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Food deprivation and refeeding in Atlantic salmon,Salmo salar: effects on brain and liver carbohydrate and ketone bodies metabolism

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Abstract

The capacity of carbohydrate and ketone bodies metabolism in brain and liver was evaluated in fed and food-deprived Atlantic salmon (Salmo salar) in a time period covering from 1 to 7 days (Experiment I), and in Atlantic salmon food deprived for 6 weeks, and food deprived for 4 weeks and refed for 2 weeks (Experiment II). The results obtained demonstrate for the first time in a teleost the existence of changes in brain metabolism due to food deprivation. Thus, decreased glucose levels in plasma are reflected in the brain by an increased mobilization of glycogen reserves, and by a decreased glycolytic capacity. Also, ketone bodies appear to increase their importance as a metabolic fuel from day 7 of food deprivation onwards. A possible increase in the gluconeogenic potential in brain simultaneously is not discarded. All these metabolic changes are reversed under refeeding conditions.

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References cited

  • Black, D. and Love, M. 1986. The sequential mobilisation and restoration of energy reserves in tissues of Atlantic cod during starvation and refeeding. J. Comp. Physiol. B. 156: 469–479.

    Google Scholar 

  • Blasco, J., Fernández, J. and Gutiérrez, J. 1992. Fasting and refeeding in carp,Cyprinus carpio L.: the mobilization of reserves and plasma metabolite and hormone variations. J. Comp. Physiol. B. 162: 539–546.

    Google Scholar 

  • Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.

    PubMed  Google Scholar 

  • Brunk, C.F., Jones, K.C. and James, T.W. 1979. Assay for nanogram quantities of DNA in cellular homogenates. Anal. Biochem. 92: 497–500.

    PubMed  Google Scholar 

  • Carrillo, M., Zanuy, S. and Herrera, E. 1982. Growth and diurnal variations in metabolic parameters in the starved bass,Dicentrarchus labrax, after experimental feeding. Comp. Biochem. Physiol. 72A: 11–16.

    Google Scholar 

  • Clarke, D.D., Lajtha, A.L. and Maker, H.S. 1989. Intermediary metabolism.In Basic Neurochemistry: Molecular, Cellular, and Medical Aspects. pp. 541–564. Edited by S.G. Siegel. Raven Press, New York.

    Google Scholar 

  • deRoos, R. 1994. Plasma ketone, glucose, lactate, and alanine levels in the vascular supply to and from brain of the spiny dogfish shark (Squalus acanthias). J. Exp. Zool. 268: 354–363.

    Google Scholar 

  • Farbridge, K.J. and Leatherland, J.F. 1992. Temporal changes in plasma thyroid hormone, growth hormone and free fatty acid concentrations, and hepatic 5′-monodeiodinase activity, lipid and protein content during chronic fasting and re-feeding in rainbow trout (Oncorhynchus mykiss). Fish Physiol. Biochem. 10: 245–257.

    Google Scholar 

  • Fideu, M.D., Soler, G. and Ruiz-Amil, M. 1983. Nutritional regulation of glycolysis in rainbow trout (Salmo gairdneri R. J. Comp. Biochem. Physiol. 74B: 795–799.

    Google Scholar 

  • Foster, G.D. and Moon, T.W. 1991. Hypometabolism with fasting in the yellow perch (Perca flavescens): a study of enzymes, hepatocyte metabolism, and tissue size. Physiol. Zool. 64: 259–275.

    Google Scholar 

  • Foster, G.D., Youson, J.H. and Moon, T.W. 1993. Carbohydrate metabolism in the brain of the adult lamprecy. J. Exp. Zool. 267: 27–32.

    Google Scholar 

  • Gutmann, I. and Wahlefeld, A.W. 1974. L-(+)-Lactate. Determination with lactate dehydrogenase and NAD.In Methods of Enzymatic Analysis. pp. 1464–1472. Edited by H.U. Bergmeyer. Academic Press, New York.

    Google Scholar 

  • Gutiérrez, J., Pérez, J., Navarro, I., Zanuy, S. and Carrillo, M. 1991. Changes in plasma glucagon and insulin associated with fasting in sea bass (Dicentrarchus labrax). Fish Physiol. Biochem. 9: 107–112.

    Google Scholar 

  • Hansen, H.J.M. and Abraham, S. 1989. Compartmentation of gluconeogenesis in the fasted eel (Anguilla anguilla). Comp. Biochem. Physiol. 92B: 697–703.

    Google Scholar 

  • Harmon, J.S. and Sheridan, M.A. 1992. Previous nutritional state and glucose modulate glucagon-mediated hepatic lipolysis in rainbow trout,Oncorhynchus mykiss. Zool. Sci. 9: 275–281.

    Google Scholar 

  • Heath, A.G. 1988. Anaerobic and aerobic energy metabolism in brain and liver tissue from rainbow trout (Salmo gairdneri) and bullhead catfish (Ictalurus nebulosus). J. Exp. Zool. 248: 140–146.

    Google Scholar 

  • Hemre, G.I., Lie, O. and Sundby, A. 1993. Dietary carbohydrate utilization in cod (Gadus morhua): metabolic responses to feeding and fasting. Fish Physiol. Biochem. 10: 455–463.

    Google Scholar 

  • Hemre, G.I., Lie, O., Lambertsen, G. and Sundby, A. 1990. Dietary carbohydrate utilization in cod (Gadus morhua). Hormonal response of insulin, glucagon and glucagon-like peptide to diet and starvation. Comp. Biochem. Physiol. 97A: 41–44.

    Google Scholar 

  • Holloway, A.C., Reddy, P.K., Sheridan, M.A. and Leatherland, J.F. 1994. Diurnal rhythms of plasma growth hormone, somatostatin, thyroid hormones, cortisol and glucose concentrations in rainbow trout,Oncorhynchus mykiss, during progressive food deprivation. Biol. Rhythm Res. 25: 415–432.

    Google Scholar 

  • Keppler, D. and Decker, K. 1974. Glycogen. Determination with amyloglucosidase.In Methods of Enzymatic Analysis. pp. 1127–1131. Edited by H.U. Bergmeyer. Academic Press, New York.

    Google Scholar 

  • Leatherland, J.F. and Farbridge, K.J. 1992. Chronic fasting reduces the response of the thyroid to growth hormone and TSH, and alters the growth hormone-related changes in hepatic 5′-monodeiodinase activity in rainbow trout,Oncorhynchus mykiss. Gen. Comp. Endocrinol. 87: 342–353.

    PubMed  Google Scholar 

  • Lim, A.L.L. and Ip, Y.K. 1989. Effect of fasting on glycogen metabolism and activities of glycolytic and gluconeogenic enzymes in the mudskipper,Baleophtalmus boddaerti. J. Fish Biol. 34: 349–367.

    Google Scholar 

  • Mellanby, J. and Williamson, D.H. 1974. Acetoacetate.In Methods of Enzymatic Analysis. pp. 1841–1843. Edited by H.U. Bergmeyer. Academic Press, New York.

    Google Scholar 

  • Mendez, G. and Wieser, W. 1993. Metabolic responses to food deprivation and refeeding in juveniles ofRutilus rutilus (Teleostei: Cyprinidae). Env. Biol. Fish. 36: 73–81.

    Google Scholar 

  • Mommsen, T.P. and Plisetskaya, E.M. 1991. Insulin in fishes and agnathans: history, structure and metabolic regulation. Rev. Aquat. Sci. 4: 225–259.

    Google Scholar 

  • Mommsen, T.P., French, C.J. and Hochachka, P.W. 1980. Sites and patterns of protein and amino acid utilization during the spawning migration of salmon. Can. J. Zool. 58: 1785–1799.

    Google Scholar 

  • Moon, T.W. 1983. Metabolic reserves and enzyme activities with food deprivation in immature American cels,Anguilla rostrata (LeSucur). Can. J. Zool. 61: 802–811.

    Google Scholar 

  • Moon, T.W. and Mommsen, T.P. 1987. Enzymes of intermediary metabolism in tissues of the little skate,Raja erinacea. J. Exp. Zool. 244: 9–15.

    Google Scholar 

  • Moon, T.W., Foster, G.D. and Plisetskaya, E.M. 1989. Changes in peptide hormones and liver enzymes in the rainbow trout deprived of food for 6 weeks. Can. J. Zool. 67: 2189–2193.

    Google Scholar 

  • Morata, P., Vargas, A.M., Sánchez-Medina, F., Garcia, M., Cardenete, G. and Zamora, S. 1982. Evolution of gluconeogenic enzyme activities during starvation in liver and kidney of the rainbow trout (Salmo gairdneri). Comp. Biochem. Physiol. 71B: 65–70.

    Google Scholar 

  • Navarro, I., Gutiérrez, J. and Planas, J. 1992. Changes in plasma glucagon, insulin and tissue metabolites associated with prolonged fasting in brown trout (Salmo trutta fario) during two different seasons of the year. Comp. Biochem. Physiol. 102A: 401–407.

    Google Scholar 

  • Passonneau, J.V. and Rottenberg, D.A. 1973. An assessment of methods for measurement of glycogen synthetase activity including a new one-step assay. Anal. Biochem. 51: 528–541.

    PubMed  Google Scholar 

  • Pereira, C., Vijayan, M.M. and Moon, T.W. 1995.In vitro hepatocyte metabolism of alanine and glucose and the reponse to insulin in fed and fasted rainbow trout. J. Exp. Zool. 271: 425–431.

    Google Scholar 

  • Sheridan, M.A. and Mommsen, T.P. 1991. Effects of nutritional state on in vivo lipid and carbohydrate metabolism of coho salmon,Oncorhynchus kisutch. Gen. Comp. Endocrinol. 81: 473–483.

    PubMed  Google Scholar 

  • Shimeno, S., Kheyyali, D. and Takeda, M. 1990. Metabolic adaptation to prolonged starvation in carp. Nippon. Suisan. Gakkaishi. 56: 35–41.

    Google Scholar 

  • Su, J.Y. and Storey, K.B. 1993. Phosphofructokinase from liver of the rainbow trout,Oncorhynchus mykiss. Arch. Biochem. Biophys. 302: 49–55.

    PubMed  Google Scholar 

  • Sumpter, J.P., LeBail, P.Y., Pickering, A.D., Pottinger, T.G. and Carragher, J.F. 1991. The effect of starvation on growth and plasma growth hormone concentrations of rainbow trout,Oncorhynchus mykiss. Gen. Comp. Endocrinol. 83: 94–102.

    PubMed  Google Scholar 

  • Sundby, A., Eliassen, K., Blom, A.K. and Asgard, T. 1991. Plasma insulin, glucagon, glucagon-like peptide and glucose levels in response to feeding, starvation and life long restricted feed ration in salmonids. Fish Physiol. Biochem. 9: 253–259.

    Google Scholar 

  • Tranulis, M.A., Christophersen, B., Blom, A.K. and Borreback, B. 1991. Glucose dehydrogenase, glucose-6-phosphate dehydrogenase and hexokinase in liver of rainbow trout (Salmo gairdneri) effects of starvation and temperature variations. Comp. Biochem. Physiol. 99B: 687–691.

    Google Scholar 

  • Vijayan, M.M. and Moon, T.W. 1992. Acute handling stress alters hepatic glycogen metabolism in food-deprived rainbow trout (Oncorhynchus mykiss). Can. J. Fish. Aquat. Sci. 49: 2260–2266.

    Google Scholar 

  • Vijayan, M.M., Maule, A.G., Schreck, C.B. and Moon, T.W. 1993. Hormonal control of hepatic glycogen metabolism in food-deprived, continuously swimming coho salmon (Oncorhynchus kisutch). Can. J. Fish. Aquat. Sci. 50: 1676–1682.

    Google Scholar 

  • Williamson, D.H. and Mellanby, J. 1974. D-(−)-3-Hydroxybutyrate.In Methods of Enzymatic Analysis. pp. 1836–1839. Edited by H.U. Bergmeyer. Academic Press, New York.

    Google Scholar 

  • Yang, T.H. and Somero, G.N. 1993. Effects of feeding and food deprivation on oxygen consumption, muscle protein concentration and activities of energy metabolism enzymes in muscle and brain of shallo-living (Scorpaena guttata) and deep-living (Sebastolobus alascanus) scorpaenid fishes. J. Exp. Biol. 181: 213–232.

    Google Scholar 

  • Zammit, V.A. and Newsholme, E.A. 1979. Activities of fat and ketone-body metabolism and effects of starvation on blood concentrations of glucose and fat fuels in teleost and clasmobranch fish. Biochem. J. 184: 313–322.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Area de Fisioloxia Animal, Facultade de Ciencias, Universidade de Vigo, Vigo, Spain

    J. L. Soengas

  2. Laboratorio de Fisioloxia Animal-Departamento de Fisioloxia, Facultade de Bioloxia, Universidade de Santiago de Compostela, 15706, Santiago de Compostela, Spain

    E. F. Strong, J. Fuentes &  M. D. Andrés

  3. Departamento de Fisioloxia, Facultade de Veterinaria, Universidade de Santiago de Compostela, Spain

    J. A. R. Veira

  4. Biological Sciences, University of Dundee, DD1 4HN, Dundee, Scotland, U.K.

    J. Fuentes

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  1. J. L. Soengas
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  2. E. F. Strong
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  3. J. Fuentes
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  4. J. A. R. Veira
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  5. M. D. Andrés
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Correspondence to M. D. Andrés.

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Soengas, J.L., Strong, E.F., Fuentes, J. et al. 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 (1996). https://doi.org/10.1007/BF01874923

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