Summary
It has long been disputed whether mammalian enterochromaffin (EC-) cells contain a peptide in addition to serotonin. Previous immunohistochemical studies have provided evidence for the presence of enkephalins in EC-cells. These findings, however, are equivocal. Therefore, the problem of opioid peptides in EC-cells has been re-examined in the gastro-intestinal mucosa of dog, guinea-pig and man. A battery of antisera against derivatives of pro-opiomelanocortin, pro-enkephalin and pro-dynorphin have been applied to semithin serial sections of the tissues, in combination with fluorescence histochemistry and serotonin immunocytochemistry. Our findings indicate that EC-cells of the investigated species contain pro-dynorphin-related peptides, i.e. dynorphin A and α-neo-endorphin, but no derivatives from pro-opiomelanocortin or pro-enkephalin. Since remarkable interspecies variations occur with respect to the number and staining characteristics of opioid immunoreactive EC-cells, it is concluded that pro-dynorphin shows specific routes of post-translational processing depending upon the species and the gastro-intestinal segment investigated. Future studies should focus on the mutual relationships between serotonin and dynorphins and on the physiological significance of these peptides in the gastrointestinal tract.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alumets J, Håkanson R, Sundler F, Chang K-J (1978) Leu-enkephalin-like material in nerves and enterochromaffin cells in the gut. Histochemistry 56:187–196
Barrett RW, Goldstein A (1985) A monoclonal antibody specific for a dynorphin precursor. Neuropeptides 6:113–120
Björklund A, Falck B, Owman Ch (1972) Fluorescence microscopic and microspectrofluorometric techniques for the cellular localization and characterization of biogenic amines. In: Rall JE, Kopin IJ (eds) Methods in investigative and diagnostic endocrinology. Vol I, North Holland, Amsterdam, pp 318–368
Cetin Y, Aunis D, Grube D (1985) Gastro-intestinal enterochromaffin cells: colocalization of serotonin, pro-dynorphin-derived peptides, and chromogranin A. Regul Pept [Abstr] 13:94
Costa M, Furness JB, Gibbins LI (1986) Chemical coding for enteric neurons. Prog Brain Res 68:217–239
De Mey J (1983) Colloidal gold probes in immunocytochemistry. In: Polak JM, Van Noorden S (eds) Immunocytochemistry, practical applications in pathology and biology. Wright-PSG, Bristol London Boston, pp 82–112
Erlandsen SL (1980) Types of pancreatic islet cells and their immunocytochemical identification. In: Fitzgerald PJ, Morrison AB (eds) The pancreas. Williams and Wilkins, Baltimore, pp 140–155
Falck B, Hillarp N-Å, Thieme G, Torp A (1962) Fluorescence of catecholamines and related compounds condensed with formaldehyde. J Histochem Cytochem 10:348–354
Fujita T (1977) Concept of paraneurons. Arch Histol Jpn 40 (Suppl):1–12
Grube D (1980) Immunoreactivities of gastrin (G-) cells. II. Nonspecific binding of immunoglobulins to G-cells by ionic interactions. Histochemistry 66:149–167
Grube D, Kusumoto Y (1986) Serial semithin sections in immunohistochemistry: techniques and applications. Arch Histol Jpn 49:391–410
Grube D, Weber E (1980) Immunoreactivities of gastrin (G-) cells. I. Dilution-dependent staining of G-cells by antisera and nonimmune sera. Histochemistry 65:223–237
Grube D, Aunis D, Bader F, Cetin Y, Jörns A, Yoshie S (1986) Chromogranin A (CGA) in the gastro-entero-pancreatic (GEP) endocrine system. I. CGA in the mammalian endocrine pancreas. Histochemistry 85:441–452
Höllt V (1983) Multiple endogenous opioid peptides. Trends Neurosci 6:24–26
Höllt V, Grimm C, Haarmann I, Seizinger BR, Herz A (1981) Substantial amounts of immunoreactive BAM-12P and BAM-22P are present in bovine adrenal medulla but not in the brain. In: Takagi T, Simon EJ (eds) Advances in endogenous and exogenous opioids. Elsevier/North Holland, Amsterdam, pp 152–154
Höllt V, Haarmann I, Grimm C, Herz A, Tulunay FC, Loh HH (1982) Pro-enkephalin intermediates in bovine brain and adrenal medulla: characterization of irnmunoreactive peptides related to BAM-22P and peptide F. Life Sci 31:1883–1886
Khachaturian H, Sherman TG, Lloyd RV, Civelli O, Douglass J, Herbert E, Akil H, Watson SJ (1986) Pro-dynorphin is endogenous to the anterior pituitary and is co-localized with LH and FSH in the gonadotrophs. Endocrinology 119:1409–1411
Lemaire S, Chouinard L, Denis D, Panico M, Morris HR (1982) Mass spectrometric identification of various molecular forms of dynorphin in bovine adrenal medulla. Biochem Biophys Res Commun 108:51–58
Mains RE, Eipper BA, Ling N (1977) Common precursor to corticotropins and endorphins. Proc Natl Acad Sci USA 74:3014–3018
Majeed NH, Lasoń W, Przewłocka B, Przewłocki R (1985) Differential regulation of the brain and gut immunoreactive dynorphin by the serotonin system. Life Sci 37:339–343
Maysinger D, Höllt V, Seizinger BR, Mehraein P, Pasi A, Herz A (1982) Parallel distribution of immunoreactive α-neo-endorphin and dynorphin in rat and human tissue. Neuropeptides 2:211–225
Millan MJ, Herz A (1985) The endocrinology of the opioids. Int Rev Neurobiol 26:1–83
Nihei K, Iwanaga T, Yanaihara N, Mochizuki T, Fujita T (1983) Preproenkephalin A occurs in the enterochromaffin (EC) cells of the porcine intestine: an immunocytochemical study using antisera to Met-enkephalin-Arg-Gly-Leu and to serotonin. Biomed Res 4:393–398
Nilsson G, Larsson L-I, Håkanson R, Brodin E, Pernow B, Sundler F (1975) Localization of substance P-like immunoreactivity in mouse gut. Histochemistry 43:97–99
Nilsson O, Ericson LE, Dahlström A, Ekholm R, Steinbusch HWM, Ahlman H (1985) Subcellular localization of serotonin immunoreactivity in rat enterochromaffin cells. Histochemistry 82:351–355
Pearse AGE (1969) 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
Pearse AGE, Polak JM (1975) Immunocytochemical localization of substance P in mammalian intestine. Histochemistry 41:373–375
Pearse AGE, Polak JM, Bloom SR, Adams C, Dryburgh JR, Brown JC (1974a) Enterochromaffin cells of the mammalian small intestine as the source of motilin. Virchows Arch [B] C 16:111–120
Pearse AGE, Polak JM, Adams C, Kendall PA (1974b) Diethylpyrocarbonate, a vapour-phase fixative for immunofluorescence studies on polypeptide hormones. Histochem J 6:347–352
Scopsi L, Wang B-L, Larsson L-I (1986) Nonspecific immunocytochemical reactions with certain neurohormonal peptides and basic peptide sequences. J Histochem Cytochem 34:1469–1475
Seizinger BR, Grimm C, Herz A (1984) Evidence for a differential postnatal development of proenkephalin B (= prodynorphin)derived opioid peptides in the rat hypothalamus. Endocrinology 115:926–935
Solcia E, Capella C, Buffa R, Frigerio B (1976) Histochemical and ultrastructural studies on the argentaffin and argyrophil cells of the gut. In: Coupland RE, Fujita T (eds) Chromaffin, enterochromaffin and related cells. Elsevier, Amsterdam, pp 209–225
Solcia E, Polak JM, Larsson L-I, Buchan AMJ, Capella C (1981) Update on Lausanne classification of endocrine cells. In: Bloom SR, Polak JM (eds) Gut hormones. 2nd ed. Churchill Livingstone, London, pp 98–100
Spampinato S, Goldstein A (1983) Immunoreactive dynorphin in rat tissues and plasma. Neuropeptides 3:193–212
Stern AS, Wurzburger RJ, Barkey R, Spector S (1982) Opioid polypeptides in guinea-pig pancreas. Proc Natl Acad Sci USA 79:6703–6706
Sternberger LA (1979) Immunocytochemistry. 2nd ed, John Wiley, New York
Sundler F, Håkanson R, Loren I, Lundquist I (1980) Amine storage and function in peptide hormone-producing cells. Invest Cell Pathol 3:87–103
Tachibana S, Araki K, Ohya S, Yoshida S (1982) Isolation and structure of dynorphin, an opioid peptide, from porcine duodenum. Nature (London) 295:339–340
Watson SJ, Akil H, Khachaturian H, Young E, Lewis ME (1984) Opioid systems: anatomical, physiological and clinical perspectives. In: Hughes J, Collier HOJ, Rance MJ, Tyers MB (eds) Opioids — past, present and future. Taylor and Francis, London, Philadelphia, pp 145–178
Weber E, Evans C, Barchas JD (1982) Predominance of the aminoterminal octapeptide fragment of dynorphin in rat brain regions. Nature (London) 299:77–79
Weihe E, Hartschuh W, Weber E (1985) Prodynorphin opioid peptides in small somatosensory primary afferents of guinea-pig. Neurosci Lett 58:347–352
Wolter HJ (1985) Colocalization of dynorphin-A (1–17) and dynorphin-A (1–8) within some perikarya of rat duodenum: immunohistochemical evidence for the presence of two separate dynorphinergic systems. Biochem Biophys Res Commun 130:774–780
Zamboni L, De Martino C (1967) Buffered picric acid formaldehyde, a new, rapid fixative for electron microscopy. J Cell Biol 35:148A
Zamir N, Palkowitz M, Weber E, Mezey E, Brownstein MJ (1984) A dynorphinergic pathway of Leu-enkephalin production in substantia nigra. Nature (London) 307:643–645
Author information
Authors and Affiliations
Additional information
Part of the results were presented at the Bayliss and Starling Society National Scientific Meeting 1985, London (Cetin et al. 1985)
Rights and permissions
About this article
Cite this article
Cetin, Y. Enterochromaffin (EC-) cells of the mammalian gastro-entero-pancreatic (GEP) endocrine system: cellular source of pro-dynorphin-derived peptides. Cell Tissue Res. 253, 173–179 (1988). https://doi.org/10.1007/BF00221752
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00221752