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Dietary Fatty Acid Metabolism is Affected More by Lipid Level than Source in Senegalese Sole Juveniles: Interactions for Optimal Dietary Formulation

  • Original Article
  • Published:
Lipids

Abstract

This study analyses the effects of dietary lipid level and source on lipid absorption and metabolism in Senegalese sole (Solea senegalensis). Juvenile fish were fed 4 experimental diets containing either 100 % fish oil (FO) or 25 % FO and 75 % vegetable oil (VO; rapeseed, linseed and soybean oils) at two lipid levels (~8 or ~18 %). Effects were assessed on fish performance, body proximate composition and lipid accumulation, activity of hepatic lipogenic and fatty acid oxidative enzymes and, finally, on the expression of genes related to lipid metabolism in liver and intestine, and to intestinal absorption, both pre- and postprandially. Increased dietary lipid level had no major effects on growth and feeding performance (FCR), although fish fed FO had marginally better growth. Nevertheless, diets induced significant changes in lipid accumulation and metabolism. Hepatic lipid deposits were higher in fish fed VO, associated to increased hepatic ATP citrate lyase activity and up-regulated carnitine palmitoyltransferase 1 (cpt1) mRNA levels post-prandially. However, lipid level had a larger effect on gene expression of metabolic (lipogenesis and β-oxidation) genes than lipid source, mostly at fasting. High dietary lipid level down-regulated fatty acid synthase expression in liver and intestine, and increased cpt1 mRNA in liver. Large lipid accumulations were observed in the enterocytes of fish fed high lipid diets. This was possibly a result of a poor capacity to adapt to high dietary lipid level, as most genes involved in intestinal absorption were not regulated in response to the diet.

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Abbreviations

ACOX1:

Acyl-CoA oxidase 1

ALA:

α-Linolenic acid

APOA4:

Apolipoprotein A4

ARA:

Arachidonic acid

CD36:

Cluster of differentiation 36 family

CPT1:

Carnitine palmitoyltransferase 1

DHA:

Docosahexaenoic acid

EPA:

Eicosapentaenoic acid

FA:

Fatty acid

FABP:

Fatty acid binding protein

FAS:

Fatty acid synthase

FCR:

Food conversion ratio

HSI:

Hepatosomatic index

MTP:

Microsomal triglyceride transfer protein

MUFA:

Monounsaturated fatty acid

LC-PUFA:

Long-chain polyunsaturated fatty acid

LNA:

Linoleic acid

PUFA:

Polyunsaturated fatty acid

SFA:

Saturated fatty acid

VSI:

Viscerosomatic index

References

  1. Turchini GM, Torstensen BE, Ng W-K (2009) Fish oil replacement in finfish nutrition. Rev Aquac 1:10–57

    Article  Google Scholar 

  2. Turchini GM, Ng W-K, Tocher DR (2010) Fish oil replacement and alternative lipid sources in aquaculture feeds. CRC Press, Boca Raton

    Book  Google Scholar 

  3. Sargent J, Bell G, McEvoy L, Tocher D, Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199

    Article  CAS  Google Scholar 

  4. Montero D, Kalinowski T, Obach A, Robaina L, Tort L, Caballero M, Izquierdo M (2003) Vegetable lipid sources for gilthead seabream (Sparus aurata): effects on fish health. Aquaculture 225:353–370

    Article  CAS  Google Scholar 

  5. Nasopoulou C, Zabetakis I (2012) Benefits of fish oil replacement by plant originated oils in compounded fish feeds. A review. LWT–Food Sci Technol 47:217–224

    Article  CAS  Google Scholar 

  6. Zuo R, Mai K, Xu W, Turchini GM, Ai Q (2015) Dietary ALA, but not LNA, increase growth, reduce inflammatory processes, and increase anti-oxidant capacity in the marine finfish Larimichthys crocea. Lipids 50(2):149–163

    Article  PubMed  CAS  Google Scholar 

  7. Sales J, Glencross B (2011) A meta-analysis of the effects of dietary marine oil replacement with vegetable oils on growth, feed conversion and muscle fatty acid composition of fish species. Aquac Nutr 17:e271–e287

    Article  Google Scholar 

  8. Jobling M, Larsen A, Andreassen B, Olsen R (2002) Adiposity and growth of post-smolt Atlantic salmon Salmo salar L. Aquac Res 33:533–541

    Article  Google Scholar 

  9. Tocher DR, Bell JG, McGhee F, Dick JR, Fonseca-Madrigal J (2003) Effects of dietary lipid level and vegetable oil on fatty acid metabolism in Atlantic salmon (Salmo salar L.) over the whole production cycle. Fish Physiol Biochem 29:193–209

    Article  CAS  Google Scholar 

  10. Kenari AA, Mozanzadeh MT, Pourgholam R (2011) Effects of total fish oil replacement to vegetable oils at two dietary lipid levels on the growth, body composition, haemato-immunological and serum biochemical parameters in caspian brown trout (Salmo trutta caspius Kessler, 1877). Aquac Res 42:1131–1144

    Article  CAS  Google Scholar 

  11. Figueiredo-Silva AC, Kaushik S, Terrier F, Schrama JW, Médale F, Geurden I (2012) Link between lipid metabolism and voluntary food intake in rainbow trout fed coconut oil rich in medium-chain TAG. Br J Nutr 107:1714–1725

    Article  PubMed  CAS  Google Scholar 

  12. Kim D-K, Kim K-D, Seo J-Y, Lee S-M (2012) Effects of dietary lipid source and level on growth performance, blood parameters and flesh quality of sub-adult olive flounder (Paralichthys olivaceus). Asian-Australas J Anim Sci 25:869

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Morais S, Aragão C, Cabrita E, Conceição LEC, Constenla M, Costas B, Dias J, Duncan N, Engrola S, Estevez A, Gisbert E, Mañanós E, Valente LMP, Yúfera M, Dinis MT (2015) New developments and biological insights into the farming of Solea senegalensis reinforcing its aquaculture potential. Rev Aquac. doi:10.1111/raq.12091

  14. Borges P, Oliveira B, Casal S, Dias J, Conceiçao L, Valente LM (2009) Dietary lipid level affects growth performance and nutrient utilisation of Senegalese sole (Solea senegalensis) juveniles. Br J Nutr 102:1007–1014

    Article  PubMed  CAS  Google Scholar 

  15. Valente LMP, Linares F, Villanueva JLR, Silva JMG, Espe M, Escórcio C, Pires MA, Saavedra MJ, Borges P, Medale F, Alvárez-Blázquez B, Peleteiro JB (2011) Dietary protein source or energy levels have no major impact on growth performance, nutrient utilisation or flesh fatty acids composition of market-sized Senegalese sole. Aquaculture 318:128–137

    Article  CAS  Google Scholar 

  16. Lee SM, Cho SH, Kim KD (2000) Effects of dietary protein and energy levels on growth and body composition of juvenile flounder Paralichthys olivaceus. J World Aquac Soc 31:306–315

    Article  Google Scholar 

  17. Borges P, Fo Medale, Dias J, Valente LMP (2013) Protein utilisation and intermediary metabolism of Senegalese sole (Solea senegalensis) as a function of protein:lipid ratio. Br J Nutr 109:1373–1381

    Article  PubMed  CAS  Google Scholar 

  18. Borges P, Medale F, Veron V, dos Anjos Pires M, Dias J, Valente LM (2013) Lipid digestion, absorption and uptake in Solea senegalensis. Comp Biochem Physiol A: Mol Integr Physiol 166:26–35

    Article  CAS  Google Scholar 

  19. Guerreiro I, Peres H, Castro-Cunha M, Olivia-Teles A (2012) Effect of temperature and dietary protein/lipid ratio on growth performance and nutrient utilization of juvenile Senegalese sole (Solea senegalensis). Aquac Nutr 18:98–106

    Article  CAS  Google Scholar 

  20. Einen O, Roem A (1997) Dietary protein/energy ratios for Atlantic salmon in relation to fish size: growth, feed utilization and slaughter quality. Aquac Nutr 3:115–126

    Article  Google Scholar 

  21. Hemre G, Sandnes K (1999) Effect of dietary lipid level on muscle composition in Atlantic salmon Salmo salar. Aquac Nutr 5:9–16

    Article  CAS  Google Scholar 

  22. Vergara JM, Robainà L, Izquierdo M, Higuera MDL (1996) Protein sparing effect of lipids in diets for fingerlings of gilthead sea bream. Fish Sci 62:624–628

    CAS  Google Scholar 

  23. Peres H, Oliva-Teles A (1999) Effect of dietary lipid level on growth performance and feed utilization by European sea bass juveniles (Dicentrarchus labrax). Aquaculture 179:325–334

    Article  CAS  Google Scholar 

  24. Skalli A, Hidalgo M, Abellán E, Arizcun M, Cardenete G (2004) Effects of the dietary protein/lipid ratio on growth and nutrient utilization in common dentex (Dentex dentex L.) at different growth stages. Aquaculture 235:1–11

    Article  CAS  Google Scholar 

  25. Borges P, Reis B, Fernandes TJ, Palmas Â, Castro-Cunha M, Médale F, Oliveira MBP, Valente LM (2014) Senegalese sole juveniles can cope with diets devoid of supplemental fish oil while preserving flesh nutritional value. Aquaculture 418:116–125

    Article  CAS  Google Scholar 

  26. Caballero MJ, Gallardo G, Robaina L, Montero D, Fernández A, Izquierdo M (2006) Vegetable lipid sources in vitro biosyntheis of triacylglycerols and phospholipids in the intestine of sea bream (Sparus aurata). Br J Nutr 95:448–454

    Article  PubMed  CAS  Google Scholar 

  27. Jump DB (2004) Fatty acid regulation of gene transcription. Crit Rev Clin Lab Sci 41:41–78

    Article  PubMed  CAS  Google Scholar 

  28. Morais S, Mourente G, Martínez A, Gras N, Tocher DR (2015) Docosahexaenoic acid biosynthesis via fatty acyl elongase and D4-desaturase and its modulation by dietary lipid level and fatty acid composition in a marine vertebrate. Biochim Biophys Acta 1851:588–597

    Article  PubMed  CAS  Google Scholar 

  29. Dias J, Yúfera M, Valente LM, Rema P (2010) Feed transit and apparent protein, phosphorus and energy digestibility of practical feed ingredients by Senegalese sole (Solea senegalensis). Aquaculture 302:94–99

    Article  CAS  Google Scholar 

  30. AOAC (2005) Official Method 968.06. In: Official methods of analysis of AOAC International, 18th edn. AOAC International, Gaithersburg

  31. AOAC (2005) Official method 942.05. In: Official methods of analysis of AOAC International, 18th edn. AOAC International, Gaithersburg

  32. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  33. Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  34. Folch J, Lees M, Sloane-Stanley G (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  35. Gisbert E, Ortiz-Delgado JB, Sarasquete C (2008) Nutritional cellular biomarkers in early life stages of fish. Histol Histopathol 23(12):1525–1539

    PubMed  CAS  Google Scholar 

  36. Boglino A, Gisbert E, Darias MJ, Estévez A, Andree KB, Sarasquete C, Bosco Ortiz-Delgado J (2012) Isolipidic diets differing in their essential fatty acid profiles affect the deposition of unsaturated neutral lipids in the intestine, liver and vascular system of Senegalese sole larvae and early juveniles. Comp Biochem Physiol B: Biochem Mol Biol 162:59–70

    Article  CAS  Google Scholar 

  37. Alvarez M, Diez A, Lopez-Bote C, Gallego M, Bautista J (2000) Short-term modulation of lipogenesis by macronutrients in rainbow trout (Oncorhynchus mykiss) hepatocytes. Brit J Nutr 84:619–628

    PubMed  CAS  Google Scholar 

  38. Kolditz C, Borthaire M, Richard N, Corraze G, Panserat S, Vachot C, Lefevre 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

    Article  PubMed  CAS  Google Scholar 

  39. Ditlecadet D, Driedzic WR (2013) Glycerol-3-phosphatase and not lipid recycling is the primary pathway in the accumulation of high concentrations of glycerol in rainbow smelt (Osmerus mordax). Am J Physiol Regul Integr Comp Physiol 304:R304–R312

    Article  PubMed  CAS  Google Scholar 

  40. Smith P, Krohn RI, Hermanson G, Mallia A, Gartner F, Provenzano M, Fujimoto E, Goeke N, Olson B, Klenk D (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  PubMed  CAS  Google Scholar 

  41. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  42. Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291

    Article  PubMed  CAS  Google Scholar 

  43. Librán-Pérez M, Polakof S, López-Patiño MA, Míguez JM, Soengas JL (2012) Evidence of a metabolic fatty acid-sensing system in the hypothalamus and Brockmann bodies of rainbow trout: implications in food intake regulation. Am J Physiol Regul Integr Comp Physiol 302:R1340–R1350

    Article  PubMed  CAS  Google Scholar 

  44. Infante C, Matsuoka MP, Asensio E, Cañavate JP, Reith M, Manchado M (2008) Selection of housekeeping genes for gene expression studies in larvae from flatfish using real-time PCR. BMC Mol Biol 9:28

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7):Research0034.1–Research0034.11

    Article  Google Scholar 

  46. Mandrioli L, Sirri R, Gatta P, Morandi F, Sarli G, Parma L, Fontanillas R, Bonaldo A (2012) Histomorphologic hepatic features and growth performances of juvenile Senegalese sole (Solea senegalensis) fed isogenertic practical diets with variable protein/lipid levels. J Appl Ichthyol 28:628–632

    Article  CAS  Google Scholar 

  47. Benítez-Dorta V, Caballero MJ, Izquierdo M, Manchado M, Infante C, Zamorano MJ, Montero D (2013) Total substitution of fish oil by vegetable oils in Senegalese sole (Solea senegalensis) diets: effects on fish performance, biochemical composition, and expression of some glucocorticoid receptor-related genes. Fish Physiol Biochem 39:335–349

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  49. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184

    Article  CAS  Google Scholar 

  50. Cabral E, Bacelar M, Batista S, Castro-Cunha M, Ozório R, Valente L (2011) Replacement of fishmeal by increasing levels of plant protein blends in diets for Senegalese sole (Solea senegalensis) juveniles. Aquaculture 322:74–81

    Article  CAS  Google Scholar 

  51. Fernandes T, Alves RC, Souza T, Silva J, Castro-Cunha M, Valente L, Oliveira M (2012) Lipid content and fatty acid profile of Senegalese sole (Solea senegalensis Kaup, 1858) juveniles as affected by feed containing different amounts of plant protein sources. Food Chem 134:1337–1342

    Article  PubMed  CAS  Google Scholar 

  52. Fernandes TJR, Alves RC, Souza T, Silva JMG, Castro-Cunha M, Valente LMP, Oliveira MBPP (2012) Lipid content and fatty acid profile of Senegalese sole (Solea senegalensis Kaup, 1858) juveniles as affected by feed containing different amounts of plant protein sources. Food Chem 134:1337–1342

    Article  PubMed  CAS  Google Scholar 

  53. Dias J, Rueda-Jasso R, Panserat S, Conceição LECd, Gomes EF, Dinis MT (2004) Effect of dietary carbohydrate-to-lipid ratios on growth, lipid deposition and metabolic hepatic enzymes in juvenile Senegalese sole (Solea senegalensis, Kaup). Aquac Res 35:1122–1130

    Article  CAS  Google Scholar 

  54. Caballero MJ, Obach A, Rosenlund G, Montero D, Gisvold M, Izquierdo MS (2002) Impact of different dietary lipid sources on growth, lipid digestibility, tissue fatty acid composition and histology of rainbow trout, Oncorhynchus mykiss. Aquaculture 214:253–271

    Article  CAS  Google Scholar 

  55. Rueda-Jasso R, Conceiçao LE, Dias J, De Coen W, Gomes E, Rees J-F, Soares F, Dinis MT, Sorgeloos P (2004) Effect of dietary non-protein energy levels on condition and oxidative status of Senegalese sole (Solea senegalensis) juveniles. Aquaculture 231:417–433

    Article  CAS  Google Scholar 

  56. Cabral E, Fernandes T, Campos S, Castro-Cunha M, Oliveira M, Cunha L, Valente L (2013) Replacement of fish meal by plant protein sources up to 75 % induces good growth performance without affecting flesh quality in ongrowing Senegalese sole. Aquaculture 380:130–138

    Article  CAS  Google Scholar 

  57. Gaylord T, Gatlin D (2000) Dietary lipid level but not l-carnitine affects growth performance of hybrid striped bass (Morone chrysops♀ × M. saxatilis♂). Aquaculture 190:237–246

    Article  CAS  Google Scholar 

  58. Borges P, Valente LM, Véron V, Dias K, Panserat S, Médale F (2014) High dietary lipid level is associated with persistent hyperglycaemia and downregulation of muscle Akt-mTOR pathway in Senegalese sole (Solea senegalensis). PLoS One 9:e102196

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Kjørsvik E, van der Meeren T, Kryvi H, Arnfinnson J, Kvenseth PG (1991) Early development of the digestive tract of cod larvae, Gadus morhua L., during start-feeding and starvation. J Fish Biol 38:1–15

    Article  Google Scholar 

  60. Bonvini E, Parma L, Mandrioli L, Sirri R, Brachelente C, Mongile F, Gatta PP, Bonaldo A (2015) Feeding common sole (Solea solea) juveniles with increasing dietary lipid levels affects growth, feed utilization and gut health. Aquaculture. doi:10.1016/j.aquaculture.2015.01.013

    Google Scholar 

  61. Clarke SD, Jump DB (1994) Dietary polyunsaturated fatty acid regulation of gene transcription. Annu Rev Nutr 14:83–98

    Article  PubMed  CAS  Google Scholar 

  62. Kim H-K, Choi S, Choi H (2004) Suppression of hepatic fatty acid synthase by feeding α-linolenic acid rich perilla oil lowers plasma triacylglycerol level in rats. J Nutr Biochem 15:485–492

    Article  PubMed  CAS  Google Scholar 

  63. Davidson MH (2006) Mechanisms for the hypotriglyceridemic effect of marine omega-3 fatty acids. Am J Cardiol 98:27–33

    Article  CAS  Google Scholar 

  64. Likimani TA, Wilson RP (1982) Effects of diet on lipogenic enzyme activities in channel catfish hepatic and adipose tissue. J Nutr 112:112–117

    PubMed  CAS  Google Scholar 

  65. Arnesen P, Krogdahl Å, Kristiansen IØ (1993) Lipogenic enzyme activities in liver of Atlantic salmon (Salmo salar L). Comp Biochem Physiol Part B: Comp Biochem 105:541–546

    Article  Google Scholar 

  66. Shimeno S, Kheyyali D, Shikata T (1995) Metabolic response to dietary carbohydrate to protein ratios in carp. Fish Sci 61:277–281

    CAS  Google Scholar 

  67. Dias J, Alvarez M, Diez A, Arzel J, Corraze G, Bautista J, Kaushik S (1998) Regulation of hepatic lipogenesis by dietary protein/energy in juvenile European seabass (Dicentrarchus labrax). Aquaculture 161:169–186

    Article  CAS  Google Scholar 

  68. Boujard T, Gélineau A, Covès D, Corraze G, Dutto G, Gasset E, Kaushik S (2004) Regulation of feed intake, growth, nutrient and energy utilisation in European sea bass (Dicentrarchus labrax) fed high fat diets. Aquaculture 231:529–545

    Article  Google Scholar 

  69. Kelley DS, Nelson GJ, Serrato CM, Schmidt PC (1987) Nutritional regulation of hepatic lipogenesis in the rat. Nutr Res 7:509–517

    Article  CAS  Google Scholar 

  70. Ferramosca A, Conte A, Damiano F, Siculella L, Zara V (2014) Differential effects of high-carbohydrate and high-fat diets on hepatic lipogenesis in rats. Eur J Nutr 53:1103–1114

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  72. Ducasse-Cabanot S, Zambonino-Infante J, Richard N, Medale F, Corraze G, Mambrini M, Robin J, Cahu C, Kaushik S, Panserat S (2007) Reduced lipid intake leads to changes in digestive enzymes in the intestine but has minor effects on key enzymes of hepatic intermediary metabolism in rainbow trout (Oncorhynchus mykiss). Animal 1(9):1272–1282

    Article  PubMed  CAS  Google Scholar 

  73. Jump DB (2008) N-3 polyunsaturated fatty acid regulation of hepatic gene transcription. Curr Opin Lipidol 19:242

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Clarke SD, Romsos DR, Leveille GA (1977) Differential effects of dietary methyl esters of long-chain saturated and polyunsaturated fatty acids on rat liver and adipose tissue lipogenesis. J Nutr 107:1170–1181

    PubMed  CAS  Google Scholar 

  75. Iritani N, Ikeda Y, Fukuda H, Katsurada A (1984) Comparative study of lipogenic enzymes in several vertebrates. Lipids 19:828–835

    Article  PubMed  CAS  Google Scholar 

  76. Torstensen B, 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

    Article  CAS  Google Scholar 

  77. Richard N, Kaushik S, Larroquet L, Sp Panserat, Corraze G (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

    Article  PubMed  CAS  Google Scholar 

  78. Richard N, Mourente G, Kaushik S, Corraze G (2006) 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

    Article  CAS  Google Scholar 

  79. Morais S, Pratoomyot J, Taggart JB, Bron JE, Guy DR, Bell JG, Tocher DR (2011) Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis. BMC Genom 12:255

    Article  CAS  Google Scholar 

  80. Derrick J, Ramsay R (1989) L-carnitine acyltransferase in intact peroxisomes is inhibited by malonyl-CoA. Biochem J 262:801–806

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Kim K-H (1997) Regulation of mammalian acetyl-coenzyme A carboxylase. Annu Rev Nutr 17:77–99

    Article  PubMed  CAS  Google Scholar 

  82. Nanton DA, Lall SP, Ross NW, McNiven MA (2003) Effect of dietary lipid level on fatty acid β-oxidation and lipid composition in various tissues of haddock, Melanogrammus aeglefinus L. Comp Biochem Physiol B: Biochem Mol Biol 135:95–108

    Google Scholar 

  83. Henderson R (1996) Fatty acid metabolism in freshwater fish with particular reference to polyunsaturated fatty acids. Arch Anim Nutr 49:5–22

    CAS  Google Scholar 

  84. Stubhaug I, Lie Ø, Torstensen BE (2007) Fatty acid productive value and β-oxidation capacity in Atlantic salmon (Salmo salar L.) fed on different lipid sources along the whole growth period. Aquac Nutr 13:145–155

    Article  CAS  Google Scholar 

  85. Vegusdal A, Gjøen T, Berge R, Thomassen M, Ruyter B (2005) Effect of 18∶ 1n–9, 20∶ 5n–3, and 22∶ 6n–3 on lipid accumulation and secretion by atlantic salmon hepatocytes. Lipids 40:477–486

    Article  PubMed  CAS  Google Scholar 

  86. Kjær MA, Vegusdal A, Gjøen T, Rustan AC, Todorčević M, Ruyter B (2008) Effect of rapeseed oil and dietary n-3 fatty acids on triacylglycerol synthesis and secretion in Atlantic salmon hepatocytes. Biochimica et Biophysica Acta (BBA) 1781:112–122

    Article  CAS  Google Scholar 

  87. Coccia E, Varricchio E, Vito P, Turchini GM, Francis DS, Paolucci M (2014) Fatty acid-specific alterations in leptin, PPARα, and CPT-1 gene expression in the rainbow trout. Lipids 49:1033–1046

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  89. Tocher DR, Fonseca-Madrigal J, Bell JG, Dick JR, Henderson RJ, Sargent JR (2002) Effects of diets containing linseed oil on fatty acid desaturation and oxidation in hepatocytes and intestinal enterocytes in Atlantic salmon (Salmo salar). Fish Physiol Biochem 26:157–170

    Article  CAS  Google Scholar 

  90. Fonseca-Madrigal J, Bell JG, Tocher DR (2006) Nutritional and environmental regulation of the synthesis of highly unsaturated fatty acids and of fatty-acid oxidation in Atlantic salmon (Salmo salar L.) enterocytes and hepatocytes. Fish Physiol Biochem 32:317–328

    Article  CAS  Google Scholar 

  91. Teitelbaum JE, Walker WA (2001) Review: the role of omega 3 fatty acids in intestinal inflammation. J Nutr Biochem 12:21–32

    Article  PubMed  CAS  Google Scholar 

  92. Bell M, Dick J, Porter A (2003) Pyloric ceca are significant sites of newly synthesized 22∶ 6n–3 in rainbow trout (Oncorhynchus mykiss). Lipids 38:39–44

    Article  PubMed  CAS  Google Scholar 

  93. Morais S, Silva T, Cordeiro O, Rodrigues P, Guy DR, Bron JE, Taggart JB, Bell JG, Tocher DR (2012) Effects of genotype and dietary fish oil replacement with vegetable oil on the intestinal transcriptome and proteome of Atlantic salmon (Salmo salar). BMC Genom 13:448

    Article  CAS  Google Scholar 

  94. Kondo H, Minegishi Y, Komine Y, Mori T, Matsumoto I, Abe K, Tokimitsu I, Hase T, Murase T (2006) Differential regulation of intestinal lipid metabolism-related genes in obesity-resistant A/J vs obesity-prone C57BL/6 J mice. Am J Physiol Endocrinol Metab 291:E1092–E1099

    Article  PubMed  CAS  Google Scholar 

  95. van Schothorst EM, Flachs P, Franssen-van Hal NL, Kuda O, Bunschoten A, Molthoff J, Vink C, Hooiveld GJ, Kopecky J, Keijer J (2009) Induction of lipid oxidation by polyunsaturated fatty acids of marine origin in small intestine of mice fed a high-fat diet. BMC Genom 10:110

    Article  CAS  Google Scholar 

  96. Silverstein RL, Febbraio M (2000) CD36 and atherosclerosis. Curr Opin Lipidol 11:483–491

    Article  PubMed  CAS  Google Scholar 

  97. Endemann G, Stanton L, Madden K, Bryant C, White RT, Protter A (1993) CD36 is a receptor for oxidized low density lipoprotein. J Biol Chem 268:11811–11816

    PubMed  CAS  Google Scholar 

  98. Febbraio M, Hajjar DP, Silverstein RL (2001) CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J Clin Investig 108:785

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Lobo MV, Huerta L, Ruiz-Velasco N, Teixeiro E, de la Cueva P, Celdrán A, Martín-Hidalgo A, Vega MA, Bragado R (2001) Localization of the lipid receptors CD36 and CLA-1/SR-BI in the human gastrointestinal tract: towards the identification of receptors mediating the intestinal absorption of dietary lipids. J Histochem Cytochem 49:1253–1260

    Article  PubMed  CAS  Google Scholar 

  100. Chen M, Yang Y, Braunstein E, Georgeson KE, Harmon CM (2001) Gut expression and regulation of FAT/CD36: possible role in fatty acid transport in rat enterocytes. Am J Physiol Endocrinol Metab 281:E916–E923

    PubMed  CAS  Google Scholar 

  101. Nassir F, Abumrad NA (2009) CD36 and intestinal fatty acid absorption. Immunol Endocr Metabol Agents Med Chem 9:3–10

    Article  CAS  Google Scholar 

  102. Schwartz GJ, Fu J, Astarita G, Li X, Gaetani S, Campolongo P, Cuomo V, Piomelli D (2008) The lipid messenger OEA links dietary fat intake to satiety. Cell Metab 8:281–288

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Gaillard D, Laugerette F, Darcel N, El-Yassimi A, Passilly-Degrace P, Hichami A, Khan NA, Montmayeur J-P, Besnard P (2008) The gustatory pathway is involved in CD36-mediated orosensory perception of long-chain fatty acids in the mouse. FASEB J 22:1458–1468

    Article  PubMed  CAS  Google Scholar 

  104. Khan NA, Besnard P (2009) Oro-sensory perception of dietary lipids: new insights into the fat taste transduction. Biochimica et Biophysica Acta (BBA) 1791:149–155

    Article  CAS  Google Scholar 

  105. Petit V, Arnould L, Martin P, Monnot M-C, Pineau T, Besnard P, Niot I (2007) Chronic high-fat diet affects intestinal fat absorption and postprandial triglyceride levels in the mouse. J Lipid Res 48:278–287

    Article  PubMed  CAS  Google Scholar 

  106. Ockner R, Manning J (1976) Fatty acid binding protein. Role in esterification of absorbed long chain fatty acid in rat intestine. J Clin Investig 58:632

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. Poirier H, Degrace P, Niot I, Bernard A, Besnard P (1996) Localization and regulation of the putative membrane fatty-acid transporter (fat) in the small intestine. Eur J Biochem 238:368–373

    Article  PubMed  CAS  Google Scholar 

  108. Andre M, Ando S, Ballagny C, Durliat M, Poupard G, Briancon C, Babin P (2000) Intestinal fatty acid binding protein gene expression reveals the cephalocaudal patterning during zebrafish gut morphogenesis. Int J Dev Biol 44:249–252

    PubMed  CAS  Google Scholar 

  109. Hussain MM, Shi J, Dreizen P (2003) Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly. J Lipid Res 44:22–32

    Article  PubMed  CAS  Google Scholar 

  110. Lin M, Arbeeny C, Bergquist K, Kienzle B, Gordon DA, Wetterau JR (1994) Cloning and regulation of hamster microsomal triglyceride transfer protein. The regulation is independent from that of other hepatic and intestinal proteins which participate in the transport of fatty acids and triglycerides. J Biol Chem 269:29138–29145

    PubMed  CAS  Google Scholar 

  111. Qiu W, Taghibiglou C, Avramoglu RK, Van Iderstine SC, Naples M, Ashrafpour H, Mhapsekar S, Sato R, Adeli K (2005) Oleate-mediated stimulation of microsomal triglyceride transfer protein (MTP) gene promoter: implications for hepatic MTP overexpression in insulin resistance. Biochemistry 44:3041–3049

    Article  PubMed  CAS  Google Scholar 

  112. Hussain MM, Nijstad N, Franceschini L (2011) Regulation of microsomal triglyceride transfer protein. Clin Lipidol 6:293–303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  113. Lu S, Yao Y, Cheng X, Mitchell S, Leng S, Meng S, Gallagher JW, Shelness GS, Morris GS, Mahan J, Frase S, Mansbach CM, Weinberg RB, Black DD (2006) Overexpression of apolipoprotein A-IV enhances lipid secretion in IPEC-1 cells by increasing chylomicron size. J Biol Chem 281:3473–3483

    Article  PubMed  CAS  Google Scholar 

  114. Hachero-Cruzado I, Rodríguez-Rua A, Román-Padilla J, Ponce M, Fernández-Díaz C, Manchado M (2014) Characterization of the genomic responses in early Senegalese sole larvae fed diets with different dietary triacylglycerol and total lipids levels. Comp Biochem Physiol Part D Genom Proteom 12:61–73

    CAS  Google Scholar 

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Acknowledgments

The authors are grateful to Jorge Dias (Sparos) for formulating the diets and organizing the logistics of the trial. The help of Helena Teixeira (CCMAR) for fish husbandry during the experiment, of Jorge Dias, Vera Rodrigues and Manuel Sardinha (Sparos) for sampling and Almudena Martínez (IRTA) for assisting with RNA extractions was deeply appreciated. KB is the recipient of a PhD grant awarded by the Agència de Gestió d’Ajuts Universitaris i de Recerca (AGAUR) and SM holds a Ramón y Cajal post-doctoral contract from the Spanish Ministry of Economy and Competitiveness (MINECO). This study was supported by the European Commission Marie Curie Actions (FP7-PEOPLE-2010-RG, Project No. 274184) and by MINECO (project AGL2011-23502).

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Bonacic, K., Estévez, A., Bellot, O. et al. Dietary Fatty Acid Metabolism is Affected More by Lipid Level than Source in Senegalese Sole Juveniles: Interactions for Optimal Dietary Formulation. Lipids 51, 105–122 (2016). https://doi.org/10.1007/s11745-015-4089-6

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  • DOI: https://doi.org/10.1007/s11745-015-4089-6

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