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Neuropeptides in the gastrointestinal canal of Necturus maculosus

Distribution and effects on motility

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Summary

The presence and distribution of regulatory peptides in nerves and endocrine cells of the stomach, intestine and rectum of a urodele amphibian, the mudpuppy, Necturus maculosus, was studied immunohistochemically in sections or whole-mount preparations of the gut wall. The effect of the occurring peptides on gut motility was studied in isolated strip preparations of circular and longitudinal smooth muscle from different parts of the gut.

Bombesin-, neurotensin-, substance P- and VIP-like immunoreactivity was present in abundant nerve fibres in the myenteric plexus of both stomach, intestine and rectum. Single fibres or bundles were present in the circular muscle layer and in a well-developed deep muscular plexus in the intestine and rectum. Immunoreactive nerve cells were found in the myenteric plexus of the stomach, intestine (neurotensin only) and rectum. Gastrin/CCK-like immunoreactivity was observed only in a few fibres in stomach and rectum.

Endocrine cells containing bombesin-, met-enkephalin-, gastrin/CCK-, neurotensin-, somatostatin- or substance P- like immunoreactivity were present in the mucosa.

The effect of bombesin was an inhibition of the rhythmic activity in circular muscle preparations and in longitudinal muscle from the rectum, while longitudinal muscle from the stomach usually responded with a weak increase in tonus. Neurotensin, like bombesin, was inhibitory on the spontaneous rhythmic activity of circular muscle throughout the gut, while the effect on longitudinal muscle was an increase in tonus. Met-enkephalin and substance P increased the tonus of all types of preparations, and often, in addition, initiated a rhythmic activity superimposed on this maintained tonus. VIP had a general inhibitory effect on the preparations, decreasing tonus and/or abolishing rhythmic activity.

It is concluded that bombesin-, neurotensin-, substance P- and VIP-like peptides are present in nerves throughout the urodele gut and may have physiological functions in regulating the motility of the gut. The gastrin/CCK-like peptide present in nerves of the stomach and rectum may affect the function of these parts of the gut. The regulatory peptides present in endocrine cells may, perhaps with the exception of the somatostatin-like peptide, affect the motility humorally.

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References

  • Andersson S, Rosell S, Hjelmquist U, Chang D, Folkers K (1977) Inhibition of gastric and intestinal motor activity by (Gln4) neurotensin. Acta Physiol Scand 100:231–235

    Google Scholar 

  • Baumgarten HG, Holstein A-F, Owman C (1970) Auerbach's plexus of mammals and man: Electron microscopic identification of three different types of neuronal processes in myenteric ganglia of the large intestine from rhesus monkeys, guinea-pigs and man. Z Zellforsch 106:376–397

    Google Scholar 

  • Bertaccini G, Impicciatore M, Molina E, Zappia L (1974) Action of bombesin on human gastrointestinal motility. Rend Gastroenterol 6:45–51

    Google Scholar 

  • Bishop AE, Polak JM, Bloom SR, Pearse AGE (1978) A new universal technique for the immunocytochemical localization of peptidergic innervation. J Endocrinol 77:25–26P

    Google Scholar 

  • Buchan AMJ, Polak JM, Pearse AGE (1980) Gut hormones in Salamandra salamandra. An immunocytochemical and electron microscopic investigation. Cell Tissue Res 211:331–343

    Google Scholar 

  • Buchan AMJ, Polak JM, Bryant MG, Bloom SR, Pearse AGM (1981) Vasoactive intestinal polypeptide (VlP)-like immunoreactivity in anuran intestine. Cell Tissue Res 216:413–422

    Google Scholar 

  • Burnstock G (1969) Evolution of the autonomic innervation of visceral and cardiovascular systems in vertebrates. Pharmacol Rev 21:247–324

    Google Scholar 

  • Burnstock G (1972) Purinergic nerves. Pharmacol Rev 24:509–581

    Google Scholar 

  • Burnstock G (1981) Review lecture: Neurotransmitters and trophic factors in the autonomic nervous system. J Physiol (London) 313:1–35

    Google Scholar 

  • Burnstock G, Hökfelt T, Gershon MD, Iversen LL, Kosterlitz HW, Szurszewski JH (1978) Non-adrenergic, non-cholinergic autonomic transmission mechanisms. Neurosci Res Prog Bull 17:377–519

    Google Scholar 

  • Carraway R, Ruane SE, Kim H-R (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 

  • Cocks T, Burnstock G (1979) Effects of neuronal polypeptides on intestinal smooth muscle; a comparison with non-adrenergic, non-cholinergic nerve stimulation. Eur J Pharmacol 54:251–259

    Google Scholar 

  • Coons AC (1956) Histochemistry with labelled antibody. Int Rev Cytol 5:1–23

    Google Scholar 

  • Corder R, Rees LH (1981) Endorphins and enkephalins. In: Bloom SR, Polak JM (eds) Gut hormones. Churchill Livingstone, Edinburgh London Melbourne, New York, pp 425–431

    Google Scholar 

  • Costa M, Buffa R, Furness JB, Solcia E (1980) Immunohistochemical localization of polypeptides in peripheral autonomic nerves using whole mount preparations. Histochemistry 65:157–169

    Google Scholar 

  • Dimaline R (1983) Is caerulein amphibian CCK? Peptides 4:457–462

    Google Scholar 

  • Dimaline R, Dockray GJ (1978) Multiple immunoreactive forms of vasoactive intestinal peptide in human colonic mucosa. Gastroenterology 75:387–392

    Google Scholar 

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

    Google Scholar 

  • Dockray GJ, Vaillant C Walsh JH (1979) The neuronal origin of bombesin-like immunoreactivity in the rat gastrointestinal tract. Neuroscience 4:1561–1568

    Google Scholar 

  • Dockray GJ, Williams RG, Zhu W-Y (1981) Development of region-specific antisera for the C-terminal tetrapeptide of gastrin/ cholecystokinin and their use in studies of immunoreactive form of cholecystokinin in rat brain. Neurochem Int 3:281–288

    Google Scholar 

  • El-Salhy M, 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 2:639–658

    Google Scholar 

  • El-Salhy M, Grimelius L, Wilander E, Abu-Sinna G, Lundqvist G (1981) Histological and immunohistochemical studies of endocrine cells of the gastrointestinal tract of the toad (Bufo regularis). Histochemistry 71:53–66

    Google Scholar 

  • Erspamer V, Melchiorri P (1973) Active polypeptides of the amphibian skin and their synthetic analogues. Pure Appl Chem 35:463–494

    Google Scholar 

  • Falkmer S, Elde RP, Hellerström C, Petersson B, Efendic S, Fohlman J, Siljevall JB (1977) Some phylogenetical aspects on the occurrence of somatostatin in the gastroenteropancreatic system. Arch Histol Jpn 40 (suppl):99–118

    Google Scholar 

  • Falkmer S, Elde RP, Hellerström C, Petersson B (1978) Phylogenetic aspects of somatostatin in the gastroenteropancreatic (GEP) endocrine system. Metabolism 27:1193–1196

    Google Scholar 

  • Falkmer S, Fahrenkrug J, Alumets J, Håkanson R, Sundler F (1980) Vasoactive intestinal polypeptide (VIP) in epithelial cells of the gut mucosa of an elasmobranchian cartilaginous fish, the ray. Endocrinol Jpn S.R. 27 (suppl 1):31–35

    Google Scholar 

  • Furness JB, Costa M (1980) Types of nerves in the enteric nervous system. Neuroscience 5:1–20

    Google Scholar 

  • Gibson RG, Mihaus AA, Colvin HW (1976) The search for submammalian gastrins: The identification of amphibian gastrin. Proc Soc Exp Biol Med 53:284–288

    Google Scholar 

  • Goodrich JT, Bernd P, Sherman D, Gershon MD (1980) Phylogeny of enteric serotonergic neurons. J Comp Neurol 190:15–28

    Google Scholar 

  • Hellström PM, Rosell S (1981) Effects of neurotensin, substance P and methionine-enkephaline on colonic motility. Acta Physiol Scand 113:147–154

    Google Scholar 

  • Holmgren S (1983) The effects of putative non-adrenergic, noncholinergic autonomic transmitters on isolated strips from the stomach of the rainbow trout, Salmo gairdneri. Comp Biochem Physiol 74C:229–238

    Google Scholar 

  • Holmgren S, Nilsson S (1983a) VIP-, bombesin-, and neurotensinlike immunoreactivity in neurons of the gut of the holostean fish, Lepisosteus platyrhincus. Acta Zool (Stockholm) 64:25–32

    Google Scholar 

  • Holmgren S, Nilsson S (1983b) 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 

  • Holmgren S, Vaillant C, Dimaline R (1982) VIP-, substance P-, gastrin/CCK-, bombesin-, somatostatinand glucagon-like immunoreactivities in the gut of the rainbow trout, Salmo gairdneri. Cell Tissue Res 223:141–153

    Google Scholar 

  • Holmgren S, Grove DJ, Nilsson S (1985) Substance P acts by releasing 5-hydroxytryptamine from enteric neurons in the stomach of the rainbow trout, Salmo gairdneri. Neuroscience 14:683–693

    Google Scholar 

  • Kitabgi P, Freychet P (1978) Effects of neurotensin on isolated intestinal smooth muscles. Eur J Pharmacol 50:349–357

    Google Scholar 

  • Kitabgi P, Vincent JP (1981) Neurotensin is a potent inhibitor of guinea-pig colon contractile activity. Eur J Pharmacol 74:311–318

    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 

  • Langley JN (1898) On the union of cranial autonomic (visceral) fibres with the nerve cells of the superior cervical ganglion. J Physiol (London) 23:240–270

    Google Scholar 

  • Langley JN (1921) The autonomic nervous system, part I. Heffer, Cambridge

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Larsson L-I, 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 

  • Lechago J, Holmquist AL, Rosenquist GL, Walsh JH (1978) Localization of bombesin-like peptides in frog gastric mucosa. Gen Comp Endocrinol 36:553–558

    Google Scholar 

  • Lundin K, Holmgren S (1984) Vasoactive intestinal polypeptidelike immunoreactivity and effects of VIP in the swimbladder of the cod, Gadus morhua. Comp Physiol 154B:627–633

    Google Scholar 

  • Lundin K, Holmgren S, Nilsson S (1984) Peptidergic functions in the dogfish rectum. Acta Physiol Scand 121:31A

    Google Scholar 

  • Mayer EA, Elashoff J, Walsh JH (1982) Characterization of bombesin effects on canine gastric muscle. Am J Physiol 243:G141-G147

    Google Scholar 

  • Nilsson S (1983) Autonomic nerve function in the vertebrates. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Noaillac-Depeyre J, Hollande E (1981) Evidence for 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

    Article  Google Scholar 

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

    Google Scholar 

  • Noorden S van, Patent GJ (1980) Vasoactive intestinal polypeptide-like immunoreactivity in nerves of the pancreatic islet of the teleost fish Gillichtys mirabilis. Cell Tissue Res 212:139–146

    Google Scholar 

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

    Google Scholar 

  • Pederson R, O'Dorisio T, Howe B, McIntosh C, Mueller M, Brown J, Cataland S (1981) Vagal release of IR-VIP and IR-gastrin from the isolated perfused rat stomach. Mol Cell Endocrinol 23:225–231

    Google Scholar 

  • Quirion R, Regoli D, Rioux F, St-Pierre S (1980) The stimulatory effects of neurotensin in rat stomach strips and guinea-pig atria. Br J Pharmacol 68:83–91

    Google Scholar 

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

    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 

  • Sakharov DA, Salimova NB (1980) Serotonin neurons in the peripheral nervous system of the larval lamprey, Lampetra planeri. A histochemical, micro-spectrofluorimetric and ultrastructural study. Zool Jb Physiol 84:231–239

    Google Scholar 

  • Schultzberg M, Hökfelt T, Nilsson G, Terenius L, Rehfeld JF, Brown M, Elde R, Goldstein M, Said S (1980) Distribution of peptideand catecholamine-containing neurons in the gastrointestinal tract of the rat and guinea-pig: Immunohistochemical studies with antisera to substance P, vasoactive intestinal polypeptide, enkephalins, somatostatin, gastrin/cholecystokinin, neurotensin and dopamine-β-hydroxylase. Neuroscience 5:689–744

    Article  CAS  PubMed  Google Scholar 

  • Seal A, Yamada T, Debas H, Hollinshead J, Osadchey B, Aponte G, Walsh J (1982) Somatostatin-14 and -28: clearance and potency on gastric function in dogs. Am J Physiol 243:G97-G102

    Google Scholar 

  • Thorndyke MC, Holmgren S, Nilsson S, Falkmer S (1984) Bombesin potentiation of the acetylcholine response in isolated strips of fish stomach. Regul Pept 9:350

    Google Scholar 

  • Vigna SR (1979) Distinction between cholecystokinin-like and gastrin-like biological activities extracted from gastrointestinal tissues of some lower vertebrates. Gen Comp Endocrinol 39:512–520

    Google Scholar 

  • Whittembury G, Sugino N, Solomon AK (1961) Ionic permeability and electrical potential differences in Necturus kidney cells. J Gen Physiol 44:689–712

    Google Scholar 

  • Williams JT, North RA (1979) Effects of endorphins on single myenteric neurons. Brain Res 165:57–65

    Google Scholar 

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Authors and Affiliations

  1. Department of Zoophysiology, University of Göteborg, Göteborg, Sweden

    Susanne Holmgren, Jörgen Jensen, Ann-Cathrine Jönsson, Kersti Lundin & Stefan Nilsson

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  1. Susanne Holmgren
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  2. Jörgen Jensen
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  3. Ann-Cathrine Jönsson
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  4. Kersti Lundin
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  5. Stefan Nilsson
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Holmgren, S., Jensen, J., Jönsson, AC. et al. Neuropeptides in the gastrointestinal canal of Necturus maculosus . Cell Tissue Res. 241, 565–580 (1985). https://doi.org/10.1007/BF00214577

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