Cooperative enhancement of insulinotropic action of GLP-1 by acetylcholine uncovers paradoxical inhibitory effect of beta cell muscarinic receptor activation on adenylate cyclase activity

Biochemical Pharmacology

Volumn 65, Issue 2, 2003, Pages 283-292

  Miguel, João C ^a,b   Abdel Wahab, Yasser H A ^a   Green, Brian D ^a   Mathias, Paulo C F ^b   Flatt, Peter R ^a  

^a UNIVERSITY OF ULSTER   (United Kingdom)

^b STATE UNIVERSITY OF MARINGÁ   (Brazil)

Author keywords

Acetylcholine; Beta cell; cAMP; GLP 1; Insulin; Muscarinic receptor

Indexed keywords

ACETYLCHOLINE; ADENYLATE CYCLASE; CYCLIC AMP; GLUCAGON LIKE PEPTIDE 1; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; METHOCTRAMINE; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; MUSCARINIC M3 RECEPTOR; MUSCARINIC M4 RECEPTOR; MUSCARINIC RECEPTOR; MUSCARINIC RECEPTOR BLOCKING AGENT; PERTUSSIS TOXIN; PIRENZEPINE; RECEPTOR SUBTYPE;

ANIMAL CELL; ARTICLE; CELL LINE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; DRUG EFFECT; DRUG MECHANISM; INHIBITION KINETICS; INSULIN LIKE ACTIVITY; INSULIN RELEASE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT; STIMULATION;

ACETYLCHOLINE; ADENYLATE CYCLASE; CYCLIC AMP; GLUCAGON; GLUCAGON-LIKE PEPTIDE 1; HUMANS; INSULIN; ISLETS OF LANGERHANS; PEPTIDE FRAGMENTS; PROTEIN PRECURSORS; RECEPTORS, MUSCARINIC;

EID: 0037437729     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(02)01482-X     Document Type: Article

References (69)

1. Morgan LM. Insulin secretion and the entero-insular axis. In: Flatt PR, editor. Nutrient Regulation of Insulin Secretion. London: Portland Press; 1992, p. 1-22.
2. Holst JJ. Role of classical and peptidergic neurotransmitters in insulin secretion. In: Flatt PR, editor. Nutrient regulation of insulin secretion. London: Portland Press; 1992, p. 23-37.
3. Berggren PO, Rorsman P, Efendic S, Ostenson CG, Flatt PR, Nilsson T, Arkhammar P, Juntti-Berggren L. Mechanisms of action of entero-insular hormones, islet peptides and neural input on the insulin secretory process. In: Flatt PR, editor. Nutrient regulation of insulin secretion. London: Portland Press; 1992, p. 289-318.
4. Ahren B. Autonomic regulation of islet hormone secretion - implications for health and disease. Diabetologia. 43:2000;393-410.
5. Berthoud H.R., Jeanrenaud B. Sham feeding-induced cephalic phase insulin release in the rat. Am. J. Physiol. Endocrinol. Metab. 242:1982;E280-E285.
6. Sjostrom L., Garellick G., Krotkiewski M., Luyckx A. Peripheral insulin in response to the sight and smell of food. Metabolism. 29:1980;901-909.
7. Strubbe J.H., Steffens A.B. Neural control of insulin secretion. Horm. Metab. Res. 25:1993;507-512.
8. Ahren B., Holst J.J. The cephalic insulin response to meal ingestion in humans is dependent on both cholinergic and noncholinergic mechanisms and is important for postprandial glycemia. Diabetes. 50:2001;1030-1038.
9. Teff K. Nutritional implications of the cephalic-phase reflexes: endocrine responses. Appetite. 34:2000;206-213.
10. Schmidt W.E., Siegel E.G., Creutzfeldt W. Glucagon-like peptide-1 but not glucagon-like peptide-2 stimulates insulin release from isolated rat pancreatic islets. Diabetologia. 28:1985;704-707.
11. Creutzfeldt W., Ebert R. New developments in the incretin concept. Diabetologia. 28:1985;565-573.
12. Fehmann H.C., Goke R., Goke B. Cell and molecular biology of the incretin hormones glucagon-like peptide-I and glucose-dependent insulin releasing polypeptide. Endocr. Rev. 16:1995;390-410.
13. Shapiro E.T., Tillil H., Miller M.A., Frank B.H., Galloway J.A., Rubenstein A.H., Polonsky K.S. Insulin secretion and clearance. Comparison after oral and intravenous glucose. Diabetes. 36:1987;1365-1371.
14. Tillil H., Shapiro E.T., Miller M.A., Karrison T., Frank B.H., Galloway J.A., Rubenstein A.H., Polonsky K.S. Dose-dependent effects of oral and intravenous glucose on insulin secretion and clearance in normal humans. Am. J. Physiol. Endocrinol. Metab. 254:1988;E349-E357.
15. Fehmann H.C., Goke R., Goke B., Arnold R. Carbachol priming increases glucose- and glucagon-like peptide-1 (7-36) amide-, but not arginine-induced insulin secretion from the isolated perfused rat pancreas. Z. Gastroenterol. 28:1990;348-352.
16. Zawalich W.S., Zawalich K.C., Rasmussen H. Cholinergic agonists prime the beta-cell to glucose stimulation. Endocrinology. 125:1989;2400-2406.
17. Sharp R., Culbert S., Cook J., Jennings A., Burr I.M. Cholinergic modification of glucose-induced biphasic insulin release in vitro. J. Clin. Invest. 53:1974;710-716.
18. Gilon P., Henquin J.C. Mechanisms and physiological significance of the cholinergic control of pancreatic beta-cell function. Endocr. Rev. 22:2001;565-604.
19. Berthoud H.R., Trimble E.R., Siegel E.G., Bereiter D.A., Jeanrenaud B. Cephalic-phase insulin secretion in normal and pancreatic islet-transplanted rats. Am. J. Physiol. Endocrinol. Metab. 238:1980;E336-E340.
20. Mathias P.C., Best L., Malaisse W.J. Stimulation by glucose and carbamylcholine of phospholipase C in pancreatic islets. Cell. Biochem. Funct. 3:1985;173-177.
21. Verspohl E.J., Tacke R., Mutschler E., Lambrecht G. Muscarinic receptor subtypes in rat pancreatic islets: binding and functional studies. Eur. J. Pharmacol. 178:1990;303-311.
22. Boschero A.C., Szpak-Glasman M., Carneiro E.M., Bordin S., Paul I., Rojas E., Atwater I. Oxotremorine-m potentiation of glucose-induced insulin release from rat islets involves M3 muscarinic receptors. Am. J. Physiol. Endocrinol. Metab. 268:1995;E336-E342.
23. Iismaa T.P., Kerr E.A., Wilson J.R., Carpenter L., Sims N., Biden T.J. Quantitative and functional characterization of muscarinic receptor subtypes in insulin-secreting cell lines and rat pancreatic islets. Diabetes. 49:2000;392-398.
24. Miguel J.C., Abdel-Wahab Y.H., Mathias P.C., Flatt P.R. Muscarinic receptor subtypes mediate stimulatory and paradoxical inhibitory effects on an insulin-secreting beta cell line. Biochim. Biophys. Acta. 1569:2002;45-50.
25. Bonner T.I. The molecular basis of muscarinic receptor diversity. Trends Neurosci. 12:1989;148-151.
26. Buckley N.J., Bonner T.I., Buckley C.M., Brann M.R. Antagonist binding properties of five cloned muscarinic receptors expressed in CHO-K1 cells. Mol. Pharmacol. 35:1989;469-476.
27. Bonner T.I., Buckley N.J., Young A.C., Brann M.R. Identification of a family of muscarinic acetylcholine receptor genes. Science. 237:1987;527-532.
28. Bonner T.I., Young A.C., Brann M.R., Buckley N.J. Cloning and expression of the human and rat m5 muscarinic acetylcholine receptor genes. Neuron. 1:1988;403-410.
29. Tang S.H., Sharp G.W. Atypical protein kinase C isozyme zeta mediates carbachol-stimulated insulin secretion in RINm5F cells. Diabetes. 47:1998;905-912.
30. Caulfield M.P., Birdsall N.J. International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol. Rev. 50:1998;279-290.
31. Wess J. Molecular basis of receptor/G-protein-coupling selectivity. Pharmacol. Ther. 80:1998;231-264.
32. Vilsboll T., Krarup T., Deacon C.F., Madsbad S., Holst J.J. Reduced postprandial concentrations of intact biologically active glucagon-like peptide 1 in type 2 diabetic patients. Diabetes. 50:2001;609-613.
33. Vilsboll T., Krarup T., Madsbad S., Holst J.J. No reactive hypoglycaemia in Type 2 diabetic patients after subcutaneous administration of GLP-1 and intravenous glucose. Diabet. Med. 18:2001;144-149.
34. Larsen J., Hylleberg B., Ng K., Damsbo P. Glucagon-like peptide-1 infusion must be maintained for 24 hr/day to obtain acceptable glycemia in type 2 diabetic patients who are poorly controlled on sulphonylurea treatment. Diabetes Care. 24:2001;1416-1421.
35. Holst J.J. Gut hormones as pharmaceuticals. From enteroglucagon to GLP-1 and GLP-2. Regul. Pept. 93:2000;45-51.
36. Larsen P.J., Fledelius C., Knudsen L.B., Tang-Christensen M. Systemic administration of the long-acting GLP-1 derivative NN2211 induces lasting and reversible weight loss in both normal and obese rats. Diabetes. 50:2001;2530-2539.
37. Gromada J., Bokvist K., Ding W.G., Holst J.J., Nielsen J.H., Rorsman P. Glucagon-like peptide 1 (7-36) amide stimulates exocytosis in human pancreatic beta-cells by both proximal and distal regulatory steps in stimulus-secretion coupling. Diabetes. 47:1998;57-65.
38. Holst J.J., Orskov C., Nielsen O.V., Schwartz T.W. Truncated glucagon-like peptide I, an insulin-releasing hormone from the distal gut. FEBS Lett. 211:1987;169-174.
39. Fehmann H.C., Habener J.F. Insulinotropic hormone glucagon-like peptide-I (7-37) stimulation of proinsulin gene expression and proinsulin biosynthesis in insulinoma beta TC-1 cells. Endocrinology. 130:1992;159-166.
40. Gromada J., Holst J.J., Rorsman P. Cellular regulation of islet hormone secretion by the incretin hormone glucagon-like peptide 1. Pflugers Arch. 435:1998;583-594.
41. Buteau J., Roduit R., Susini S., Prentki M. Glucagon-like peptide-1 promotes DNA synthesis, activates phosphatidylinositol 3-kinase and increases transcription factor pancreatic and duodenal homeobox gene 1 (PDX-1) DNA binding activity in beta (INS-1)-cells. Diabetologia. 42:1999;856-864.
42. Holz G.G., Kuhtreiber W.M., Habener J.F. Pancreatic beta-cells are rendered glucose-competent by the insulinotropic hormone glucagon-like peptide-1 (7-37). Nature. 361:1993;362-365.
43. McClenaghan N.H., Barnett C.R., Ah-Sing E., Abdel-Wahab Y.H., O'Harte F.P., Yoon T.W., Swanston-Flatt S.K., Flatt P.R. Characterization of a novel glucose-responsive insulin-secreting cell line, BRIN-BD11, produced by electrofusion. Diabetes. 45:1996;1132-1140.
44. Flatt P.R., Bailey C.J. Abnormal plasma glucose and insulin responses in heterozygous lean (ob/+) mice. Diabetologia. 20:1981;573-577.
45. Farndale RW, Allan LM, Martin BR. Adenylate cyclase and cAMP. In: Milligan G, editor. Signal Transduction: A Practical Approach. Oxford: IRL Press; 1995, p. 75-103.
46. Salomon Y., Londos C., Rodbell M. A highly sensitive adenylate cyclase assay. Anal. Biochem. 58:1974;541-548.
47. Widmann C., Burki E., Dolci W., Thorens B. Signal transduction by the cloned glucagon-like peptide-1 receptor: comparison with signaling by the endogenous receptors of beta cell lines. Mol. Pharmacol. 45:1994;1029-1035.
48. Zawalich W.S., Zawalich K.C., Rasmussen H. Interactions between cholinergic agonists and enteric factors in the regulation of insulin secretion from isolated perifused rat islets. Acta Endocrinol. (Copenhagen). 120:1989;702-707.
49. Zawalich W.S., Zawalich K.C., Rasmussen H. Influence of glucagon-like peptide-1 on beta cell responsiveness. Regul. Pept. 44:1993;277-283.
50. Hallbrink M., Holmqvist T., Olsson M., Ostenson C.G., Efendic S., Langel U. Different domains in the third intracellular loop of the GLP-1 receptor are responsible for Galpha(s) and Galpha(i)/Galpha(o) activation. Biochim. Biophys. Acta. 1546:2001;79-86.
51. Zawalich W.S., Zawalich K.C. Regulation of insulin secretion by phospholipase C. Am. J. Physiol. Endocrinol. Metab. 271:1996;E409-E416.
52. Zawalich W.S., Zawalich K.C., Kelley G.G. Regulation of insulin release by phospholipase C activation in mouse islets: differential effects of glucose and neurohumoral stimulation. Endocrinology. 136:1995;4903-4909.
53. Tian Y.M., Urquidi V., Ashcroft S.J. Protein kinase C in beta-cells: expression of multiple isoforms and involvement in cholinergic stimulation of insulin secretion. Mol. Cell. Endocrinol. 119:1996;185-193.
54. Wollheim C.B., Regazzi R. Protein kinase C in insulin releasing cells. Putative role in stimulus secretion coupling. FEBS Lett. 268:1990;376-380.
55. Gao Z.Y., Gilon P., Henquin J.C. The role of protein kinase-C in signal transduction through vasopressin and acetylcholine receptors in pancreatic B-cells from normal mouse. Endocrinology. 135:1994;191-199.
56. Tang S.H., Sharp G.W. Identification of muscarinic receptor subtypes in RINm5F cells by means of polymerase chain reaction, subcloning, and DNA sequencing. Diabetes. 46:1997;1419-1423.
57. 2+-signaling pathway in pancreatic beta-cells by the insulinotropic hormone glucagon-like peptide-1. J. Biol. Chem. 270:1995;17749-17757.
58. Tian Y., Laychock S.G. Protein kinase C and calcium regulation of adenylyl cyclase in isolated rat pancreatic islets. Diabetes. 50:2001;2505-2513.
59. Guenifi A., Simonsson E., Karlsson S., Ahren B., Abdel-Halim S.M. Carbachol restores insulin release in diabetic GK rat islets by mechanisms largely involving hydrolysis of diacylglycerol and direct interaction with the exocytotic machinery. Pancreas. 22:2001;164-171.
60. Liu Y.J., Grapengiesser E., Gylfe E., Hellman B. Crosstalk between the cAMP and inositol trisphosphate-signalling pathways in pancreatic beta-cells. Arch. Biochem. Biophys. 334:1996;295-302.
61. Gromada J., Dissing S., Rorsman P. Desensitization of glucagon-like peptide 1 receptors in insulin-secreting beta TC3 cells: role of PKA-independent mechanisms. Br. J. Pharmacol. 118:1996;769-775.
62. Tang S.H., Yaney G.C., Sharp G.W. Unusual carbachol responses in RINm5F cells: evidence for a distal site of action in stimulus-secretion coupling. Mol. Pharmacol. 47:1995;863-870.
63. Olianas M.C., Adem A., Karlsson E., Onali P. Identification of rat brain muscarinic M4 receptors coupled to cyclic AMP using the selective antagonist muscarinic toxin 3. Eur. J. Pharmacol. 357:1998;235-242.
64. Murthy K.S., Makhlouf G.M. Differential coupling of muscarinic m2 and m3 receptors to adenylyl cyclases V/VI in smooth muscle. Concurrent M2-mediated inhibition via Galphai3 and m3-mediated stimulation via Gbetagammaq. J. Biol. Chem. 272:1997;21317-21324.
65. Peralta E.G., Ashkenazi A., Winslow J.W., Ramachandran J., Capon D.J. Differential regulation of PI hydrolysis and adenylyl cyclase by muscarinic receptor subtypes. Nature. 334:1988;434-437.
66. Luthin G.R., Wang P., Zhou H., Dhanasekaran D., Ruggieri M.R. Role of m1 receptor-G protein coupling in cell proliferation in the prostate. Life Sci. 60:1997;963-968.
67. Cooper D.M., Mons N., Karpen J.W. Adenylyl cyclases and the interaction between calcium and cAMP signalling. Nature. 374:1995;421-424.
68. 2+ mobilization in NCB-20 cells leading to direct inhibition of adenylylcyclase. A novel mechanism for inhibition of cAMP production. J. Biol. Chem. 266:1991;4995-5003.
69. DeBernardi M.A., Seki T., Brooker G. Inhibition of cAMP accumulation by intracellular calcium mobilization in C6-2B cells stably transfected with substance K receptor cDNA. Proc. Natl. Acad. Sci. U.S.A. 88:1991;9257-9261.