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The role of glycogen phosphorylase in the regulation of glycogenolysis by insulin and glucagon in isolated eel (Anguilla rostrata) hepatocytes

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Abstract

The effects of porcine, scombroid, and salmon insulins, and bovine and anglerfish glucagons on glycogen depletion and glycogen phosphorylase (GPase) activities were examined in freshly isolated American eel (Anguilla rostrata) hepatocytes. Eel liver GPase in crude homogenates was activated (increase in % GPase a) by phosphorylating conditions and was rapidly inactivated (less than 1 h) when a phosphatase inhibitor (fluoride) was absent. Caffeine inhibits, and AMP activates, the b form of GPase consistent with their effects on rat liver GPase. Both mammalian and fish glucagons increased glucose production in eel hepatocytes, but had more ambiguous effects on glycogen levels and GPase activities. The magnitude of bovine glucagon effects were dependent on the initial glycogen content of the cells; only at glycogen concentrations less than approximately 70 μmoles.g−1 did glucagon significantly increase % GPase a. Anglerfish glucagon significantly increased cyclic AMP (cAMP) concentrations by 90% at 10−7 M, but had no effects at 10−9 M and 10−8 M. Scombroid and salmon insulins maintained hepatocyte glycogen concentrations and decreased glucose production, with these effects more pronounced at low (10−9 to 10−8 M) rather than high (10−7 M) hormone concentrations. Porcine and salmon insulins decreased total GPase and % GPase a activities, and salmon insulin decreased CAMP levels, but only at 10−8 M (by 44%).

Glycogen is, therefore, depleted by glucagon and maintained by insulin in freshly isolated American eel hepatocytes, and these changes are accomplished, at least in part, by changes in the activities of GPase. Changes in cAMP do not explain all of the observed hormone effects.

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References cited

  • Andrews, P.C., Hawke, D.H., Lee, T.D., Legasse, K., Noe, B.D. and Shively, J.E. 1986. Isolation and structure of the principal products of preglucagon processing including an amidated glucagon-like peptide. J. Biol. Chem. 261: 8125–8133.

    Google Scholar 

  • Birnbaum, M.J., Schultz, J. and Fain, T.N. 1976. Hormone-stimulated glycogenolysis in isolated goldfish hepatocytes. Am. J. Physiol. 231: 191–197.

    PubMed  CAS  Google Scholar 

  • Chan, D.K.O. and Woo, N.Y.S. 1978. Effects of glucagon on the metabolism of the Japanese eel. Gen. Comp. Endocrinol. 35: 216–225.

    Article  PubMed  CAS  Google Scholar 

  • Conlon, J.M., Dacon, C.F., Hazon, N., Henserson, I.W. and Thim, L. 1988. Somatostatin-related and glucagon-related peptides with unusual structural features from the European eel (Anguilla anguilla). Gen. Comp. Endocrinol. 72: 181–189.

    Article  PubMed  CAS  Google Scholar 

  • Demaël-Suard, A. et Garin, D. 1970. L'interaction entre l'adrenaline et l'insuline dans la regulation du metabolisme glucidique de la tanche. C.R. Soc. Biol. 164: 1505–1509.

    Google Scholar 

  • Foster, G.D. and Moon, T.W. 1986. Cortisol and liver metabolism of immature American eels, Anguilla rostrata (LeSueur). Fish Physiol. Biochem. 1: 113–124.

    Article  CAS  Google Scholar 

  • Foster, G.D. and Moon, T.W. 1987. Metabolism in sea raven (Hemitripterus americanus) hepatocytes: the effects of insulin and glucagon. Gen. Comp. Endocrinol. 66: 102–115.

    Article  PubMed  CAS  Google Scholar 

  • Foster, G.D. and Moon, T.W. 1989. Insulin and the regulation of glycogen metabolism and gluconeogenesis in American eel (Anguilla rostrata) hepatocytes. Gen. Comp. Endocrinol. 73: 374–381.

    Article  PubMed  CAS  Google Scholar 

  • Foster, G.D., Storey, K.B. and Moon, T.W. 1989. The regulation of 6-phosphofructo-1-kinase by insulin and glucagon in isolated hepatocytes of the American eel (Anguilla rostrata). Gen. Comp. Endocrinol. 73: 382–389.

    Article  PubMed  CAS  Google Scholar 

  • Freig, W.E., Nother-Freig, G., Steudter, S., Enderle, D. and Ditschuneit, H. 1985. Regulation of insulin binding and glycogenesis by insulin and dexamethasone in cultured rat hepatocytes. Biochim. Biophys. Acta 847: 325–331.

    Google Scholar 

  • Goldfine, I.D. 1987. The insulin receptor: molecular biology and transmembrane signalling. Endocr. Res. 8: 235–255.

    CAS  Google Scholar 

  • Hayashi, S. and Ooshiro, Z. 1985. Effects of glucagon, insulin, and the eel serum in the eel liver cells in primary culture. Bull. Jap. Soc. Sci. Fish. 51: 1123–1127.

    CAS  Google Scholar 

  • Hems, D.A. and Whitton, P.D. 1980. Control of hepatic glycogenolysis. Physiol. Rev. 60: 1–50.

    PubMed  CAS  Google Scholar 

  • Hers, H.G. 1976. The control of glycogen metabolism in the liver. Am. Rev. Biochem. 45: 167–189.

    Article  CAS  Google Scholar 

  • Katz, J., Golden, S. and Wals, P.A. 1979. Glycogen synthesis by rat hepatocytes. Biochem. J. 180: 389–402.

    PubMed  CAS  Google Scholar 

  • Mommsen, T.P. 1986. Comparative gluconeogenesis in hepatocytes from salmonid fishes. Can. J. Zool. 64: 1110–1115.

    Article  CAS  Google Scholar 

  • Mommsen, T.P. and Moon, T.W. 1989. Metabolic action of glucagon-family hormones in liver. Fish Physiol. Biochem. 7: 279–288.

    CAS  Google Scholar 

  • Mommsen, T.P., Andrews, P.C. and Plisetskaya, E.M. 1987. Glucagon-like peptides activate hepatic gluconeogenesis. FEBS Lett. 219: 227–232.

    Article  PubMed  CAS  Google Scholar 

  • Morata, P., Vargas, A.M., Pita, M.L. and Sanchez-Medina, F. 1982. Involvement of gluconeogenesis in the hyperglycemia induced by glucagon, adrenaline, and cyclic AMP in rainbow trout (Salmo gairdneri). Comp. Biochem. Physiol. 73A: 379–381.

    Article  Google Scholar 

  • Murat, J.C. 1976. Studies on glycogenolysis in carp liver: evidence for an amylase pathway for glycogen breakdown. Comp. Biochem. Physiol. 55B: 461–465.

    Article  CAS  Google Scholar 

  • Ottolenghi, C., Puviani, A.C., Baruffaldi, A. and Brighenti, L. 1984. Effect of insulin on glycogen metabolism in isolated catfish hepatocytes. Comp. Biochem. Physiol. 78A: 705–710.

    Article  CAS  Google Scholar 

  • Ottolenghi, C., Puviani, A.C., Gavioli, M.E. and Brighenti, L. 1986. Epinephrine effect on glycogen phosphorylase activity in catfish liver and muscles. Gen. Comp. Endocrinol. 61: 469–475.

    Article  PubMed  CAS  Google Scholar 

  • Ottolenghi, C., Puviani, A.C., Baruffaldi, A., Gavioli, M.E. and Brighenti, L. 1988. Glucagon control of glycogenolysis in catfish tissues. Comp. Biochem. Physiol. 90B: 285–290.

    CAS  Google Scholar 

  • Picukans, I. and Umminger, B.L. 1979. Comparative activities of glycogen phosphorylase and τ-amylase in livers of carp (Cyprinus carpio) and goldfish (Carassius auratus). Comp. Biochem. Physiol. 62B: 455–457.

    Article  CAS  Google Scholar 

  • Plisetskaya, E.M., Bhattucharya, S., Dickoff, W.W. and Gorbman, A. 1984. The effect of insulin on amino acid metabolism and glycogen content in isolated liver cells of juvenile coho salmon Oncorhynchus kisutsch. Comp. Biochem. Physiol. 78A: 773–778.

    Article  CAS  Google Scholar 

  • Plisetskaya, E.M., Ottolenghi, C., Sheridan, M.A. Jr., Mommsen, T.P. and Gorbman, A. 1989. Metabolic effects of salmon glucagon and glucagon-like peptide in Coho and Chinook salmon. Gen. Comp. Endocrinol. 73: 205–216.

    Article  PubMed  CAS  Google Scholar 

  • Renaud, J.M. and Moon, T.W. 1980. Characterization of gluconeogenesis in hepatocytes isolated from the American eel Anguilla rostrata (LeSueur). J. Comp. Physiol. 135: 115–125.

    CAS  Google Scholar 

  • Schwartz, A.L. and Rall, T.W. 1975. Hormonal regulation of incorporation of U-14C-alanine into glucose in human fetal liver explants. Effect of dibutyryl cAMP, glucagon, insulin, and triamcinolone. Diabetes 24: 650–657.

    PubMed  CAS  Google Scholar 

  • Stalman, W. and Hers, H.G. 1975. The stimulation of liver phosphorylase b by AMP, fluoride, and sulphate. A technical note on the specific determination of the a and b forms of liver glycogen phosphorylase. Eur. J. Biochem. 54: 341–350.

    Article  Google Scholar 

  • Storey, K.B. 1988. Tissue-specific controls on carbohydrate catabolism during anoxia in goldfish. Physiol. Zool. 60: 601–607.

    Google Scholar 

  • Umminger, B.L. and Benzinger, D. 1975. In vitro stimulation of hepatic glycogen phosphorylase activity by epinephrine and glucagon in the brown bullhead. Gen. Comp. Endocrinol. 25: 96–104.

    Article  PubMed  CAS  Google Scholar 

  • Umminger, B.L., Benziger, D. and Levy, S. 1975. In vitro stimulation of hepatic glycogen phosphorylase activity by epinephrine and glucagon in the killifish Fundulus heteroclitus. Comp. Biochem. Physiol. 51C: 111–115.

    CAS  Google Scholar 

  • Vernier, J.M. and Sire, M.F. 1978. In vitro study of hepatic glycogen phosphorylase in rainbow trout: its control by glucose, corticoids, adrenaline, and glucagon. Gen. Comp. Endocrinol. 34: 360–369.

    Article  PubMed  CAS  Google Scholar 

  • Wakelam, J.O., Murphy, G.J. Hruby, V.J. and Houslay, M.D. 1986. Activation of two signal transduction systems in hepatocytes by glucagon. Nature, Lond. 323: 68–71.

    Article  CAS  Google Scholar 

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  1. Department of Biology, University of Ottawa, Ottawa, Ontario, K1N 6N5, Canada

    Glen D. Foster & T. W. Moon

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  1. Glen D. Foster
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  2. T. W. Moon
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Foster, G.D., Moon, T.W. The role of glycogen phosphorylase in the regulation of glycogenolysis by insulin and glucagon in isolated eel (Anguilla rostrata) hepatocytes. Fish Physiol Biochem 8, 299–309 (1990). https://doi.org/10.1007/BF00003425

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