Skip to main content
SpringerLink
Log in

Modulation of the Expression of Components of the Stress Response by Dietary Arachidonic Acid in European Sea Bass (Dicentrarchus labrax) Larvae

  • Original Article
  • Published:
Lipids

Abstract

This study reports for the first time on European sea bass, Dicentrarchus labrax (L.), larvae, the effect of different levels of dietary arachidonic acid (ARA; 20:4n-6) on the expression of genes related to the fish stress response. Copies of mRNA from genes related to steroidogenesis [StAR (steroidogenic acute regulatory protein), c-Fos, and CYP11β (11β-hydroxylase gene)], glucocorticoid receptor complex [GR (glucocorticoid receptor) and HSP (heat shock proteins) 70 and 90) and antioxidative stress (catalase (CAT), superoxide dismutase (SOD), and glutathione peroxidase] were quantified. Eighteen day-old larvae were fed for 14 days with three experimental diets with increasing levels of ARA (0.3, 0.6 and 1.2 % d.w.) and similar levels of docosahexaenoic (22:6n-3) and eicosapentaenoic (20:5n-3) acids (5 and 3 %, respectively). The quantification of stress-related genes transcripts was conducted by One-Step TaqMan real time RT-PCR with the standard curve method (absolute quantification). Increase dietary levels of ARA induced a significantly (p < 0.05) down-regulation of genes related to cortisol synthesis, such as StAR and CYP11β and up-regulated genes related to glucocorticoid receptor complex, such as HSP70 and GR. No effects were observed on antioxidant enzymes gene expression. These results revealed the regulatory role of dietary ARA on the expression of stress-related genes in European sea bass larvae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ACTH:

Adrenocorticotropic hormone

ARA:

Arachidonic acid (204n-6)

CAT:

Catalase

COX:

Cyclooxygenase

CYP11β:

Cytochrome 11β-hydroxylase

DHA:

Docosahexaenoic acid (226n-3)

EPA:

Eicosapentaenoic acid (205n-3)

GH:

Growth hormone

GLC:

Gas liquid chromatography

GPX:

Glutathione peroxidase

GR:

Glucocorticoid receptor

HSP:

Heat shock protein

HPI:

Hypothalamic-pituitary-interrenal

IGF:

Insulin growth factor

LC-PUFA:

Long chain polyunsaturated fatty acid(s)

MW:

Molecular weight

PIn:

Peroxidation index

PGE:

Prostaglandin E

RT-PCR:

Real time polymerase chain reaction

SGR:

Specific growth rate

SOD:

Superoxide dismutase

StAR:

Steroidogenic acute regulatory protein

References

  1. Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  3. Iwama GK, Alfonso LOB, Vijayan MM (2006) Stress in fish. In: Evans DH, Claiborne JB (eds) The physiology of fishes, 3rd edn. CRC Press, Boca Raton, pp 319–342

    Google Scholar 

  4. 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

    Article  CAS  PubMed  Google Scholar 

  5. Aluru N, Vijayan MM (2009) Stress transcriptomics in fish: a role for genomic cortisol signaling. Gen Comp Endocrinol 164:142–150

    Article  CAS  PubMed  Google Scholar 

  6. Tort L (2011) Stress and immune modulation in fish. Dev Comp Immunol 35:1366–1375

    Article  CAS  PubMed  Google Scholar 

  7. Jiang JQ, Young G, Kobayashi T, Nagahama Y (1998) Eel, Anguilla japonica, testis 11beta-hydroxylase gene is expressed in interrenal tissue and its product lacks aldosterone synthesizing activity. Mol Cel Endocrinol 146:207–211

    Article  CAS  Google Scholar 

  8. Stocco DM, Wang X, Jo Y, Manna PR (2005) Multiple signaling pathways regulation steroidogenesis and steroidogenic acute regulatory protein expression: more complicated than we thought. Mol Endocrinol 19:2647–2659

    Article  CAS  PubMed  Google Scholar 

  9. Filby AL, Tyler CR (2007) Cloning and characterization of cDNAs for hormones and/or receptors of growth hormone, insulin-like growth factor-I, thyroid hormone, and corticosteroid and the gender-, tissue-, and developmental-specific expression of their mRNA transcripts in fathead minnow (Pimephales promelas). Gen Comp Endocrinol 150:151–163

    Article  CAS  PubMed  Google Scholar 

  10. Pratt WB (1993) The role of heat shock proteins in regulating the function, folding, and trafficking of the glucocorticoid receptor. J Biol Chem 268:21455–21458

    CAS  PubMed  Google Scholar 

  11. 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

    Article  CAS  PubMed  Google Scholar 

  12. Srivastava PK (2002) Roles of heat shock proteins in innate and adaptative immunity. Nat Rev Immunol 2:184–194

    Article  Google Scholar 

  13. Kanazawa A (1997) Effects of docosahexaenoic acid and phospholipids on stress tolerance of fish. Aquaculture 155:129–134

    Article  CAS  Google Scholar 

  14. Montero D, Tort L, Izquierdo MS, Robaina L, Vergara JM (1998) Depletion of serum alternative complement pathway activity in gilthead sea bream caused by [alpha]-tocopherol and n-3 HUFA dietary deficiencies. Fish Physiol Biochem 18:399–407

    Article  CAS  Google Scholar 

  15. Koven W, Barr Y, Lutzky S, Ben-Atia I, Weiss R, Harel M, Behrens P, Tandler A (2001) The effect of dietary arachidonic acid (20:4n-6) on growth, survival and resistance to handling stress in gilthead sea bream (Sparus aurata) larvae. Aquaculture 193:107–122

    Article  CAS  Google Scholar 

  16. Koven W, Van Anholt R, Lutzky S, Ben Atia I, Nixon O, Ron B, Tandler A (2003) The effect of dietary arachidonic acid on growth, survival, and cortisol levels in different-age gilthead sea bream larvae (Sparus aurata) exposed to handling or daily salinity change. Aquaculture 228:307–320

    Article  CAS  Google Scholar 

  17. Van Anholt RD, Koven WM, Lutzky S, Wendelaar Bonga SE (2004) Dietary supplementation with arachidonic acid alters the stress response of gilthead sea bream (Sparus aurata) larvae. Aquaculture 238:369–383

    Article  Google Scholar 

  18. 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

    Chapter  Google Scholar 

  19. 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

    Article  CAS  PubMed  Google Scholar 

  20. Ganga R, Bell JG, Montero D, Atalah E, Vraskou Y, Tort L, Fernández A, Izquierdo MS (2011) 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

    Article  CAS  PubMed  Google Scholar 

  21. Montero D, Terova G, Rimoldi S, Tort L, Negrin D, Zamorano MJ, Izquierdo MS (2015) Modulation of ACTH-induced expression of stress-related genes by polyunsaturated fatty acids in interrenal cells from European sea bass, Dicentrarchus labrax. J Nutr Sci 4:e16

    Article  PubMed Central  PubMed  Google Scholar 

  22. Watanabe T, Izquierdo MS, Takeuchi T, Satoh S, Kitajima C (1989) Comparison between eicosapentaenoic and docosahexaenoic acids in terms of essential fatty acids efficacy in larval red sea bream. Nippon Suisan Gakkaishi 55:635–1640

    Google Scholar 

  23. Bessonart M, Izquierdo MS, Salhi M, Hernández-Cruz CM, González MM, Fernández-Palacios H (1999) Effect of dietary arachidonic acid levels on growth and survival of gilthead sea bream (Sparus aurata L.) larvae. Aquaculture 179:265–275

    Article  CAS  Google Scholar 

  24. Atalah E, Hernández-Cruz CM, Ganuza E, Benítez-Santana T, Ganga R, Roo J, Montero D, Izquierdo MS (2011) Importance of dietary arachidonic acid for survival, growth and stress resistance of larval European sea bass (Dicentrarchus labrax) fed high dietary docosahexaenic and eicosapentaenoic acids. Aquac Res 42:1261–1268

    Article  CAS  Google Scholar 

  25. Liu J, Caballero MJ, Izquierdo MS, El-Sayed Ali T, Hernández-Cruz CM, Valencia A, Fernández-Palacios H (2002) Necessity of dietary lecithin and eicosapentaenoic acid for growth, survival, stress resistance and lipoprotein formation in gilthead sea bream Sparus aurata. Fish Sci 68:1165–1172

    Article  CAS  Google Scholar 

  26. Ganga R, Tort L, Acerete L, Montero D, Izquierdo MS (2006) Modulation of ACTH-induced cortisol release by polyunsaturated fatty acids in interrenal cells from gilthead sea bream, Sparus aurata. J Endocrinol 190:39–45

    Article  CAS  PubMed  Google Scholar 

  27. Wang X, Shen CL, Dyson MT, Yin X, Schiffer RB, Grammas P, Stocco MD (2006) The involvement of epoxygenase metabolites of arachidonic acid in cAMP-stimulated steroidogenesis and steroidogenic acute regulatory protein gene expression. J Endocrinol 190:871–878

    Article  CAS  PubMed  Google Scholar 

  28. Alves Martins D, Rocha F, Castanheira F, Mendes A, Pousao-Ferreira P, Bandarra N, Coutinho J, Morais S, Yúfera M, Conceiçao L, Martínez-Rodriguez G (2013) Effects of dietary arachidonic acid on cortisol production and gene expression in stress response in Senegalese sole (Solea senegalensis) post larvae. Fish Physiol Biochem 39:1223–1238

    Article  CAS  Google Scholar 

  29. Shah NG, Tulapurkar ME, Singh IS, Shelhamer JH, Cowan MJ, Hasday JD (2010) Prostaglandin E2 potentiates heat shock-induced heat shock-induced heat shock protein 72 expression in A549 cells. Prostaglandins Other Lipid Mediat 93:1–7

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Benitez-Dorta V, Caballero MJ, Izquierdo MS, 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  CAS  PubMed  Google Scholar 

  31. AOAC (1995) Official methods of analysis of the association analytical chemist. AOAC, Arlington, p 1018

    Google Scholar 

  32. 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 226:497–509

    CAS  PubMed  Google Scholar 

  33. Christie WW (1982) Lipid analysis. Pergamon Press, Oxford

    Google Scholar 

  34. Izquierdo M, WatanabeT Takeuchi T, Arakawa T, Kitajima C (1990) Optimum EFA levels in Artemia to meet the EFA requirements of red seabream (Pagrus major). In: Takeda M, Watanabe T (eds) The current status of fish nutrition in aquaculture. Tokyo University Fisheries, Tokyo, pp 221–232

    Google Scholar 

  35. Witting LA, Horwitt MK (1964) Effect of degree of fatty acid unsaturation in tocopherol deficiency-induced creatinuria. J Nutr 82:19–33

    CAS  PubMed  Google Scholar 

  36. Rimoldi S, Terova G, Brambilla F, Bernardini G, Gornati R, Saroglia M (2009) Molecular characterization and expression analysis of Na+/H+ exchanger NHE-1 and c-Fos genes in sea bass Dicentrarchus labrax, L. exposed to acute and chronic hypercapnia. J Exp Mar Biol Ecol 375:32–40

    Article  CAS  Google Scholar 

  37. Izquierdo MS (1996) Essential fatty acid requirements of cultured marine fish larvae. Aquac Nutr 2:183–191

    Article  CAS  Google Scholar 

  38. Boglino A, Darias MJ, Estevez A, Andree KB, Gisbert E (2012) The effect of dietary arachidonic acid during the Artemia feeding period on larval growth and skeletogenesis in Senegalese sole, Solea senegalensis. J Appl Ichthyol 28:411–418

    Article  CAS  Google Scholar 

  39. Alves Martins D, Rocha F, Martínez-Rodriguez G, Bell G, Morais S, Castanheira F, Bandarra N, Coutinho J, Yúfera M, Conceiçao LEC (2012) Teleost fish larvae adapt to dietary arachidonic acid supply through modulation of the expression of lipid metabolism and stress genes. Br J Nutr 108:864–874

    Article  CAS  PubMed  Google Scholar 

  40. Li Y, Seifert MF, Ney DM, Grahn M, Grant AL, Allen KGD, Watkins BA (1999) Dietary conjugated linoleic acids alter serum IGF-I and IGF binding protein concentrations and reduce bone formation in rats fed (n-6) or (n-3) fatty acids. J Bone Min Res 14:1153–1162

    Article  CAS  Google Scholar 

  41. Celil AB, Campbell PG (2005) BMP-2 and insulin-like growth factor-I mediate osterix (Osx) expression in human mesenchymal stem cells via the MAPK and protein kinase D signaling pathways. J Biol Chem 280:31353–31359

    Article  CAS  PubMed  Google Scholar 

  42. Carnevali O, de Vivo L, Sulpizio R, Gioacchini G, Olivotto I, Silvi S, Cresci A (2006) Growth improvement by probiotic in European sea bass juveniles (Dicentrarchus labrax L.), with particular attention to IGF-1, myostatin and cortisol gene expression. Aquaculture 258:430–438

    Article  CAS  Google Scholar 

  43. Leung LY, Kwong AKY, Man AKY, Woo NYS (2008) Direct actions of cortisol, thyroxine and growth hormone on IGF-I mRNA expression in sea bream hepatocytes. Comp Biochem Physiol A Mol Int Physiol 151:705–710

    Article  CAS  Google Scholar 

  44. Aluru N, Vijayan MM (2006) Aryl hydrocarbon receptor activation impairs cortisol response to stress in rainbow trout by disrupting the rate-limiting steps in steroidogenesis. Endocrinol 147:1895–1903

    Article  CAS  Google Scholar 

  45. Rowley AF, Pettitt TR, Secombes CJ, Sharp GJE, Barrow SE, Vickers PJ (1995) Eicosanoids and their role in immune modulation in fish—a brief overview. Fish Shellfish Immunol 5:63–105

    Article  Google Scholar 

  46. Mohn CE, Fernandez-Solari J, De Laurentiis A, Prestifilippo JP, de la Cal C, Funk R, Bornstein SR, McCann SM, Rettori V (2005) The rapid release of corticosterone from the adrenal induced by ACTH in mediated by nitric oxide acting by prostaglandin E2. Proc Nat Acad Sci USA 102:6213–6218

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Wang X, Dyson MT, Jo Y, Stocco DM (2003) Inhibition of cyclooxygenase-2 activity enhances steroidogenesis and steroidogenic acute regulatory gene expression in MA-10 mouse Leydig cells. Endocrinology 144:3368–3375

    Article  CAS  PubMed  Google Scholar 

  48. Karin M, Liu Z, Zandi E (1997) Ap-1 function and regulation. Curr Opin Cell Biol 9:240–246

    Article  CAS  PubMed  Google Scholar 

  49. Okimoto DK, Blaus A, Schmidt M, Gordon K, Dent GW, Levine S (2002) Differential expression of c-Fos and tyrosine hydroxylase mRNA in the adrenal gland of the infant rat: evidence for an adrenal hyporesponsive period. Endocrinology 143:1717–1725

    Article  CAS  PubMed  Google Scholar 

  50. Yudt MR, Cidlowski JA (2002) The glucocorticoid receptor: coding a diversity of proteins and responses through a single gene. Mol Endocrinol 16:1719–1726

    Article  CAS  PubMed  Google Scholar 

  51. Sathiyaa R, Vijayan MM (2003) Autoregulation of glucocorticoid receptor by cortisol in rainbow trout hepatocytes. Am J Physiol Cell Physiol 284:C1508–C1515

    Article  CAS  PubMed  Google Scholar 

  52. 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

    Article  CAS  PubMed  Google Scholar 

  53. Ranhotra HS, Sharma R (2004) Polyunsaturated fatty acids inhibit mouse hepatic glucocorticoid receptor activation in vitro. Ind J Biochem Biophys 41:246–249

    CAS  Google Scholar 

  54. Jurivich DA, Sistonen L, Kevin D, Sarge KD, Morimoto RI (1994) Arachidonate is a potent modulator of human heat-shock gene-transcription. Proc Natl Acad Sci USA 91:2280–2284

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  55. Basu N, Kennedy CJ, Iwama GK (2003) The effect of stress on the association between HSP70 and the glucocorticoid receptor in rainbow trout. Comp Biochem Physiol A Mol Integr Physiol 134:655–663

    Article  CAS  PubMed  Google Scholar 

  56. Basu N, Todgham AE, Ackerman MA, Bibeau MR, Nakano K, Schulte PM, Iwama GK (2002) Heat shock protein genes and their functional significance in fish. Gene 295:173–183

    Article  CAS  PubMed  Google Scholar 

  57. Samples BL (1999) Polyunsaturated fatty acids enhance the heat induced stress response in rainbow trout (Oncorhynchus mykiss) leukocytes. Comp Biochem Physiol Part B Biochem Mol Biol 123:389–397

    Article  CAS  Google Scholar 

  58. Perez-Sanchez J, Borrel M, Bermejo-Nogales A, Benedito-Palos L, Saera-Vila A, Calduch-Giner JA, Kaushik S (2013) Dietary oils mediate cortisol kinetics and the hepatic mRNA expression profile of stress-responsive genes in gilthead sea bream (Sparus aurata) exposed to crowding stress. Implications on energy homeostasis and stress susceptibility. Comp Biochem Physiol Part D Genom Proteom 8:123–130

    CAS  Google Scholar 

  59. Sanz A, Furne E, Trenzado CE, De Haro C, Sanchez-Muros MJ (2012) Study of the oxidative state, as a Marker of Welfare, on Gilthead Sea Bream, Sparus aurata, subjected to handling stress. J World Aquac Soc 43:707–715

    Article  Google Scholar 

  60. Leonardi F, Attorri L, Di Benedetto R, Di Biase A, Sanchez M, Nardini M, Salvati S (2005) Effect of arachidonic, eicosapentaenoic and docosahexaenoic acids on the oxidative status of C6 glioma cells. Free Radical Res 39:865–874

    Article  CAS  Google Scholar 

  61. Betancor MB, Almaida-Pagán PF, Sprague M, Hernández A, Tocher DR (2015) Roles of selenoprotein antioxidant protection in zebrafish, Danio rerio, subjected to dietary oxidative stress. Fish Physiol Biochem 41:705–720

    Article  CAS  PubMed  Google Scholar 

  62. Carrier JK, Watanabe WO, Harel M, Rezek TC, Seaton PJ, Shafer TH (2011) Effects of dietary arachidonic acid on larval performance, fatty acid profiles, stress resistance, and expression of Na+/K+ ATPase mRNA in black sea bass Centropristis striata. Aquaculture 319:111–121

    Article  CAS  Google Scholar 

  63. Furuita H, Takeuchi T, Toyota M, Watanabe T (1996) EPA and DHA requirements in early juvenile red sea bream using HUFA enriched Artemia nauplii. Fish Sci 62:246–251

    CAS  Google Scholar 

  64. Izquierdo MS, Socorro J, Arantzamendi L, Hernández-Cruz CM (2000) Recent advances in lipid nutrition in fish larvae. Fish Physiol Biochem 22:97–107

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work has been partly funded under the EU seventh Framework Programme by the ARRAINA project N288925: Advanced Research Initiatives for Nutrition & Aquaculture.

Author information

Authors and Affiliations

  1. Grupo de Investigación en Acuicultura (GIA), Parque Científico Tecnológico Marino de Taliarte, Universidad de Las Palmas de Gran Canaria (ULPGC), Muelle de Taliarte s/n, Telde, 35214, Las Palmas, Canary Islands, Spain

    Daniel Montero, Eyad Atalah, Silvia Torrecillas, María J. Caballero, María J. Zamorano & Marisol Izquierdo

  2. Department of Biotechnology and Life Sciences, University of Insubria, Via Dunant, 3-21100, Varese, Italy

    Genciana Terova & Simona Rimoldi

  3. Institute of Aquaculture, School of Natural Sciences, University of Stirling, Stirling, FK9-4LA, UK

    Mónica B. Betancor

Authors
  1. Daniel Montero
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Genciana Terova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simona Rimoldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mónica B. Betancor
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eyad Atalah
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Silvia Torrecillas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. María J. Caballero
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. María J. Zamorano
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Marisol Izquierdo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel Montero.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Montero, D., Terova, G., Rimoldi, S. et al. Modulation of the Expression of Components of the Stress Response by Dietary Arachidonic Acid in European Sea Bass (Dicentrarchus labrax) Larvae. Lipids 50, 1029–1041 (2015). https://doi.org/10.1007/s11745-015-4057-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-015-4057-1

Keywords

Search

Navigation