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 Physiology and Biochemistry

Volumn 39, Issue 2, 2013, Pages 335-349

  Benítez Dorta, Vanessa ^a   Caballero, María J ^a   Izquierdo, Marisol ^a   Manchado, Manuel ^b   Infante, Carlos ^b   Zamorano, María J ^a   Montero, Daniel ^a  

^a UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

^b IFAPA CENTRO EL TORUÑO   (Spain)

Author keywords

Essential fatty acids; Glucocorticoid receptor gene expression; Senegalese sole; Stress response; Vegetable oils

Indexed keywords

GLYCINE MAX; SOLEA SENEGALENSIS;

EID: 84875221600     PISSN: 09201742     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10695-012-9703-4     Document Type: Article

References (75)

1. Alami-Durante H, Wrutniak-Cabello C, Kaushik SJ, Médale F (2010) Skeletal muscle cellularity and expression of myogenic regulatory factors and myosin heavy chains in rainbow trout (Oncorhynchus mykiss): effects of changes in dietary plant protein sources and amino acid profiles. Comp Biochem Physiol Part A 156: 561-568.
2. Aluru N, Vijayan MM (2009) Stress transcriptomics in fish: a role for genomic cortisol signaling. Gen Comp Endocrinol 164: 142-150.
3. Alves-Martins D, Valente LMP, Lall SP (2011) Partial replacement of fish oil by flaxseed oil in Atlantic halibut (Hippoglossus hippoglossus L.) diets: effects on growth, nutritional and sensory quality. Aquacult Nutr 17: 671-684.
4. AOAC (1995) Official methods of analysis, 16th edn. Association of Official Analytical Chemist, Washington, DC.
5. Aragão C, Corte-Real J, Costas B, Dinis MT, Conceição LEC (2008) Stress response and changes in amino acid requirements in Senegalese sole Solea senegalensis Kaup 1758. Amino Acids 34: 143-148.
6. Arjona FJ, Vargas-Chacoff L, Ruiz-Jarabo I, Gonçalves O, Páscoa I, Martín del Río MP, Mancera JM (2009) Tertiary stress responses in Senegalese sole (Solea senegalensis Kaup, 1858) to osmotic challenge: implications for osmoregulation, energy metabolism and growth. Aquaculture 287: 419-426.
7. Bell JG, Tocher DR, MacDonald FM, Sargent JR (1994) Effects of diets rich in linoleic (18: 2n-6) and alpha-linolenic (18: 3n-3) acids on the growth, lipid class and fatty acid compositions and eicosanoid production in juvenile turbot (Scophthalmus maximus L.). Fish Physiol Biochem 13: 105-118.
8. Bell JG, Castell JD, Tocher DR, MacDonald FM, Sargent JR (1995) Effects of different dietary arachidonic acid: docosahexaenoic acid ratios on phospholipids fatty acid compositions and prostaglandin production in juvenile turbot (Scophthalmus maximus). Fish Physiol Biochem 14: 139-151.
9. Borges P, Oliveira B, Casal S, Dias J, Conceição L, Valente L (2009) Dietary lipid levels affects growth performance and nutrient utilisationutilization of Senegaleses sole (Solea senegalensis) juveniles. Br J Nutr 102: 1007-1014.
10. Bury NR, Sturm A (2007) Evolution of the corticosteroid receptor signaling pathway in fish. Gen Comp Endocrinol 153: 47-56.
11. Bury NR, Sturm A, Le Rouzic P, Lethimonier C, Ducouret B, Guiguen Y, Robinson-Rechavi M, Laudet V, Rafestin-Oblin ME, Prunet P (2003) Evidence for two distinct functional glucocorticoid receptors in teleost fish. J Mol Endocrinol 31: 141-156.
12. Caballero MJ, Izquierdo MS, Kjorsvik E, Montero D, Socorro J, Fernández A, Rosenlund G (2003) Morphological aspects of the intestinal cells from gilthead seabream (Sparus aurata) fed diets containing different lipid sources. Aquaculture 225: 325-340.
13. Caballero MJ, Izquierdo MS, Kjorsvik E, Fernández AJ, Rosenlund G (2004) Histological alterations in the liver of sea bream, Sparus aurata L., caused by short- or long- term feeding with vegetable oils: recovery of normal morphology after feeding fish oil as the sole lipid source. J Fish Dis 27: 531-541.
14. Caballero MJ, Gallardo G, Robaina L, Montero D, Fernández A, Izquierdo MS (2006) Vegetable lipid sources affect in vitro biosynthesis of triacylglycerols and phospholipids in the intestine of seabream (Sparus aurata). Br J Nutr 95: 448-454.
15. Campos C, Valente LMP, Borges P, Bizuayehu T, Fernandes JMO (2010) Dietary lipid levels have a remarkable impact on the expression of growth-related genes in Senegalese sole (Solea senegalensis Kaup). J Exp Biol 213: 200-209.
16. Cara JB, Aluru N, Moyano FJ, Vijayan MM (2005) Food-deprivation induces HSP70 and HSP90 protein expression in larval gilthead sea bream and rainbow trout. Comp Biochem Physiol 142: 426-431.
17. Charmandari E, Tsigos C, Chrousus G (2005) Endocrinology of the stress response. Ann Rev Physiol 67: 259-284.
18. Christie WW (1982) Lipid analysis. Pergamon Press, Oxford.
19. Costas B, Aragão C, Mancera JM, Dinis MT, Conceição LEC (2008) High stocking density induces crowding stress and affects amino acid metabolism in Senegalese sole, Solea senegalensis (Kaup 1858) juveniles. Aquac Res 39: 1-9.
20. Costas B, Conceição LEC, Aragão C, Martos JA, Ruiz-Jarabo I, Mancera JM, Afonso A (2011a) Physiological responses of Senegalese sole (Solea senegalensis Kaup, 1858) after stress challenge: effects on non-specific immune parameters, plasma free amino acids and energy metabolism. Aquaculture 316: 68-76.
21. Costas B, Conceição LEC, Dias J, Novoa B, Figueras A, Afonso A (2011b) Dietary arginine and repeated handling increase disease resistance and modulate innate immune mechanisms of Senegalese sole (Solea senegalensis Kaup, 1858). Fish Shellfish Immunol 31: 838-847.
22. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 193: 265-275.
23. Ganga R, Bell JG, Montero D, Robaina L, Caballero MJ, Izquierdo MS (2005) Effect of dietary lipids on plasma fatty acid profiles and prostaglandin and leptin production in gilthead seabream (Sparus aurata). Comp Biochem Physiol 142: 410-418.
24. Ganga R, Montero D, Bell JG, Atalah E, Ganuza E, Vega Orellana L, Tort L, Acerete JM, Afonso JM, Benítez-Santana T, Fernández-Palacios H, Izquierdo MS (2011a) Stress response in sea bream (Sparus aurata) held under crowded conditions and fed diets containing linseed and/or soybean oil. Aquaculture 311: 215-223.
25. Ganga R, Bell JG, Montero D, Atalah E, Vraskou Y, Tort L, Fernández A, Izquierdo MS (2011b) Adrenocorticotrophic hormone-stimulated cortisol release by the head kidney inter-renal tissue from sea bass (Sparus aurata) fed with linseed oil and soybean oil. Br J Nutr 105: 238-247.
26. Grad I, Picard D (2007) The glucocorticoid responses are shaped by molecular chaperones. Mol Cell Endocrinol 275: 2-12.
27. Greenwood AK, Butler PC, White RB, DeMarco U, Pearce D, Fernald RD (2003) Multiple corticosteroid receptors in a teleost fish: distinct sequences, expression patterns, and transcriptional activities. Endocrinology 144: 4226-4236.
28. Heck TG, Schöler CM, Bitterncourt PIH (2011) HSP70 expression: does it a novel fatigue signaling factor from immune system to the brain? Cell Biochem Func 29: 215-226.
29. Heydari AR, Wu B, Takahashi R, Strong R, Richardson A (1993) Expression of heat shock protein 70 is altered by age and diet at the level of transcription. Mol Cel Biol 13: 2909-2918.
30. Hori T, Kimball J, Johnson SC, Afonso LOB, Bowman S, Hubert S, Gamperl AK, Rise ML (2010) Heat-shock responsive genes identified and validated in Atlantic cod (Gadus morhua) liver, head kidney and skeletal muscle using genomic techniques. BMC Genomics 11: 72.
31. 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.
32. Izquierdo MS, Arakawa T, Takeuchi T, Haroun R, Watanabe T (1992) Effect of n-3 HUFA levels in Artemia on growth of larval Japanese flounder (Paralichthys olivaceus). Aquaculture 105: 73-82.
33. Izquierdo MS, Montero D, Robaina LE, Caballero MJ, Rosenlund G, Ginés R (2005) Alteration in fillet fatty acid profile and flesh quality in gilthead sea bream (Sparus aurata) fed vegetable oils for a long period. Recovery of fatty acid profiles by fish oil feeding. Aquaculture 250: 431-444.
34. Jurivich DA, Sistonen L, Sarge KD, Morimoto RI (1994) Arachidonate is a potent modulator of human heat shock gene transcription. Proc Natl Acad Sci USA 91: 2280-2284.
35. Jutfelt F, Olsen RE, Bjornsson BT, Sundell K (2007) Parr-smolt transformation and dietary vegetable lipids affect intestinal nutrient uptake, barrier function and plasma cortisol levels in Atlantic salmon. Aquaculture 273: 298-311.
36. Kang KI, Meng X, Devin-Leclerc J, Bouhouche I, Chadli A, Cadepond F, Baulieu EE, Catelli MG (1999) The molecular chaperone Hsp90 can negatively regulate the activity of a glucocorticosteroid-dependent promoter. PNAS 96: 1439-1444.
37. Kokura S, Yoshikawa T (2006) Large intestine and heat shock protein (HSP). J Clin Biochem Nutr 38: 156-160.
38. Lin HZ, Liu YJ, He JG, Zheng WH, Tian LX (2007) Alternative vegetable lipid sources in diets for grouper, Epinephelus coioides (Hamilton): effects on growth, and muscle and liver fatty acid composition. Aquacult Res 38: 1605-1611.
39. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-2DDCT method. Methods 25: 402-408.
40. Manchado M, Salas-Leiton E, Infante C, Ponce M, Asensio E, Crespo A, Zuasti E, Cañavate JP (2008) Molecular characterization, gene expression and transcriptional regulation of cytosolic HSP90 genes in the flatfish Senegalese sole (Solea senegalensis Kaup). Gene 416: 77-84.
41. Martins DA, Engrola S, Morais S, Bandarra N, Coutinho J, Yúfera M, Conceição LEC (2011) Cortisol response to air exposure in Solea senegalensis post-larvae is affected by dietary arachidonic acid to eicosapentaenoic acid ratio. Fish Physiol Biochem 37: 733-743.
42. Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9: 211-268.
43. Montero D, Izquierdo MS (2010) Welfare and health of fish fed vegetable oils as alternative lipid sources to fish oil. In: Turchini G, Ng W, Tocher D (eds) Fish oil replacement and alternative lipid sources in aquaculture feeds. CRC Press, Cambridge, pp 439-486.
44. Montero D, Kalinowski T, Obach A, Robaina L, Tort L, Caballero MJ, Izquierdo MS (2003) Vegetable lipid sources for gilthead seabream (Sparus aurata): effects on fish health. Aquaculture 225: 353-370.
45. Montero D, Robaina LE, Caballero MJ, Ginés R, Izquierdo MS (2005) Growth, feed utilization and flesh quality of European sea bass (Dicentrarchus labrax) fed diets containing vegetable oils, a time-course study on the effects of re-feeding period with a 100 % fish oil diet. Aquaculture 248: 121-134.
46. Montero D, Grasso V, Izquierdo MS, Ganga R, Real F, Tort L, Caballero MJ, Acosta F (2008) Total substitution of fish oil by vegetable oils in gilthead seabream (Sparus aurata) diets: effects on hepatic Mx expression and some immune parameters. Fish Shellfish Immunol 24: 147-155.
47. Montero D, Mathlouthi F, Tort L, Afonso JM, Torrecillas S, Fernández-Vaquero A, Negrín D, Izquierdo MS (2010) Replacement of dietary fish oil by vegetable oils affects humoral immunity and expression of pro-inflammatory cytokines genes in gilthead sea bream Sparus aurata. Fish Shellfish Immunol 29: 1073-1081.
48. Morais S, Narciso L, Dores E, Pousão-Ferreira P (2004) Lipid enrichment for Senegalese sole (Solea senegalensis) larvae: effect on larval growth, survival and fatty acid profile. Aquacult Int 12: 281-298.
49. Morais S, Caballero MJ, Conceição LEC, Izquierdo MS, Dinis MT (2006) Dietary neutral lipid level and source in Senegalesesole (Solea senegalensis) larvae: effect on growth, lipid metabolism and digestive capacity. Comp Biochem Physiol B 144: 57-69.
50. Oarada M, Gonoi T, Tsuzuki T, Igarashi M, Hirasaka K, Nikawa T, Onishi Y, Toyotome T, Kamei K, Miyazawa T, Nakagawa K, Kashima M, Kurita N (2007) Effect of dietary oils on lymphocyte immunological activity in psychologically stressed mice. Biosci Biotechnol Biochem 71: 174-182.
51. Oxley A, Jolly C, Eide T, Jordal AEO, Svardal A, Olsen RE (2010) The combined impact of plant-derived dietary ingredients and acute stress on the intestinal arachidonic acid cascade in Atlantic salmon (Salmo salar). Br J Nutr 103: 851-861.
52. Pratt WB, Toft DO (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18: 306-360.
53. Prunet P, Sturm A, Milla S (2006) Multiple corticosteroid in fish: from old ideas to new concepts. Gen Comp Endocrinol 147: 17-23.
54. Regost C, Arzel J, Robin J, Rosenlund G, Kaushik SJ (2003) Total replacement of fish oil by soybean oil with return to fish oil in turbot (Psetta maxima). I. Growth performance, flesh fatty acid profile, and lipid metabolism. Aquaculture 217: 465-482.
55. Roberts RJ, Agius C, Saliba C, Bossier P, Sung YY (2010) Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. J Fish Dis 33: 789-801.
56. Rotllant J, Balm PH, Pérez-Sánchez J, Wenderlaar-Bonga SE, Tort L (2001) Pituitary and interrenal function in gilthead sea bream (Sparus aurata L. Teleostei) after handling and confinement stress. Gen Comp Endocrinol 121: 333-342.
57. Rueda-Jasso R, Conceição LEC, Dias J, De Coen W, Gomes E, Rees JF, 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.
58. Salas-Leiton E, Anguis V, Martín-Antonio B, Crespo D, Planas JV, Infante C, Cañavate JP, Manchado M (2010) Effects of stocking density and feed ratio non growth and gene expression in the Senegalese sole (Solea senegalensis): potential effects on the immune response. Fish Shellfish Immun 28: 296-302.
59. Sales J, Glencross B (2010) 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. Aquacult Nutr 17: e271-e287.
60. Sargent JR, Tocher DR, Bell JG (2002) The lipids. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, San Diego, pp 181-257.
61. Sealey WM, Barrows FT, Smith CE, Hardy RW (2010) Dietary supplementation strategies to improve performances of rainbow trout Oncorhynchus mykiss fed plant-based diets. Bull Fish Res Agen 31: 15-23.
62. Silva J, Espe M, Conceição LEC, Dias J, Costas B, Valente LMP (2010) Feed intake and growth performance of Senegalese sole (Solea senegalensis Kaup, 1858) fed diets with partial replacement of fish meal with plant proteins. Aquacul Res 41: 20-30.
63. Sokal RR, Rohlf FJ (1995) Biometry. In: Sokal RR, Rohlf FJ (eds) The principles and practice of statistics in biological research, 3rd edn. W. H. Freeman, New York.
64. Stolte EH, Mazon AF, Leon-Koosterziel KM, Jesia KM, Bury NR, Sturm A, Savelkoul HFJ, van Kemenade BMLV, Flik G (2008) Corticosteroid receptors involved in stress regulation in common carp, Cyprinus carpio. J Endocrinol 198: 403-417.
65. Tacon AGJ, Metian M (2008) Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 285: 146-158.
66. Terova G, Gornati R, Rimoldi S, Bernardini G, Saroglia M (2005) Quantification of a glucocorticoid receptor in sea bass (Dicentrarchus labrax, L.) reared at high stocking density. Gene 357: 144-151.
67. Turchini GM, Ng WK, Torstensen BE (2009) Fish oil replacement in finfish nutrition. Rev Aquacult 1: 10-57.
68. Vazzana M, Vinizzi A, Sanfratello MA, Celi M, Salerno G, Parrinello N (2010) Differential expression of two glucocorticoid receptors in seabass (teleost fish) head kidney after exogenous cortisol inoculation. Comp Biochem Physiol A 157: 49-54.
69. Vijayan MM, Raptis S, Sathiyaa R (2003) Cortisol treatment affects glucocorticoid receptor and glucocorticoid-responsive genes in the liver of rainbow trout. Gen Comp Endocrinol 132: 256-263.
70. Vijayan MM, Prunet P, Boone AN (2005) Xenobiotic impact on corticosteroid signaling. In: Moon TW, Mommsen TP (eds) Biochemical and molecular biology of fishes. Environmental toxicology, vol 6. Elsevier, Amsterdam, pp 365-394.
71. Vizzini A, Vazzana M, Cammarata M, Parrinello N (2007) Peritoneal cavity phagocytes from the teleost sea bass express a glucocorticoid receptor (cloned and sequenced) involved in genomic modulation of the in vitro chemiluminescence response to zymosan. Gen Comp Endocrinol 150: 114-123.
72. Webster JC, Oakley RH, Jewell CM, Cidlowsky JA (2001) Proinflammatory cytokines regulate human glucocorticoid receptor gene expression and lead to the accumulation of the dominant negative β isoform: a mechanism for the generation of glucocorticoid resistance. Proc Natl Acad Sci USA 98: 6865-6870.
73. Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77: 591-625.
74. Wu X, Ruan Z, Gao Y, Yin Y, Zhou X, Wang L, Geng M, Hou Y, Wu G (2010) Dietary supplementation with l-arginine or N-carbamylglutamate enhances intestinal growth and heat shock protein-70 expression in weanlings pigs fed a corn- and soybean meal-based diet. Amino Acids 39: 831-839.
75. Wunderink YS, Engels S, Halm S, Yufera M, Martínez-Rodríguez G, Flik G, Klaren PH, Mancera JM (2011) Chronic and acute stress response in Senegalese sole (Solea senegalensis): the involvement of cortisol, CRH and CRH-BP. Gen Comp Endocrinol 171: 203-210.