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Physiology of fish endocrine pancreas

Fish Physiology and Biochemistry volume 7, Article number: 39 (1989) Cite this article

Abstract

From the very beginning of physiological studies on the endocine pancreas, fish have been used as experimental subjects. Fish insulin was one of the first vertebrate insulins isolated and one of the first insulins whose primary and then tertiary structures were reported. Before a second pancreatic hormone, glucagon, was characterized, a physiologically active ‘impurity’, similar to that in mammalian insulin preparations, was found in fish insulins.

Fish have become the most widely used model for studies of biosynthesis and processing of the pancreatic hormones. It seems inconceivable, therefore, that until the recent past cod and tuna insulins have been the only purified piscine islet hormones available for physiological experiments. The situation has changed remarkably during the last decade.

In this review the contemporary status of physiological studies on the fish pancreas is outlined with an emphasis on the following topics: 1) contents of pancreatic peptides in plasma and in islet tissue; 2) actions of piscine pancreatic hormones in fish; 3) specific metabolic consequences of an acute insufficiency of pancreatic peptides; 4) functional interrelations among pancreatic peptides which differ from those of mammals. The pitfalls, lacunae and the perspectives of contemporary physiological studies on fish endocrine pancreas are outlined.

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References cited

  • Ablett, R.F., Taylor, M.J. and Selivonchick, D.P. 1985. The effect of high protein and high-carbohydrate diets on (I-125) iodoinsulin binding in skeletal muscle membranes and isolated hepatocytes of rainbow trout (Salmo gairdneri). Br. J. Nutr. 50: 129–140.

    Article  Google Scholar 

  • Ahrén, B., Rorsman, P. and Berggren, P.-O. 1988. Galanin and the endocrine pancreas. FEBS Letters 229: 233–237.

    PubMed  Article  Google Scholar 

  • Andrews, P.C., Hawke, D., Shively, J.E. and Dixon, J.E. 1984a. Anglerfish prosomatostatin II is processed to somatostatin-28 and contains hydroxylysine as residue 23. J. Biol. Chem. 259: 15021–15024.

    PubMed  CAS  Google Scholar 

  • Andrews, P.C., Pollock, H.G., Elliott, W.M., Youson, J.H. and Plisetskaya, E.M. 1988. Isolation and characterization of a variant somatostatin-14 and two related somatostatins of 34- and 37-residues from lamprey (Petromyzon marinus). J. Biol. Chem. 263: 15809–15814.

    PubMed  CAS  Google Scholar 

  • Andrews, P.C., Pubols, M.N., Hermodson, M.A., Sheares, B.T. and Dixon, J.E. 1984b. Structure of 22-residue somatostatin from catfish. An O-glycosylated peptide having multiple forms. J. Biol. Chem. 259: 13267–13272.

    PubMed  CAS  Google Scholar 

  • Audy, G. and Kerly, M. 1952. The content of glycogenolytic factor in pancreas from different species. Biochem. J. 52: 77–78.

    PubMed  CAS  Google Scholar 

  • Bauer, G.E., Lindall, A.W. and Lazarow, A. 1965. The biosynthesis of14C and3H labeled insulin. Adv. Tracer Met. 2: 73–81.

    CAS  Google Scholar 

  • Cherel, Y., Robin, J.-P. and Le Maho, Y. 1988. Physiology and biochemistry of the long-term fasting in birds. Can. J. Zool. 66: 159–166.

    CAS  Article  Google Scholar 

  • Clark, J.T., Kalra, P.S. and Kalra, S.P. 1985. Neuropeptide Y stimulates feeding but inhibits sexual behavior in rats. Endocrinology 117: 2435–2442.

    PubMed  CAS  Google Scholar 

  • Conlon, J.M. 1989. Biosynthesis of regulatory peptides: evolutionary aspects.In Comparative Physiology of Regulatory Peptides. Edited by S. Holmgren. Groom Helm, Beckenham. (In press).

  • Cutfield, J.F., Cutfield, S.M., Dodson, E.J., Dodson, G.G., Emdin, S.O. and Reynolds, S.D. 1979. Structure and biological activity of hagfish insulin. J. Mol. Biol. 132: 85–100.

    PubMed  CAS  Article  Google Scholar 

  • Diamare, V. 1906. Weitere Beobachtungen über den Experimentaldiabetes nach Pankreasextirpation bei Selachiern. II Mitt. Zbl. Physiol. 20: 617–620.

    Google Scholar 

  • Diamare, V. 1908. Vergleichende anatomisch-physiologische Studien über den Pankreasdiabetes. III Mitt. Zbl. Physiol. 21: 863–869.

    Google Scholar 

  • Diamare, V. and Kuljabko, A. 1904. Zur Frage nach der physiologischen Bedeutung der Langerhansschen Inseln in Pankreas. Zbl. Physiol. 18: 432–435.

    Google Scholar 

  • Dickhoff, W.W., Yan, L., Plisetskaya, E.M., Sullivan, C.V., Swanson, P., Hara, A. and Bernard, M.G. 1989. Relationship between metabolic and reproductive hormones in salmonid fish. Fish Physiol. Biochem. (In press).

  • Epple, A. and Brinn, J.E. 1987. The Comparative Physiology of the Pancreatic Islets. Zoophysiol. v. 21. Springer-Verlag, Berlin.

    Google Scholar 

  • Goodman, R.H., Jacobs, J.W., Chin, W.W., Lund, P.K., Dee, P.C. and Habener, J.F. 1980. Nucleotide sequence of a cloned structural gene coding for a precursor of pancreatic somatostatin. Proc. Nat. Acad. Sci. USA. 77: 5869–5873.

    PubMed  CAS  Article  Google Scholar 

  • Gutierrez, J., Fernandez, J., Blasco, J., Gesse, J.M. and Planas, J. 1986. Plasma glucagon levels in different species of fish. Gen. Comp. Endocrinol. 63: 328–333.

    PubMed  CAS  Article  Google Scholar 

  • Hilton, J.W., Plisetskaya, E.M. and Leatherland, J.F. 1987. Effect of oral 3,5,3′-triiodo-L-thyronine on dietary glucose utilization and plasma insulin levels in rainbow trout (Salmo gairdneri). Fish Physiol. Biochem. 4: 113–120.

    CAS  Article  Google Scholar 

  • Hobart, P., Crawford, R., Shen, L.-P., Pictet, R. and Rutter, W.J. 1980. Cloning and sequence analysis of cDNAs encoding two distinct somatostatin precursors found in the endocrine pancreas of anglerfish. Nature, Lond. 288: 137–141.

    CAS  Article  Google Scholar 

  • Humbel, R.E., Bosshard, H.R. and Zahn, H. 1972. Chemistry of insulin.In Handbook of Physiology. Sect. 7. Endocrinology. Vol. 1. pp. 111–132. Williams and Wilkins Co., Baltimore.

    Google Scholar 

  • Jensen, H., Wintersteiner, O. and Geiling, E.M.K. 1929. Studies on crystalline insulin; isolation of crystalline insulin from fish islets (cod and pollock) and from pig's pancreas; activity of crystalline insulin and further remarks on its preparation. J. Pharmacol. Exp. Ther. 36: 115–128.

    CAS  Google Scholar 

  • Kimmel, J.R., Plisetskaya, E.M., Pollock, H.G., Hamilton, J.W., Rouse, J.B., Ebner, K.E. and Rawitch, A.B. 1986. Structure of a peptide from coho salmon endocrine pancreas with homology to neuropeptide Y. Biochem. Biophys. Res. Commun. 141: 1084–1091.

    PubMed  CAS  Article  Google Scholar 

  • Leibush, B.N. and Bondareva, V.M. 1987. Insulin receptors in the river lamprey,Lampetra fluviatilis, during pre-spawning natural fasting. Zh. Evol. Biokhim. Fhysiol. 23: 193–198 (in Russian).

    CAS  Google Scholar 

  • Leibush, B.N., Soltitskaya, L.P. and Uchanova, M.B. 1987. The reaction of insulin receptors of the river lamprey (Lampetra fluviatilis) to hyperinsulinemia induced by administration of the hormone. Zh. Evol. Biokhim. Fiziol. 23: 468–472 (in Russian).

    PubMed  CAS  Google Scholar 

  • Lund, P.K., Goodman, R.H. and Habener, J.F. 1981. Pancreatic pre-proglucagons are encoded by two separate mRNAs. J. Biol. Chem. 256: 6515–6518.

    PubMed  CAS  Google Scholar 

  • Macleod, J.J.R. 1922. The source of insulin. A study of the effect produced on blood sugar by extracts of the pancreas and principal islets of fishes. J. Metab. Res. 2: 149–172.

    CAS  Google Scholar 

  • Marchant, T.A. 1987. The hypothalamic regulation of growth hormone secretion in the goldfish (Carassius auratus L.) Ph.D. Thesis. University of Alberta, Edmonton.

  • McCormick, N.A. and Noble, E.C. 1924. The yield of insulin from fish. Contr. Can. Biol. Fish. New ser. 2: 115–120.

    Google Scholar 

  • McDonald, J.K., Greiner, F., Bauer, G.E., Elde, R.P., and Noe, B.D. 1987. Separate cell types that express two different forms of somatostatin in anglerfish islets can be immunohistochemically differentiated. J. Histochem. Cytochem. 35: 155–162.

    PubMed  CAS  Google Scholar 

  • Miahle, P. 1976. The role of glucagon in birds and mammals.In The evolution of pancreatic islets. pp. 291–300. Edited by T.A.I. Grillo, L. Leibson and A. Epple. Pergamon Press, Oxford.

    Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  • Mommsen, T.P. and Moon, T.W. 1989. Metabolic actions of glucagon-family hormones in liver. Fish Physiol. Biochem. (In press).

  • Noe, B.D. and Bauer, G.E. 1971. Evidence for glucagon biosynthesis involving a protein intermediate in islets of the anglerfish (Lophius americanus). Endocrinology 89: 642–651.

    PubMed  CAS  Article  Google Scholar 

  • Noe, B.D., Fletcher, D.J. and Spiess, J. 1979. Evidence for the existence of a biosynthesis precursor for somatostatin. Diabetes 28: 724–730.

    PubMed  CAS  Google Scholar 

  • Nozaki, M., Miyata, K., Oota, Y., Gorbman, A. and Plisetskaya, E.M. 1988a. Differential cellular distributions of two somatostatins in brain and pancreas of salmonids, and their separate associations with insulin and glucagon producing cells. Gen. Comp. Endocrinol. 69: 271–280.

    Article  Google Scholar 

  • Nozaki, M., Miyata, K., Oota, Y., Gorbman, A. and Plisetskaya, E.M. 1988b. Glucagon-like peptide and glucagon immunoreactivities in the same cells in pancreatic islets and intestine of salmonids. Cell Tiss. Res. 253: 371–375.

    CAS  Article  Google Scholar 

  • Ørskov, C. and Holst, J.J. 1987. Radioimmunoassays for glucagon-like peptides 1 and 2 (GLP-1 and GLP-2). Scand. J. Clin. Invest. 47: 165–174.

    PubMed  Article  Google Scholar 

  • Peterson, J.D., Coulter, C.L., Steiner, D.F., Emdin, S.O. and Falkmer, S. 1974. Structural and crystallographic observation on hagfish insulin. Nature, Lond. 254: 239–240.

    Article  Google Scholar 

  • Plisetskaya, E.M. 1975. Hormonal regulation of carbohydrate metabolism in lower vertebrates. Leningrad. Nauka. 215 pp. (in Russian).

    Google Scholar 

  • Plisetskaya, E.M. 1989. Pancreatic petides.In Comparative Physiology of Regulatory Peptides. Edited by S. Holmgren. Groom Helm, Beckenham. (In press).

  • Plisetskaya, E.M., Pollock, H.G., Rouse, J.B., Hamilton, J.W., Kimmel, J.R. and Gorbman, A. 1985. Characterization of coho salmon (Oncorhynchus kisutch) insulin. Reg. Pept. 11: 105–116.

    CAS  Article  Google Scholar 

  • Plisetskaya, E.M., Pollock, H.G., Rouse, J.B., Hamilton, J.W., Kimmel, J.R., Andrews, P.C. and Gorbman, A. 1986a. Characterization of coho salmon (Oncorhynchus kisutch) islet somatostatins. Gen. Comp. Endocrinol. 63: 252–263.

    PubMed  CAS  Article  Google Scholar 

  • Plisetskaya, E.M., Pollock, H.G., Rouse, J.B., Hamilton, J.W., Kimmel, J.R. and Gorbman, A. 1986b. Isolation and structures of coho salmon (Oncorhynchus kisutch) glucagon and glucagon-like peptide. Reg. Pept. 14: 57–67.

    CAS  Article  Google Scholar 

  • Plisetskaya, E.M., Dickhoff, W.W., Paquette, T.L. and Gorbman, A. 1986c. The assay of salmon insulin in homologous radioimmunoassay. Fish Physiol. Biochem. 1: 37–43.

    CAS  Google Scholar 

  • Plisetskaya, E.M., Sundby, A. and Gorbman, A. 1987. Unorthodox interrelations among pancreatic islet hormones in fish. Am. Zool. 27: 97A.

  • Plisetskaya, E.M., Swanson, P., Bernard, M.G. and Dickhoff, W.W. 1988. Insulin in coho salmon (Oncorhynchus kisutch) during the parr to smolt transformation. Aquaculture 72: 151–164.

    CAS  Article  Google Scholar 

  • Plisetskaya, E.M., Ottolenghi, C., Sheridan, M.A., Mommsen, T.P. and Gorbman, A. 1989a. Metabolic effects of salmon glucagon and glucagon-like peptide on coho and chinook salmon. Gen. Comp. Endocrinol. 173: 205–216.

    Article  Google Scholar 

  • Plisetskaya, E.M., Sheridan, M.A. and Mommsen, T.P. 1989b. Metabolic changes in coho and chinook salmon resulting from an acute insufficiency in the pancreatic hormones. J. Exp. Zool. (In press).

  • Plisetskaya, E.M. and Sullivan, C.V. 1989c. Pancreatic and thyroid hormones in rainbow trout (Salmo gairdneri); what concentration does the liver see? Gen. Comp. Endocrinol. (In press).

  • Pollock, H.G., Kimmel, J.R. Ebner, K.E., Hamilton, J.W., Rouse, J.B., Lance, V. and Rawitch, A.B. 1988. Isolation of alligator gar (Lepisosteus spatula) glucagon, oxyntomodulin, and glucagon-like peptide: amino acid sequences of oxyntomodulin and glucagon-like peptide. Gen. Comp. Endocrinol. 69: 133–140.

    PubMed  CAS  Article  Google Scholar 

  • Reid, K.B.M., Grant, P.T. and Youngson, A. 1968. The sequence of amino acids in insulin isolated from islet tissue of the cod (Gadus callarias). Biochem. J. 110: 289–296.

    PubMed  CAS  Google Scholar 

  • Rennie, J. and Fraser, T. 1906. The islets of Langerhans in relation to diabetes. Biochem. J. 2: 7–19.

    Google Scholar 

  • Rusacov, Yu.I., Karasev, V.S., Pertseva, M.N. and Pankov, Yu.A. 1987a. Amino acid sequence of humpback salmon (Oncorhynchus gorbuscha) insulin. Biokhimya 52: 211–217. Plenum Press, English Translation.

    Google Scholar 

  • Rusacov, Yu.I., Karasev, V.S., Pertseva, M.N. and Pankov, Yu.A. 1987b. Amino acid sequence of chum salmon (O. keta) insulin. Zh. evol. Biokhim. Fiziol. 23: 473–480. (in Russian).

    Google Scholar 

  • Sheridan, M.A. and Bern, H.A. 1986. Both somatostatin and the caudal neuropeptide, urotensin II, stimulate lipid metabolism from coho salmon liver incubatedin vitro. Reg. Pept. 14: 333–344.

    CAS  Article  Google Scholar 

  • Sheridan, M.A., Plisetskaya, E.M., Bern, H.A. and Gorbman, A. 1987. Effects of somatostatin-25 and urotensin II on lipid and carbohydrate metabolism of coho salmon,Oncorhynchus kisutch. Gen. Comp. Endocrinol. 66: 405–414.

    PubMed  CAS  Article  Google Scholar 

  • Sitbon, G. 1976. Hormones pancréatiques, glucose plasmatique et mécanismes de leurs régulations dans les conditions physiologiques. Thèse, Université Strasbourg.

  • Sorokin, A.V., Petrenko, O.I., Kavsan, V.M., Kozlov, Yu.I., Debabov, V.G. and Zlochevskij, M.L. 1982. Nucleotide sequence analysis of the cloned salmon preproinsulin cDNA. Gene 20: 367–376.

    PubMed  CAS  Article  Google Scholar 

  • Staub, A., Sin, L.G. and Behrens, O.K. 1953. Purification and crystallization of hyperglycemic-glycogenolytic factor (HGF). Science 117: 628–629.

    PubMed  CAS  Google Scholar 

  • Tan, K., Atabani, G. and Marks, V. 1985. Divergent effect of glucagon antibodies on arginine and glucose-stimulated insulin secretion in the rat. Diabetologia 28: 441–444.

    PubMed  CAS  Article  Google Scholar 

  • Tatemoto, K., Efendic, S., Mutt, V., Makk, G., Feistner, G.J. and Barchas, J.D. 1986. Isolation and structure of pancreastatin, a novel pancreatic peptide that inhibits insulin secretion. Nature, Lond. 324: 476–478.

    CAS  Article  Google Scholar 

  • Unger, R.H. and Lefèbvre, P.J. 1972. Glucagon physiology.In Glucagon, Molecular Physiology, Clinical and Therapeutic Implications. pp. 213–244. Edited by P.J. Lefèbvre and R.H. Unger. Pergamon Press, Oxford-New York.

    Google Scholar 

  • Vincent, S., Dodds, E.C. and Dickens, F. 1925. The pancreas of teleostean fishes and the source of insulin. Quart. J. Exp. Physiol. 15: 313–317.

    CAS  Google Scholar 

  • Wagner, G.F. and McKeown, B.A. 1981. Immunocytochemical localization of hormone-producing cells within the pancreatic islets of the rainbow trout (Salmo gairdneri). Cell Tiss. Res. 221: 181–192.

    CAS  Article  Google Scholar 

  • Yone, Y. 1979. Utilization of carbohydrate by fishes. Proc. 7th Japan-Soviet Joint Symp. Aquaculture. Tokyo. 39–48.

  • Zapf, J., Scheiwiller, E., Guler, H.P. and Froesch, E.R. 1987. Insulin and insulin-like growth factor I: comparative aspects of theirin vivo actions on growth and glucose homeostasis. Endocrinol. Jap. 34, Suppl. 1: 123–129.

    CAS  Google Scholar 

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  1. Department of Zoology NJ-15, University of Washington, Seattle, WA, 98195, USA

    Erika M. Plisetskaya

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Plisetskaya, E.M. Physiology of fish endocrine pancreas. Fish Physiol Biochem 7, 39 (1989). https://doi.org/10.1007/BF00004688

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  • DOI: https://doi.org/10.1007/BF00004688

Keywords

  • insulin
  • glucagon
  • glucagon-like peptide
  • somatostatin
  • pancreatic peptide: structure
  • localization
  • plasma content
  • interrelations
  • metabolic effects