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Functional and anatomical relationships between antral gastrin cells and gastrin-releasing peptide neurons

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Summary

The present studies were directed to examine the effect of gastrin-releasing peptide (GRP) on β-adrenergic stimulated gastrin release by cultured rat antral mucosa and to assess the anatomical relationship between gastrin cells and GRP nerves in rat and human antrum. Peptide-containing cells were identified by application of an avidinbiotin-peroxidase immunocytochemical double staining method utilizing antibodies to GRP and gastrin prepared in rabbits. Rat antral mucosa was cultured for 60 min and gastrin released into the culture medium was measured by radioimmunoassay. Inclusion of antibodies to GRP in culture medium did not affect carbachol-stimulated gastrin release, whereas isoproterenol-stimulated gastrin release into the medium was inhibited significantly by addition of GRP antiserum to the culture medium. GRP-containing neurons and axonal fibers were stained immunocytochemically with diaminobenzidine (reddish-brown specific staining) and were located in the lamina propria adjacent to and surrounding the main lobules of antral glands. After double staining utilizing 4-Cl-1-Naphthol as substrate, blue stained gastrin-containing cells were identified in the middle and deeper regions of antral glands in close proximity to GRP neuronal elements. These studies suggest that β-adrenergic, but not cholinergic, stimulation of gastrin release is mediated, at least in part, through GRP. They also demonstrate intimate anatomical, as well as functional, relationships between gastrin cells and GRP-containing neurons.

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References

  • Bertaccini G, Erspamer V, Melchiorri P, Sopranzin (1974) Gastrin release by bombesin in the dog. Br J Pharmacol 52:219–225

    PubMed  CAS  Google Scholar 

  • Brandsborg O, Brandsborg M, Christensen NJ (1975) Plasma adrenaline and serum gastrin: studies in insulin-induced hypoglycemia and after adrenaline infusions. Gastroenterology 58:455–460

    Google Scholar 

  • Buffa R, Solovieva I, Fiocca R, Giorgino S, Rindi G, Solcia E, Mochizuchi T, Yanaihara O, Yanaihara N (1982) Localization of bombesin and GRP (gastrin releasing peptide) sequences in gut nerves or endocrine cells. Histochemistry 76:457–467

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • DuVal JW, Saffouri B, Weir GC, Walsh JH, Arimura A, Makhlouf GM (1981) Stimulation of gastrin and somatostatin secretion from the isolated rat stomach by bombesin. Am J Physiol 241:G242-G247

    PubMed  CAS  Google Scholar 

  • Erlandsen SL, Orion DH, Parsons JA, McEvoy RC, Elde RP (1976) Pancreatic islet cell hormones: distribution of cell types in the islet and evidence for the presence of somatostatin and gastrin within the D cell. J Histochem Cytochem 24:883–897

    PubMed  CAS  Google Scholar 

  • Hayes JR, Ardill J, Kennedy TL, Shanks RG, Buchanan KD (1972) Stimulation of gastrin release by catecholamines. Lancet 1:819–821

    Article  PubMed  CAS  Google Scholar 

  • Hayes JR, Ardill J, Shanks RG, Buchanan KD (1978) Effect of catecholamines of gastrin release. Metabolism 27:385–391

    Article  PubMed  CAS  Google Scholar 

  • Hsu SM, Raine L, Fanger H (1981) The use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577–580

    PubMed  CAS  Google Scholar 

  • Inoue K, McKay D, Yajima H, Rayford PL (1983) Effect of synthetic porcine gastrin-releasing peptide on plasma levels of immunoreactive cholecystokinin, pancreatic polypeptide, and gastrin in dogs. Peptides 4:153–157

    Article  PubMed  CAS  Google Scholar 

  • Kondo H, Iwanaga T, Yanaihara N (1983) On the occurence of gastrin releasing peptide (GRP)-like immunoreactive nerve fibers in the celiac ganglion of rats. Brain Res 289:326–329

    Article  PubMed  CAS  Google Scholar 

  • Lowry OH, Rosebrough HJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Martindale R, Kauffman GL, Levin S, Walsh JH, Yamada T (1982) Differential regulation of gastrin and somatostatin secretion from isolated perfused rat stomachs. Gastroenterology 83:240–244

    PubMed  CAS  Google Scholar 

  • McDonald TJ, Jörvnall H, Nilsson G, Vagne M, Ghatei M, Bloom SR, Mutt V (1979) Characterization of a gastrin releasing peptide from porcine non-antral gastrin tissue. Biochem Biophys Res Commun 90:227–233

    Article  PubMed  CAS  Google Scholar 

  • McGuigan JE, Wolfe MM (1982) Gastrin radioimmunoassay. Clin Chem 28:368–373

    PubMed  CAS  Google Scholar 

  • Moghimzadeh E, Ekman R, Hakanson R, Yanaihara N, Sundler F (1983) Neuronal gastrin-releasing peptides in the mammalian gut and pancreas. Neuroscience 10:553–563

    Article  PubMed  CAS  Google Scholar 

  • Moody TW, Thoa NB, O'Donohue TL, Pert CB (1980) Bombesin-like peptides in rat brain: localization in synaptosomes and release from hypothalamic slices. Life Sci 26:1707–1712

    Article  PubMed  CAS  Google Scholar 

  • Nakane PK (1968) Simultaneous localization of multiple tissue antigens using the peroxidase-labeled antibody method: a study of pituitary glands of the rat. J Histochem Cytochem 16:557–560

    PubMed  CAS  Google Scholar 

  • Pappas TN, Hamel D, Debas HT, Taché Y (1984) Bombesin (BBS) in the dog brain to inhibit gastric acid secretion. Gastroenterology 86:1206 Abstr

    Google Scholar 

  • Pearse AGE (1968) Histochemistry; theoretical and applied. J & A Churchil, London

    Google Scholar 

  • Peters MN, Walsh JH, Ferrari J, Feldman M (1982) Adrenergic regulation of distention-induced gastrin release in humans. Gastroenterology 82:659–663

    PubMed  CAS  Google Scholar 

  • Schiller LR, Walsh JH, Feldman M (1980) Distention-induced gastrin release. Effects of luminal acidification and intravenous atropine. Gastroenterology 78:912–917

    PubMed  CAS  Google Scholar 

  • Schubert ML, Makhlouf GM (1982) Regulation of gastrin and somatostatin secretion by intramural neurons: effect of nicotinic receptor stimulation with dimethyl-phenylpiperazinium. Gastroenterology 83:626–632

    PubMed  CAS  Google Scholar 

  • Schubert ML, Bitar KN, Makhlouf GM (1982) Regulation of gastrin and somatostatin secretion by cholinergic and noncholinergic intramural neurons. Am J Physiol 243:G442-G447

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Solcia E, Capella C, Vassollo G, Buffa R (1975) Endocrine cells of the gastric mucosa. Int Rev Cytol 42:222–286

    Google Scholar 

  • Taché Y, Marki W, Rivier J, Vale W, Brown M (1981) Central nervous system inhibition of gastric secretion in the rat by gastrin-releasing peptide, a mammalian bombesin. Gastroenterology 81:298–302

    PubMed  Google Scholar 

  • Vandesande F, Dierickx K (1975) Identification of the vasopressin producing and of the oxytocin producing neurons in the hypothalamic magnocellular neurosecretory system of the rat. Cell Tissue Res 164:153–162

    Article  PubMed  CAS  Google Scholar 

  • Wolfe MM, McGuigan JE (1984) The immunochemical characterization of gastrinlike and cholecystokininlike peptides released in response to a peptone meal. Gastroenterology 87:323–334

    PubMed  CAS  Google Scholar 

  • Wolfe MM, Reel GM, McGuigan JE (1983) Inhibition of gastrin release by secretin is mediated by somatostatin in cultured rat antral mucosa. J Clin Invest 72:1586–1593

    Article  PubMed  CAS  Google Scholar 

  • Wolfe MM, Jain DK, Reel GM, McGuigan JE (1984) Effects of carbachol on gastrin and somatostatin release in rat antral tissue culture. Gastroenterology 87:86–93

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Medicine, University of Florida College of Medicine, Box J-277, JHMHC, 32610, Gainesville, Florida, USA

    D. K. Jain,  M. M. Wolfe (recipient of Clinical Investigator Award AM 00147 from the National Institutes of Health and the AGA/Pharmacia Research Scholar Award) & J. E. McGuigan

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  1. D. K. Jain
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  2. M. M. Wolfe
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  3. J. E. McGuigan
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These studies were supported by Grant AM 13711 from the National Institutes of Health

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Jain, D.K., Wolfe, M.M. & McGuigan, J.E. Functional and anatomical relationships between antral gastrin cells and gastrin-releasing peptide neurons. Histochemistry 82, 463–467 (1985). https://doi.org/10.1007/BF02450481

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