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An immunocytochemical and electron-microscopical study of endocrine cells in the gut and pancreas of a stomachless teleost fish, Barbus conchonius (Cyprinidae)

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Summary

Four immunoreactive endocrine cell types can be distinguished in the pancreatic islets of B. conchonius: insulin-producing B cells, somatostatin-producing A1 (= D) cells, glucagon-producing A2 cells and pancreatic poly-peptide-producing PP cells. The principal islet of this species contains only a few PP cells, while many PP cells are present in the smaller islets. Except for the B cell all pancreatic endocrine cell types are also present in the pancreatic duct.

At least six enteroendocrine cell types are present in the gut of B. conchonius: 1. a cell type (I) with small secretory granules, present throughout the intestine, and possibly involved in the regulation of gut motility; 2. a C-terminal gastrin immunoreactive cell, probably producing a caerulein-like peptide; these cells are located at the upper parts of the folds, especially in the proximal part of the intestinal bulb; 3. a met-enkephalin-immunoreactive cell, present throughout the first segment; 4. a glucagon-immunoreactive cell, which is rare in the first segment; 5. a PP-immunoreactive cell, mainly present in the first half of the first segment; 6. an immunoreactive cell, which cannot at present be specified, located in the intestinal bulb. The latter four cell types are mostly located in the basal parts of the folds, although some PP-immunoreactive cells can also be found in the upper parts.

Most if not all enteroendocrine cells are of the open type. The possible functions of all enteroendocrine cell types are discussed.

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Abbreviations

BPP:

bovine pancreatic polypeptide

CCK:

cholecystokinin

GEP:

gastro-entero-pancreatic

GIP:

gastric inhibitory peptide or glucose-dependent insulin releasing peptide

PPP:

pig pancreatic polypeptide

VIP:

vasoactive intestinal polypeptide

References

  • Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247

    Google Scholar 

  • Alumets J, Håkanson R, Sundler F, Chang KJ (1978) Leu-enkephalin-like material in nerves and enterochromaffin cells in the gut. Histochemistry 56:187–196

    Google Scholar 

  • Buchan AMI, Polak JM (1980) The classification of the human gastroenteropancreatic endocrine cells. Invest Cell Pathol 3:51–71

    Google Scholar 

  • Buffa R, Solcia E, Fiocca R, Crivelli O, Pera A (1979) Complement-mediated binding of immunoglobulins to some endocrine cells of the pancreas and gut. J Histochem Cytochem 27:1279–1280

    Google Scholar 

  • Dubois MP, Billard R, Breton R (1978) Use of immunofluorescence for localization of somatostatin-like antigen in the rainbow trout (Salmo gairdneri). Comparative distributions of LH-RF and neurophysin. Ann Biol Anim Bioch Biophys 18:843–850

    Google Scholar 

  • Dubois MP, Billard R, Breton R, Peter RE (1979) Comparative distribution of somatostatin, LH-RH, neurophysin and α-endorphin in the rainbow trout: an immunocytological study. Gen Comp Endocrinol 37:220–232

    Google Scholar 

  • Erspamer V (1954) Pharmacology of indolealkylamines. Pharmacol Rev 6:425–487

    Google Scholar 

  • Erspamer V (1958) Occurrence and distribution of 5-hydroxytryptamine (enteramine) in the living organism. Z Vitamin-, Hormon-, u. Fermentforsch 9:74–96

    Google Scholar 

  • Erspamer V (1970) Progress report: Caerulein. Gut 11:74–87

    Google Scholar 

  • Falkmer S (1979) Immunocytochemical studies of the evolution of islet hormones. J Histochem Cytochem 27:1281–1282

    Google Scholar 

  • Falkmer S, Patent GJ (1972) Comparative and embryological aspects of the pancreatic islets. In: Steiner DF, Freinkel N (eds) Handbook of physiology. Endocrinology, Vol I, Williams and Wilkins, Baltimore, pp 1–23

    Google Scholar 

  • Falkmer S, Stefan Y (1978) Pancreatic polypeptide (PP): Phylogenetic aspects in gastro-intestinal mucosa and endocrine pancreas. Scand. J Gastroenterol 13: suppl 69, 59

    Google Scholar 

  • Fänge R (1962) Pharmacology of poikilothermic vertebrates and invertebrates. Pharmacol Rev 14:281–316

    Google Scholar 

  • Gabe M, Martoja M (1971) Donees histologiques sur les cellules endocrines gastriques et pancréatiques de Mugil auratus (Téléostéen, Mugiliforme). Arch Anat Micro Morph Exp 60:214–234

    Google Scholar 

  • Gersell DJ, Gingerich RL, Greider MH (1979) Regional distribution of pancreatic polypeptide in the human and canine pancreas. Diabetes 28:11–15

    Google Scholar 

  • Grube D, Weber E (1980) Immunoreactivities of gastrin (G-)cells. I. Dilution-dependent staining of G cells by antisera and non-immune sera. Histochemistry 65:223–237

    Google Scholar 

  • Huebner E, Chee G (1978) Histological and ultrastructural specialisation of the digestive tract of the intestinal air breather, Hoplosternum thoracatum (Teleost). J Morphol 157:301–328

    Google Scholar 

  • Ito S, Takai K, Shibata A, Matsubara Y, Yanaihara N (1979) Met-enkephalin-immunoreactive cells in the human and canine pyloric antrum. Gen Comp Endocrinol 38:238–245

    Google Scholar 

  • Johnson DE, Torrence L, Elde RP, Bauer GE, Noe BD, Fletcher DJ (1976) Immunohistochemical localization of somatostatin, insulin and glucagon in the principal islets of the anglerfish (Lophius americanus) and the channel catfish (Ictalurus punctata). Am J Anat 147:119–124

    Google Scholar 

  • Klein C, Lange RH (1977) Principal cell types in the pancreatic islets of a teleost fish, Xiphophorus helleri H. Cell Tissue Res 176:529–551

    Google Scholar 

  • Klein C, Van Noorden S (1978) Use of immunocytochemical staining of somatostatin for correlative light and electron microscopic investigation of D cells in the pancreatic islet of Xiphophorus helleri H. (Teleostei). Cell Tissue Res 194:399–404

    Google Scholar 

  • Klein C, Van Noorden S (1980) Pancreatic polypeptide (PP)-and glucagon cells in the pancreatic islet of Xiphophorus helleri H. (Teleostei). Cell Tissue Res 205:187–198

    Google Scholar 

  • Lange RH, Klein C (1976) The lack of specificity of granule shapes in relation to gastro-enteropancreatic secretion. In: Coupland RE, Fujita T (eds) Chromaffin, enterochromaffin and related cells. Elsevier, Amsterdam, pp 293–301

    Google Scholar 

  • Lange RH, Syed Ali S, Klein C, Trandaburu R (1975) Immunohistochemical demonstration of insulin and glucagon in islet tissue of reptiles, amphibians and teleosts using epoxy-embedded material and anti-porcine hormone sera. Acta Histochem 525:71–78

    Google Scholar 

  • Langer M, Van Noorden S, Polak JM, Pearse AGE (1979) Peptide hormone-like immunoreactivity in the gastrointestinal tract and endocrine pancreas of eleven teleost species. Cell Tissue Res 199:493–508

    Google Scholar 

  • Larsson LI, Rehfeld JF (1977) Evidence for a common evolutionary origin of gastrin and cholecystokinin. Nature 269:335–338

    Google Scholar 

  • Larsson LI, Rehfeld JF (1978) Evolution of CCK-like hormones. In: Bloom SR (ed) Gut hormones. Churchill Livingstone, Edinburgh, pp 68–73

    Google Scholar 

  • Larsson LI, Stengaard-Pedersen K (1981) Enkephalin/Endorphin-related peptides in antropyloric gastrin cells. J Histochem 29:1088–1098

    Google Scholar 

  • Larsson LI, Polak JM, Buffa R, Sundler F, Solcia E (1979) On the immunocytochemical localization of the vasoactive intestinal polypeptide. J Histochem Cytochem 27:936–938

    Google Scholar 

  • Lin TM (1980) Pancreatic polypeptide isolation, chemistry and histological function. In: Jerzy Glass GB (ed) Gastrointestinal hormones. Raven Press, New York, pp 275–306

    Google Scholar 

  • Ling EA, Tan CK (1975) Fine structure of the gastric epithelium of the coral fish, Chelmon rostratus Curvier. Okajimas Fol Anat Jap 51:285–310

    Google Scholar 

  • Noaillac-Depeyre J, Gas N (1978) Ultrastructural and cytochemical study of the gastric epithelium in a fresh water teleostean fish (Perca fluviatilis). Tissue Cell 10:23–37

    Google Scholar 

  • Noaillac-Depeyre J, Gas N (1979) Structure and function of the intestinal epithelial cells in the perch (Perca fluviatilis) Anat Rec 195:621–640

    Google Scholar 

  • Noaillac-Depeyre J, Hollande E (1981) Evidence of somatostatin, gastrin and pancreatic polypeptide-like substances in the mucosa cells of the gut in fishes with and without stomach. Cell Tissue Res 216:193–203

    Google Scholar 

  • Orci L, Baetens D, Ravazolla M, Stefan Y, Malaise-Lague F (1976) Pancreatic polypeptide and glucagon: non random distribution in pancreatic islets. Life Sciences, 19:1811–1816

    Google Scholar 

  • Orci L, Malaisse-Lague F, Baetens D, Perrelet A (1978) Pancreatic polypeptide-rich regions in human pancreas. Lancet II:1200–1201

    Google Scholar 

  • Pictet R, Rutter WJ (1972) Development of the embryonic endocrine pancreas. In: Steiner DF, Freinkel M (eds) Handbook of Physiology. Endocrinology Vol. I. Williams and Wilkins, Baltimore, pp 25–66

    Google Scholar 

  • Polak JM, Bloom SE (1980) Neural and cellular origin of gastrointestinal hormonal peptides in health and disease. In: Jerzy Glass GB (ed) Gastrointestinal hormones. Raven Press, New York, pp 19–51

    Google Scholar 

  • Polak JM, Sullivan SM, Bloom SR, Facer P, Pearse AGE (1977) Enkephalin-like immunoreactivity in the human gastrointestinal tract. Lancet I:972–974

    Google Scholar 

  • Read JB, Burnstock G (1968) Fluorescent histochemical studies on the mucosa of the vertebrate gastrointestinal tract. Histochemie 16:324–332

    Google Scholar 

  • Reinecke M (1981) Immunohistochemical localization of polypeptide hormones in endocrine cells of the digestive tract of Branchiostoma lanceolatum. Cell Tissue Res 219:445–456

    Google Scholar 

  • Reinecke M, Almasan K, Carraway RE, Helmstaedter V, Forssmann WG (1980a) Distribution patterns of neurotensin-like immunoreactive cells in the gastro-intestinal tract of higher vertebrates. Cell Tissue Res 205:383–395

    Google Scholar 

  • Reinecke M, Carraway RE, Falkmer S, Feurle GE, Forssmann WG (1980b) Occurrence of neurotensinimmunoreactive cells in the digestive tract of lower vertebrates and deuterostomian invertebrates. A correlated immunohistochemical and radioimmunochemical study. Cell Tissue Res 212:173–183

    Google Scholar 

  • Rombout JHWM (1977) Enteroendocrine cells in the digestive tract of Barbus conchonius (Teleostei, Cyprinidae). Cell Tissue Res 185:435–450

    Google Scholar 

  • Rombout JHWM, Rademakers LHPM, Hess JP van (1979) Pancreatic endocrine cells of Barbus conchonius (Teleostei, Cyprinidae) and their relation to the enteroendocrine cells. Cell Tissue Res 203:9–23

    Google Scholar 

  • Romeis B (1968) Mikroskopische Technik, R. Oldenbourg Verlag München

    Google Scholar 

  • Seino Y, Porte D, Yanaihara M, Smith PH (1979) Immunohistochemical localization of motilin containing cells in the intestines of several vertebrate species and a comparison of antisera against natural and synthetic motilin. Gen Comp Endocrinol 38:224–233

    Google Scholar 

  • Solcia E, Polak JM, Pearse AGE, Forssmann WG, Larsson LI, Sundler F, Lechago J, Grimelius L, Fujita T, Creutzfeldt W, Gepts W, Falkmer S, Lefranc G, Heitz Ph, Hage E, Buchan AMJ, Bloom SR, Grossman MI (1978) Lausanne 1977 Classification of gastroenteropancreatic endocrine cells. In: Bloom SR (ed) Gut Hormones. Churchill Livingstone, London pp. 40–48

    Google Scholar 

  • Solcia E, Capella C, Buffa R, Frigerio B, Usellini L, Fiocca R (1980) Morphological and functional classification of endocrine cells and related growth in the gastrointestinal tract. In: Jerzy Glass GB (ed) Gastrointestinal hormones. Raven Press, New York, pp 1–17

    Google Scholar 

  • Stefan Y, Falkmer S (1980) Identification of four endocrine cell types in the pancreas of Cottus scorpius (teleostei) by immunofluorescence and electron microscopy. Gen Comp Endocrinol 42:171–178

    Google Scholar 

  • Stefan Y, Dufour C, Falkmer S (1978) Mise en évidence par immunofluorescence de cellules a polypeptide pancréatique (PP) dans le pancréas et le tube digestif de poissons osseux et cartilagineux. CR Acad Sci 286:1074–1075

    Google Scholar 

  • Van Noorden S, Falkmer S (1980) Gut-islet endocrinology — some evolutionary aspects. Invest Cell Pathol 3:21–35

    Google Scholar 

  • Van Noorden S, Patent GJ (1978) Localization of pancreatic polypeptide (PP)-like immunoreactivity in the pancreatic islets of some teleost fishes. Cell Tissue Res 188:521–525

    Google Scholar 

  • Van Noorden S, Polak JM (1980) Hormones of the alimentary tract. In: Barrington EJW (ed) Hormones and Evolution. Acad Press, New York, pp 791–828

    Google Scholar 

  • Van Noorden S, Langer M, Polak JM, Pearse AGE (1980) Immunostaining of peptides in the diffuse neuro-endocrine system of the gut in some teleost fishes. Gen Comp Endocrinol 40:351

    Google Scholar 

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  1. Department of Experimental Animal Morphology and Cell Biology, Agricultural University, Wageningen, The Netherlands

    J. H. W. M. Rombout & J. J. Taverne-Thiele

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  1. J. H. W. M. Rombout
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  2. J. J. Taverne-Thiele
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Rombout, J.H.W.M., Taverne-Thiele, J.J. 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, 577–593 (1982). https://doi.org/10.1007/BF00204788

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