Gastrin/cholecystokinin-related peptides — comparative aspects

  • Ann-Cathrine Jönsson

Abstract

This chapter will focus on the peptides of the gastrin/cholecystokinin (CCK) family, from a comparative point of view. Most of the information available about these peptides regarding sequence, biosynthesis, metabolism and physiological actions is based on studies performed in mammals, and will be used as a basis for the review. During the past few years, interest in the comparative aspects has increased substantially, although most of the work is still at the basic level of identification and scanning, often performed with immunological techniques. The majority of available antisera are raised against mammalian peptides, which could mean that the antisera do not recognize the non-mammalian peptide, or that the antisera recognize a similar sequence of an unrelated peptide. In some studies, antisera specific to gastrin or CCK have been used, but the main body of information is based on observations with antisera raised to the common C-terminus, making it impossible to differentiate between the closely related peptides.

Keywords

Endocrine Cell Immunoreactive Material Gallbladder Contraction Alligator Mississippiensis Spiral Intestine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abad, M.E., Peeze Binkhorst, F.M., Elbal, M.T. and Rombout, J.H.W.M. (1987) A comparative immunocytochemical study of the gastro-entero-pancreatic (GEP) endocrine system in a stomachless and a stomach-containing teleost. Gen. Comp. Endocrinol., 66, 123–36.Google Scholar
  2. Aldman, G. and Holmgren, S. (1987) Control of gallbladder motility in the rainbow trout, Salmo gairdneri. Fish Physiol. Biochem., 4, 143–55.Google Scholar
  3. Aldman, G., Jonsson, A.-C., Jensen, J. and Holmgren, S. (1989) Gastrin/CCK-like peptides in the spiny dogfish, Squalus acanthias: concentration and actions in the gut. Comp. Biochem. Physiol., 92C, 103–8. Google Scholar
  4. Anastasi, A., Erspamer, V. and Bucci, M. (1968a) Isolation and structure of caerulein, an active decapeptide from the skin of Hyla caerulea. Experientia, 23, 699–700.Google Scholar
  5. Anastasi, A., Erspamer, V. and Endean, R. (1968b) Isolation and amino acid sequence of caerulein, the active decapeptide of the skin of Hyla caerulea. Arch. Biochem. Biophys., 125, 57–68.Google Scholar
  6. Andersen, B.N. (1985) Species variation in the tyrosine sulfation of mammalian gastrins. Gen. Comp. Endocrinol., 58, 44–50.Google Scholar
  7. Angelucci, L., Baldieri, M. and Linari, G. (1970) The action of caerulein on pancreatic and biliary secretions of the chicken. Eur.J. Pharmacol., 11, 217–32.Google Scholar
  8. Barrington, E.J.W. and Dockray, G.J. (1972) Cholecystokinin-pancreozymin-like activity in the eel (Angui Ua anguilla L). Gen. Comp. Endocrinol., 19, 80–87.Google Scholar
  9. Barrington, E.J.W. and Dockray, G.J. (1976) Review. Gastrointestinal hormones. J. Endocrinol., 69, 299–325.Google Scholar
  10. Bevis, P.J.R. and Thorndyke, M.C. (1981) Stimulation of gastric enzyme secretion by porcine cholecystokinin in the ascidian, Styela clava. Gen. Comp. Endocrinol, 45, 458–64.Google Scholar
  11. Bjenning, C. and Holmgren, S. (1988) Neuropeptides in the fish gut. An immunohistochemical study of evolutionary patterns. Histochemistry, 88, 155–63.Google Scholar
  12. Blair, E.L., Falkmer, S., Hellerström, C, Östberg, H. and Richardson, D.D. (1969) Investigation of gastrin activity in pancreatic islet tissue. Acta Pathol. Microbiol Scand., 75, 583–97.Google Scholar
  13. Buchan, A.M.J. (1986) An immunocytochemical study of regulatory peptides in the amphibian gastrointestinal tract. Can. J. Zool., 64, 1–7.Google Scholar
  14. Buchan, A.M.J., Lance, V. and Polak, J.M. (1982) The endocrine pancreas of Alligator mississippiensis. An immunocytochemical investigation. Cell Tissue Res., 224, 117–28.Google Scholar
  15. Buchan, A.M.J., Lance, V. and Polak, J.M. (1983) Regulatory peptides in the gastrointestinal tract of Alligator mississipiensis. An immunocytochemical study. Cell Tissue Res., 231, 439–49.Google Scholar
  16. Buchan, A.M.J., Polak, J.M. and Pearse, A.G.E. (1980) Gut hormones in Salamandra salamandra. An immunocytochemical and electron microscopic investigation. Cell Tissue Res., 211, 331–43.Google Scholar
  17. Cimini, V., Van Noorden, S., Giordano-Lanza, G., Nardini, V., McGregor, G.P., Bloom, S.R. and Polak, J.M. (1985) Neuropeptides and 5-HT immunoreactivity in the gastric nerves of the dogfish (Scyliorhinus stellaris). Peptides, 6 (Suppl. 3), 373–7.Google Scholar
  18. Crim, J. W. and Vigna, S.R. (1983) Brain, gut and skin peptide hormones in lower vertebrates. Am. Zool., 23, 621–38.Google Scholar
  19. Diaz de Rada, O., Sesma, M.P. and Vazquez, J.J. (1987) Localization of G cells in the antral mucosa of Rana temporaria: immunocytochemical and electron microscopy study. Gen. Comp. Endocrinol., 67, 189–93.Google Scholar
  20. Dimaline, R. (1983) Is caerulein amphibian CCK? Peptides, 4, 457–62.Google Scholar
  21. Dimaline, R., Rawdon, B.B., Brandes, S., Andrew, A. and Loveridge, J.P. (1982) Biologically active gastrin/CCK-related peptides in the stomach of a reptile, Crocodylus niloticus identified and characterized by immunochemical methods. Peptides, 3, 977–84.Google Scholar
  22. Dimaline, R., Young, J. and Gregory, H. (1986) Isolation from chicken antrum, and primary amino acid sequence of a novel 36-residue peptide of the gastrin/CCK family. FEBS Lett., 205, 318–22.Google Scholar
  23. Dockray, G.J. (1975) Comparison of the actions of porcine secretin and the extracts of chicken duodenum on pancreatic exocrine secretion in cat and turkey. J. Physiol. (Lond.), 244, 625–37.Google Scholar
  24. Dockray, G.J. (1977) Immunoreactive component resembling cholecystokinin octapeptide in intestine. Nature, Lond., 270, 359–61.Google Scholar
  25. Dockray, G.J. (1979) Cholecystokinin-like peptides in avian brain and gut. Experientia, 35, 628–30.Google Scholar
  26. Dockray, G.J. (1981) Cholecystokinin. In Gut Hormones (eds S.R. Bloom and J.M. Polak), Churchill Livingstone, Edinburgh, pp. 228–39.Google Scholar
  27. Dockray, G.J., Desmond, H., Gayton, R.J., Jönsson, A.-C., Raybould, H., Sharkey, K.A., Varro, A. and Williams, R.G. (1985) Cholecystokinin and gastrin forms in the nervous system. Ann. N.Y. Acad. Sei., 448, 32–43.Google Scholar
  28. Dockray, G.J. and Dimaline, R. (1984) Evolution of the gastrin/CCK family. In Evolution and Tumour Pathology of the Neuroendocrine System, (eds S. Falkmer, R. Häkanson and F. Sundler), Elsevier Science Publishers B.U., pp. 313–33.Google Scholar
  29. Dockray, G.J. and Dimaline, R. (1985) FMRFamide- and gastrin/CCK-like peptides in birds. Peptides, 6 (Suppl. 3), 333–7.Google Scholar
  30. Dockray, G.J., Vaillant, C. and Hopkins, C.R. (1978) Biosynthetic relationships of big and little gastrins. Nature, Lond., 273, 770–2.Google Scholar
  31. Doerr-Schott, J., Garaud, J.-C. and Clauss, R.-O. (1979) Immunohistochemical localization of a gastrin-like peptide in the brain of an amphibian, Xenopus laevis Daud. Cell Tissue Res., 203, 65–78.Google Scholar
  32. Edkins, J.S. (1905) On the chemical mechanism of gastric secretion. Proc. R. Soc. Lond., 76, 376.Google Scholar
  33. El-Salhy, M. (1984) Immunocytochemical investigation of the gastro-enteropancreatic (GEP) neurohormonal peptides in the pancreas and gastrointestinal tract of the dogfish Squalus acanthias. Histochemistry, 80, 193–205.Google Scholar
  34. El-Salhy, M. and Grimelius, L. (1981) The endocrine cells of the gastrointestinal mucosa of a squamate reptile, the grass lizard (Mabuya quinquetaeniata). A histological and immunohistochemical study. Biomed. Res., 2, 639–58.Google Scholar
  35. El-Salhy, M., Grimelius, L., Wilander, E., Abu-Sinna, G. and Lundqvist, G. (1981) Histological and immunohistochemical studies of the endocrine cells of the gastrointestinal mucosa of the toad (Bufo regularis). Histochemistry, 71, 53–65.Google Scholar
  36. Elbal, M.T. and Agulleiro, B. (1986) An immunocytochemical and ultrastructural study of endocrine cells in the gut of a teleost fish, Sparus auratus L. Gen. Comp. Endocrinol., 64, 339–54.Google Scholar
  37. Erspamer, V., Falconieri Erspamer, G., Mazzanti, G. and Endean, R. (1984) Active peptides in the skins of one hundred amphibian species from Australia and Papua New Guinea. Comp. Biochem. Physiol., 77C, 99–108.Google Scholar
  38. Falkmer, S., Carraway, R.E., El-Salhy, M., Emdin, S.O., Grimelius, L., Rehfeld, J.F., Reinecke, M. and Schwartz, T.W. (1981) Phylogeny of the gastro-enteropancreatic neuroendocrine system: A review. In Cellular Basis of Chemical Messengers in the Digestive System, (eds M.I. Grossman, A.B. Brazier and J. Lechago), Academic Press, New York, pp. 21–42.Google Scholar
  39. Gater, S. and Balls, M. (1977) Amphibian pancreas function in long term organ culture. Gen. Comp. Endocrinol, 33, 82–93.Google Scholar
  40. Gibson, R.G., Mihas, A.A., Colvin, H.W. and Hirschowitz, B.I. (1976) The search for submammalian gastrins: the identification of amphibian gastrin. Proc. Soc. Exp. Biol. Med., 53, 284–8.Google Scholar
  41. Gregory, R.A. and Tracy, H.J. (1964) The constitution and properties of two gastrins extracted from hog antral mucosa. Gut, 5, 103–14.Google Scholar
  42. Grimmelikhuijzen, C.J.P., Sundler, F. and Rehfeld, J.F. (1980) Gastrin/CCK-like immunoreactivity in the nervous system of coelenterates. Histochemistry, 69, 61–8.Google Scholar
  43. Hansen, D. (1975) Evidence of a gastrin-like substance in Rhinobatus productus. Comp. Biochem. Physiol, 52C, 61–3.Google Scholar
  44. Harper, A.A. and Raper, H.S. (1943) Pancreozymin, a stimulant of the secretion of pancreatic enzymes in extracts of the small intestine. J. Physiol (Lond.), 102, 115–25.Google Scholar
  45. Hogben, C. A.M. (1966) Response of isolated dogfish gastric mucosa to histamine. Proc. Soc. Exp. Biol. Med., 120, 890–93.Google Scholar
  46. Holm-Rutili, L. and Berglindh, T. (1986) Pentagastrin and gastric mucosal blood flow. Am. J. Physiol, 250, G575–80.Google Scholar
  47. Holmgren, S., Jensen, J., Jönsson, A.-C., Lundin, K. and Nilsson, S. (1985) Neuropeptides in the gastrointestinal canal of Necturus maculosus. Distribution and effects on motility. Cell Tissue Res., 241, 565–80.Google Scholar
  48. Holmgren, S. and Nilsson, S. (1983) Bombesin-, gastrin/CCK-, 5-hydroxytryptamine-, neurotensin-, somatostatin-, and VIP-like immunoreactivity and catecholamine fluorescence in the gut of the elasmobranch, Squalus acanthias. Cell Tissue Res., 234, 595–618.Google Scholar
  49. Holmgren, S., Vaillant, C. and Dimaline, R. (1982) VIP-, Substance P-, gastrin/CCK-, bombesin-, somatostatin- and glucagon-like immunoreactivities in the gut of the rainbow trout, Salmo gairdneri. Cell Tissue Res., 223, 141–53.Google Scholar
  50. Holmquist, A.L., Dockray, G.J., Rosenquist, G.L. and Walsh, J.H. (1979) Immunochemical characterization of cholecystokinin-like peptides in lamprey gut and brain. Gen. Comp. Endocrinol., 37, 474–81.Google Scholar
  51. Ivy, A.C. and Oldberg, E. (1928) A hormone mechanism for gallbladder contraction and evacuation. Am. J. Physiol., LXXXVI, 599–613.Google Scholar
  52. Jorpes, J.E. and Mutt, V. (1971) Secretin and cholecystokinin (CCK). Handb. Exp. Pharmacol., 34, 1–179.Google Scholar
  53. Jönsson, A.-C., Holmgren, S. and Holstein, B. (1987a) Gastrin/CCK-like immunoreactivity in endocrine cells and nerves in the gastrointestinal tract of the cod, Gadus morhua, and the effect of peptides of the gastrin-CCK family on cod gastrointestinal smooth muscle. Gen. Comp. Endocrinol., 66, 190–202.Google Scholar
  54. Jönsson, A.-C., Varro, A. and Dockray, G.J. (1987b) Antibodies to the C-terminus of the cholecystokinin precursor: radioimmunoassay and immunohistochemical studies in adult and developing rat gut. Peptides, 8, 95–101.Google Scholar
  55. Ketterer, H., Ruoff, H.-J. and Sewing, K.-Fr. (1973) Do chickens have gastrin-like compounds? Experientia, 29, 1096.Google Scholar
  56. Langer, M., Van Noorden, S., Polak, J.M. and Pearse, A.G.E. (1979) Peptide hormone-like immunoreactivity in the gastrointestinal tract and endocrine pancreas of eleven teleost species. Cell Tissue Res., 199, 493–508.Google Scholar
  57. Larsson, B.A. and Vigna, S.R. (1983) Gastrin/cholecystokinin-like immunoreactive peptides in the Dungeness crab, Cancer magister (Dana): immunochemical and biological characterization. Regul. Pept., 7, 155–70.Google Scholar
  58. Larsson, L.-I. (1979) Innervation of the pancreas by substance P, enkephalin, vasoactive intestinal polypeptide and gastrin/CCK immunoreactive nerves. J. Histochem. Cytochem., 27, 1283–4.Google Scholar
  59. Larsson, L.-I. and Rehfeld, J.F. (1977) Evidence for a common evolutionary origin of gastrin and cholecystokinin. Nature, Lond., 269, 335–8.Google Scholar
  60. Larsson, L.-I., Sundler, F., Hakanson, R., Rehfeld, J.F. and Stadil, F. (1974) Distribution and properties of gastrin cells in the gastrointestinal tract of chicken. Cell Tissue Res., 154, 409–21.Google Scholar
  61. Lundberg, J.M., Hokfelt, T., Nilsson, G., Terenius, L., Rehfeld, J., Elde, R. and Said, S. (1978) Peptide neurons in the vagus, splanchnic and sciatic nerves. Acta Physiol. Scand., 104, 499–501.Google Scholar
  62. Nachman, R.J., Holman, G.M., Cook, B.J., Haddon, W.F. and Ling, N. (1986a) Leucosulfakinin-II, a blocked sulfated insect neuropeptide with homology to cholecystokinin and gastrin. Biochem. Biophys. Res. Commun., 140, 357–64.Google Scholar
  63. Nachman, R.J., Holman, G.M., Haddon, W.F. and Ling, N. (1986b) Leucosulfakinin, a sulfated insect neuropeptide with homology to gastrin and cholecystokinin. Science, 234, 71–3.Google Scholar
  64. Noaillac-Depeyre, J. and Hollande, E. (1981) Evidence for somatostatin, gastrin, and pancreatic polypeptide-like substances in the mucosa of the gut in fishes with and without stomach. Cell Tissue Res., 216, 193–203.Google Scholar
  65. Notenboom, C.D., Garaud, J.C., Doerr-Schott, J. and Terlou, M. (1981) Localization by immunofluorescence of a gastrin-like substance in the brain of the rainbow trout, Salmo gairdneri. Cell Tissue Res., 214, 247–55.Google Scholar
  66. Olowo-Okorun, M.O. and Amure, B.O. (1973) Gastrin activity in the chicken proventriculus. Nature, Lond., 246, 424–5.Google Scholar
  67. Östberg, Y., Van Noorden, S., Pearse, A.G.E. and Thomas, N.W. (1976) Cytochemical, immunofluorescence, and ultrastructural investigations on polypeptide hormone containing cells in the intestinal mucosa of a cyclostome, Myxine glutinosa. Gen. Comp. Endocrinol., 28, 213–27.Google Scholar
  68. Oyebola, D.D.O. and Elegbe, R. A. (1975) Gastrin activity in the stomach extracts of Bufo regularis (the common African Toad). Comp. Biochem. Physiol, 52A, 209–11.Google Scholar
  69. Power, D.M., Bunnett, N., Turner, A.J. and Dimaline, R. (1987) Degradation of endogenous heptadecapeptide gastrin by endopeptidase 24.11 in the pig. Am. J. Physiol, 253, G33–9.Google Scholar
  70. Reifel, C.W., Marin-Sorensen, M. and Samloff, I.M. (1983) Gastrin immunoreactive cells in the gastrointestinal tracts from four species of fish. Can. J. Zool., 61, 1464–8.Google Scholar
  71. Reiner, A. and Beinfeld, M.C. (1985) The distribution of cholecystokinin-8 in the central nervous system of turtles: an immunohistochemical and biochemical study. Brain Res. Bull., 15, 167–81.Google Scholar
  72. Reiner, A., Eldred, W.D., Beinfeld, M.C. and Krause, J.E. (1985) The cooccurrence of a substance P-like peptide and cholecystokinin-8 in a fiber system of turtle cortex. J. Neurosci., 5, 1527–44.Google Scholar
  73. Richter, K., Egger, R. and Kreil, G. (1986) Sequence of preprocaerulein cDNAs cloned from skin of Xenopus laevis. A small family of precursors containing one, three, or four copies of the final product. J. Biol. Chem., 261, 3676–80.Google Scholar
  74. Rombout, J.H.W.M., Bol, J. and Taverne-Thiele, J.J. (1986) Ultrastructural characterization of 6 immunoreactive enteroendocrine cells in Barbus conchonius (Teleostei, Cyprinidae). Histochemistry, 85, 467–73.Google Scholar
  75. Rombout, J.H.W.M. and Taverne-Thiele, J.J. (1982) An immunocytochemical and electron-microscopical study of endocrine cells in the gut and pancreas of a stomachless teleost fish, Barbus conchonius (Cyprinidae). Cell Tissue Res., 227, 577–93.Google Scholar
  76. Rozsa, Z. and Varro, V. (1985) Mechanism of action of cholecystokinin on intestinal blood flow; interactions with opioid peptides and vasoactive intestinal peptide. Neuropeptides, 6, 71–81.Google Scholar
  77. Schneider, B.S., Maimon, J. and Friedman, J. (1986) Expression of a cholecystokinin precursor-related peptide in vertebrate and invertebrate tissues. Am. J. Physiol, 251, E707–14.Google Scholar
  78. Schultzberg, M., Hökfelt, T., Nilsson, G., Terenius, L., Rehfeld, J.F., Brown, M., Eide, R., Goldstein, M. and Said, S. (1980) Distribution of peptide- and catecholamine-containing neurons in the gastrointestinal tract of rat and guinea-pig: immunohistochemical studies with antisera to substance P, vasoactive intestinal polypeptide, enkephalins, somatostatin, gastrin/ cholecystokinin, neurotensin and dopamines-hydroxylase. Neuroscience, 5, 689–744.Google Scholar
  79. Sewing, K.-Fr. and Ruoff, H.J. (1972) Control of gastric acid secretion in chickens. Acta Hepato-Gastroenterol, 19, 296–300.Google Scholar
  80. Shinomura, Y., Eng, J. and Yalow, R.S. (1987) Chinchilla “Big” and “Little” gastrins. Biochem. Biophys. Res. Commun., 143, 7–14.Google Scholar
  81. Shulkes, A., Stephens, D. and Hardy, K.J. (1983) Distribution of vasoactive intestinal peptide, bombesin, and gastrin-cholecystokinin like peptides in the avian intestinal tract and brain. Comp. Biochem. Physiol., 76C, 345–9.Google Scholar
  82. Soll, A.H. and Berglindh, T. (1987) Physiology of isolated gastric glands and parietal cells: Receptors and effectors regulating function. In Physiology of the Gastrointestinal Tract, 2nd edn (ed. R. Johnson), Raven Press, New York, pp. 883–909.Google Scholar
  83. Thorndyke, M.C. and Bevis, P.J.R. (1984) Comparative studies on the effects of cholecystokinins, caerulein, bombesin 6–14 nonapeptide, and physalaemin on gastric secretion in the ascidian Styela clava. Gen. Comp. Endocrinol., 55, 251–9.Google Scholar
  84. Thorndyke, M. and Dockray, G.J. (1986) Identification and localization of material with gastrin-like immunoreactivity in the neural ganglion of a protochordate, dona intestinalis. Regul. Pept., 16, 269–79.Google Scholar
  85. Van Noorden, S. and Pearse, A.G.E. (1974) Immunoreactive polypeptide hormones in the pancreas and gut of the lamprey. Gen. Comp. Endocrinol., 23, 311–24.Google Scholar
  86. Van Noorden, S. and Pearse, A.G.E. (1976) The localisation of immunoreactivity to insulin, glucagon and gastrin in the gut of Amphioxus (Branchiostoma) lanceolatus. In The Evolution of the Pancreatic Islets (eds T.A. Grillo, L. Leibson and A. Epple), Pergamon Press, Oxford, pp. 163–78.Google Scholar
  87. Vanderhaegen, J.J., Signeau, J.C. and Gepts, W. (1975) New peptide in the vertebrate CNS reacting with antigastrin antibodies. Nature, Lond., 257, 604–5. Google Scholar
  88. Vigna, S.R. (1979) Distinction between cholecystokinin-like and gastrin-like biological activities extracted from gastrointestinal tissues of some lower vertebrates. Gen. Comp. Endocrinol., 39, 512–20.Google Scholar
  89. Vigna, S.R. (1984) Radioreceptor and biological characterization of cholecystokinin and gastrin in the chicken. Am. J. Physiol., 246, G296–304.Google Scholar
  90. Vigna, S.R. (1985) Evolution of hormone and receptor diversity: cholecystokinin and gastrin. Am. Zool., 26, 1033–40.Google Scholar
  91. Vigna, S.R., Fischer, B.L., Morgan, J.L.M. and Rosenquist, G.L. (1985) Distribution and molecular heterogeneity of cholecystokinin-like immunoreactive peptides in the brain and gut of the rainbow trout, Salmo gairdneri. Comp. Biochem. Physiol., 82C, 143–6.Google Scholar
  92. Vigna, S.R. and Gorbman, A. (1977) Effects of cholecystokinin, gastrin, and related peptides on coho salmon gallbladder contraction in vitro. Am. J. Physiol., 232, E485–91.Google Scholar
  93. Vigna, S.R. and Gorbman, A. (1979) Stimulation of intestinal lipase secretion by porcine cholecystokinin in the hagfish, Eptatretus stouti. Gen. Comp. Endocrinol., 38, 356–9.Google Scholar
  94. Vigna, S.R., Thorndyke, M.C. and Williams, J. A. (1986) Evidence for a common evolutionary origin of brain and pancreas cholecystokinin receptors. Proc. Natl. Acad. Sci. USA, 83, 4355–9.Google Scholar
  95. Walsh, J.H. (1987) Gastrointestinal hormones. In Physiology of the Gastrointestinal Tract, 2nd edn (ed. R. Johnson), Raven Press, New York, pp. 181–253.Google Scholar
  96. Williams, J.A. (1982) Cholecystokinin: A hormone and a neurotransmitter. Biomed. Res., 3, 107–21.Google Scholar
  97. Williams, J.A., Vigna, S.R., Sakamoto, C. and Goldstein, I.D. (1985) Brain cholecystokinin receptors. Binding characteristics, covalent cross-linking, and evolutionary aspects. Ann. N.Y. Acad. Sci., 448, 220–30.Google Scholar
  98. Yamada, J., Campos, V.J.M., Kitamura, N., Pacheco, A.C., Yamashita, T. and Yanaihara, N. (1987) An immunohistochemical study of the endocrine cells in the gastrointestinal mucosa of the Caiman latirostris. Arch. Histol. Jap., 50, 229–41.Google Scholar
  99. Yamada, J., Kitamura, N., Yamashita, T. and Yanaihara, N. (1986) Immunohistochemical studies on the endocrine cells in avian gizzard. Biomed. Res., 7, 39–45.Google Scholar
  100. Yamamura, T., Takahashi, T., Kusunoki, M., Kantoh, M., Ishikawa, Y. and Utsunomiya, J. (1986) Cholecystokinin octapeptide-evoked [3H]acetylcholine release from guinea pig gallbladder. Neurosci. Lett., 65, 167–70.Google Scholar
  101. Yoshida, K., Iwanaga, T. and Fujita, T. (1983) Gastro-entero-pancreatic (GEP) endocrine system of the flatfish, Paralichtys olivaceus. An immunocytochemical study. Arch. Histol. Jap., 46, 259–66.Google Scholar

Copyright information

© Chapman and Hall 1989

Authors and Affiliations

  • Ann-Cathrine Jönsson

There are no affiliations available

Personalised recommendations