L. J Fish Biol 2007, 71:550-568.