Skip to main content
Log in

Peptide hormone-like immunoreactivity in the gastrointestinal tract and endocrine pancreas of eleven teleost species

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The distribution of peptide hormone-like immunostaining in the gastrointestinal tract of 11 teleost species was investigated by immunofluorescence.

Cells immunoreactive for somatostatin were found in the glandular epithelium of the stomach of four species and in the epithelium of the pyloric appendage of one species. The mid-gut epithelium contained cells reactive with antibodies to glucagon (three species), gastrin (five species), pancreatic polypeptide (five species), and substance P (two species). Cells immunoreactive for met-enkephalin were found in the epithelium of both the mid-gut and the stomach of six species.

In six species in which the endocrine pancreas was investigated, insulin-, glucagon-, and somatostatin-like immunoreactivity was observed. Pancreatic polypeptide was definitely localised by immunostaining in cells of the endocrine pancreas of only one out of three species examined.

Vasoactive intestinal polypeptide-, neurotensin-, bombesin-, and enkephalin-like immunoreactivity was identified in the gastrointestinal nerve fibres in various species.

In view of the considerable species variation found, caution should be exercised in generalising about the peptides present in the gastrointestinal tract of fish.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barrington, E.J.W., Dockray, G.J.: Cholecystokinin-pancreomyzin-like activity in the eel (Anguilla anguilla L.). Gen. Comp. Endocrinol. 19, 80–87 (1972)

    Google Scholar 

  • Baumgarten, H.G.: Über die Muskulatur und die Nerven in der Darmwand der Schleie (Tinca vulgaris Cuv.). Z. Zellforsch. 68, 116–137 (1965)

    Google Scholar 

  • Bloom, S.R., Polak, J.M.: Gut hormone overview. In: Gut hormones. (S.R. Bloom, ed.), pp. 3–18. Edinburgh-London-New York: Churchill Livingstone 1978

    Google Scholar 

  • Capella, C., Solcia, E., Vassallo, G.: Identification of six types of endocrine cells in the gastrointestinal mucosa of the rabbit. Arch. Histol. Jpn. 30, 479–495 (1969)

    CAS  PubMed  Google Scholar 

  • Dawson, I.: The endocrine cells of the gastrointestinal tract. Histochem. J. 2, 527–549 (1970)

    Google Scholar 

  • Dockray, G.J.: Extraction of a secretin-like factor from the intestines of pike (Esox lucius). Gen. Comp. Endocrinol. 23, 340–347 (1974)

    Google Scholar 

  • Dockray, G.J.: Comparative studies on secretin. Gen. Comp. Endocrinol. 25, 203–210 (1975)

    Google Scholar 

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

    Google Scholar 

  • Erspamer, V.: Occurrence and distribution of 5-hydroxytryptamine (enteramine) in the living organism. Z. Vit.-Horm.-Ferm. Forsch. 9, 74–96 (1958)

    Google Scholar 

  • Euler, U.S. von, Östlund, E.: Occurrence of a substance P-like polypeptide in fish intestine and brain. Brit. J. Pharmacol. 11, 323–325 (1956)

    Google Scholar 

  • Falkmer, S.: Insulin production in vertebrates and invertebrates. Gen. Comp. Endocrinol. 3, 184–191 (1972)

    Google Scholar 

  • Falkmer, S., Östberg, Y.: Comparative morphology of pancreatic islets in animals. In: the diabetic pancreas. (B.W. Volk and K.F. Wellmann, eds.), pp. 15–60. New York: Plenum Publishing Corporation 1977

    Google Scholar 

  • Falkmer, S., Elde, R.P., Hellerström, C., Peterson, B.: Phylogenetic aspects of somatostatin in the gastroenteropancreatic (GEP) endocrine system. Metabolism 27, No. 9. Suppl. 1, 1193–1196 (1978)

    Google Scholar 

  • Forssmann, W.G.: Ultrastructure of hormone-producing cells of the upper gastrointestinal tract. In: Origin, chemistry, physiology and pathophysiology of the gastrointestinal hormones. (W. Creutzfeldt, ed.), pp. 31–70. Stuttgart-New York: Schattauer 1970

    Google Scholar 

  • Fritsch, H.A.R., Van Noorden, S., Pearse, A.G.E.: Cytochemical and immunofluorescence investigations on insulin-like producing cells in the intestine of Mytilus edulis L. Cell Tissue Res. 165, 365–369 (1976)

    Google Scholar 

  • Fritsch, H.A.R., Van Noorden, S., Pearse, A.G.E.: Localisation of somatostatin- and gastrin-like immunoreactivity in the gastrointestinal tract of Ciona intestinalis L. Cell Tissue Res. 186, 181–185 (1978)

    Google Scholar 

  • Gabe, M.: Données histologiques sur les cellules endocrines intestinales de Protopterus annectus Owen. Bull. Biol. Fr. Belg. 107, 3–20 (1973)

    Google Scholar 

  • Gabe, M., Martoja, M.: Données histologiques sur les cellules endocrines gastriques et pancreatiques de Mugil auratus (Téléostéen, Mugiliformes). Arch. Anat. Microsc. Morphol. Exp. 60, 219–234 (1971)

    Google Scholar 

  • Gabe, M., Martoja, M.: Contribution a l'histologie des cellules endocrines gastriques des selaciens. Arch. Anat. Microsc. Morphol. Exp. 61, 17–32 (1972)

    Google Scholar 

  • Hansen, D.: Evidence of a gastrin-like substance in Rhinobatus productus. Comp. Biochem. Physiol. 520, 61–63 (1975)

    Google Scholar 

  • Heitz, P., Polak, J.M., Bloom, S.R., Pearse, A.G.E.: Identification of the D1 cell as the source of human pancreatic polypeptide. Gut 17, 755–758 (1976)

    Google Scholar 

  • Hökfelt, T., Efendic, S., Hellerström, C., Johansson, O., Luft, R., Arimura, A.: Cellular localisation of somatostatin in endocrine-like cells and neurons of the rat with special reference to the A1-cells of the pancreatic islets and to the hypothalamus. Acta Endocrinol. Suppl. 200, 1–41 (1975a)

    Google Scholar 

  • Hökfelt, T., Johansson, O., Efendic, S., Luft, R., Arimura, A.: Are there somatostatin-containing nerves in the rat gut? Immunohistochemical evidence for a new type of peripheral nerves. Experientia 31, 852–853 (1975b)

    Google Scholar 

  • Ishay, I., Gitter, S., Galun, R., Doron, M., Laron, Z.: The presence of insulin in and some effects of exogenous insulin on Hymenoptera tissues and body fluids. Comp. Biochem. Physiol. 54A, 203–206 (1976)

    Google Scholar 

  • Johnson, D.E., Torrence, J.L., Elde, R.P., Bauer, G.E., Noe, B.D., Fletcher, D.J.: Immunohistochemical localization of somatostatin, insulin and glucagon in the principal islets of the anglerfish (Lophius americanus) and the channel catfish (Ictalurus punctata). Amer. J. Anat. 147, 119–124 (1976)

    Google Scholar 

  • Klein, C., Van Noorden, S.: 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 (1978)

    Google Scholar 

  • Lange, R.H., Syed Ali, S., Klein, C., Trandaburu, T.: Immunohistochemical demonstration of insulin and glucagon in islet tissue of reptiles, amphibians and teleosts using epoxy-embedded material and antiporcine hormone sera. Acta Histochem. 52S, 71–78 (1975)

    Google Scholar 

  • Larsson, L.-I., Rehfeld, J.F.: Evidence for a common evolutionary origin of gastrin and cholecystokinin. Nature 269, 335–338 (1977)

    Google Scholar 

  • Larsson, L.-I., Sundler, F., Håkanson, R.: Immunohistochemical localization of avian pancreatic polypeptide to a population of islet cells. Cell Tissue Res. 156, 167–171 (1975)

    Google Scholar 

  • Nilsson, A.: Gastrointestinal hormones in the holocephalian fish, Chimaera monstrosa L. Comp. Biochem. Physiol. 32, 387–390 (1970)

    Google Scholar 

  • Nilsson, G., Larsson, L.-I., Håkanson, R., Brodin, E., Pernow, B., Sundler, F.: Localization of substance P-like immunoreactivitiy in mouse gut. Histochemistry 43, 97–99 (1975)

    Google Scholar 

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

    Google Scholar 

  • Östberg, Y., Van Noorden, S., Pearse, A.G.E.: Cytochemical immunofluorescence and ultrastructural investigations on polypeptide hormone localisation in the islet parenchyma and bile duct mucosa of a cyclostome, Myxine glutinosa. Gen. Comp. Endocrinol. 25, 274–291 (1975)

    Google Scholar 

  • Östberg, Y., Van Noorden, S., Pearse, A.G.E., Thomas, N.W.: Cytochemical immunofluorescence and ultrastructural investigations on polypeptide hormone containing cells in the intestinal mucosa of a cyclostome, Myxine glutinosa. Gen. Comp. Endocrinol. 28, 213–227 (1976)

    Google Scholar 

  • Pearse, A.G.E.: Common cytochemical and ultrastructural characteristics of cells producing polypeptide hormones (the APUD-series) and their relevance to thyroid and ultimobranchial C cells and calcitonin. Proc. R. Soc. Ser. B. 170, 71–80 (1968)

    Google Scholar 

  • Pearse, A.G.E.: The cytochemistry and ultrastructure of polypeptide hormone producing cells of the APUD-series and the embryologic, physiologic and pathologic implications of the concept. J. Histochem. Cytochem. 17, 303–313 (1969)

    Google Scholar 

  • Pearse, A.G.E.: The endocrine polypeptide cells of the APUD-series (structural and functional correlations). Mem. Soc. Endocrin. 19, 543–550 (1971)

    Google Scholar 

  • Pearse, A.G.E.: The gut as an endocrine organ. Brit. J. Hosp. Med. 11, 697–704 (1974a)

    Google Scholar 

  • Pearse, A.G.E.: The endocrine cells of the GI tract: Origins, morphology and functional relationship in health and disease. Clin. Gastroenterol. 3, 491–510 (1974b)

    Google Scholar 

  • Pearse, A.G.E., Polak, J.M.: Immunocytochemical localisation of substance P in mammalian intestine. Histochemistry 41, 373–375 (1975)

    Google Scholar 

  • Plisetskaya, E., Kazakow, V.K., Solitskaya, L., Leibson, L.G.: Insulin producing cells in the gut of freshwater bivalve molluscs Anodonta cygnea and Unio pictorum and the role of insulin in the regulation of their carbohydrate metabolism. Gen. Comp. Endocrinol. 35, 133–145 (1978)

    Google Scholar 

  • Polak, J.M., Bloom, S.R.: Peptidergic innervation of the gastrointestinal tract. In: Gastrointestinal hormones and pathology of the digestive system. (M. Grossmann, V. Speranza, N. Basso and E. Lezoche, eds.), pp. 183–194. New York-London: Plenum Press 1978

    Google Scholar 

  • Polak, J.M., Bloom, S.R.: The hormones of the gastrointestinal tract. In: Scientific basis of gastroenterology (H.L. Duthie and K.G. Wormsley, eds.), pp. 71–111. Edinburgh-London-New York: Churchill Livingstone 1979

    Google Scholar 

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

    Google Scholar 

  • Rombout, J.H.W.M., Lamers, C.H.J., Hanstede, J.G.: Enteroendocrine APUD cells in the digestive tract of larval Barbus conchonius (Teleostei, Cyprinidae). J. Embryol. Exp. Morphol. 47, 121–135 (1978)

    Google Scholar 

  • Solcia, E., Pearse, A.G.E., Grube, D., Kobayashi, S., Bussolati, G., Creutzfeldt, W., Gepts, W.: Revised Wiesbaden classification of gut endocrine cells. Rendic. Gastroent. 5, 13–16 (1973)

    Google Scholar 

  • Solcia, E., Capella, G., Vassallo, G., Buffa, R.: Endocrine cells of the gastric mucosa. Int. Rev. Cytol. 42, 223–286 (1975)

    Google Scholar 

  • Stefan, Y., Dufour, C., Falkmer, S.: Mise en évidence par immunofluorescence de cellules á polypeptide pancréatique (PP) dans le pancréas et le tube digestif de Poissons osseux et cartilagineux. C. R. Acad. Sci. (Paris) Ser. D. 286, 1073–1076 (1978)

    Google Scholar 

  • Sternberger, L.: Immunocytochemistry. Englewood Cliffs (New Jersey): Prentice-Hall, Inc. 1974

    Google Scholar 

  • Sundler, F., Alumets, J., Håkanson, R., Fahrenkrug, J., Schaffalitzky de Muckadell, O.: Peptidergic (VIP) nerves in the pancreas. Histochemistry 55, 173–176 (1978)

    Google Scholar 

  • Tramu, G., Pillez, A., Leonardelli, J.: An efficient method of antibody elution for the successive or simultaneous localization of two antigens by immunocytochemistry. J. Histochem. Cytochem. 26, 322–324 (1978)

    Google Scholar 

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

    Google Scholar 

  • Van Noorden, S., Pearse, A.G.E.: Immunoreactive polypeptide hormones in the pancreas and gut of the lamprey. Gen. Comp. Endocrinol. 23, 311–324 (1974)

    Google Scholar 

  • Van Noorden, S., Pearse, A.G.E.: The localisation of immunoreactivity to insulin, glucagon, and gastrin in the gut of Amphioxus (Branchiostoma) lanceolatus. In: The evolution of pancreatic islets (T.A.I. Grillo, L. Leibson, and A. Epple, eds.), pp. 163–178. Oxford: Pergamon Press 1976

    Google Scholar 

  • Van Noorden, S., Greenberg, J., Pearse, A.G.E.: Cytochemical and immunofluorescence investigations on polypeptide hormone localization in the pancreas and gut of larval lamprey. Gen. Comp. Endocrinol. 19, 192–199 (1972)

    Google Scholar 

  • Van Noorden, S., Östberg, Y., Pearse, A.G.E.: Localization of somatostatin-like immunoreactivity in the pancreatic islets of the hagfish, Myxine glutinosa, and the lamprey, Lampetra fluviatilis. Cell Tissue Res. 177, 281–285 (1977)

    Google Scholar 

  • Zetler, G.: The peptidergic neuron: A working hypothesis. Biochem. Pharmacol. 25, 1817–1818 (1976)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Langer, M., Van Noorden, S., Polak, J.M. et al. Peptide hormone-like immunoreactivity in the gastrointestinal tract and endocrine pancreas of eleven teleost species. Cell Tissue Res. 199, 493–508 (1979). https://doi.org/10.1007/BF00236085

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00236085

Key words

Navigation