Summary
Paneth cells located at the bottom of intestinal crypts may play a role in controlling the bacterial milieu of the intestine. Using morphometry to clarify the secretory mechanism of the Paneth cells, we studied the ultrastructural changes in mouse Paneth cells produced following intra-arterial perfusion with Hanks' balanced salt solution containing a cholinergic muscarinic secretagogue (bethanechol), a neuroblocking agent (tetrodotoxin), or a G-protein activator (NAF/AlCl3). Bethanechol (2×10-4 mol/l) induced Paneth-cell secretion. Many Paneth cells massively exocytosed their secretory material into the crypt lumen; the enhanced secretion caused degranulation and vacuole formation. However, tetrodotoxin (2×10-6 mol/l) did not prevent the bethanechol-enhanced secretion by the Paneth cells. NaF (1×10-2 mol/l) and AlCl3 (1×10-5 mol/l) induced massive exocytosis of the Paneth cells; the exocytotic figures were similar to those observed in mice stimulated by bethanechol. G-protein activation was followed by a sequence of intracellular events, resulting in exocytosis.
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References
Ahonen A, Penttilä A (1975) Effects of fasting and feeding and pilocarpine on Paneth cells of the mouse. Scand J Gastroenterol 10:347–352
Balas D, Senegas F, Frexinos J, Pradayrol L, Broussy J, Ribet A (1974) Action des hormones digestives sur la muqueuse jéjunale et iléale chez la souris et le hamster. Étude histophysiologique. Biol Gastroenterol 7:187–199
Basbaum CB, Ueki I, Brezina L, Nadel JA (1981) Tracheal submucosal gland serous cells stimulated in vitro with adrenergic and cholinergic agonists: a morphometric study. Cell Tissue Res 220:481–498
Batzri S, Amsterdam A, Selinger Z, Ohad I, Schramm M (1971) Epinephrine-induced vacuole formation in parotid gland cells and its independence of the secretory process. Proc Natl Acad Sci USA 68:121–123
Bigay J, Deterre P, Pfister C, Chabre M (1985) Fluoroaluminates activate transducin-GDP by mimicking the γ-phosphate of GTP in its binding site. FEBS Lett 191:181–185
Birnbaumer L, Abramowitz J, Brown AM (1990) Receptor-effector coupling by G proteins. Biochim Biophys Acta 1031:163–224
Brom C, Brom J, König W (1991) G protein activation and mediator release from human neutrophils and platelets after stimulation with sodium fluoride and receptor-mediated stimuli. Immunology 73:287–292
Chung LP, Keshav S, Gordon S (1988) Cloning the human lysozyme cDNA: inverted Alu repeat in the mRNA and in situ hybridization for macrophages and Paneth cells. Proc Natl Acad Sci USA 85:6227–6231
Cordier R (1923) Contribution à l'étude de la cellule de Ciaccio-Masson et de la cellule de Paneth. C R Soc Biol (Paris) 88:1227–1230
Elferink JGR, Alsbach EJJ, Riemersma JC (1980) The interaction of fluoride with rabbit polymorphonuclear leukocytes: induction of exocytosis and cytolysis. Biochem Pharmacol 29:3051–3057
Erlandsen SL, Chase DG (1972a) Paneth cell function: phagocytosis and intracellular digestion of intestinal microorganisms. I. Hexamita muris. J Ultrastruct Res 41:296–318
Erlandsen SL, Chase DG (1972b) Paneth cell function: phagocytosis and intracellular digestion of intestinal microorganisms. II. Spiral microorganism. J Ultrastruct Res 41:319–333
Erlandsen SL, Parsons JA, Taylor TD (1974) Ultrastructural immunocytochemical localization of lysozyme in the Paneth cells of man. J Histochem Cytochem 22:401–413
Erlandsen SL, Rodning CB, Montero C, Parsons JA, Lewis EA, Wilson ID (1976) Immunocytochemical identification and localization of immunoglobulin A within Paneth cells of the rat small intestine. J Histochem Cytochem 24:1085–1092
Furness JB, Costa M (1987) The enteric nervous system. Churchill Livingstone, Edinburgh London Melbourne
Gomperts BD (1990) GE: a GTP-binding protein mediating exocytosis. Annu Rev Physiol 52:591–606
Habara Y, Satoh Y, Saito T, Kanno T (1990) A G-protein activator, NaF, induces [Ca2+]o-dependent [Ca2+]c oscillation and secretory response in rat pancreatic acini. Biomed Res 11:389–398
Hally AD (1958) The fine structure of the Paneth cell. J Anat 92:268–277
Hughes BP, Barritt GJ (1987) The stimulation by sodium fluoride of plasma-membrane Ca2+ inflow in isolated hepatocytes. Evidence that a GTP-binding regulatory protein is involved in the hormonal stimulation of Ca2+ inflow. Biochem J 245:41–47
Kanno T, Matsumoto T, Mori M, Oyamada M, Nevalainen TJ (1984) Secretion prevents hyporeactive and morphological responses of rat pancreatic acinar cells to stimulation with supraoptimal concentration of cholecystokinin-octapeptide. Biomed Res 5:355–370
Klockars M (1974) Concentration and immunohistochemical localization of lysozyme in germ-free and conventionally reared rats. Acta Pathol Microbiol Scand [A] 82:675–682
Knight DE, Grafenstein H, Athayde CM (1989) Calcium-dependent and calcium-independent exocytosis. Trend Neurosci 12:451–458
Kraal B, Graaf JM de, Mesters JR, Hoof PJM van, Jacquet E, Parmeggiani A (1990) Fluoroalminates do not affect the guanine-nucleotide binding centre of the peptide chain elongation factor EF-Tu. Eur J Biochem 192:305–309
Kurosumi K, Shibuichi I, Tosaka H (1981) Ultrastructural studies on the secretory mechanism of goblet cells in the rat jejunal epithelium. Arch Histol Jpn 44:263–284
Masty J, Stradley RP (1991) Paneth cell degranulation and lysozyme secretion during acute equine alimentary laminitis. Histochemistry 95:529–533
Matozaki T, Sakamoto C, Nagao M, Nishizaki H, Baba S (1988) G protein in stimulation of PI hydrolysis by CCK in isolated rat pancreatic acinar cells. Am J Physiol 255:E652-E659
McNabb PC, Tomasi TB (1981) Host defense mechanisms at mucosal surfaces. Annu Rev Microbiol 35:477–496
Mertz LM, Horn VJ, Baum BJ, Ambudkar IS (1990) Calcium entry in rat parotid acini: activation by carbachol and aluminium fluoride. Am J Physiol 258:C654-C661
Mürer EH, Davenport K, Siojo E, Day HJ (1981) Metabolic aspects of the secretion of stored compounds from blood platelets. The effect of NaF at different pH on nucleotide metabolism and function of washed platelets. Biochem J 194:187–192
Neutra MR, O'Malley LJ, Specian RD (1982) Regulation of intestinal goblet cell secretion. II. A survey of potential secretagogues. Am J Physiol 242:G380-G387
Olson RE, Erlandsen SL (1981) Paneth cell function: the effects of cholinergic and adrenergic drugs on lysozyme secretion. Anat Rec 199:186A
Otto HF (1974) Die intestinale Paneth-Zelle. Fischer, Stuttgart
Otto HF, Lewerenz I (1973) Untersuchungen zur Ultrastruktur des Dünndarms keimfrei aufgezogener FW 49-Ratten 1. Epitheliale Befunde unter besonderer Berücksichtigung der Paneth-Zellen. Virchows Arch [A] 360:235–251
Ouellette AJ, Greco RM, James M, Frederick D, Naftilan J, Fallon JT (1989) Developmental regulation of cryptdin, a corticostatin/defensin precursor mRNA in mouse small intestinal crypt epithelium. J Cell Biol 108:1687–1695
Paneth J (1888) Über die secernierenden Zellen des Dünndarmepithels. Arch Mikrosk Anat 31:113–191
Ritchie JM, Green NM (1985) Local anesthetics. In: Gilman AG, Goodman LS, Rall TW, Murad F (eds) Goodman and Gilman's the pharmacological basis of therapeutics, 7th edn. Macmillan, New York, pp 302–321
Rodning CB, Wilson ID, Erlandsen SL (1976) Immunoglobulins within human small intestinal Paneth cells. Lancet I:984–987
Rodning CB, Erlandsen SL, Wilson ID, Carpenter A-M (1982) Light microscopic morphometric analysis of rat ileal mucosa. II. Component quantitation of Paneth cells. Anat Rec 204:33–38
Saito H, Kasajima T, Masuda A, Imai Y, Ishikawa M (1988) Lysozyme localization in human gastric and duodenal epithelium. An immunocytochemicla study. Cell Tissue Res 251:307–313
Satoh Y (1984) Ultrastructure of Paneth cells in germ-free rats, with special reference to the secretory granules and lysosomes. Arch Histol Jpn 47:293–301
Satoh Y (1988a) Effect of live and heat-killed bacteria on the secretory activity of Paneth cells in germ-free mice. Cell Tissue Res 251:87–93
Satoh Y (1988b) Atropine inhibits the degranulation of Paneth cells in ex-germ-free mice. Cell Tissue Res 253:397–402
Satoh Y, Vollrath L (1986) Quantitative electron microscopic observations on Paneth cells of germfree and ex-germfree Wistar rats. Anat Embryol (Berl) 173:317–322
Satoh Y, Ishikawa K, Ono K, Vollrath L (1986a) Quantitative light microscopic observations on Paneth cells of germfree and ex-germfree Wistar rats. Digestion 34:115–121
Satoh Y, Ishikawa K, Tanaka H, Ono K (1986b) Immunohistochemical observations of immunoglobulin A in the Paneth cells of germ-free and formely-germ-free rats. Histochemistry 85:197–201
Satoh Y, Ishikawa K, Tanaka H, Oomori Y, Ono K (1988) Immunohistochemical observations of lysozyme in the Paneth cells of specific-pathogen-free and germ-free mice. Acta Histochem (Jena) 83:185–188
Satoh Y, Ishikawa K, Oomori Y, Yamano Y, Ono K (1989) Effects of cholecystokinin and carbamylcholine on Paneth cell secretion in mice: a comparison with pancreatic acinar cells. Anat Rec 225:124–132
Satoh Y, Ishikawa K, Oomori Y, Ono K (1991) Effect of sodium fluoride on Paneth cells, goblet cells, and exocrine pancreatic acinar cells in mice (abstract). Acta Anat Nippon 66:368
Scheele G, Adler G, Kern H (1987) Exocytosis occurs at the lateral plasma membrane of the pancreatic acinar cell during supramaximal segretagogue stimulation. Gastroenterology 92:345–353
Schwalbe G (1872) Beiträge zur Kenntnis der Drüsen in den Darmwandungen, insbesondere der Brunner'schen, Drüsen. Arch Mikrosk Anat 8:92–140
Senegas-Balas F, Balas D, Pradayrol L, Laval J, Ribet A (1979) Comparative effects of CCK-PZ on certain intestinal hydrolases in the mucosa and in the luminal content of hamster jejunoileum. Acta Hepato-gastroenterol 26:486–492
Shuttleworth TJ (1990) Fluoroalminate activation of different components of the calcium signal in an exocrine cell. Biochem J 269:417–422
Sorimachi M, Nishimura S, Yamagami K, Yada T (1990) Histamine release by calcium from fluoride-activated rat mast cells: possible involvement of CaF2 formation. Med J Kagoshima Univ 42:11–21
Specian RD, Neutra MR (1982) Regulation of intestinal goblet cell secretion. I. Role of parasympathetic stimulation. Am J Physiol 242:G370-G379
Speece AJ (1964) Histochemical distribution of lysozyme activity in organs of normal mice and radiation chimeras. J Histochem Cytochem 12:384–391
Stadel JM, Crooke ST (1989) Fluoride interaction with G-proteins. Biochem J 258:932–933
Staley MW, Trier JS (1965) Morphologic heterogeneity of mouse Paneth cell granules before and after secretory stimulation. Am J Anat 117:365–384
Sternweis PC, Gilman AG (1982) Aluminium: a requirement for activation of the regulatory component of adenylate cyclase by fluoride. Proc Natl Acad Sci USA 79:4888–4891
Tojyo Y, Tanimura A, Matsui S, Matsumoto Y, Sugija H, Furuyama S (1991) NaF-induced amylase release from rat parotid cells is mediated by PI breakdown leading to Ca2+ mobilization. Am J Physiol 260:C194-C200
Watanabe O, Baccino FM, Steer ML, Meldolesi J (1984) Supraximal caerulein stimulation and ultrastructure of rat pancreatic acinar cell: early morphological changes during development of experimental pancreatitis. Am J Physiol 246:G457-G467
Zeng YY, Benishin CG, Pang PKT (1989), Guanine nucleotide binding proteins may modulate gating of calcium channels in vascular smooth muscle. I. Studies with fluoride. J Pharmacol Exp Ther 250:343–351
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Satoh, Y., Ishikawa, K., Oomori, Y. et al. Bethanechol and a G-protein activator, NaF/AlCl3, induce secretory response in Paneth cells of mouse intestine. Cell Tissue Res 269, 213–220 (1992). https://doi.org/10.1007/BF00319611
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DOI: https://doi.org/10.1007/BF00319611