Teleost fish larvae adapt to dietary arachidonic acid supply through modulation of the expression of lipid metabolism and stress response genes

British Journal of Nutrition

Volumn 108, Issue 5, 2012, Pages 864-874

  Martins, Dulce Alves ^a,b   Rocha, Filipa ^a   Martínez Rodríguez, Gonzalo ^b   Bell, Gordon ^c   Morais, Sofia ^d   Castanheira, Filipa ^a   Bandarra, Narcisa ^e   Coutinho, Joana ^e   Yúfera, Manuel ^b   Conceição, Luís E C ^a  

^a UNIVERSITY OF ALGARVE   (Portugal)

^b INSTITUTO DE CIENCIAS MARINAS DE ANDALUCÍA   (Spain)

^c UNIVERSITY OF STIRLING   (United Kingdom)

^d IRTA   (Spain)

^e INSTITUTO PORTUGUÊS DO MAR E DA ATMOSFERA   (Portugal)

Author keywords

Gene expression; PUFA; Sparus aurata; Stress

Indexed keywords

ARACHIDONATE 5 LIPOXYGENASE; ARACHIDONIC ACID; CYCLOOXYGENASE 2; GLUCOCORTICOID RECEPTOR; HORMONE SENSITIVE LIPASE; HYDROCORTISONE; ICOSANOID; LEUKOTRIENE B4; LIPID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PHOSPHOENOLPYRUVATE CARBOXYLASE; PHOSPHOLIPASE A2; STEROIDOGENIC ACUTE REGULATORY PROTEIN; PRIMER DNA;

5 LOX GENE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BETA ACTIN GENE; BODY GROWTH; CONTROLLED STUDY; COX 2 GENE; FAT INTAKE; GENE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GR GENE; HSL GENE; LARVAL STAGE; LIPID METABOLISM; NONHUMAN; PEPCK GENE; PHENOTYPE; PLA2 GENE; REAL TIME POLYMERASE CHAIN REACTION; STAR GENE; SURVIVAL; TELEOST; ANIMAL; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SEA BREAM;

ANIMALS; ARACHIDONIC ACID; BASE SEQUENCE; DIETARY FATS; DNA PRIMERS; GENE EXPRESSION REGULATION; LARVA; LIPID METABOLISM; POLYMERASE CHAIN REACTION; SEA BREAM; STRESS, PHYSIOLOGICAL;

EID: 84871893388     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114511006143     Document Type: Article

References (72)

1. Conte FS (2004) Stress and the welfare of cultured fish. Appl Anim Behav Sci 86, 205-223.
2. Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42, 517-525.
3. Portz DE, Woodley CM & Cech JJ (2006) Stress-associated impacts of short-term holding on fishes. Rev Fish Biol Fisher 16, 125-170.
4. Fletcher TC (1997) Dietary effects on stress and health. In Fish Stress and Health in Aquaculture, pp. 223-246 [GK Iwama, AD Pickering, JP Sumpter and CB Schreck, editors]. Cambridge: Cambridge University Press.
5. Weirich CR & Reigh RC (2001) Dietary Lipids and Stress Tolerance of Larval Fish. Binghamton, NY: Food Products Press.
6. Montero D, Kalinowski T, Obach A, et al. (2003) Vegetable lipid sources for gilthead seabream (Sparus aurata): effects on fish health. Aquaculture 225, 353-370.
7. Sargent J, McEvoy L, Estévez A, et al. (1999) Lipid nutrition of marine fish during early development: current status and future directions. Aquaculture 179, 1-4.
8. Cahu CL, Gisbert E, Villeneuve LAN, et al. (2009) Influence of dietary phospholipids on early ontogenesis of fish. Aquac Res 40, 989-999.
9. Bessonart M, Izquierdo MS, Salhi M, et al. (1999) Effect of dietary arachidonic acid levels on growth and survival of gilthead sea bream (Sparus aurata L.) larvae. Aquaculture 179, 1-4.
10. Bell JG & Sargent JR (2003) Arachidonic acid in aquaculture feeds: current status and future opportunities. Aquaculture 218, 491-499.
11. Koven W (2002) Gilthead sea bream, Sparus aurata. In Nutrient Requirements and Feeding of Finfish for Aquaculture, pp. 64-78 [CD Webster and C Lim, editors]. New York, NY: CAB International Publishers.
12. Koven W, Barr Y, Lutzky S, et al. (2001) The effect of dietary arachidonic acid (20:4n-6) on growth, survival and resistance to handling stress in gilthead seabream (Sparus aurata) larvae. Aquaculture 193, 1-2.
13. Koven W, Van Anholt R, Lutzky S, et al. (2003) The effect of dietary arachidonic acid on growth, survival, and cortisol levels in different-age gilthead seabream larvae (Sparus auratus) exposed to handling or daily salinity change. Aquaculture 228, 307-320.
14. Van Anholt RD, Koven WM, Lutzky S, et al. (2004) Dietary supplementation with arachidonic acid alters the stress response of gilthead seabream (Sparus aurata) larvae. Aquaculture 238, 369-383.
15. Dhert P, Lavens P, Duray M, et al. (1990) Improved larval survival at metamorphosis of Asian sea bass Lates calcarifer using omega-3 hufa-enriched live food. Aquaculture 90, 63-74.
16. Kraul S, Brittain K, Cantrell R, et al. (1993) Nutritional factors affecting stress resistance in the larval mahimahi Coryphaena hippurus. J World Aquacult Soc 24, 186-193.
17. Kanazawa A (1997) Effects of docosahexaenoic acid and phospholipids on stress tolerance of fish. Aquaculture 155, 1-4.
18. Kanazawa A (1998) Importance of dietary lipids in flatfish. In Nutrition and Technical Development of Aquaculture, Proceedings of the Twenty-sixth US-Japan Aquaculture Symposium, Durham, NH, 1997, pp. 181-186
19. [WH Howell, BJ Keller, PK Park, JP McVey, K Takayanagi and Y Uekita, editors]. United States-Japan Cooperative Program in Natural Resources Technical Report 26.
20. Liu J-K, Wang W-Q, Li K-R, et al. (2002) Effects of fish oil, DHA oil and lecithin in microparticulate diets on stress tolerance of larval gilthead seabream (Sparus aurata). Chin J Oceanol Limnol 20, 338-343.
21. McKenzie DJ (2005) Effects of dietary fatty acids on the physiology of environmental adaptation in fish. In Physiological and Ecological Adaptations to Feeding in Vertebrates, pp. 363-388 [JM Starck and T Wang, editors]. Enfield, New Hampshire: Science Publishers.
22. Wales NAM (1988) Hormone studies in Myxine glutinosa-effects of the eicosanoids arachidonic-acid, prostaglandin-E1, prostaglandin-E2, prostaglandin-A2, prostaglandin-F2, thromboxane B2 and of indomethacin on plasma cortisol, blood pressure, urine flow and electrolyte balance. J Comp Physiol B 158, 621-626.
23. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11, 107-184.
24. Calder PC (2009) Polyunsaturated fatty acids and inflammatory processes: new twists in an old tale. Biochimie 91, 791-795.
25. Ganga R, Tort L, Acerete L, et al. (2006) Modulation of ACTH-induced cortisol release by polyunsaturated fatty acids in interrenal cells from gilthead seabream. Sparus aurata. J Endocrinol 190, 39-45.
26. Ganga R, Bell JG, Montero D, et al. (2011) Adrenocorticotrophic hormone-stimulated cortisol release by the head kidney inter-renal tissue from sea bream (Sparus aurata) fed with linseed oil and soyabean oil. Brit J Nutr 105, 238-247.
27. Stocco DM, Wang XJ, Jo Y, et al. (2005) Multiple signalling pathways regulating steroidogenesis and steroidogenic acute regulatory protein expression: more complicated than we thought. Mol Endocrinol 19, 2647-2659.
28. Wang XJ, Dyson MT, Jo Y, et al. (2003) Involvement of 5-lipoxygenase metabolites of arachidonic acid in cyclic AMP-stimulated steroidogenesis and steroidogenic acute regulatory protein gene expression. J Steroid Biochem 85, 159-166.
29. Wang XJ, Dyson MT, Jo Y, et al. (2003) Inhibition of cyclooxygenase-2 activity enhances steroidogenesis and steroidogenic acute regulatory gene expression in MA-10 mouse Leydig cells. Endocrinology 144, 3368-3375.
30. Wang XJ, Shen CL, Dyson MT, et al. (2006) The involvement of epoxygenase metabolites of arachidonic acid in cAMPstimulated steroidogenesis and steroidogenic acute regulatory protein gene expression. J Endocrinol 190, 871-878.
31. Desvergne B & Wahli W (1999) Peroxisome proliferatoractivated receptors: nuclear control of metabolism. Endocr Rev 20, 649-688.
32. Zhang Y & Mangelsdorf DJ (2002) LuXuRies of Lipid homeostasis: the unity of nuclear hormone receptors, transcription regulation, and cholesterol sensing. Mol Interv 2, 78-87.
33. Xie YI, Yang Q & DePierre JW (2002) The effects of peroxisome proliferators on global lipid homeostasis and the possible significance of these effects to other responses to these xenobiotics: an hypothesis. Ann NY Acad Sci 973, 17-25.
34. Kowalewski MP, Dyson MT, Manna PR, et al. (2009) Involvement of peroxisome proliferator-activated receptor gamma in gonadal steroidogenesis and steroidogenic acute regulatory protein expression. Reprod Fert Develop 21, 909-922.
35. Borch J, Metzdorff SB, Vinggaard AM, et al. (2006) Mechanisms underlying the anti-androgenic effects of diethylhexyl phthalate in fetal rat testis. Toxicology 233, 144-155.
36. Pavlikova N, Kortner TM & Arukwe A (2010) Modulation of acute steroidogenesis, peroxisome proliferator-activated receptors and CYP3A/PXR in salmon interrenal tissues by tributyltin and the second messenger activator, forskolin. Chem-Biol Interact 185, 119-127.
37. Striggow F & Ehrlich BE (1997) Regulation of intracellular calcium release channel function by arachidonic acid and leukotriene B4. Biochem Biophys Res Commun 237, 413-418.
38. Shuttleworth TJ, Thompson JL & Mignen O (2004) ARC channels: a novel pathway for receptor-activated calcium entry. Physiology 19, 355-361.
39. Holmes AM, Roderick HL, McDonald F, et al. (2007) Interaction between store-operated and arachidonate-activated calcium entry. Cell Calcium 41, 1-12.
40. Meves H (2008) Arachidonic acid and ion channels: an update. Br J Pharmacol 155, 4-16.
41. Prunet P, Sturm A & Milla S (2006) Multiple corticosteroid receptors in fish: From old ideas to new concepts. Gen Comp Endocrinol 147, 17-23.
42. Pottinger TG & Brierley I (1997) A putative cortisol receptor in the rainbow trout erythrocyte: stress prevents starvationinduced increases in specific binding of cortisol. J Exp Biol 200, 2035-2043.
43. Borski RJ (2000) Nongenomic membrane actions of glucocorticoids in vertebrates. Trends Endocrinol Metab 11, 427-436.
44. Alves Martins D, Estévez A, Stickland NC, et al. (2010) Dietary lecithin source affects growth potential and gene expression in Sparus aurata larvae. Lipids 45, 1011-1023.
45. Lee PC & Struve M (1992) Unsaturated fatty-acids inhibit glucocorticoid receptor-binding of trout hepatic cytosol. Comp Biochem Phys B 102, 707-711.
46. Junzo K, Akiko T, Naoki M, et al. (1987) Modulation of brain progestin and glucocorticoid receptors by unsaturated fatty acid and phospholipid. J Steroid Biochem 27, 641-648.
47. Viscardi RM & Max SR (1993) Unsaturated fatty acid modulation of glucocorticoid receptor binding in L2 cells. Steroids 58, 357-361.
48. Hedman E, Widen C, Asadi A, et al. (2006) Proteomic identification of glucocorticoid receptor interacting proteins. Proteomics 6, 3114-3126.
49. Le PP, Friedman JR, Schug J, et al. (2005) Glucocorticoid receptor-dependent gene regulatory networks. PLoS Genet 1, 159-170.
50. Lampidonis AD, Stravopodis DJ, Voutsinas GE, et al. (2008) Cloning and functional characterization of the 50 regulatory region of ovine Hormone Sensitive Lipase (HSL) gene. Gene 427, 65-79.
51. Yúfera M, Fernández-D́az C & Pascual E (2005) Food microparticles for larval fish prepared by internal gelation. Aquaculture 248, 253-262.
52. Cohen Z, Vonshak A & Richmond A (1988) Effect of environmental conditions on fatty acid composition of the red alga Porphyridium cruentum: correlation to growth rate. J Phycol 24, 328-332.
53. Bell JG, Tocher DR, MacDonald FM, et al. (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.
54. Livak KJ & Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta]CT method. Methods 25, 402-408.
55. Ricker WE (1958) Handbook of computations for biological statistics of fish populations. Can J Fish Aquat Sci 119, 1-300.
56. Aragão C, Conceição LEC, Lacuisse M, et al. (2007) Do dietary amino acid profiles affect performance of larval gilthead seabream Aquat Living Resour 20, 155-161.
57. Yúfera M, Fernández-D́az C, Pascual E, et al. (2000) Towards an inert diet for first-feeding gilthead seabream Sparus aurata L. larvae. Aquacult Nutr 6, 143-152.
58. Sargent J, Bell G, McEvoy L, et al. (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177, 191-199.
59. Ganga R, Bell JG, Montero D, et al. (2005) Effect of dietary lipids on plasma fatty acid profiles and prostaglandin and leptin production in gilthead seabream (Sparus aurata). Comp Biochem Phys B 142, 410-418.
60. Maloberti P, Maciel EC, Castillo AF, et al. (2007) Enzymes involved in arachidonic acid release in adrenal and Leydig cells. Mol Cell Endocrinol 265, 113-120.
61. Liu J, Caballero MJ, Izquierdo M, et al. (2002) Necessity of dietary lecithin and eicosapentaenoic acid for growth, survival, stress resistance and lipoprotein formation in gilthead sea bream Sparus aurata. Fisheries Sci 68, 1165-1172.
62. Zheng F, Takeuchi T, Yoseda K, et al. (1996) Requirement of larval cod for arachidonic acid, eicosapentaenoic acid, and docosahexaenoic acid using by their enriched Artemia nauplii. Nippon Suisan Gakk 62, 669-676.
63. Ishizaki Y, Takeuchi T, Watanabe T, et al. (1998) A preliminary experiment on the effect of artemia enriched with arachidonic acid on survival and growth of yellowtail. Fisheries Sci 64, 295-299.
64. Komar CM (2005) Peroxisome proliferator-activated receptors (PPARs) and ovarian function-implications for regulating steroidogenesis, differentiation, and tissue remodeling. Reprod Biol Endocrinol 3, 14.
65. Lin Q, Ruuska SE, Shaw NS, et al. (1999) Ligand selectivity of the peroxisome proliferator-activated receptor a. Biochemistry 38, 185-190.
66. Geslin M & Auperin B (2004) Relationship between changes in mRNAs of the genes encoding steroidogenic acute regulatory protein and P450 cholesterol side chain cleavage in head kidney and plasma levels of cortisol in response to different kinds of acute stress in the rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 135, 70-80.
67. Hagen IJ, Kusakabe M & Young G (2006) Effects of ACTH and cAMP on steroidogenic acute regulatory protein and P450 11b-hydroxylase messenger RNAs in rainbow trout interrenal cells: relationship with in vitro cortisol production. Gen Comp Endocrinol 145, 254-262.
68. Castillo J, Castellana B, Acerete L, et al. (2008) Stress-induced regulation of steroidogenic acute regulatory protein expression in head kidney of Gilthead seabream (Sparus aurata). J Endocrinol 196, 313-322.
69. Arakane F, King SR, Du Y, et al. (1997) Phosphorylation of steroidogenic acute regulatory protein (StAR) modulates its steroidogenic activity. J Biol Chem 272, 32656-32662.
70. Dichtl W, Nilsson L, Goncalves I, et al. (1999) Very lowdensity lipoprotein activates nuclear factor-kappa B in endothelial cells. Circ Res 84, 1085-1094.
71. Yudt MR & Cidlowski JA (2002) The glucocorticoid receptor: coding a diversity of proteins and responses through a single gene. Mol Endocrinol 16, 1719-1726.
72. Jia Y & Turek JJ (2005) Altered NF-kappa B gene expression and collagen formation induced by polyunsaturated fatty acids. J Nutr Biochem 16, 500-506.