Fish Physiology and Biochemistry

, Volume 27, Issue 3–4, pp 179–188 | Cite as

Energy Metabolism in Fish Tissues Related to Osmoregulation and Cortisol Action

  • Raúl Laiz-Carrión
  • Susana Sangiao-Alvarellos
  • José M. Guzmán
  • María P. Martín del Río
  • Jesús M. Míguez
  • José L. Soengas
  • Juan M. Mancera
Article

Abstract

This is an overview of our recent studies of energy metabolism in fish brain and other organs regulated by exogenous (feeding, salinity) and endogenous (hormones) factors. To highlight our approach, we present latest results concerned osmoregulation in the gills of gilthead seabream, Sparus auratus. Our model, the seabream, is a euryhaline teleost capable of adaptation to extreme changes in environmental salinity. Treatment with cortisol allowed us to achieve circulating cortisol levels similar to those observed during osmotic adaptation and to assess how elevated hormonal levels affected simultaneously metabolic and osmoregulatory capacities of the gill tissue. Cortisol-implanted fish showed higher gill Na+,K+-ATPase activity than control fish but no changes were observed in plasma osmolality and ion levels. Plasma levels of glucose and lactate increased in cortisol-implanted fish while protein levels decreased. Cortisol treatment elicited metabolic changes in liver and brain reflecting an activation of the glycogenic and gluconeogenic potential in liver, and the glycogenic potential in brain, which are confirmatory of data obtained in previous experiments. In gills, we demonstrated that cortisol treatment elicited changes in their energy metabolism that can be summarized as a decreased capacity in the use of exogenous glucose (decreased HK activity), a decrease in the capacity of the pentose phosphate pathway (decreased G6PDH activity), and an increased glycolytic potential (increased PK activity). Observed metabolic changes in gills can be associated with those occurring in nature during osmotic adaptation in the same fish species.

gilthead sea bream; gills; cortisol; osmoregulation; energy metabolism 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aldegunde, M., Andrés, M.D. and Soengas, J.L. 2000a. Uptake of 3–O-methyl-D-[U14C]glucose into brain of rainbow trout: possible effects of melatonin. J. Comp. Physiol. B. 170: 237–243.PubMedCrossRefGoogle Scholar
  2. Aldegunde, M., Soengas, J.L. and Rozas, G. 2000b. Acute effects of L-tryptophan on tryptophan hydroxylation rate in brain regions (hypothalamus and medulla) of rainbow trout (Oncorhynchus mykiss). J. Exp. Zool. 286: 131–135.PubMedCrossRefGoogle Scholar
  3. Aldegunde, M., García, J., Soengas, J.L. and Rozas, G. 1998. Uptake of tryptophan into brain of rainbow trout (Oncorhynchus mykiss). J. Exp. Zool. 282: 285–289.CrossRefGoogle Scholar
  4. Aldegunde, M., Soengas, J.L., Ruibal, C. and Andres, M.D. 1999. Effects of chronic exposure to γ-HCH (lindane) on brain serotonergic and gabaergic systems, and serum cortisol and thyroxine levels of rainbow trout, Oncorhynchus mykiss. Fish Physiol. Biochem. 20: 325–330.CrossRefGoogle Scholar
  5. Andersen, D.E., Reid, S.D., Moon, T.W. and Perry, S.F. 1991. Metabolic effects associated with chronically elevated cortisol in rainbow trout (Oncorhynchus mykiss). Can. J. Fish. Aquat. Sci. 48: 1811–1817.Google Scholar
  6. Arends, R.J., Mancera, J.M., Muñoz, J.L., Wendelaar Bonga, S.E. and Flik G. 1999. The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement. J. Endocrinol. 163: 149–157.PubMedCrossRefGoogle Scholar
  7. Arends, R.J., Rotllant, J., Metz, JR, Mancera, J.M., Wendelaar Bonga, S.E. and Flik, G. 2000. α-MSH acetylation in the pituitary gland of the sea bream (Sparus aurata L.) in response to different backgrounds, confinement and air exposure. J. Endocrinol. 166: 427–435.PubMedCrossRefGoogle Scholar
  8. Chervinski, J. 1984. Salinity tolerance of young gilthead sea bream Sparus aurata. Bamidgeh 36: 121–124.Google Scholar
  9. Deane, E.E., Kelly, S.P. and Woo, N.Y.S. 2000. Hypercortisolemia does not affect the branchial osmoregulatory response of the marine teleost Sparus sarba. Life Science 15: 1436–1444.Google Scholar
  10. Dugan, S.G. and Moon, T.W. 1998. Cortisol does not affect hepatic alfa-and beta-adrenoceptor properties in rainbow trout (Oncorhynchus mykiss). Fish Physiol. Biochem. 18: 343–352.CrossRefGoogle Scholar
  11. Figueroa, R.I., Rodríguez-Sabarís, R., Aldegunde, M. and Soengas, J.L. 2000. Effects of food deprivation on 24h-changes in brain and liver carbohydrate and ketone body metabolism of rainbow trout. J. Fish Biol. 57: 631–646.Google Scholar
  12. Gamperl, A.K., Vijayan, M.M. and Boutilier, R.G. 1994. Experimental control of stress hormone levels in fishes: techniques and applications. Rev. Fish Biol. Fish. 4: 215–255.CrossRefGoogle Scholar
  13. Gradín, A., Ceinos, R.M., Sangiao, S., Míguez, J.M. and Soengas, J.L. 2002. Preparation of astrocyte-rich primary cultures from rainbow trout (Oncorhynchus mykiss) brain. In: Proceedings of the 21st Conference of European Comparative Endocrinologists. pp. 195–198. Edited by R. Keller, H. Dircksen, D. Seldmeier, and H. Vaudry. Monduzzi Editore, Bologna.Google Scholar
  14. Kloas, W., Stahl, L. and Hanke, W. 1998. Characterization of corticosteroid receptors in two fish species, euryhaline tilapia and stenohaline carp. Ann. N.Y. Acad. Sci. 839: 602–603.CrossRefGoogle Scholar
  15. Knoebl, I., Fitzpatrick, M.S. and Schreck, C.B. 1996. Characterization of a glucocorticoid receptor in the brains of Chinook salmon, Oncorhynchus tschawytscha. Gen. Comp. Endocrinol. 89: 17–27.Google Scholar
  16. Laiz-Carrión, R., Martín del Río, M.P., Miguez, J.M., Mancera, J.M. and Soengas, J.L. 2003. Influence of cortisol on osmoregulation and energy metabolism in gilthead seabream Sparus aurata. J. Exp. Zool. 298A: 105–118.CrossRefGoogle Scholar
  17. Lynshiang, D. and Gupta B.B.P. 2000. Role of catecholamines and corticosteroids in regulation of the oxidative metabolism in male Clarias batrachus. Current Sci. 78: 1112–1117.Google Scholar
  18. Madsen, S.S., Jensen, M.K., Nohr, J. and Kristiansen, K. 1995. Expression of Na+-K+-ATPase in the brown trout, Salmo trutta: in vivo modulation by hormones and seawater. Am. J. Physiol. 269: R1339–1345.PubMedGoogle Scholar
  19. Magnoni, L.J., Míguez, J.M. and Soengas, J.L. 2001. Glucagon effects on brain carbohydrate and ketone body metabolism in rainbow trout. J. Exp. Zool. 290: 662–671.PubMedCrossRefGoogle Scholar
  20. Mancera, J.M. and McCormick, S.D. 1998a. Evidence for growth hormone/insulin-like growth factor I axis regulation of seawater acclimation in the euryhaline teleost Fundulus heteroclitus. Gen. Comp. Endocrinol. 111: 103–112.PubMedCrossRefGoogle Scholar
  21. Mancera, J.M. and McCormick, S.D. 1998b. Osmoregulatory actions of the GH/IGF-I axis in non-salmonid teleosts. Comp. Biochem. Physiol. 121B: 43–48.Google Scholar
  22. Mancera, J.M. and McCormick, S.D. 1999. Influence of cortisol, growth hormone, insulin-like growth factor I and 3,3′, 5–triiodo-L-thyronine on hypoosmoregulatory ability in the euryhaline teleot Fundulus heteroclitus. Fish Physiol. Biochem. 21: 25–33.CrossRefGoogle Scholar
  23. Mancera, J.M., Fernández-Llebrez, P. and Pérez-Fígares, J.M. 1995. Effect of decreased environmental salinity on growth hormone cells in the gilthead sea bream (Sparus aurata). J. Fish Biol. 46: 494–500.CrossRefGoogle Scholar
  24. Mancera, J.M., Laiz-Carrión, R. and Martín del Río, M.P. 2002. Osmoregulatory action of PRL, GH and cortisol in the gilthead seabream (Sparus aurata L.). Gen. Comp. Endocrinol. 129: 95–103.CrossRefGoogle Scholar
  25. Mancera, J.M., Pérez-Fígares, J.M. and Fernández-Llebrez, P. 1993a. Osmoregulatory responses to abrupt salinity changes in the euryhaline gilthead sea bream (Sparus aurata). Comp. Biochem. Physiol. 106A: 245–250.CrossRefGoogle Scholar
  26. Mancera, J.M., Pérez-Fígares, J.M. and Fernández-Llebrez, P. 1994. Effect of cortisol on brackish water adaptation in the euryhaline gilthead sea bream (Sparus aurata L.). Comp. Biochem. Physiol. 107A: 397–402.CrossRefGoogle Scholar
  27. Mancera, J.M., Fernández-Llebrez, P., Grondona, J.M. and Pérez-Fígares, J.M. 1993b. Influence of environmental salinity on prolactin and corticotropic cells in the euryhaline gilthead sea bream (Sparus aurata L.). Gen. Comp. Endocrinol. 90: 220–231.PubMedCrossRefGoogle Scholar
  28. McCormick, S.D. 1990. Cortisol directly stimulates differentiation of chloride cells in tilapia opercular membrane. Am. J. Physiol. 259: R857–863.PubMedGoogle Scholar
  29. McCormick, S.D. 1995. Hormonal control of gill Na+,K+-ATPase and chloride cell function. In: Fish Physiology, Vol. 14. pp. 285–315, Edited by C.M. Wood and T.J. Shuttlewoth. Academic Press, San Diego.Google Scholar
  30. McCormick, S.D. 2001. Endocrine control of osmoregulation in fish. Am. Zool. 41: 781–794.CrossRefGoogle Scholar
  31. Mommsen, T.P. 1984. Metabolism of the fish gill. In: Fish Physiology, Vol. XB. pp. 203–238. Edited by W.S. Hoar and D.J. Randall DJ. Academic Press, New York.Google Scholar
  32. Mommsen, T.P, Vijayan, M.M. and Moon, T.W. 1999. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev. Fish Biol. Fish. 9: 211–268.CrossRefGoogle Scholar
  33. Morgan, J.D. and Iwama, G.K. 1996. Cortisol induced changes in oxygen consumption and ionic regulation in coastral cutthroat trout parr. Fish Physiol. Biochem. 15: 385–394.CrossRefGoogle Scholar
  34. Morgan, J.D., Sakamoto, T., Grau, E.G. and Iwama, G.K. 1997. Physiological and respiratory responses of the Mozambique tilapia (Oreochromis mossambicus) to salinity acclimation. Comp. Biochem. Physiol. 117A: 391–398.CrossRefGoogle Scholar
  35. Perry, S.F. and Walsh, P.J. 1989. Metabolism of isolated fish gill cells: contribution of epithelial chloride cells. J. Exp. Biol. 144: 507–520.PubMedGoogle Scholar
  36. Pottinger, T.G., Carrick, T.R., Appleby, A. and Yeomans, W.E. 2000. High blood cortisol levels and low cortisol receptor affinity: is the chub, Leuciscus cephalus, a cortisol-resistant teleost? Gen. Comp. Endocrinol. 120: 108–117.CrossRefGoogle Scholar
  37. Ruibal, C., Soengas, J.L. and Aldegunde, M. 2002. Brain serotonin and the control of food intake in rainbow trout (Oncorhynchus mykiss): Effects of changes in plasma glucose levels. J. Comp. Physiol. A. 188: 479–484.CrossRefGoogle Scholar
  38. Sangiao-Alvarellos, S., Lapido, M., Míguez, J.M. and Soengas, J.L. 2004. Effects of central administration of arginine vasotocin on monoaminergic and energy metabolism of rainbow trout brain. J. Fish. Biol. In press.Google Scholar
  39. Sangiao-Alvarellos, S., Bouça, P., Miguez, J.M. and Soengas, J.L. 2003a. Intracerebroventricular injections of noradrenaline affect brain energy metabolism of rainbow trout, Oncorhynchus mykiss. Physiol. Biochem. Zool. 76: 663–671.PubMedCrossRefGoogle Scholar
  40. Sangiao-Alvarellos, S., Laiz-Carrión, R., Guzmán, J.M., Martín del Río, M.P., Miguez, J.M., Mancera, J.M. and Soengas, J.L 2003b. Aclimation of S. aurata to various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs. Am. J. Physiol. 285: R897–R907.Google Scholar
  41. Seidelin, M. and Madsen, S.S. 1997. Prolactin antagonizes the seawater-adaptative effect of cortisol and growth hormone in anadromous brown trout (Salmo trutta). Zool. Sci. 14: 249–256.CrossRefGoogle Scholar
  42. Smith, O.K., Krohon, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J. and Klenk, D.C. 1985. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150: 76–85.PubMedCrossRefGoogle Scholar
  43. Soengas, J.L. and Aldegunde, M. 2002. Energy metabolism of fish brain. Comp. Biochem. Physiol. 131B: 271–296.Google Scholar
  44. Soengas, J.L., Strong, E.F. and Andrés, M.D. 1998a. Glucose, lactate, and β-hydroxybutyrate utilization by rainbow trout brain: changes during food deprivation. Physiol. Zool. 71: 285–293.PubMedGoogle Scholar
  45. Soengas, J.L., Strong, E.F., Aldegunde, M. and Andrés, M.D. 1997. Effects of the acute exposure to lindane (γ-hexachlorocyclohexane) on brain and liver carbohydrate metabolism of rainbow trout. Ecotox. Environ. Saf. 38: 99–107.CrossRefGoogle Scholar
  46. Soengas, J.L., Strong, E.F., Andrés, M.D. and Aldegunde, M. 1998b. Dose-dependent effects of acute melatonin treatments on brain carbohydrate metabolim of rainbow trout. Fish Physiol. Biochem. 18: 311–319.CrossRefGoogle Scholar
  47. Soengas, J.L., Strong, E.F., Fuentes, J., Aldegunde, M. and Andrés, M.D. 1996a. Post-feeding carbohydrate and ketone bodies metabolism in brain and liver of Atlantic salmon. J. Physiol. Biochem. 52: 131–142.Google Scholar
  48. Soengas, J.L., Barciela, P., Aldegunde, M. and Andrés, M.D. 1995. Gill carbohydrate metabolism of rainbow trout is modified during gradual adaptation to sea water. J. Fish Biol. 46: 845–856.CrossRefGoogle Scholar
  49. Soengas, J.L., Rey, P., Rozas, G., Andrés, M.D. and Aldegunde, M. 1992. Effects of cortisol and thyoid hormone treatment on the glycogen metabolism of selected tissues of domesticated rainbow trout, Oncorhynchus mykiss. Aquaculture 101: 317–328.CrossRefGoogle Scholar
  50. Soengas, J.L., Strong, E.F., Fuentes, J., Veira, J.A.R. and Andrés, M.D. 1996b. Food deprivation and refeeding in Atlantic salmon, Salmo salar: effects on brain and liver carbohydrate and ketone bodies metabolism. Fish Physiol. Biochem. 15: 491–511.CrossRefGoogle Scholar
  51. Van der Boon, J., Van den Thillart, G.E.E.J.M. and Addink, A.D.F. 1991. The effects of cortisol administration on intermediaty metabolism in teleost fish. Comp. Biochem. Physiol. 100A: 47–53.CrossRefGoogle Scholar
  52. Vijayan, M.M., Ballantyne, J.S. and Leatherland, J.F. 1991. Cortisol-induced changes in some aspects of the intermediary metabolism of Salvelinus fontinalis. Gen. Comp. Endocrinol. 82: 476–486.PubMedCrossRefGoogle Scholar
  53. Vijayan, M,M., Morgan, J.D., Sakamoto, T., Grau, E.G. and Iwama, G.K. 1996. Food-deprivation affects seawater acclimation in tilapia: hormonal and metabolic changes. J. Exp. Biol. 199: 2467–2475.PubMedGoogle Scholar
  54. Wendelaar Bonga, S.E. 1997. The stress response in fish. Physiol. Rev. 7: 591–625.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Raúl Laiz-Carrión
    • 1
  • Susana Sangiao-Alvarellos
    • 2
  • José M. Guzmán
    • 1
  • María P. Martín del Río
    • 1
  • Jesús M. Míguez
    • 2
  • José L. Soengas
    • 2
  • Juan M. Mancera
    • 1
  1. 1.Departamento de Biología, Facultad de Ciencias del Mar y AmbientalesUniversidad de CádizPuerto Real, CádizSpain
  2. 2.Laboratorio de Fisioloxía Animal, Facultade de CienciasUniversidade de VigoVigoSpain

Personalised recommendations