Role and mechanisms of action of acetylcholine in the regulation of rat cholangiocyte secretory functions

Journal of Clinical Investigation

Volumn 100, Issue 6, 1997, Pages 1349-1362

  Alvaro, D ^a,d   Alpini, G ^b   Jezequel, A M ^c   Bassotti, C ^c   Francia, C ^a   Fraioli, F ^a   Romeo, R ^a   Marucci, L ^c   Le Sage, G ^b   Glaser, S S ^b   Benedetti, A ^c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b TEXAS A AND M UNIVERSITY   (United States)

^c UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^d NONE   (Italy)

Author keywords

Acetylcholine; Adenylyl cyclase; Ca2+; Calcineurin; cAMP; Secretin

Indexed keywords

1 (2 CHLOROETHYL) 4 DIPHENYLACETOXYPIPERIDINE; ACETYLCHOLINE; ADENYLATE CYCLASE; BICARBONATE; CALCINEURIN; CHLORIDE; CHOLINERGIC RECEPTOR; CYCLIC AMP; CYCLOSPORIN A; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; PROTEIN KINASE C; RECEPTOR SUBTYPE; SECRETIN; STAUROSPORINE; TACROLIMUS;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BILE DUCT; CELL PH; CONTROLLED STUDY; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 0030844035     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119655     Document Type: Article

References (66)

1. Roberts, S.K., and N.F. LaRusso. 1994. Pathobiology of biliary epithelia. Curr. Opin. Gastroenterol. 10:526-533.
2. Boyer, J.L. 1996. Bile duct epithelium: frontiers in transport physiology. Am. J. Physiol. 270:G1-G5.
3. Alpini, G., I.O. Phillips, and N.F. LaRusso. 1994. The biology of biliary epithelia. In The Liver: Biology and Pathobiology. I.M. Arias, N. Fausto, W.B. Jacoby, D.A. Schachter, and D.A. Shafritz, editors. Raven Press, Ltd., New York. 623-653.
4. Alvaro, D., W.K. Cho, A. Mennone, and J.L. Boyer. 1993. Effect of secretin on intracellular pH regulation in isolated rat bile duct epithelial cells. J. Clin. Invest. 92:1314-1325.
5. Cho, W.K., A. Mennone, and J.L. Boyer. 1995. Effect of bombesin on secretion in isolated polarized intrahepatic bile ductular units (IBDU). Gastroenterology. 108:A1049.
6. Cho, W.K., A. Mennone, S.A. Rydberg, and J.L. Boyer. 1995. VIP is a potent stimulus of bicarbonate and fluid secretion in bile ducts. Hepatology. 22: A294.
7. Tietz, P.S., G. Alpini, L.D. Pham, and N.F. LaRusso. 1995. Somatostatin inhibits secretin-induced ductal hypercholeresis and exocytosis by cholangiocytes. Am. J. Physiol. 269:G110-G118.
8. Glaser, S.S., R. Rodgers, J. Phinizy, W.E. Robertson, J. Lasater, G. LeSage, and G. Alpini. 1996. Gastrin inhibits secretin-induced hypercholeresis in the bile duct ligated rat liver through the cAMP system. Gastroenterology. 110:1197.
9. Walsh, J.H., and E.A. Mayer. 1993. Gastrointestinal hormones. In Gastrointestinal Disease, 5th Ed. M.H. Sleisenger and J.S. Fordtran, editors. W.B. Saunders Company Ltd., London. 18-44.
10. Walsh, J.H. Gastrointestinal hormones and peptides. 1981. In Physiology of the Gastrointestinal Tract. L.R. Johnson, editor. Raven Press, Ltd., New York. 59-144.
11. Tanturi, C.A., and A.C. Ivy. 1938. On the existence of secretory nerves in the vagi for and the reflex excitation and inhibition of bile secretion. Am. J. Physiol. 121:270-283.
12. Kaminski, D.L., J. Dorighi, and M. Jellinek. 1994. Effect of electrical vagal stimulation on canine hepatic bile flow. Effect of electrical vagal stimulation on canine hepatic bile flow. Am. J. Physiol. 227:487-493.
13. Pass, M., and T. Heath. 1976. Effect of electrical stimulation of the vagus nerves on bile secretion in anaesthetized sheep. Aust. J. Biol. Sci. 29:351-355.
14. Nahrwold, D.L., D.L. Kaminski, and R.C. Rose. 1972. Cholinergic control of bile flow and composition. Physiologist. 15:224.
15. Frizzel, R.A., and A.P. Morris. 1994. Chloride conductance of salt-secreting epithelial cells. In Current Topics in Membranes. Academic Press, Inc., Orlando. 42:173-214.
16. Larsson, O., and L. Olgart, 1989. The enhancement of carbachol-induced salivary secretion by VIP and CGRP in rat parotid gland is mimicked by forskolin. Acta Physiol. Scand. 137:231-236.
17. Sato, K., and F. Sato. 1981. Role of calcium in cholinergic and adrenergic mechanisms of eccrine sweat secretion. Am. J. Physiol. 241:C113-C120.
18. 2+ signaling in rat bile duct epithelia. Am. J. Physiol. 271:G86-G96.
19. Mennone, A., D. Alvaro, W. Cho, and J.L. Boyer. 1995. Isolation of small polarized bile duct units. Proc. Natl. Acad. Sci. USA. 92:6527-6531.
20. Benedetti, A., L. Marucci, C. Bassotti, R. Mancini, S. Contucci, A.M. Jezequel, and F. Orlandi. 1993. Tubulo-vesicular transcytotic pathway in rat biliary epithelium: a study in perfused liver and in isolated intrahepatic bile duct. Hepatology. 18:422-432.
21. Andre, C., J.B. DeBacker, J.P. Guillet, J.C. Venderheyden, P. Vauquelin, and A.D. Strosberg. 1983. Purification of muscarinic acetylcholine receptors by affinity chromatography. EMBO (Eur. Mol. Biol. Organ.) J. 2:499-504.
22. Andre, C., J.P. Guillet, J.P. DeBacker, J.G. Venderheyden, J. Hoebeke, and A.D. Strosberg. 1984. Monoclonal antibodies against the native or denaturated forms of muscarinic acetylcholine receptor. EMBO (Eur. Mol. Biol. Organ.) J. 3:17-21.
23. Andre, C., S. Marullo, J.G. Guillet, A. Convents, M. Lauwereys, S. Kaveri, J. Hoebeke, and A.D. Strosberg. 1987. Immunochemical studies of the muscarinic acetylcholine receptor. J. Recept. Res. 7:65-107.
24. Takahashi, T., J.M. Lasker, A.S. Rosman, and C.S. Lieber. 1993. Induction of cytochrome P-4502E1 in the human liver by ethanol is caused by a corresponding increase in encoding messenger RNA. Hepatology. 17:236-245.
25. Alvaro, D., P. Della Guardia, A. Bini, A. Gigliozzi, S. Furfaro, T. La Rosa, C. Piat, and L. Capocaccia. 1995. Effect of glucagon on intracellular pH regulation in isolated rat hepatocyte couplets. J. Clin. Invest. 96:665-675.
26. Alvaro, D., A. Mennone, and J.L. Boyer. 1993. Effect of ursodeoxycholic acid on intracellular pH regulation in isolated rat bile duct epithelial cells. Am. J. Physiol. 265:G783-G791.
27. Ishii, M., B. Vroman, and N.F. LaRusso. 1989. Isolation and morphologic characterization of bile duct epithelial cells from normal rat liver. Gastroenterology. 97:1236-1247.
28. Alpini, G., S. Roberts, J. Phinizy, W. Robertson, S. Gubba, O. Colegio, G. LeSage, and N.F. LaRusso. 1995. Heterogeneity of the proliferative capacity of rat cholangiocytes. Gastroenterology. 1098:A1025. (Abstr.)
29. LeSage, G., S.S. Glaser, S. Gubba, W.E. Robertson, J.L. Phinizy, J. Lasater, R.E. Rodgers, and G. Alpini. 1996. Regrowth of the rat biliary tree after 70% partial hepatectomy is coupled to increased secretin-induced ductal secretion. Gastroenterology. 111:1633-1644.
30. Alpini, G., G.D. Ulrich, J.O. Phillips, L.D. Pham, L.J. Miller, and N.F. LaRusso. 1994. Upregulation of secretin receptor gene expression in rat cholangiocytes after bile ligation. Am. J. Physiol. 266:G922-G928.
31. Alpini, G., S.K. Roberts, S.M. Kuntz, Y. Ueno, S. Gubba, P. Podila, G. LeSage, and N.F. LaRusso. 1996. Morphological, molecular and functional heterogeneity of cholangiocytes from normal rat liver. Gastroenterology. 110:1636-1643.
32. Rutemburg, A.M., H. Kim, J.W. Fischbein, J.S. Hanker, H.L. Wasserkrug, and A.M. Seligman. 1969. Histochemical and ultrastructural demonstration of gamma-glutamyl transpeptidase activity. J. Histochem. Cytochem. 17:517-526.
33. Alpini, G., R. Lenzi, L. Sarkozi, and N. Tavoloni. 1988. Biliary physiology in rats with bile ductular cell hyperplasia. Evidence for a secretory function of proliferated bile ductules. J. Clin. Invest. 81:569-578.
34. Alpini, G., R. Lenzi, W.R. Zhai, M.H. Liu, P.A. Slott, F. Paronetto, and N. Tavoloni. 1989. Isolation of a nonparenchymal liver cell fraction enriched in cells with biliary epithelial phenotypes. Gastroenterology. 97:1248-1260.
35. Bonner, T., N. Buckely, A. Young, and M. Brann. 1987. Identification of a family of muscarinic acetylcholine genes. Science (Wash. DC). 237:527-532.
36. Peralta, E.G., J.W. Winslow, G.L. Peterson, D.H. Smith, A. Ashkenazi, J. Ramachandran, M.I. Schimerlik, and D.J. Capon. 1987. Primary structure and biochemical properties of an M2 muscarinic receptor. Science (Wash. DC). 236:600-606.
37. Elsing, C., C. Hübner, B.A. Fitscher, A. Kassner, and W. Stremmel. 1997. Muscarinic acetylcholine receptor stimulation of biliary epithelial cells and its effect on bile secretion in the isolated perfused rat liver. Hepatology. 25: 804-813.
38. Calnek, D., and A. Quaroni. 1993. Differential localization by in situ hybridization of distinct keratin mRN A species during intestinal epithelial cell development and differentiation. Differentiation. 53:95-104.
39. Kato, A., G.J. Gores, and N.F. LaRusso. 1992. Secretin stimulates exocytosis in isolated bile duct epithelial cells by a cyclic AMP-mediated mechanism. J. Biol. Chern. 267:15523-15529.
40. Morris, R. 1994. Model of action of FK506, cyclosporin A and rapamycin. Transplant. Proc. 26:3272-3275.
41. Schreiber, S.L., and G.R. Crabtree. 1992. The mechanism of action of cyclosporin A and FK506. Immunol. Today. 13:136-142.
42. Caulfield, M.P. 1993. Muscarinic receptors - Characterization, coupling and function. Pharmacol. Ther. 58:319-379.
43. Done, F., A.I. Levey, and M.R. Brann. 1991. Immunological detection of muscarinic receptor subtype proteins (m1-m5) in rabbit peripheral tissue. Mol. Pharmacol. 40:459-462.
44. Maeda, A., T. Kubo, M. Mishina, and S. Numa. 1988. Tissue distribution of mRNAs encoding muscarinic acetylcholine receptor subtypes. FEBS Lett. 239:339-342.
45. Weigert, N., K. Schaffer, U. Wegner, V. Schusdziarra, M. Classen, and W. Schepp. 1994. Functional characterization of a muscarinic receptor stimulating gastrin release from rabbit antral G-cells in primary culture. Eur. J. Pharmacol. 264:337-344.
46. Barlow, R.B., K.J. Berry, P.A.M. Glenton, N.M. Nikolaou, and K.S. Soh. 1976. A comparison of affinity constant for muscarinic-sensitive acetylcholine receptors in guinea-pig atrial pacemaker cells at 29°C and in ileum at 29°C and 37°C. Br. J. Pharmacol. 58:613-620.
47. Martinez-Anso, E., J.E. Castillo, J. Diez, J.F. Medina, and J. Prieto. 1994. Immunohistochemical detection of chloride/bicarbonate anion exchanger in human liver. Hepatology. 19:1400-1406.
48. Strazzabosco, M., R. Joplin, A. Zeembery, A, Granato, C. Spirli, C. Poci, and S. Crepaldi 1994. Bicarbonate transport in cultured human intrahepatic bile duct epithelial cells (hBDE) from normal subjects and patients with primary biliary cirrhosis (PBC). Hepatology. 2:404A.
49. Jones, S.V.P., A.I. Levey, D.M. Weiner, J. Ellis, E. Novotny, S.H. Yu, F. Dorje, J. Wess, and M.R. Brann. 1992. Muscarinic acetylcholine receptors. In Molecular Biology of G-protein Coupled Receptors. M. Brann, editor. Birkhauser Boston, Cambridge, MA. 170-197.
50. Felder, C.C., R.Y. Kanterman, A.L. Ma, and J. Axelrod. 1989. A transfected m1 muscarinic acetylcholine receptor stimulates adenylate cyclase via phosphatidylinositol hydrolysis. J. Biol. Chem. 264:20356-20362.
51. Pan, G.-Z., M.J. Collen, and J.D. Gardner. 1982. Action of cholera toxin on dispersed acini from rat pancreas. Post-receptor modulation involving cyclic AMP and calcium. Biochim. Biophys. Acta. 720:338-345.
52. Baukal, A.J., L. Hunyady, K.J. Catt, and T. Balla. 1994. Evidence for participation of calcineurin in potentiation of agonist-stimulated cyclic AMP formation by the calcium-mobilizing hormone, Angiotensin II. J. Biol. Chem. 269:24546-24549.
53. i and protein kinase C. Cell Calcium. 15:162-174.
54. Aminaroff, B.M., M.C. Laburthe, C.M. Rouyer-Fessard, J.G. Demaille, and G.E. Rossellin. 1983. Calmodulin stimulation of adenylate cyclase of intestinal epithelium. Eur. J. Biochem. 130:33-37.
55. 2+/calmodulin-dependent protein phosphatase and secretion in pancreatic acinar cells. J. Biol. Chem. 269:15111-15117.
56. Raufman, J.P., J. Lin, and R.D. Raffaniello. 1996. Calcineurin mediates calcium-induced potentiation of adenylyl cyclase activity in dispersed chief cells from guinea pig stomach. J. Biol. Chem. 271:19877-19822.
57. Antoni, F.A., R.J.O. Barnard, M.J. Shipston, S.M. Smith, J. Simpson, and J.M. Paterson. 1995. Calcineurin feedback inhibition of agonist-evoked cAMP formation. J. Biol. Chem. 270:28055-28061.
58. Harrison, J.K., G.H.K. Hewlett, and M.E. Gnegy. 1989. Regulation of calmodulin-sensitive adenylate cyclase by the stimulatory G-protein, Gs. J. Biol. Chem. 264:15880-15885.
59. ++)-calmodulin-dependent phosphorylation and dephosphorylation of rat parotid secretion granules. Biochem. Biophys. Res. Comm. 215:75-81.
60. ++ and calmodulin on adenylyl cyclase activity in plasma membranes derived from neural and non-neural cells. Cell Calcium. 13:107-121.
61. Cooper, D.M.F., N. Mons, and J.W. Kerpen. 1995. Adenylyl cyclase and the interaction between calcium and cAMP signalling. Nature (Lond.). 374: 421-424.
62. Paterson, J.M., S.M. Smith, A.J. Harmar, and F.A. Antoni. 1995. Control of a novel adenylyl cyclase by calcineurin. Biochem. Biophys. Res. Comm. 214:1000-1008.
63. Tang, W.J., J. Krupinski, and A.G. Gilman. 1991. Expression and characterization of calmodulin-activated (type I) adenylyl cyclase. J. Biol. Chem. 266:8595-8603.
64. Choi, E.J., Z. Xia, and D.R. Storm. 1992. Stimulation of the type III olfactory adenylyl cyclase by calcium and calmodulin. Biochemistry. 31:6492-6498.
65. 2+/calmodulin-stimulated enzyme expressed in discrete regions of rat brain. J. Biol. Chem. 269:12190-12195.
66. Salter, R.S., M.H. Krinks, C.B. Klee, and E.J. Neer. 1981. Calmodulin activates the isolated catalytic unit of brain adenylate cyclase. J. Biol. Chem. 256:9830-9833.