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Characteristics and metabolism of different adipose tissues in fish

Abstract

Lipids are the predominant source of energy for fish and are stored in fat depots in different parts of the body regions. This review focuses on visceral, subcutaneous and intramuscular adipose tissues that interfere with carcass and fillet yields and with flesh quality. The morphological, cellular and biochemical characteristics of these tissues are discussed as well as the different mechanisms involved in the regulation of their lipid metabolism. Particular emphasis is given to the modulation of these characteristics and mechanisms by different extrinsic (food composition, water parameters) and intrinsic (selective breeding, life cycle status) factors. This review focuses on recent studies that take into account the present challenges of fin-fish aquaculture, which are principally (1) the replacement of fish oil and meal by vegetable oil and meal due to the need for sustainability and the limited availability of fish to prepare food pellets, and (2) selective breeding programs to improve fish growth and flesh quality. These studies apply various modern technologies to different fish species, including the development of cell culture systems and transcriptomic and proteomic techniques. This review highlights that fish adipose tissues differ in their localization and their morphological characteristics and that they show a large plasticity in their responses to variations of both extrinsic and intrinsic factors. These different responses reinforce the idea of their differential participation in fish lipid homeostasis.

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References

  • Agulleiro MJ, André M, Morais S, Cerda J, Babin PJ (2007) High transcript level of fatty acid-binding protein 11 but not of very low-density lipoprotein receptor is correlated to ovarian follicle atresia in a teleost fish (Solea senegalensis). Biol Reprod 77:504–516

    PubMed  CAS  Google Scholar 

  • Albalat A, Gómez-Requeni P, Rojas P, Médale F, Kaushik S, Vianen GJ, Van den Thillart G, Gutiérrez J, Pérez-Sánchez J, Navarro I (2005a) Nutritional and hormonal control of lipolysis in isolated gilthead seabream (Sparus aurata) adipocytes. Am J Physiol Regul Integr Comp Physiol 289:R259–R265

    PubMed  CAS  Google Scholar 

  • Albalat A, Gutiérrez J, Navarro I (2005b) Regulation of lipolysis in isolated adipocytes of rainbow trout (Oncorhynchus mykiss): the role of insulin and glucagon. Gen Comp Biochem Physiol A 142:347–354

    Google Scholar 

  • Albalat A, Liarte C, MacKenzie S, Tort L, Planas JV, Navarro I (2005c) Control of adipose tissue lipid metabolism by tumor necrosis factor-α in rainbow trout (Oncorhynchus mykiss). J Endocrinol 184:527–534

    PubMed  CAS  Google Scholar 

  • Albalat A, Sánchez-Gurmaches J, Gutiérrez J, Navarro I (2006) Regulation of lipoprotein lipase activity in rainbow trout (Oncorhynchus mykiss) tissues. Gen Comp Endocrinol 146:226–235

    PubMed  CAS  Google Scholar 

  • Albalat A, Saera-Vila A, Capilla E, Gutiérrez J, Pérez-Sánchez J, Navarro I (2007) Insulin regulation of lipoprotein lipase (LPL) activity and expression in gilthead sea bream (Sparus aurata). Comp Biochem Physiol B 148:151–159

    PubMed  CAS  Google Scholar 

  • Ando S, Mori Y, Nakamura K, Sugawara A (1993) Characteristics of lipid accumulation types in five species of fish. Nippon Suisan Gakk 59:1559–1664

    CAS  Google Scholar 

  • Aussanasuwannakul A, Kenney PB, Weber GM, Yao J, Slider SD, Manor ML, Salem M (2011) Effect of sexual maturation on growth, fillet composition, and texture of female rainbow trout (Oncorhynchus mykiss) on a high nutritional plane. Aquaculture 317:79–88

    Google Scholar 

  • Batista-Pinto C, Rodrigues P, Rocha E, Lobo-da-Cunha A (2005) Identification and organ expression of peroxisome proliferator activated receptors in brown trout (Salmo trutta f. fario). Biochim Biophys Acta 1731:88–94

    PubMed  CAS  Google Scholar 

  • Benedito-Palos L, Navarro JC, Sitjà-Bobadilla A, Gordon Bell J, Kaushik S, Pérez-Sanchez J (2008) High levels of vegetable oils in plant protein-rich diets fed to gilthead sea bream (Sparus aurata L.,): growth performance, muscle fatty acid profiles and histological alterations of target tissues. Br J Nutr 100:992–1003

    PubMed  CAS  Google Scholar 

  • Bjerkeng B, Refstie S, Fjalestad KT, Storebakken T, Rødbotten M, Roem AJ (1997) Quality parameters of the flesh of Atlantic salmon (Salmo salar) as affected by dietary fat content and full-fat soybean meal as a partial substitute for fish meal in the diet. Aquaculture 157:297–309

    Google Scholar 

  • Boukouvala E, Antonopoulou E, Favre-Krey L, Diez A, Bautista JM, Leaver MJ, Tocher DR, Krey G (2004) Molecular characterization of three peroxisome proliferators-activated receptors from the sea bass (Dicentrarchus labrax). Lipids 39:1085–1092

    PubMed  CAS  Google Scholar 

  • Bouraoui L, Gutiérrez J, Navarro I (2008) Regulation of proliferation and differentiation of adipocyte precursor cells in rainbow trout (Oncorhynchus mykiss). J Endocrinol 198:459–469

    PubMed  CAS  Google Scholar 

  • Bouraoui L, Capilla E, Gutiérrez J, Navarro I (2010) Insulin and insulin-like growth factor I signaling pathways in rainbow trout (Oncorhynchus mykiss) during adipogenesis and their implication in glucose uptake. Am J Physiol Regul Integr Comp Physiol 299:R33–R41

    PubMed  CAS  Google Scholar 

  • Bouraoui L, Cruz-Garcia J, Gutiérrez J, Capilla E, Navarro I (2011a) Regulation of lipoprotein lipase gene expression by insulin and troglitazone in rainbow trout (Oncorhynchus mykiss) adipocyte cells in culture. Comp Biochem Physiol A 161:83–88

    Google Scholar 

  • Bouraoui L, Sánchez-Gurmaches J, Cruz-Garcia J, Gutiérrez J, Benedito-Palos L, Pérez-Sánchez J, Navarro I (2011b) Effect of dietary fish meal and fish oil replacement on lipogenic and lipoprotein lipase activities and plasma insulin on gilthead sea bream (Sparus aurata). Aquac Nut 17:54–63

    CAS  Google Scholar 

  • Breton B, Horoszewicz L, Bieniarz K, Epler P (1980a) Temperature and reproduction in tench: effect of a rise in the annual temperature regime on gonadotropin level, gametogenesis and spawning. I. The male. Reprod Nutr Dev 20:105–118

    PubMed  CAS  Google Scholar 

  • Breton B, Horoszewicz L, Bieniarz K, Epler P (1980b) Temperature and reproduction in tench: effect of a rise in the annual temperature regime on gonadotropin level, gametogenesis and spawning. II. The female. Reprod Nutr Dev 20:1011–1024

    PubMed  CAS  Google Scholar 

  • Capilla E, Dίaz M, Gutiérrez J, Planas JV (2002) Physiological regulation of the expression of a GLUT4 homolog in fish skeletal muscle. Am J Physiol Endocrinol Metab 283:E44–E49

    PubMed  CAS  Google Scholar 

  • Capilla E, Dίaz M, Albalat A, Navarro I, Pessin JE, Keller K, Planas JV (2004) Functional characterization of an insulin-responsive glucose transporter (GLUT4) from fish adipose tissue. Am J Physiol Endocrinol Metab 287:E348–E357

    PubMed  CAS  Google Scholar 

  • Chmurzynska A (2006) The multigene family of fatty acid-binding proteins (FABPs): function, structure and polymorphism. J Appl Genet 47:39–48

    PubMed  Google Scholar 

  • Christodoulides C, Vidal-Puig A (2010) PPARs and adipocyte function. Mol Cel Endocrinol 318:61–68

    CAS  Google Scholar 

  • Cristancho AG, Lazar MA (2011) Forming functional fat: a growing understanding of adipocyte differentiation. Nat RevMol Cell Biol 12:722–734

    CAS  Google Scholar 

  • Cruz-Garcia L, Saera-Vila A, Navarro I, Calduch-Giner J, Pérez-Sánchez J (2009) Targets for TNFα-induced lipolysis in gilthead sea bream (Sparus aurata L) adipocytes isolated from lean and fat juvenile fish. J Exp Biol 212:2254–2260

    PubMed  CAS  Google Scholar 

  • Cruz-Garcia L, Sánchez-Gurmaches J, Bouraoui L, Saera-Vila A, Pérez-Sánchez J, Gutiérrez J, Navarro I (2011) Changes in adipopcyte cell size, gene expression of lipid metabolism markers, and lipolytic responses induced by dietary fish oil replacement in gilthead sea bream (Sparus aurata L). Comp Biochem Physiol A158:391–399

    Google Scholar 

  • Dίaz M, Capilla E, Planas JV (2007) Physiological regulation of glucose transporter (GLUT4) protein content in brown trout (Salmo trutta) skeletal muscle. Am J Physiol Endocrinom Metab 283:E44–E49

    Google Scholar 

  • Farmer SR (2006) Transcriptional control of adipocyte formation. Cell Metab 4:263–273

    PubMed  CAS  Google Scholar 

  • Fauconneau B, Corraze G, Le Bail PY, Vernier JM (1990) Les lipides de dépôt chez les poissons d’élevage: contrôle cellulaire, métabolique et hormonal (1). INRA Prod Anim 3:369–381

    Google Scholar 

  • Fauconneau B, Alami-Durante GH, Laroche M, Marcel J, Vallot D (1995) Growth and meat quality relations in carp. Aquaculture 129:265–297

    Google Scholar 

  • Fauconneau B, André S, Chmaitilly J, Le Bail PY, Krieg F, Kaushik S (1997) Control of skeletal muscle fibres and adipose cells size in the flesh of rainbow trout. J Fish Biol 50:296–314

    Google Scholar 

  • Frøyland L, Madsen L, Eckhoff KM, Lie Ø, Berge RK (1998) Carnitine palmitoyltransferase I, carnitine palmitoyltransferase II, and acyl-CoA oxidase activities in atlantic Salmon (Salmo salar). Lipids 33:923–930

    PubMed  Google Scholar 

  • Gatlin DM III, Barrows FT, Brown P, Dabrowski K, Gibson Gaylord T, Hardy RW, Herman E, Hu G, Krogdahl Å, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza EJ, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38:551–579

    CAS  Google Scholar 

  • Gélineau A, Corraze G, Boujard T, Larroquet L, Kaushik S (2001) Relation between dietary lipid level and voluntary feed intake, growth, nutrient gain, lipid deposition and hepatic lipogenesis in rainbow trout. Reprod Nutr Dev 41:487–503

    PubMed  Google Scholar 

  • Glatz JFC, Luiken JJFP, Bonen A (2010) Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol Rev 90:367–417

    PubMed  CAS  Google Scholar 

  • Green HS, Selivonchick DP (1987) Lipid metabolism in fish. Prog Lipid Res 26:53–85

    Google Scholar 

  • Guderley H (2004) Metabolic responses to low temperature in fish muscle. Biol Rev 79:409–427

    PubMed  Google Scholar 

  • Guijarro AI, Lopez-Patiño MA, Pinillos ML, Isorna E, De Pedro N, Alonso-Gómez AL, Alonso-Bedate M, Delgado MJ (2003) Seasonal changes in haematology and metabolic resources in the tench. J Fish Biol 62:803–815

    Google Scholar 

  • Gutiérrez J, Pérez J, Navarro I, Zanuy S, Carrillo M (1991) Changes in plasma glucagon and insulin associated with fasting in sea bass (Dicentrarchus labrax). Fish Physiol Biochem 9:107–112

    Google Scholar 

  • Hall JR, MacCormack TJ, Barry CA, Driedzic WR (2004) Sequence ad expression of a constitutive, facilitated glucose transporter (GLUT1) in Atlantic cod Gadus morhua. J Exp Biol 207:4697–4706

    PubMed  CAS  Google Scholar 

  • Hall JR, Richards RC, MacCormack TJ, Ewart KV, Driedzic WR (2005) Cloning of GLUT3 cDNA from Atlantic cod (Gadus morhua) and expression of Glut1 and Glut3 in response to hypoxia. Biochem Biophys Acta 1730:245–252

    PubMed  CAS  Google Scholar 

  • Hall JR, Short CE, Driedzic WR (2006) Sequence of Atlantic cod (Gadus morhua) GLUT4, GLUT2 and GPDH: developmental stage expression, tissue expression and relationship to starvation induced changes in blood glucose. J Exp Biol 209:4490–4502

    PubMed  CAS  Google Scholar 

  • Harmon JS, Sheridan MA (1992) Effects of nutritional state, insulin, and glucagon on lipid mobilization in rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 8:214–221

    Google Scholar 

  • Harmon JS, Michelsen KG, Sheridan MA (1991) Purification and characterization of hepatic triacylglycerol lipase isolated from rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 9:361–368

    CAS  Google Scholar 

  • Hazel JR, Sidell BD (2004) The substrate specificity of hormone-sensitive lipase from adipose tissue of the Antartic fish Trematomus newnesi. J Exp Biol 207:897–903

    PubMed  CAS  Google Scholar 

  • Henderson RJ, Tocher DR (1987) The lipid-composition and biochemistry of fresh-water fish. Prog Lipid Res 26:281–347

    PubMed  CAS  Google Scholar 

  • Hillgartner FB, Salati LM, Goodridge AG (1995) Physiological and molecular mechanisms involved in nutritional regulation of fatty acid synthesis. Physiol Rev 75:47–76

    PubMed  CAS  Google Scholar 

  • Holm C, Østerlund T, Laurell H, Contreras JA (2000) Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Annu Rev Nutr 20:365–393

    PubMed  CAS  Google Scholar 

  • Huang TS, Todorčević M, Ruyter B, Torstensen BE (2010) Altered expression of CCAAT/enhancer binding protein and FABP11 genes during adipogenesis in vitro in Atlantic salmon (Salmo salar). Aquac Nut 16:72–80

    CAS  Google Scholar 

  • Hung SSO, Liu W, Li H, Storebakken T, Cui Y (1997) Effect of starvation on some morphological and biochemical parameters in white sturgeon, Acipenser transmontanus. Aquaculture 151:357–363

    Google Scholar 

  • Hunt SMV, Simpson TH, Wright RS (1982) Seasonal changes in the levels of 11-oxotestosterone and testosterone in the serum of male salmon, Salmo salar L., and their relationship to growth and maturation cycle. J Fish Biol 20:105–119

    CAS  Google Scholar 

  • Ishiki M, Klip A (2005) Minireview: recent developments in the regulation of glucose transporter-4 traffic: new signals, locations, and partners. Endocrinology 146:5071–5078

    PubMed  CAS  Google Scholar 

  • Jezierska B, Hazel JR, Gerking SD (1982) Lipid mobilization during starvation in the rainbow trout, Salmo gairdneri Richardson, with attention to fatty acids. J Fish Biol 21:681–692

    CAS  Google Scholar 

  • Jobling M, Johansen SJS (2003) Fat distribution in Atlantic salmon Salmo salar L. in relation to body size and feeding regime. Aquac Res 34:311–316

    Google Scholar 

  • Jobling M, Koskela J, Savolainen R (1998) Influence of dietary fat level and increased adiposity on growth and fat deposition in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquac Res 29:601–607

    Google Scholar 

  • Jobling M, Larsen A, Andreassen B, Sigholt T, Olsen RL (2002) Influence of a dietary shift on temporal changes in fat deposition and fatty acid composition of Atlantic salmon post-smolt during the early phase of sea water rearing. Aquac Res 33:875–889

    CAS  Google Scholar 

  • Johnston IA (1981) Structure and function of fish muscles. Symp zool Soc Lond 48:71–113

    CAS  Google Scholar 

  • Jordal AEO, Hordvik I, Pelsers M, Bernlohr DA, Torstensen BE (2006) FABP3 and FABP10 in Atlantic salmon (Salmo salar L.)—general effects of dietary fatty acid composition and life cycle variations. Comp Biochem Physiol B 145:147–158

    PubMed  Google Scholar 

  • Katikou P, Hughes SI, Robb DHF (2001) Lipid distribution within Atlantic salmon (Salmo salar) fillets. Aquaculture 202:89–99

    CAS  Google Scholar 

  • Kaushik SJ (1986) Environmental effects on feed utilization. Fish Physiol Biochem 2:131–140

    Google Scholar 

  • Kiessling A, Kiesling KH, Storebakken T, Åsgård T (1991) Changes in the structure and function of the epaxial muscle of rainbow trout (Oncorhynchus mykiss) in relation to ration and age III. Chemical composition. Aquaculture 93:373–387

    CAS  Google Scholar 

  • Kittilson JD, Reindl KM, Sheridan MA (2011) Rainbow trout (Oncorhynchus mykiss) possess two hormone-sensitive lipase-encoding mRNAs that are differentially expressed and independently regulated by nutritional state. Comp Biochem Physiol A 158:52–60

    Google Scholar 

  • Kolditz C, Borthaire M, Richard N, Corraze G, Panserat S, Vachot C, Lefèvre F, Médale F (2008) 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 294:R1154–R1164

    PubMed  CAS  Google Scholar 

  • Kolditz CI, Plagnes-Juan E, Quillet E, Lefèvre F, Médale F (2010) Changes in white muscle transcriptome induced by dietary energy levels in two lines of rainbow trout (Oncorhynchus mykiss) selected for muscle fat content. Br J Nutr 103:629–642

    PubMed  CAS  Google Scholar 

  • Krasnov A, Teerijoki H, Molsa H (2001) Rainbow trout (Oncorhynchus mykiss) hepatic glucose transporter. Biochim Biophys Acta 1520:174–178

    PubMed  CAS  Google Scholar 

  • Lampidonis AD, Rogdakis E, Voutsinas GE, Stravopodis DJ (2011) The resurgence of hormone-sensitive lipase (HSL) in mammalian lipolysis. Gene 477:1–11

    PubMed  CAS  Google Scholar 

  • Le Bail PY (1988) Growth reproduction interaction in salmonids. In: Zohar Y, Breton B (eds) Reproduction in fish. Basic and applied aspects in endocrinology and genetics. Les Colloques de l’INRA vol 44, pp 91–108

  • Le Bail PY, Bœuf G (1997) What hormones may regulate food intake in fish? Aquat Living Resour 10:371–379

    Google Scholar 

  • Le Boucher R, Vandeputte M, Dupont-Nivet M, Quillet E, Mazurais D, Robin J, Vergnet A, Médale F, Kaushik S, Chatain B (2011) A first insight into genotype-diet interactions in European sea bass (Dicentrarchus labrax L. 1756) in the context of plant-based diet use. Aquac Res 42:583–592

    Google Scholar 

  • Leaver MJ, Boukouvala E, Antonopoulou E, Diez A, Favre-Krey L, Ezaz MT, Bautista JM, Tocher DR, Krey G (2005) Three peroxisome proliferators-activated receptor isotypes from each of two species of marine fish. Endocrinology 146:3150–3162

    PubMed  CAS  Google Scholar 

  • Leaver MJ, Bautista JM, Björnsson BT, Jönsson E, Krey G, Tocher DR, Torstensen BE (2008) Towards fish lipid nutrigenomics: current state and prospects for fin-fish aquaculture. Rev Fish Sci 16(S1):73–94

    CAS  Google Scholar 

  • Lefterova MI, Lazar MA (2009) New developments in adipogenesis. Trends Endocrinol Metab 20:107–114

    PubMed  CAS  Google Scholar 

  • Lefterova MI, Zhang Y, Steger DV, Schupp M, Schug J, Cristancho A, Feng D, Zhuo D, Stoeckert CJ, Liu XS, Lazar MA (2011) PPAR-γ and C/EBP factors orchestrate adipocyte biology via adjacent binding on a genome-wide scale. Genes Dev 22:2941–2952

    Google Scholar 

  • Leng XJ, Wu XF, Tian J, Li XQ, Guan L, Weng DC (2012) Molecular cloning of fatty acid synthase from grass carp (Ctenopharyngodon idella) and the regulation of its expression by dietary fat level. Aquaculture Nutr. doi:10.1111/j.1365-2095.2011.00917.x

  • Liang XF, Oku H, Ogata HY (2002a) 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 131:335–342

    Google Scholar 

  • Liang XF, Ogata HY, Oku H (2002b) Effects of dietary fatty acids on lipoprotein lipase gene expression in liver and visceral adipose tissue of fed and starved red sea bream Pagrus major. Comp Biochem Physiol A 132:913–919

    Google Scholar 

  • Lin H, Romsos DR, Tack PI, Leveille G (1977) Influence of dietary lipid on lipogenic enzyme activities in coho salmon (Oncorhynchus kisutch (Walbaum)). J Nutr 107:846–854

    PubMed  CAS  Google Scholar 

  • Lindberg A, Olivecrona G (2002) Lipoprotein lipase from rainbow trout differs in several respects from the enzyme in mammals. Gene 292:213–223

    PubMed  CAS  Google Scholar 

  • Magnoni L, Vaillancourt E, Weber JM (2008) In vivo regulation of rainbow trout lipolysis by catecholamines. J Exp Biol 211:2460–2466

    PubMed  CAS  Google Scholar 

  • Mead JR, Irvine SA, Ramji DP (2002) Lipoprotein lipase: structure, function, regulation, and role in disease. J Mol Med 80:753–769

    PubMed  CAS  Google Scholar 

  • Michelsen KG, Harmon JS, Sheridan MA (1994) Adipose tissue lipolysis in rainbow trout, Oncorhynchus mykiss, is modulated by phosphorylation of triacylglycerol lipase. Comp Biochem Physiol B 107:509–513

    Google Scholar 

  • Nanton DA, Vegusdal B, Rørå AMB, Ruyter B, Baeverfjord G, Torstensen BE (2007) Muscle lipid storage pattern, composition, and adipocyte distribution in different parts of Atlantic salmon (Salmo salar) fed fish oil and vegetable oil. Aquaculture 265:230–243

    CAS  Google Scholar 

  • Navarro I, Gutiérrez J (1995) Fasting and starvation. In: Hochachka W, Mommsen T (eds) Biochemistry and molecular biology of fishes, vol 4. Elsevier, London, pp 393–433

    Google Scholar 

  • Nordgarden U, Torstensen BE, Frøyland L, Hansen T, Hemre GI (2003) Seasonally changing metabolism in Atlantic salmon (Salmo salar L.) II—β-oxidation capacity and fatty acid composition in muscle tissues and plasma lipoproteins. Aquaculture Nutr 9:295–303

    CAS  Google Scholar 

  • Ntambi JM, Kim YC (2000) Adipocyte differentiation and gene expression. J Nutr 130:3122S–3126S

    PubMed  CAS  Google Scholar 

  • Oku H, Umino T (2008) Molecular characterization of peroxisome proliferator-activated receptors (PPARs) and their gene expression in the differentiating adipocytes of red sea bream Pagrus major. Comp Biochem Physiol B 151:268–277

    PubMed  Google Scholar 

  • Oku H, Ogata HY, Liang XF (2002) Organization of the lipoprotein lipase gene of red sea bream Pagrus major. Comp Biochem Physiol B 131:775–785

    PubMed  Google Scholar 

  • Oku H, Tokuda M, Okumura T, Umino T (2006) Effects of insulin, triiodothyronine and fat soluble vitamins on adipocyte differentiation and LPL gene expression in the stromal-vascular cells of red sea bream, Pagrus major. Comp Biochem Physiol B 144:326–333

    PubMed  Google Scholar 

  • Palmeri G, Turchini GM, Keast R, Marriorr PJ, Morrisson P, DeSilva SS (2008) Effects of starvation and water quality on the purging process of farmed Murray Cod (Maccullochella peelii peelii). J Agric Food Chem 56:9037–9045

    PubMed  CAS  Google Scholar 

  • Palti Y, Silverstein JT, Wieman H, Phillips JG, Barrows FT, Parsons JE (2006) Evaluation of family growth response to fishmeal and gluten-based diets in rainbow trout (Oncorhynchus mykiss). Aquaculture 255:548–556

    CAS  Google Scholar 

  • Pierce LR, Palti Y, Silverstein JT, Barrows FT, Hallerman EM, Parsons JE (2008) Family growth response to fishmeal and plant-based diets shows genotypeXdiet interaction in rainbow trout (Oncorhynchus mykiss). Aquaculture 278:37–42

    Google Scholar 

  • Planas JV, Capilla E, Gutiérrez J (2000) Molecular identification of a glucose transporter from fish muscle. FEBS Lett 481:266–270

    PubMed  CAS  Google Scholar 

  • Polakof S, Médale F, Skiba-Cassy S, Corraze G, Panserat S (2010) Molecular regulation of lipid metabolism in liver and muscle of rainbow trout subjected to acute and chronic insulin treatments. Domest Anim Endocrinol 39:26–33

    PubMed  CAS  Google Scholar 

  • Polakof S, Médale F, Larroquet L, Vachot C, Corraze G, Panserat S (2011) Insulin stimulates lipogenesis and attenuates beta-oxidation in white adipose tissue of fed rainbow trout. Lipids 46:189–199

    PubMed  CAS  Google Scholar 

  • Pottinger TG (2006) Context dependent differences in growth of two rainbow trout (Oncorhynchus mykiss) lines selected for divergent stress responsiveness. Aquaculture 256:140–147

    Google Scholar 

  • Pottinger TG, Carrick TR (1999) Modification of the plasma cortisol response to stress in rainbow trout by selective breeding. Gen Comp Endocrinol 116:122–132

    PubMed  CAS  Google Scholar 

  • Quillet E, Le Guillou S, Aubin J, Fauconneau B (2005) Two-way selection for muscle lipid content in pan-size rainbow trout (Oncorhynchus mykiss). Aquaculture 245:49–61

    CAS  Google Scholar 

  • Quillet E, Le Guillou S, Aubin J, Labbé L, Fauconneau B, Médale F (2007a) Response of a lean muscle and a fat muscle rainbow trout (Oncorhynchus mykiss) line on growth, nutrient utilization, body composition and carcass traits when fed two different diets. Aquaculture 269:220–231

    CAS  Google Scholar 

  • Quillet E, Bugeon J, Le Guillou S, Davenel A, Collewet G, Labbé L, Médale F (2007b) Effect of selection for muscle lipid content on body shape, fat deposition and dressing yields in rainbow trout. Aquaculture 272:S303

    Google Scholar 

  • Quinton CD, Kause A, Ruohonen K, Koskela J (2007) Genetic relationships of body composition and feed utilization traits in European whitefish (Coregonus lavaretus L.) and implications for selective breeding in fishmeal- and soybean meal-based diet environments. J Anim Sci 85:3198–3208

    PubMed  CAS  Google Scholar 

  • Regost C, Arzel J, Cardinal M, Robin J, Laroche M, Kaushik SJ (2001) Dietary lipid level, hepatic lipogenesis and flesh quality in turbot (Psetta maxima). Aquaculture 193:291–309

    CAS  Google Scholar 

  • Richard N, Kaushik S, Larroquet L, Panserat S, Corraze G (2006a) 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 Nut 96:299–309

    CAS  Google Scholar 

  • Richard N, Mourente G, Kaushik S, Corraze G (2006b) Replacement of a large portion of fish oil by vegetable oils does not affect lipogenesis, lipid transport and tissue lipid uptake in European seabass (Dicentrarchus labrax L.). Aquaculture 261:1077–1087

    CAS  Google Scholar 

  • Saera-Vila A, Calduch-Giner JA, Gómez-Requeni P, Médale F, Kaushik S, Pérez-Sánchez J (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 142:224–232

    PubMed  Google Scholar 

  • Sánchez-Gurmaches J, Cruz-Garcia L, Gutiérrez J, Navarro I (2010) Endocrine control of oleic acid and glucose metabolism in rainbow trout (Oncorhynchus mykiss) muscle cells in culture. Am J Physiol Regul Integr Comp Physiol 299:R562–R572

    PubMed  Google Scholar 

  • Sánchez-Gurmaches J, Østbye TK, Navarro I, Torgersen J, Hevrøy EM, Ruyter B, Torstensen BE (2011) In vivo and in vitro insulin and fasting control of the transmembrane fatty acid transport proteins inAtlantic salmon (Salmo salar). Am J Physiol Regul Integr Comp Physiol 301:R947–R957

    PubMed  Google Scholar 

  • Sánchez-Gurmaches J, Cruz-Garcia L, Gutiérrez J, Navarro I (2012) mRNA expression of fatty acid transporters in rainbow trout: in vivo and in vitro regulation by insulin, fasting and inflammation and infection mediators. Comp Biochem Physiol A Mol Int Physiol 163:177–188

    Google Scholar 

  • Santinha PJM, Medale F, Corraze G, Gomes EFS (1999) Effects of the dietary protein: lipid ratio on growth and nutrient utilization in gilthead seabream (Sparus aurata L.). Aquac Nutr 5:147–156

    CAS  Google Scholar 

  • Scheepers A, Joost A, Schurmann HG (2004) The glucose transporter families SGLT and GLUT: molecular basis of normal and aberrant function. J Parenter Enteral Nutr 28:364–371

    CAS  Google Scholar 

  • Sethi JK, Hotamisligil GS (1999) The role of TNFα in adipocyte metabolism. Sem Cell Dev Biol 10:19–29

    CAS  Google Scholar 

  • Sharma MK, Liu RZ, Thisse C, Thisse B, Denovan-Wright EM, Wright JM (2006) Hierarchical subfunctionalization of fabp1a, fabp1b and fabp10 tissue-specific expression may account for retention of these duplicated genes in the zebrafish (Danio rerio) genome. FEBS J 273:3216–3229

    PubMed  CAS  Google Scholar 

  • Sheridan MA (1986) Effects of thyroxin, cortisol, growth hormone and prolactin on lipid metabolism of coho salmon, Oncorhynchus kisutch, during smoltification. Gen Comp Endocrinol 64:220–238

    PubMed  CAS  Google Scholar 

  • Sheridan MA (1988) Lipid dynamics in fish: aspect of absorption, transportation, deposition and mobilization. Comp Biochem Physiol 90B:679–690

    CAS  Google Scholar 

  • Sheridan MA (1994) Regulation of lipid metabolism in poikilothermic vertebrates. Comp Biochem Physiol 107B:495–508

    CAS  Google Scholar 

  • Shindo K, Tsuchiya T, Matsumoto JJ (1986) Histological study on white and dark muscles of various fishes. Bull Japan Soc Sci Fish 52:1377–1399

    Google Scholar 

  • Skinner ER, Youssef AM (1982) The characterization of lipoprotein lipase isolated from the post-heparin plasma of the rainbow trout, Salmo gairdneri Richardson. Biochem J 203:727–734

    PubMed  CAS  Google Scholar 

  • Smith RB, Kincaid HL, Regenstein JM, Rumsey GL (1988) Growth, carcass composition, and taste of rainbow trout of different strains fed diets containing primarily plant or animal protein. Aquaculture 70:309–321

    Google Scholar 

  • Smith S, Witkowski A, Joshi AK (2003) Structural and functional organization of the animal fatty acid synthase. Progr Lipid Res 42:289–317

    CAS  Google Scholar 

  • Strable MS, Ntambi JM (2010) Genetic control of de novo lipogenesis: role in diet-induced obesity. Crit Rev Biochem Mol Biol 45:199–214

    PubMed  CAS  Google Scholar 

  • Stubhaug I, Frøyland L, Torstensen BE (2005) β-Oxidation capacity of red and white muscle and liver in Atlantic Salmon (Salmo salar L.)—effects of increasing dietary rapeseed oil and olive oil to replace capelin oil. Lipids 40:39–47

    PubMed  CAS  Google Scholar 

  • Teerijoki H, Krasnov A, Pitkanen TI, Molsa H (2000) Cloning and characterization of glucose transporter in teleost fish rainbow trout (Oncorhynchus mykiss). Biochim Biophys Acta 1494:290–294

    PubMed  CAS  Google Scholar 

  • Teerijoki H, Krasnov A, Pitkänen TI, Molsa H (2001) Monosaccharide uptake in common carp (Cyprinus carpio) EPC cells is mediated by a facilitative glucose carrier. Comp Biochem Physiol 128B:483–491

    CAS  Google Scholar 

  • Todorčević M, Vegusdal A, Gjøen T, Sundvold H, Torstensen BE, Kjær MA, Ruyter B (2008) Changes in fatty acids metabolism during differentiation of Atlantic salmon preadipocytes; effects of n-3 and n-9 fatty acids. Biochim Biophys Acta 1781:326–335

    PubMed  Google Scholar 

  • Todorčević M, Škugor S, Krasnov A, Ruyter B (2010) Gene expression profiles in Atlantic salmon adipose-derived stromo-vascular fraction during differentiation into adipocytes. BMC Genomics 11:39–56

    PubMed  Google Scholar 

  • Torstensen BE, Lie Ø, Frøyland L (2000) Lipid 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 35:653–664

    PubMed  CAS  Google Scholar 

  • Torstensen BE, Frøyland L, Lie Ø (2004) 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. Aquac Nutr 10:175–192

    CAS  Google Scholar 

  • Torstensen BE, Espe M, Stubhaug I, Lie Ø (2011) Dietary plant proteins and vegetable oil blends increase adiposity and plasma lipids in Atlantic salmon (Salmo salar L.). Br J Nutr 106:633–647

    Google Scholar 

  • Torstensen BE, Nanton DA, Olsvik PA, Shundvold H, Stubhaug I (2009) Gene expression of fatty acid-binding proteins, fatty acid transport proteins (cd36 and FATP) and β-oxidation-related genes in Atlantic salmon (Salmo salar L.) fed fish oil or vegetable oil. Aquac Nutr 15:440–451

    CAS  Google Scholar 

  • van Heeswijk JCF, Vianen GJ, van den Thillart EEJM, Zaagsma J (2005) Beta-adrenergic control of plasma glucose and free fatty acid levels in the air-breathing African catfish Clarias gariepinus Burchell 1822. J Exp Biol 208:2217–2225

    PubMed  Google Scholar 

  • Vegusdal A, Sundvold H, Gjøen T, Ruyter B (2003) An in vitro method for studying the proliferation and differentiation of Atlantic salmon preadipocytes. Lipids 38:289–296

    PubMed  CAS  Google Scholar 

  • Vianen GJ, Obels PP, van den Thillart GEEJM, Zaagsma J (2002) ß-adrenoceptors mediate inhibition of lipolysis in adipocytes of tilapia (Oreochromis mossambicus). Am J Physiol Endocrinol Metab 282:E318–E325

    PubMed  CAS  Google Scholar 

  • Volkoff H, Peter RE (2006) Feeding behavior in fish and its control. Zebrafish 3:131–140

    PubMed  CAS  Google Scholar 

  • Volkoff H, Hoskins LJ, Tuziak SM (2010) Influence of intrinsic signals and environmental cues on the endocrine control of feeding in fish: potential application in aquaculture. Gen Comp Endocrinol 167:352–359

    PubMed  CAS  Google Scholar 

  • Weil C, Blaise O, Breton B, Carré F, Fauconneau B, Gomez JM, Le Bail PY, Le Gac F (2000) Puberty in rainbow trout: role of growth and metabolic hormones. In: Proceedings of the molecular mechanisms of morphogenesis in the early development of fish. National Research Institute of Aquaculture, Nansei, Mie Japan, pp 34–36

  • Weil C, Goupil AS, Quillet E, Labbé L, Le Gac F (2008) Two-way selection for muscle lipid content modifies puberty and gametogenesis in rainbow trout. Cybium 32(2S):198

    Google Scholar 

  • Weil C, Sabin N, Bugeon J, Paboeuf G, Lefèvre F (2009) Differentially expressed proteins in rainbow trout adipocytes isolated from visceral and subcutaneous tissues. Comp Biochem Physiol D 4:235–241

    Google Scholar 

  • Zhou S, Ackman RG, Morrison C (1995) Storage of lipids in the myosepta of Atlantic salmon (Salmo salar). Fish Physiol Biochem 14:171–178

    CAS  Google Scholar 

  • Zhou S, Ackman RG, Morrison C (1996) Adipocytes and lipid distribution in the muscle tissue of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 53:326–332

    Google Scholar 

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Acknowledgments

For non published results, the authors received funding from Institut National de la Recherche Agronomique, Département de Physiologie animale et système d’Elevage and the European Community’s Sixth and Seventh Framework Programme, under grant agreement no. 513962, AQUAFIRST project and no. 222719, LIFECYCLE project, respectively. The authors are grateful to the staff of the PEIMA facilities and to D. Abel (Centre for Ecology and Hydrology, Lancaster) for fish rearing and assistance with slaughter measurements, and to N. Sabin for image analysis of adipose tissues.

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Weil, C., Lefèvre, F. & Bugeon, J. Characteristics and metabolism of different adipose tissues in fish. Rev Fish Biol Fisheries 23, 157–173 (2013). https://doi.org/10.1007/s11160-012-9288-0

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Keywords

  • Adipose tissue
  • Regional localization
  • Adiposity regulation
  • Intrinsic and extrinsic factors
  • Fish