Journal of Comparative Physiology B

, Volume 186, Issue 8, pp 1009–1021 | Cite as

The satiety factor oleoylethanolamide impacts hepatic lipid and glucose metabolism in goldfish

  • Miguel Gómez-Boronat
  • Cristina Velasco
  • Esther Isorna
  • Nuria De Pedro
  • María J. Delgado
  • José L. Soengas
Original Paper
  • 254 Downloads

Abstract

Oleoylethanolamide (OEA) is an acylethanolamide synthesized mainly in the gastrointestinal tract with known effects in mammals on food intake and body mass through activation of peroxisome proliferator-activated receptor type α (PPARα). Since we previously demonstrated that acute treatment with OEA in goldfish resulted in decreased food intake and locomotor activity, as in mammals, we hypothesize that OEA would be involved in the control of energy metabolism in fish. Therefore, we assessed the effects of acute (for 6 h) and chronic (for 11 days) treatments with OEA (5 µg g−1 body mass) on metabolite concentrations and enzyme activities related to glucose and lipid metabolism in liver of goldfish (Carassius auratus). In the chronic treatment, OEA impairs the increase in body mass and reduces locomotor activity, without any signs of stress. The lipolytic capacity in liver decreased after both acute and chronic OEA treatments, whereas lipogenic capacity increased after acute and decreased after chronic treatment with OEA. These results are different from those observed to date in mammalian adipose tissue, but not so different from those known in liver, and might be attributed to the absence of changes in the expression of pparα, and/or to the increase in the expression of the clock gene bmal1a after chronic OEA treatment. As for glucose metabolism, a clear decrease in the capacity of hepatic tissue to use glucose was observed in OEA-treated fish. These results support an important role for OEA in the regulation of liver lipid and glucose metabolism, and could relate to the metabolic changes associated with circadian activity and the regulation of food intake in fish.

Keywords

Oleoylethanolamide (OEA) Goldfish Liver Lipid metabolism Glucose metabolism Body mass 

Notes

Acknowledgments

This study was supported by Spanish Ministerio de Economía y Competitividad (MINECO) research grant (AGL2013-46448-C3-2-R) to M.J.D, and by MINECO and European Fund for Regional Development research grant (AGL2013-46448-C3-1-R and FEDER) to J.L.S. M.G-B. and C.V. were recipients of predoctoral fellowship from MINECO (BES-2014-068103) and Universidade de Vigo, respectively.

References

  1. Astarita G, Rourke BC, Andersen JB, Fu J, Kim JH, Bennett AF, Hicks JW, Piomelli D (2006) Postprandial increase of oleoylethanolamide mobilization in small intestine of the Burmese python (Python molurus). Am J Physiol Regul Integr Comp Physiol 290:R1407–R1412CrossRefPubMedGoogle Scholar
  2. Azari EK, Ramachandran D, Weibel S, Arnold M, Romano A, Gaetani S, Langhans W, Mansouri A (2014) Vagal afferents are not necessary for the satiety effect of the gut lipid messenger oleoylethanolamide. Am J Physiol Regul Integr Comp Physiol 307:R167–R178CrossRefPubMedGoogle Scholar
  3. Azpeleta C, Martínez-Álvarez RM, Delgado MJ, Isorna E, de Pedro N (2010) Melatonin reduces locomotor activity and circulating cortisol in goldfish. Horm Behav 57:323–329CrossRefPubMedGoogle Scholar
  4. Berger J, Moller DE (2002) The mechanisms of action of PPARs. Annu Rev Med 53:409–435CrossRefPubMedGoogle Scholar
  5. Caruso MA, Sheridan MA (2011) New insights into the signaling system and function of insulin in fish. Gen Comp Endocrinol 173:227–247CrossRefPubMedGoogle Scholar
  6. De Pedro N, Martínez-Álvarez R, Delgado MJ (2006) Acute and chronic leptin reduces food intake and body weight in goldfish (Carassius auratus). J Endocrinol 188:513–520CrossRefPubMedGoogle Scholar
  7. Decara JM, Romero-Cuevas M, Rivera P, Macías-González M, Vida M, Pavón FJ, Serrano A, Cano C, Fresno N, Pérez-Fernández R, Rodríguez de Fonseca F, Suárez J (2012) Elaidyl-sulfamide, an oleoylethanolamide-modelled PPARα agonist, reduces body weight gain and plasma cholesterol in rats. Dis Models Mech 5:660–670CrossRefGoogle Scholar
  8. Fu J, Oveisi F, Gaetani S, Lin E, Piomelli D (2005) Oleoylethanolamide, and endogenous PPAR-α agonist, lowers body weight and hyperlipidemia in obese rats. Neuropharmacology 48:1147–1153CrossRefPubMedGoogle Scholar
  9. González-Yanes C, Serrano A, Bermúdez-Silva FJ, Hernández-Domínguez M, Páez-Ochoa MA, Rodríguez de Fonseca F, Sánchez-Margalet V (2005) Oleoylethanolamide impairs glucose tolerance and inhibits insulin-stimulated glucose uptake in rat adipocytes through p38 and JNK MAPK pathways. Am J Physiol Endocrinol Metab 289:E923–E929CrossRefPubMedGoogle Scholar
  10. Guzmán M, Lo Verme J, Fu J, Oveisi F, Blázquez C, Piomelli D (2004) Oleoylethanolamide stimulates lipolysis by activating the nuclear receptor peroxisome proliferator-activated receptor α (PPAR-α). J Biol Chem 279:27849–27854CrossRefPubMedGoogle Scholar
  11. Hernández-Pérez J, Míguez JM, Librán-Pérez M, Otero-Rodiño C, Naderi F, Soengas JL, López-Patiño MA (2015) Daily rhythms in activity and mRNA abundance of enzymes involved in glucose and lipid metabolism in liver of rainbow trout, Oncorhynchus mykiss. Influence of light and food availability. Chronobiol Int 32:1391–1408CrossRefPubMedGoogle Scholar
  12. Jönsson E (2013) The role of ghrelin in energy balance regulation in fish. Gen Comp Endocrinol 187:79–85CrossRefPubMedGoogle Scholar
  13. Keppler D, Decker K (1974) Glycogen determination with amyloglucosidase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York, pp 1127–1131Google Scholar
  14. 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–R1350CrossRefPubMedGoogle Scholar
  15. Librán-Pérez M, Figueiredo-Silva AC, Panserat S, Geurden I, Míguez JM, Polakof S, Soengas JL (2013a) Response of hepatic lipid and glucose metabolism to a mixture or single fatty acids: possible presence of fatty acid-sensing mechanisms. Comp Biochem Physiol A 164:241–248CrossRefGoogle Scholar
  16. Librán-Pérez M, López-Patiño MA, Míguez JM, Soengas JL (2013b) In vitro response of putative fatty acid-sensing systems in rainbow trout liver to increased levels of oleate or octanoate. Comp Biochem Physiol A 165:288–294CrossRefGoogle Scholar
  17. Librán-Pérez M, Geurden I, Dias K, Corraze G, Panserat S, Soengas JL (2015) Feeding rainbow trout with a lipid-enriched diet: effects on fatty acid sensing, regulation of food intake and cellular signaling pathways. J Exp Biol 218:2610–2619CrossRefPubMedGoogle Scholar
  18. Liu S, Alexander RK, Lee CH (2014) Lipid metabolites as metabolic messengers in inter-organ communication. Trends Endocrinol Metab 25:356–363CrossRefPubMedPubMedCentralGoogle Scholar
  19. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  20. Piomelli D (2013) A fatty gut feeling. Trends Endocrinol Metab 7:332–341CrossRefGoogle Scholar
  21. Polakof S, Míguez JM, Moon TW, Soengas JL (2007a) Evidence for the presence of a glucosensor in hypothalamus, hindbrain, and Brockmann bodies of rainbow trout. Am J Physiol Regul Integr Comp Physiol 292:R1657–R1666CrossRefPubMedGoogle Scholar
  22. Polakof S, Míguez JM, Soengas JL (2007b) In vitro evidences for glucosensing capacity and mechanisms in hypothalamus, hindbrain, and Brockmann bodies of rainbow trout. Am J Physiol Regul Integr Comp Physiol 293:R1410–R1420CrossRefPubMedGoogle Scholar
  23. Polakof S, Míguez JM, Soengas JL (2008a) Changes in food intake and glucosensing function of hypothalamus and hindbrain in rainbow trout subjected to hyperglycemic or hypoglycemic conditions. J Comp Physiol A 194:829–839CrossRefGoogle Scholar
  24. Polakof S, Míguez JM, Soengas JL (2008b) Dietary carbohydrates induce changes in glucosensing capacity and food intake in rainbow trout. Am J Physiol Regul Integr Comp Physiol 295:R478–R489CrossRefPubMedGoogle Scholar
  25. Polakof S, Panserat S, Plagnes-Juan E, Soengas JL (2008c) Altered dietary carbohydrates significantly affect gene expression of the major glucosensing components in Brockmann bodies and hypothalamus of rainbow trout. Am J Physiol Regul Integr Comp Physiol 295:R1077–R1088CrossRefPubMedGoogle Scholar
  26. Polakof S, Panserat S, Soengas JL, Moon TW (2012) Glucose metabolism in fish: a review. J Comp Physiol B 182:1015–1045CrossRefPubMedGoogle Scholar
  27. Proulx K, Cota D, Castaneda TR, Tschop MH, D’Alessio DA, Tso P, Woods SC, Seeley RJ (2005) Mechanisms of oleoylethanolamide-induced changes in feeding behavior and motor activity. Am J Physiol Regul Integr Comp Physiol 289:R729–R737CrossRefPubMedGoogle Scholar
  28. Rodríguez de Fonseca F, Navarro M, Gómez R, Escuredo L, Nava F, Fu J, Murillo-Rodríguez E, Giuffrida A, Lo Verme J, Gaetani S (2001) An anorexic lipid mediator regulated by feeding. Nature 414:209–212CrossRefPubMedGoogle Scholar
  29. Romano A, Soares Potes C, Tempesta B, Cassano T, Cuomo V, Lutz T, Gaetani S (2013) Hindbrain noradrenergic input to the hypothalamic PVN mediates the activation of oxytocinergic neurons induced by the satiety factor oleoylethanolamide. Am J Physiol Endocrinol Metab 305:E1266–E1273CrossRefPubMedGoogle Scholar
  30. Romano A, Tempesta B, Provensi G, Passani MB, Gaetani S (2015) Central mechanisms mediating the hypophagic effects of oleoylethanolamide and N-acylphosphatidylethanolamines: different lipid signals? Front Pharmacol 6:137CrossRefPubMedPubMedCentralGoogle Scholar
  31. Sánchez-Bretaño A, Callejo M, Montero M, Alonso-Gómez AL, Delgado MJ, Isorna E (2016) Performing a hepatic timing signal: glucocorticoids induce gper1a and gper1b expression and repress gclock1a and gbmal1a in the liver of goldfish. J Comp Physiol B 186:73–82CrossRefPubMedGoogle Scholar
  32. Sánchez-Gurmaches J, Cruz-Garcia L, Gutiérrez J, Navarro I (2012) Adiponectin effects and gene expression in rainbow trout: an in vivo and in vitro approach. J Exp Biol 215:1373–1383CrossRefPubMedGoogle Scholar
  33. Serrano A, Del Arco I, Pavón FJ, Macías M, Perez-Valero V, Rodríguez de Fonseca F (2008) The cannabinoid CB1 receptor antagonist SR141716A (Rimonabant) enhances the metabolic benefits of long-term treatment with oleoylethanolamide in Zucker rats. Neuropharmacology 54:226–234CrossRefPubMedGoogle Scholar
  34. Serrano A, Pavón FJ, Tovar S, Casanueva F, Señarís R, Diéguez C, Rodríguez de Fonseca F (2011) Oleoylethanolamide: effects on hypothalamic transmitters and gut peptides regulating food intake. Neuropharmacology 60:593–601CrossRefPubMedGoogle Scholar
  35. Shimba S, Ishii N, Ohta Y, Ohno T, Watabe Y, Hayashi M, Wada T, Aoyagi T, Tezuka M (2005) Brain and muscle Arnt-like protein-1 (BMAL1) a component of the molecular clock, regulates adipogenesis. Proc Natl Acad Sci USA 102:12071–12076CrossRefPubMedPubMedCentralGoogle Scholar
  36. Shimba S, Ogawa T, Hitosugi S, Ichihashi Y, Nakadaira Y, Kobayashi M, Tezuka M, Kosuge Y, Ishige K, Ito Y, Komiyama K, Okamatsu-Ogura Y, Kimura K, Saito M (2011) Deficient of a clock gene, brain and muscle Arnt-Like Protein-1 (BMAL1), induces dyslipidemia and ectopic fat formation. PLoS One 6:e325231CrossRefGoogle Scholar
  37. Soengas JL (2014) Contribution of glucose- and fatty acid sensing systems to the regulation of food intake in fish. A review. Gen Comp Endocrinol 205:36–48CrossRefPubMedGoogle Scholar
  38. Suárez J, Rivera P, Arrabal S, Crespillo A, Serrano A, Baixeras E, Pavón FJ, Cifuentes M, Nogueiras R, Ballesteros J, Diéguez C, Rodríguez de Fonseca F (2014) Oleoylethanolamide enhances β-adrenergic-mediated thermogenesis and white-to-brown adipocyte phenotype in epididymal white adipose tissue in rat. Dis Models Mech 7:129–141CrossRefGoogle Scholar
  39. Thabuis C, Destaillats F, Lambert DM, Muccioli GG, Maillot M, Harach T, Tissot-Favre D, Martin J-C (2011) Lipid transport function is the main target of oral oleoylethanolamide to reduce adiposity in high-fat-fed-mice. J Lipid Res 52:1373–1382CrossRefPubMedPubMedCentralGoogle Scholar
  40. Tinoco AB, Armirotti A, Isorna E, Delgado MJ, Piomelli D, De Pedro N (2014) Role of oleoylethanolamide as a feeding regulator in goldfish. J Exp Biol 217:2761–2769CrossRefPubMedGoogle Scholar
  41. Valenti M, Cottone E, Martínez R, De Pedro N, Rubio M, Viveros MP, Franzoni MF, Delgado MJ, Di Marzo V (2005) The endocannabinoid system in the brain of Carassius auratus and its possible role in the control of food intake. J Neurochem 95:662–672CrossRefPubMedGoogle Scholar
  42. Velasco C, Otero-Rodiño C, Librán-Pérez M, López-Patiño MA, Míguez JM, Cerdá-Reverter JM, Soengas JL (2016a) Ghrelin modulates hypothalamic fatty acid sensing and control of food intake in rainbow trout. J Endocrinol 228:25–37CrossRefPubMedGoogle Scholar
  43. Velasco C, Librán-Pérez M, Otero-Rodiño C, López-Patiño MA, Míguez JM, Soengas JL (2016b) Intracerebroventricular ghrelin treatment affects lipid metabolism in liver of rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 228:33–39CrossRefPubMedGoogle Scholar
  44. Yang Y, Chen M, Georgeson KE, Harmon CM (2007) Mechanism of oleoylethanolamide on fatty acid uptake in small intestine after food intake and body weight reduction. Am J Physiol Regul Integr Comp Physiol 292:R235–R241CrossRefPubMedGoogle Scholar
  45. Zhang D, Tong X, Arthurs B, Guha A, Rui L, Kamath A, Inoki K, Yin L (2014) Liver clock protein BMAL1 promotes de novo lipogenesis through insulin-mTORC2-AKT signaling. J Biol Chem 289:25925–25935CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Miguel Gómez-Boronat
    • 1
  • Cristina Velasco
    • 2
  • Esther Isorna
    • 1
  • Nuria De Pedro
    • 1
  • María J. Delgado
    • 1
  • José L. Soengas
    • 2
  1. 1.Departamento de Fisiología (Fisiología Animal II), Facultad de BiologíaUniversidad Complutense de MadridMadridSpain
  2. 2.Laboratorio de Fisioloxía Animal, Departamento de Bioloxía Funcional e Ciencias da Saúde, Facultade de Bioloxía, Edificio de Ciencias ExperimentaisUniversidade de VigoVigoSpain

Personalised recommendations