Advertisement

Reviews in Fish Biology and Fisheries

, Volume 23, Issue 2, pp 157–173 | Cite as

Characteristics and metabolism of different adipose tissues in fish

  • Claudine WeilEmail author
  • Florence Lefèvre
  • Jerôme Bugeon
Reviews

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.

Keywords

Adipose tissue Regional localization Adiposity regulation Intrinsic and extrinsic factors Fish 

Notes

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.

References

  1. 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 77:504–516PubMedGoogle Scholar
  2. 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–R265PubMedGoogle Scholar
  3. 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 142:347–354Google Scholar
  4. 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 184:527–534PubMedGoogle Scholar
  5. Albalat A, Sánchez-Gurmaches J, Gutiérrez J, Navarro I (2006) Regulation of lipoprotein lipase activity in rainbow trout (Oncorhynchus mykiss) tissues. Gen Comp Endocrinol 146:226–235PubMedGoogle Scholar
  6. 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 148:151–159PubMedGoogle Scholar
  7. Ando S, Mori Y, Nakamura K, Sugawara A (1993) Characteristics of lipid accumulation types in five species of fish. Nippon Suisan Gakk 59:1559–1664Google Scholar
  8. 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 317:79–88Google Scholar
  9. 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 1731:88–94PubMedGoogle Scholar
  10. 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 100:992–1003PubMedGoogle Scholar
  11. 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 157:297–309Google Scholar
  12. 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 39:1085–1092PubMedGoogle Scholar
  13. Bouraoui L, Gutiérrez J, Navarro I (2008) Regulation of proliferation and differentiation of adipocyte precursor cells in rainbow trout (Oncorhynchus mykiss). J Endocrinol 198:459–469PubMedGoogle Scholar
  14. 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–R41PubMedGoogle Scholar
  15. 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 161:83–88Google Scholar
  16. 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 17:54–63Google Scholar
  17. 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 20:105–118PubMedGoogle Scholar
  18. 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 20:1011–1024PubMedGoogle Scholar
  19. 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–E49PubMedGoogle Scholar
  20. 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–E357PubMedGoogle Scholar
  21. Chmurzynska A (2006) The multigene family of fatty acid-binding proteins (FABPs): function, structure and polymorphism. J Appl Genet 47:39–48PubMedGoogle Scholar
  22. Christodoulides C, Vidal-Puig A (2010) PPARs and adipocyte function. Mol Cel Endocrinol 318:61–68Google Scholar
  23. Cristancho AG, Lazar MA (2011) Forming functional fat: a growing understanding of adipocyte differentiation. Nat RevMol Cell Biol 12:722–734Google Scholar
  24. 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 212:2254–2260PubMedGoogle Scholar
  25. 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 A158:391–399Google Scholar
  26. 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–E49Google Scholar
  27. Farmer SR (2006) Transcriptional control of adipocyte formation. Cell Metab 4:263–273PubMedGoogle Scholar
  28. 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 3:369–381Google Scholar
  29. Fauconneau B, Alami-Durante GH, Laroche M, Marcel J, Vallot D (1995) Growth and meat quality relations in carp. Aquaculture 129:265–297Google Scholar
  30. 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 50:296–314Google Scholar
  31. 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 33:923–930PubMedGoogle Scholar
  32. 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 38:551–579Google Scholar
  33. 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 41:487–503PubMedGoogle Scholar
  34. Glatz JFC, Luiken JJFP, Bonen A (2010) Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol Rev 90:367–417PubMedGoogle Scholar
  35. Green HS, Selivonchick DP (1987) Lipid metabolism in fish. Prog Lipid Res 26:53–85Google Scholar
  36. Guderley H (2004) Metabolic responses to low temperature in fish muscle. Biol Rev 79:409–427PubMedGoogle Scholar
  37. 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 62:803–815Google Scholar
  38. 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 9:107–112Google Scholar
  39. 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 207:4697–4706PubMedGoogle Scholar
  40. 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 1730:245–252PubMedGoogle Scholar
  41. 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 209:4490–4502PubMedGoogle Scholar
  42. Harmon JS, Sheridan MA (1992) Effects of nutritional state, insulin, and glucagon on lipid mobilization in rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 8:214–221Google Scholar
  43. Harmon JS, Michelsen KG, Sheridan MA (1991) Purification and characterization of hepatic triacylglycerol lipase isolated from rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 9:361–368Google Scholar
  44. Hazel JR, Sidell BD (2004) The substrate specificity of hormone-sensitive lipase from adipose tissue of the Antartic fish Trematomus newnesi. J Exp Biol 207:897–903PubMedGoogle Scholar
  45. Henderson RJ, Tocher DR (1987) The lipid-composition and biochemistry of fresh-water fish. Prog Lipid Res 26:281–347PubMedGoogle Scholar
  46. Hillgartner FB, Salati LM, Goodridge AG (1995) Physiological and molecular mechanisms involved in nutritional regulation of fatty acid synthesis. Physiol Rev 75:47–76PubMedGoogle Scholar
  47. Holm C, Østerlund T, Laurell H, Contreras JA (2000) Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Annu Rev Nutr 20:365–393PubMedGoogle Scholar
  48. 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 16:72–80Google Scholar
  49. 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 151:357–363Google Scholar
  50. 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 20:105–119Google Scholar
  51. Ishiki M, Klip A (2005) Minireview: recent developments in the regulation of glucose transporter-4 traffic: new signals, locations, and partners. Endocrinology 146:5071–5078PubMedGoogle Scholar
  52. 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 21:681–692Google Scholar
  53. Jobling M, Johansen SJS (2003) Fat distribution in Atlantic salmon Salmo salar L. in relation to body size and feeding regime. Aquac Res 34:311–316Google Scholar
  54. 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 29:601–607Google Scholar
  55. 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 33:875–889Google Scholar
  56. Johnston IA (1981) Structure and function of fish muscles. Symp zool Soc Lond 48:71–113Google Scholar
  57. 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 145:147–158PubMedGoogle Scholar
  58. Katikou P, Hughes SI, Robb DHF (2001) Lipid distribution within Atlantic salmon (Salmo salar) fillets. Aquaculture 202:89–99Google Scholar
  59. Kaushik SJ (1986) Environmental effects on feed utilization. Fish Physiol Biochem 2:131–140Google Scholar
  60. 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 93:373–387Google Scholar
  61. 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 158:52–60Google Scholar
  62. 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–R1164PubMedGoogle Scholar
  63. 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 103:629–642PubMedGoogle Scholar
  64. Krasnov A, Teerijoki H, Molsa H (2001) Rainbow trout (Oncorhynchus mykiss) hepatic glucose transporter. Biochim Biophys Acta 1520:174–178PubMedGoogle Scholar
  65. Lampidonis AD, Rogdakis E, Voutsinas GE, Stravopodis DJ (2011) The resurgence of hormone-sensitive lipase (HSL) in mammalian lipolysis. Gene 477:1–11PubMedGoogle Scholar
  66. 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 91–108Google Scholar
  67. Le Bail PY, Bœuf G (1997) What hormones may regulate food intake in fish? Aquat Living Resour 10:371–379Google Scholar
  68. 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 42:583–592Google Scholar
  69. 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 146:3150–3162PubMedGoogle Scholar
  70. 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):73–94Google Scholar
  71. Lefterova MI, Lazar MA (2009) New developments in adipogenesis. Trends Endocrinol Metab 20:107–114PubMedGoogle Scholar
  72. 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 22:2941–2952Google Scholar
  73. 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
  74. 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 131:335–342Google Scholar
  75. 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 132:913–919Google Scholar
  76. 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 107:846–854PubMedGoogle Scholar
  77. Lindberg A, Olivecrona G (2002) Lipoprotein lipase from rainbow trout differs in several respects from the enzyme in mammals. Gene 292:213–223PubMedGoogle Scholar
  78. Magnoni L, Vaillancourt E, Weber JM (2008) In vivo regulation of rainbow trout lipolysis by catecholamines. J Exp Biol 211:2460–2466PubMedGoogle Scholar
  79. Mead JR, Irvine SA, Ramji DP (2002) Lipoprotein lipase: structure, function, regulation, and role in disease. J Mol Med 80:753–769PubMedGoogle Scholar
  80. 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 107:509–513Google Scholar
  81. 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 265:230–243Google Scholar
  82. 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 393–433Google Scholar
  83. 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 9:295–303Google Scholar
  84. Ntambi JM, Kim YC (2000) Adipocyte differentiation and gene expression. J Nutr 130:3122S–3126SPubMedGoogle Scholar
  85. 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 151:268–277PubMedGoogle Scholar
  86. Oku H, Ogata HY, Liang XF (2002) Organization of the lipoprotein lipase gene of red sea bream Pagrus major. Comp Biochem Physiol B 131:775–785PubMedGoogle Scholar
  87. 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 144:326–333PubMedGoogle Scholar
  88. 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 56:9037–9045PubMedGoogle Scholar
  89. 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 255:548–556Google Scholar
  90. 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 278:37–42Google Scholar
  91. Planas JV, Capilla E, Gutiérrez J (2000) Molecular identification of a glucose transporter from fish muscle. FEBS Lett 481:266–270PubMedGoogle Scholar
  92. 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 39:26–33PubMedGoogle Scholar
  93. 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 46:189–199PubMedGoogle Scholar
  94. Pottinger TG (2006) Context dependent differences in growth of two rainbow trout (Oncorhynchus mykiss) lines selected for divergent stress responsiveness. Aquaculture 256:140–147Google Scholar
  95. Pottinger TG, Carrick TR (1999) Modification of the plasma cortisol response to stress in rainbow trout by selective breeding. Gen Comp Endocrinol 116:122–132PubMedGoogle Scholar
  96. 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 245:49–61Google Scholar
  97. 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 269:220–231Google Scholar
  98. 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:S303Google Scholar
  99. 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 85:3198–3208PubMedGoogle Scholar
  100. 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 193:291–309Google Scholar
  101. 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 96:299–309Google Scholar
  102. 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 261:1077–1087Google Scholar
  103. 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 142:224–232PubMedGoogle Scholar
  104. 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–R572PubMedGoogle Scholar
  105. 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–R957PubMedGoogle Scholar
  106. 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 163:177–188Google Scholar
  107. 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 5:147–156Google Scholar
  108. 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 28:364–371Google Scholar
  109. Sethi JK, Hotamisligil GS (1999) The role of TNFα in adipocyte metabolism. Sem Cell Dev Biol 10:19–29Google Scholar
  110. 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 273:3216–3229PubMedGoogle Scholar
  111. Sheridan MA (1986) Effects of thyroxin, cortisol, growth hormone and prolactin on lipid metabolism of coho salmon, Oncorhynchus kisutch, during smoltification. Gen Comp Endocrinol 64:220–238PubMedGoogle Scholar
  112. Sheridan MA (1988) Lipid dynamics in fish: aspect of absorption, transportation, deposition and mobilization. Comp Biochem Physiol 90B:679–690Google Scholar
  113. Sheridan MA (1994) Regulation of lipid metabolism in poikilothermic vertebrates. Comp Biochem Physiol 107B:495–508Google Scholar
  114. Shindo K, Tsuchiya T, Matsumoto JJ (1986) Histological study on white and dark muscles of various fishes. Bull Japan Soc Sci Fish 52:1377–1399Google Scholar
  115. 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 203:727–734PubMedGoogle Scholar
  116. 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 70:309–321Google Scholar
  117. Smith S, Witkowski A, Joshi AK (2003) Structural and functional organization of the animal fatty acid synthase. Progr Lipid Res 42:289–317Google Scholar
  118. Strable MS, Ntambi JM (2010) Genetic control of de novo lipogenesis: role in diet-induced obesity. Crit Rev Biochem Mol Biol 45:199–214PubMedGoogle Scholar
  119. 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 40:39–47PubMedGoogle Scholar
  120. 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 1494:290–294PubMedGoogle Scholar
  121. 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:483–491Google Scholar
  122. 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 1781:326–335PubMedGoogle Scholar
  123. 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 11:39–56PubMedGoogle Scholar
  124. 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 35:653–664PubMedGoogle Scholar
  125. 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 10:175–192Google Scholar
  126. 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 106:633–647Google Scholar
  127. 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 15:440–451Google Scholar
  128. 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 208:2217–2225PubMedGoogle Scholar
  129. Vegusdal A, Sundvold H, Gjøen T, Ruyter B (2003) An in vitro method for studying the proliferation and differentiation of Atlantic salmon preadipocytes. Lipids 38:289–296PubMedGoogle Scholar
  130. 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–E325PubMedGoogle Scholar
  131. Volkoff H, Peter RE (2006) Feeding behavior in fish and its control. Zebrafish 3:131–140PubMedGoogle Scholar
  132. 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 167:352–359PubMedGoogle Scholar
  133. 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 34–36Google Scholar
  134. 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):198Google Scholar
  135. 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 4:235–241Google Scholar
  136. Zhou S, Ackman RG, Morrison C (1995) Storage of lipids in the myosepta of Atlantic salmon (Salmo salar). Fish Physiol Biochem 14:171–178Google Scholar
  137. 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 53:326–332Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Claudine Weil
    • 1
    Email author
  • Florence Lefèvre
    • 1
  • Jerôme Bugeon
    • 1
  1. 1.INRA, UR1037 Laboratoire de Physiologie et Génomique des Poissons (ex SCRIBE)RennesFrance

Personalised recommendations