Skip to main content
Log in

Immunohistochemical localization of (neuro)peptide hormones in endocrine cells and nerves of the gut of a stomachless teleost fish, Barbus conchonius (Cyprinidae)

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

Summary

Enteroendocrine cells containing glucagon-, substance P-, neurotensin- and VIP-like substances have been demonstrated immunocytochemically in the gut of Barbus conchonius. Mainly based on the distribution of the immunoreactive endocrine cells in this and a previous* study, at least eight different enteroendocrine cell types appear to be present in this stomachless fish: 1. C-terminal-gastrinimmunoreactive cells*, predominantly present in the upper parts of the folds of the proximal part of the intestinal bulb. 2. Metenkephalin-immunoreactive cells*, basally located in the folds of the first segment. 3. Pancreatic polypeptide (PP)-immunoreactive cells*, mainly present in the first half of the first segment. 4. Glucagon-like-immunoreactive (GLI) cells that are basally located in the folds of the first segment and that contain a different polypeptide (possibly glicentin) than pancreatic glucagon cells. 5. Substance P-immunoreactive cells, present in the upper parts of the folds throughout the gut. 6. C-terminal-neurotensin-immunoreactive cells, basally located in the folds throughout the first segment. 7. Vasoactive intestinal polypeptide (VIP)-immunoreactive cells, present in small numbers in the proximal part of the intestinal bulb. 8. Nonspecifically-immunoreactive cells*, found throughout the intestinal bulb. Many VIP-immunoreactive nerves have been demonstrated in the smooth muscle layer and myenteric plexus of the gut; furthermore some of them are peptide histidineisoleucine (PHI)-immunoreactive. Substance P-, somatostatin-, neurotensin- and met-enkephalin-immunoreactive nerves are also found. Thus, at least partial sequences of four different mammalian neuropeptide hormones (VIP, substance P, neurotensin, met-enkephalin) occur both in endocrine cells and enteric nerves of the gut of B. conchonius.

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

  • Bishop AE, Blank MA, Christofides ND, Bloom SR, Tatemoto K, Polak JM (1983) Co-localisation of VIP and PHI in the human gut. Regul Pept 6:287

    Google Scholar 

  • Bloom SR, Sagor GR, Al-Mukhtar MYT, Ghatei MA, Wright NA, Polak JM (1981) Enteroglucagon and crypt cell turnover. Fed Proc 40:550

    Google Scholar 

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

    Google Scholar 

  • Burnweit C, Forssmann WG (1979) Somatostatinergic nerves in the cervical spinal cord of the monkey. Cell Tissue Res 200:83–90

    Google Scholar 

  • Camilleri M, Cooper BT, Adrian TE, Bloom SR, Schadwick V (1981) Effects of vasoactive intestinal peptide and pancreatic polypeptide in rabbit intestine. Gut 22:14–18

    Google Scholar 

  • Carraway RE (1979) Neurotensin and related substances. In: Jaffe BM, Behrmann HR (eds) Methods of hormone radioimmunoassay. Academic Press, New York, pp 139–169

    Google Scholar 

  • Carraway RE, Ruane SE, Kim HR (1982) Distribution and immunochemical character of neurotensin-like material in representative vertebrates and invertebrates: apparent conservation of the COOH-terminal region during evolution. Peptides 1:115–123

    Google Scholar 

  • Carraway RE, Reinecke M, Forssmann WG (1983) Region-specific radio-immunoassay and its application to the study of neurotensin-related peptides in the chicken. In: Yoshida H, Yamamura HI (eds) Pharmacologic and biochemical aspects of neurotransmitter receptors. John Wiley & Sons, New York, pp 205–222

    Google Scholar 

  • Dimaline R, Vaillant C, Dockray GJ (1980) The use of regionspecific antibodies in the characterization and localization of vasoactive intestinal polypeptide-like substances in the rat gastrointestinal tract. Regul Pept 1:1–16

    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 

  • El-Salhy M, Grimelius L, Lundberg JM, Tatemoto K, Terenius L (1982a) Immunocytochemical evidence for the occurrence of PYY, a newly isolated gut polypeptide, in endocrine cells in the gut of amphibians and reptiles. Biomed Res 3:303–306

    Google Scholar 

  • El-Salhy M, Wilander E, Grimelius L, Terenius L, Lundberg JM, Tatemoto K (1982b) The distribution of polypeptide YY (PYY)-and pancreatic polypeptide (PP)-immunoreactive cells in the domestic fowl. Histochemistry 75:25–30

    Google Scholar 

  • El-Salhy M, Grimelius L, Wilander E, Ryberg B, Terenius L, Lundberg JM, Tatemoto K (1983a) Immunocytochemical identification of polypeptide YY (PYY) cells in the human gastrointestinal tract. Histochemistry 77:15–23

    Google Scholar 

  • El-Salhy M, Wilander E, Juntti-Berggren L, Grimelius L (1983b) The distribution and ontogeny of polypeptide YY (PYY) and pancreatic polypeptide (PP)-immunoreactive cells in the gastrointestinal tract of rat. Histochemistry 78:53–60

    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 

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

    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 

  • Falkmer S, Van Noorden S (1983) Ontogeny and phylogeny of the glucagon cell. Handbook Exp Pharmacol 66/1:1935–1984

    Google Scholar 

  • Falkmer S, Carraway RE, El-Salhy M, Emdin SO, Grimelius L, Rehfeld JF, Reinecke M, Schwartz TW (1981) Phylogeny of the gastroenteropancreatic neuroendocrine system: A review. In: Grossmann MI, Brazier MA, Lechago J (eds) Cellular basis of chemical messengers in the digestive system. UCLA Forum Med Sci, pp 21–42

  • Fatemi SH, Cullan GE, Crouse DA, Sharp JG (1980) Relative roles of gastrin and glucagon in the control of intestinal cell proliferation. Cell Tissue Kinet 13:685–686

    Google Scholar 

  • Forssmann WG, Pickel VM, Reinecke M, Hock D, Metz J (1981) In: Heym Ch, Forssmann WG (eds) Techniques in neuroanatomical research. Springer Berlin, Heidelberg, New York, pp 171–205

    Google Scholar 

  • Fouchereau-Peron M, Laburthe M, Besson J, Rosselin G, Le Gal Y (1980) Characterization of the vasoactive intestinal polypeptide (VIP) in the gut of fishes. Comp Biochem Physiol 65A:489–492

    Google Scholar 

  • Fritsch HAR, Van Noorden S, Pearse AGE (1982) Gastro-intestinal and neurohormonal peptides in the alimentary tract and cerebral complex of Ciona intestinalis (Ascidiaceae). Cell Tissue Res 233:369–402

    Google Scholar 

  • Gabe M, Martoja M (1971) Données histologiques sur les cellules endocrines gastriques et pancréatiques de Mugil auratus (Té-léostéen, Mugiliforme). Arch Anat Microsc Morphol Exp 60:214–234

    Google Scholar 

  • Grube D (1982) Die endokrinen Zellen des Verdauungsapparats. Klin Wochenschr 60:213–227

    Google Scholar 

  • Grube D, Forssmann WG (1979) Morphology and function of enteroendocrine cells. Horm Res 11:589–606

    Google Scholar 

  • Hartschuh W, Weihe E, Büchler M, Helmstaedter V, Feurle GE, Forssmann WG (1979) Met-enkephalin-like immunoreactivity in Merkel cells. Cell Tissue Res 201:343–348

    Google Scholar 

  • Helmstaedter V, Feurle GE, Forssmann WG (1976) Insulin-, glucagon-, and somatostatin-immunoreactive endocrine cells in the equine pancreas. Cell Tissue Res 172:447–454

    Google Scholar 

  • Helmstaedter V, Feurle GE, Forssmann WG (1977) Relationship of glucagon-somatostatin and gastrin-somatostatin cells in the stomach of the monkey. Cell Tissue Res 177:29–46

    Google Scholar 

  • Holmgren S, Vaillant C, 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 223:141–153

    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 

  • 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, 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 

  • Modlin IM, Sank A, Albert D (1981) Current aspects of gut hormones. J Surg Res 30:602–618

    Google Scholar 

  • Noaillac-Depeyre J, Gas N (1982) Ultrastructure of endocrine cells in the stomach of two teleost fish, Perca fluviatilis L. and Ameiurus nebulosus L. Cell Tissue Res 221:657–678

    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 

  • Polak JM, Sullivan SM, Bloom SR, Facer P, Pearse AGE (1977) Enkephalin-like immunoreactivity in the human gastrointestinal tract. Lancet 1:972–974

    Google Scholar 

  • Rawdon BB, Andrew A (1981) An immunocytochemical survey of endocrine cells in the gastrointestinal tract of chicks at hatching. Cell Tissue Res 220:279–292

    Google Scholar 

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

    Google Scholar 

  • Reifel CW, Marin-Sorensen M, Samlof IM (1983) Gastrin immunoreactive cells in the gastrointestinal tracts from four species of fish. Can J Zool 61:1464–1468

    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 WB (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 neurotensin-immunoreactive 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 

  • Reinecke M, Weihe E, Forssmann WG (1980c) Substance P-immunoreactive nerve fibers in the heart. Neurosci Lett 20:265–269

    Google Scholar 

  • Reinecke M, Schlüter P, Yanaihara N, Forssmann WG (1981) VIP-immunoreactivity in enteric nerves and endocrine cells of the vertebrate gut. Peptides 2: (suppl 2):149–156

    Google Scholar 

  • Reinecke M, Forssmann WG, Thiekötter G, Triepel J (1983) Localization of neurotensin-immunoreactivity in the spinal cord and peripheral nervous system of the guinea pig. Neurosci Lett 37:37–42

    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, Taverne-Thiele JJ (1982) An immunocytochemical and electronmicroscopical study of endocrine cells in the gut and pancreas of a stomachless teleost fish, Barbus conchonius (Cyprinidae). Cell Tissue Res 227:577–593

    Google Scholar 

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

    Google Scholar 

  • Rombout JHWM, Stroband HWJ, Taverne-Thiele JJ (1984) Proliferation and differentiation of intestinal epithelial cells during development of Barbus conchonius (Teleostei, Cyprinidae). Cell Tissue Res 236:207–216

    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 

  • Sternberger LA (1979) Immunohistochemistry. John Wiley and Sons, New York, Chicester, Brisbane, Toronto

    Google Scholar 

  • Takahata G (1981) Ultrastructure of the endocrine cells in the digestive organs of the medaka, Oryzias latipes. Jpn J Ichthyol 27:333–338

    Google Scholar 

  • Tatemoto K, Mutt V (1980) Isolation of two novel candidate hormones using a chemical method for finding naturally occurring polypeptides. Nature 285:417–418

    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 (1980) Vasoactive intestinal polypeptide-like immunoreactivity in nerves of the pancreatic islet of the teleost fish, Gillichthys mirabilis. Cell Tissue Res 212:139–146

    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 

  • Yau WM (1978) Effect of substance P on intestinal muscle. Gastroenterology 74:228–231

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rombout, J.H.W.M., Reinecke, M. Immunohistochemical localization of (neuro)peptide hormones in endocrine cells and nerves of the gut of a stomachless teleost fish, Barbus conchonius (Cyprinidae). Cell Tissue Res. 237, 57–65 (1984). https://doi.org/10.1007/BF00229200

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00229200

Key words

Navigation