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Published in: Diabetologia 8/2012

01-08-2012 | Review

Cell signalling in insulin secretion: the molecular targets of ATP, cAMP and sulfonylurea

Author: S. Seino

Published in: Diabetologia | Issue 8/2012

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Abstract

Clarification of the molecular mechanisms of insulin secretion is crucial for understanding the pathogenesis and pathophysiology of diabetes and for development of novel therapeutic strategies for the disease. Insulin secretion is regulated by various intracellular signals generated by nutrients and hormonal and neural inputs. In addition, a variety of glucose-lowering drugs including sulfonylureas, glinide-derivatives, and incretin-related drugs such as dipeptidyl peptidase IV (DPP-4) inhibitors and glucagon-like peptide 1 (GLP-1) receptor agonists are used for glycaemic control by targeting beta cell signalling for improved insulin secretion. There has been a remarkable increase in our understanding of the basis of beta cell signalling over the past two decades following the application of molecular biology, gene technology, electrophysiology and bioimaging to beta cell research. This review discusses cell signalling in insulin secretion, focusing on the molecular targets of ATP, cAMP and sulfonylurea, an essential metabolic signal in glucose-induced insulin secretion (GIIS), a critical signal in the potentiation of GIIS, and the commonly used glucose-lowering drug, respectively.
Literature
1.
go back to reference Berson SA, Yalow RS (1959) Quantitative aspects of the reaction between insulin and insulin-binding antibody. J Clin Invest 38:1996–2016PubMedCrossRef Berson SA, Yalow RS (1959) Quantitative aspects of the reaction between insulin and insulin-binding antibody. J Clin Invest 38:1996–2016PubMedCrossRef
2.
go back to reference Wollheim CB, Sharp GW (1981) Regulation of insulin release by calcium. Physiol Rev 61:914–973PubMed Wollheim CB, Sharp GW (1981) Regulation of insulin release by calcium. Physiol Rev 61:914–973PubMed
3.
go back to reference Malaisse WJ, Malaisse-Lagae F (1984) The role of cyclic AMP in insulin release. Experientia 40:1068–1074PubMedCrossRef Malaisse WJ, Malaisse-Lagae F (1984) The role of cyclic AMP in insulin release. Experientia 40:1068–1074PubMedCrossRef
4.
go back to reference Prentki M, Matschinsky FM (1987) Ca2+, cAMP, and phospholipid-derived messengers in coupling mechanisms of insulin secretion. Physiol Rev 67:1185–1248PubMed Prentki M, Matschinsky FM (1987) Ca2+, cAMP, and phospholipid-derived messengers in coupling mechanisms of insulin secretion. Physiol Rev 67:1185–1248PubMed
5.
go back to reference Davis B, Lazarus NR (1976) An in vitro system for studying insulin release caused by secretory granules–plasma membrane interaction: definition of the system. J Physiol 256:709–729PubMed Davis B, Lazarus NR (1976) An in vitro system for studying insulin release caused by secretory granules–plasma membrane interaction: definition of the system. J Physiol 256:709–729PubMed
6.
go back to reference Grodsky GM, Batts AA, Bennett LL, Vcella C, McWilliams NB, Smith DF (1963) Effects of carbohydrates on secretion of insulin from isolated rat pancreas. Am J Physiol 205:638–644PubMed Grodsky GM, Batts AA, Bennett LL, Vcella C, McWilliams NB, Smith DF (1963) Effects of carbohydrates on secretion of insulin from isolated rat pancreas. Am J Physiol 205:638–644PubMed
7.
go back to reference Coore HG, Randle PJ (1964) Regulation of insulin secretion studied with pieces of rabbit pancreas incubated in vitro. Biochem J 93:66–78PubMed Coore HG, Randle PJ (1964) Regulation of insulin secretion studied with pieces of rabbit pancreas incubated in vitro. Biochem J 93:66–78PubMed
8.
go back to reference Hedeskov CJ (1980) Mechanism of glucose-induced insulin secretion. Physiol Rev 60:442–509PubMed Hedeskov CJ (1980) Mechanism of glucose-induced insulin secretion. Physiol Rev 60:442–509PubMed
10.
go back to reference Cook DL, Hales CN (1984) Intracellular ATP directly blocks K+ channels in pancreatic B-cells. Nature 311:271–273PubMedCrossRef Cook DL, Hales CN (1984) Intracellular ATP directly blocks K+ channels in pancreatic B-cells. Nature 311:271–273PubMedCrossRef
11.
go back to reference Ashcroft FM, Harrison DE, Ashcroft SJ (1984) Glucose induces closure of single potassium channels in isolated rat pancreatic β-cells. Nature 312:446–448PubMedCrossRef Ashcroft FM, Harrison DE, Ashcroft SJ (1984) Glucose induces closure of single potassium channels in isolated rat pancreatic β-cells. Nature 312:446–448PubMedCrossRef
12.
go back to reference Rorsman P, Trube G (1985) Glucose dependent K+-channels in pancreatic β-cells are regulated by intracellular ATP. Pflugers Arch 405:305–309PubMedCrossRef Rorsman P, Trube G (1985) Glucose dependent K+-channels in pancreatic β-cells are regulated by intracellular ATP. Pflugers Arch 405:305–309PubMedCrossRef
13.
go back to reference Ashcroft FM, Rorsman P (1989) Electrophysiology of the pancreatic β-cell. Prog Biophys Mol Biol 54:87–143PubMedCrossRef Ashcroft FM, Rorsman P (1989) Electrophysiology of the pancreatic β-cell. Prog Biophys Mol Biol 54:87–143PubMedCrossRef
14.
go back to reference Henquin JC (2009) Regulation of insulin secretion: a matter of phase control and amplitude modulation. Diabetologia 52:739–751PubMedCrossRef Henquin JC (2009) Regulation of insulin secretion: a matter of phase control and amplitude modulation. Diabetologia 52:739–751PubMedCrossRef
15.
go back to reference Detimary P, Gilon P, Nenquin M, Henquin JC (1994) Two sites of glucose control of insulin release with distinct dependence on the energy state in pancreatic B cells. Biochem J 297:455–461PubMed Detimary P, Gilon P, Nenquin M, Henquin JC (1994) Two sites of glucose control of insulin release with distinct dependence on the energy state in pancreatic B cells. Biochem J 297:455–461PubMed
16.
go back to reference Eliasson L, Renstrom E, Ding WG, Proks P, Rorsman P (1997) Rapid ATP-dependent priming of secretory granules precedes Ca2+-induced exocytosis in mouse pancreatic B cells. J Physiol 503:399–412PubMedCrossRef Eliasson L, Renstrom E, Ding WG, Proks P, Rorsman P (1997) Rapid ATP-dependent priming of secretory granules precedes Ca2+-induced exocytosis in mouse pancreatic B cells. J Physiol 503:399–412PubMedCrossRef
17.
go back to reference Takahashi N, Kadowaki T, Yazaki Y, Ellis-Davies GC, Miyashita Y, Kasai H (1999) Post-priming actions of ATP on Ca2+-dependent exocytosis in pancreatic β cells. Proc Natl Acad Sci USA 96:760–765PubMedCrossRef Takahashi N, Kadowaki T, Yazaki Y, Ellis-Davies GC, Miyashita Y, Kasai H (1999) Post-priming actions of ATP on Ca2+-dependent exocytosis in pancreatic β cells. Proc Natl Acad Sci USA 96:760–765PubMedCrossRef
18.
go back to reference Nolan CJ, Madiraju MS, Delghingaro-Augusto V, Peyot ML, Prentki M (2006) Fatty acid signaling in the β-cell and insulin secretion. Diabetes 55(Suppl 2):S16–S23PubMedCrossRef Nolan CJ, Madiraju MS, Delghingaro-Augusto V, Peyot ML, Prentki M (2006) Fatty acid signaling in the β-cell and insulin secretion. Diabetes 55(Suppl 2):S16–S23PubMedCrossRef
19.
go back to reference Curry DL, Bennett LL, Grodsky GM (1968) Dynamics of insulin secretion by the perfused rat pancreas. Endocrinology 83:572–584PubMedCrossRef Curry DL, Bennett LL, Grodsky GM (1968) Dynamics of insulin secretion by the perfused rat pancreas. Endocrinology 83:572–584PubMedCrossRef
20.
go back to reference Rorsman P, Renstrom E (2003) Insulin granule dynamics in pancreatic β cells. Diabetologia 46:1029–1045PubMedCrossRef Rorsman P, Renstrom E (2003) Insulin granule dynamics in pancreatic β cells. Diabetologia 46:1029–1045PubMedCrossRef
21.
go back to reference Porte D Jr (1991) Banting lecture 1990. β-cells in type II diabetes mellitus. Diabetes 40:166–180PubMedCrossRef Porte D Jr (1991) Banting lecture 1990. β-cells in type II diabetes mellitus. Diabetes 40:166–180PubMedCrossRef
22.
23.
go back to reference Eliasson L, Abdulkader F, Braun M, Galvanovskis J, Hoppa MB, Rorsman P (2008) Novel aspects of the molecular mechanisms controlling insulin secretion. J Physiol 586:3313–3324PubMedCrossRef Eliasson L, Abdulkader F, Braun M, Galvanovskis J, Hoppa MB, Rorsman P (2008) Novel aspects of the molecular mechanisms controlling insulin secretion. J Physiol 586:3313–3324PubMedCrossRef
24.
go back to reference Straub SG, Shanmugam G, Sharp GW (2004) Stimulation of insulin release by glucose is associated with an increase in the number of docked granules in the β-cells of rat pancreatic islets. Diabetes 53:3179–3183PubMedCrossRef Straub SG, Shanmugam G, Sharp GW (2004) Stimulation of insulin release by glucose is associated with an increase in the number of docked granules in the β-cells of rat pancreatic islets. Diabetes 53:3179–3183PubMedCrossRef
25.
go back to reference Tsuboi T, Zhao C, Terakawa S, Rutter GA (2000) Simultaneous evanescent wave imaging of insulin vesicle membrane and cargo during a single exocytotic event. Curr Biol 10:1307–1310PubMedCrossRef Tsuboi T, Zhao C, Terakawa S, Rutter GA (2000) Simultaneous evanescent wave imaging of insulin vesicle membrane and cargo during a single exocytotic event. Curr Biol 10:1307–1310PubMedCrossRef
26.
go back to reference Ohara-Imaizumi M, Nakamichi Y, Tanaka T, Ishida H, Nagamatsu S (2002) Imaging exocytosis of single insulin secretory granules with evanescent wave microscopy: distinct behavior of granule motion in biphasic insulin release. J Biol Chem 277:3805–3808PubMedCrossRef Ohara-Imaizumi M, Nakamichi Y, Tanaka T, Ishida H, Nagamatsu S (2002) Imaging exocytosis of single insulin secretory granules with evanescent wave microscopy: distinct behavior of granule motion in biphasic insulin release. J Biol Chem 277:3805–3808PubMedCrossRef
27.
go back to reference Shibasaki T, Takahashi H, Miki T et al (2007) Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci USA 104:19333–19338PubMedCrossRef Shibasaki T, Takahashi H, Miki T et al (2007) Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci USA 104:19333–19338PubMedCrossRef
28.
go back to reference Kasai K, Fujita T, Gomi H, Izumi T (2008) Docking is not a prerequisite but a temporal constraint for fusion of secretory granules. Traffic 9:1191–1203PubMedCrossRef Kasai K, Fujita T, Gomi H, Izumi T (2008) Docking is not a prerequisite but a temporal constraint for fusion of secretory granules. Traffic 9:1191–1203PubMedCrossRef
29.
go back to reference Axelrod D (1981) Cell–substrate contacts illuminated by total internal reflection fluorescence. J Cell Biol 89:141–145PubMedCrossRef Axelrod D (1981) Cell–substrate contacts illuminated by total internal reflection fluorescence. J Cell Biol 89:141–145PubMedCrossRef
30.
go back to reference Takahashi N, Hatakeyama H, Okado H, Noguchi J, Ohno M, Kasai H (2010) SNARE conformational changes that prepare vesicles for exocytosis. Cell Metab 12:19–29PubMedCrossRef Takahashi N, Hatakeyama H, Okado H, Noguchi J, Ohno M, Kasai H (2010) SNARE conformational changes that prepare vesicles for exocytosis. Cell Metab 12:19–29PubMedCrossRef
31.
go back to reference Seino S, Shibasaki T, Minami K (2011) Dynamics of insulin secretion and the clinical implications for obesity and diabetes. J Clin Invest 121:2118–2125PubMedCrossRef Seino S, Shibasaki T, Minami K (2011) Dynamics of insulin secretion and the clinical implications for obesity and diabetes. J Clin Invest 121:2118–2125PubMedCrossRef
32.
go back to reference Seino S, Takahashi H, Fujimoto W, Shibasaki T (2009) Roles of cAMP signalling in insulin granule exocytosis. Diabetes Obes Metab 11(Suppl 4):180–188PubMedCrossRef Seino S, Takahashi H, Fujimoto W, Shibasaki T (2009) Roles of cAMP signalling in insulin granule exocytosis. Diabetes Obes Metab 11(Suppl 4):180–188PubMedCrossRef
33.
go back to reference Wang Z, Thurmond DC (2009) Mechanisms of biphasic insulin-granule exocytosis—roles of the cytoskeleton, small GTPases and SNARE proteins. J Cell Sci 122:893–903PubMedCrossRef Wang Z, Thurmond DC (2009) Mechanisms of biphasic insulin-granule exocytosis—roles of the cytoskeleton, small GTPases and SNARE proteins. J Cell Sci 122:893–903PubMedCrossRef
34.
go back to reference Ozaki N, Shibasaki T, Kashima Y et al (2000) cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat Cell Biol 2:805–811PubMedCrossRef Ozaki N, Shibasaki T, Kashima Y et al (2000) cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat Cell Biol 2:805–811PubMedCrossRef
35.
go back to reference Dulubova I, Lou X, Lu J et al (2005) A Munc13/RIM/Rab3 tripartite complex: from priming to plasticity? EMBO J 24:2839–2850PubMedCrossRef Dulubova I, Lou X, Lu J et al (2005) A Munc13/RIM/Rab3 tripartite complex: from priming to plasticity? EMBO J 24:2839–2850PubMedCrossRef
36.
go back to reference Fukuda M (2003) Distinct Rab binding specificity of Rim1, Rim2, rabphilin, and Noc2. Identification of a critical determinant of Rab3A/Rab27A recognition by Rim2. J Biol Chem 278:15373–15380PubMedCrossRef Fukuda M (2003) Distinct Rab binding specificity of Rim1, Rim2, rabphilin, and Noc2. Identification of a critical determinant of Rab3A/Rab27A recognition by Rim2. J Biol Chem 278:15373–15380PubMedCrossRef
37.
go back to reference Ohara-Imaizumi M, Ohtsuka T, Matsushima S et al (2005) ELKS, a protein structurally related to the active zone-associated protein CAST, is expressed in pancreatic β cells and functions in insulin exocytosis: interaction of ELKS with exocytotic machinery analyzed by total internal reflection fluorescence microscopy. Mol Biol Cell 16:3289–3300PubMedCrossRef Ohara-Imaizumi M, Ohtsuka T, Matsushima S et al (2005) ELKS, a protein structurally related to the active zone-associated protein CAST, is expressed in pancreatic β cells and functions in insulin exocytosis: interaction of ELKS with exocytotic machinery analyzed by total internal reflection fluorescence microscopy. Mol Biol Cell 16:3289–3300PubMedCrossRef
38.
go back to reference Inoue E, Deguchi-Tawarada M, Takao-Rikitsu E et al (2006) ELKS, a protein structurally related to the active zone protein CAST, is involved in Ca2+-dependent exocytosis from PC12 cells. Genes Cells 11:659–672PubMedCrossRef Inoue E, Deguchi-Tawarada M, Takao-Rikitsu E et al (2006) ELKS, a protein structurally related to the active zone protein CAST, is involved in Ca2+-dependent exocytosis from PC12 cells. Genes Cells 11:659–672PubMedCrossRef
39.
go back to reference Fujimoto K, Shibasaki T, Yokoi N et al (2002) Piccolo, a Ca2+ sensor in pancreatic β-cells. Involvement of cAMP-GEFII⋅Rim2⋅Piccolo complex in cAMP-dependent exocytosis. J Biol Chem 277:50497–50502PubMedCrossRef Fujimoto K, Shibasaki T, Yokoi N et al (2002) Piccolo, a Ca2+ sensor in pancreatic β-cells. Involvement of cAMP-GEFII⋅Rim2⋅Piccolo complex in cAMP-dependent exocytosis. J Biol Chem 277:50497–50502PubMedCrossRef
40.
go back to reference Shibasaki T, Sunaga Y, Fujimoto K, Kashima Y, Seino S (2004) Interaction of ATP sensor, cAMP sensor, Ca2+ sensor, and voltage-dependent Ca2+ channel in insulin granule exocytosis. J Biol Chem 279:7956–7961PubMedCrossRef Shibasaki T, Sunaga Y, Fujimoto K, Kashima Y, Seino S (2004) Interaction of ATP sensor, cAMP sensor, Ca2+ sensor, and voltage-dependent Ca2+ channel in insulin granule exocytosis. J Biol Chem 279:7956–7961PubMedCrossRef
41.
go back to reference Gustavsson N, Lao Y, Maximov A et al (2008) Impaired insulin secretion and glucose intolerance in synaptotagmin-7 null mutant mice. Proc Natl Acad Sci USA 105:3992–3997PubMedCrossRef Gustavsson N, Lao Y, Maximov A et al (2008) Impaired insulin secretion and glucose intolerance in synaptotagmin-7 null mutant mice. Proc Natl Acad Sci USA 105:3992–3997PubMedCrossRef
42.
go back to reference Iezzi M, Kouri G, Fukuda M, Wollheim CB (2004) Synaptotagmin V and IX isoforms control Ca2+-dependent insulin exocytosis. J Cell Sci 117:3119–3127PubMedCrossRef Iezzi M, Kouri G, Fukuda M, Wollheim CB (2004) Synaptotagmin V and IX isoforms control Ca2+-dependent insulin exocytosis. J Cell Sci 117:3119–3127PubMedCrossRef
43.
go back to reference Yasuda T, Shibasaki T, Minami K et al (2010) Rim2α determines docking and priming states in insulin granule exocytosis. Cell Metab 12:117–129PubMedCrossRef Yasuda T, Shibasaki T, Minami K et al (2010) Rim2α determines docking and priming states in insulin granule exocytosis. Cell Metab 12:117–129PubMedCrossRef
44.
45.
go back to reference Saito T, Shibasaki T, Seino S (2008) Involvement of Exoc3l, a protein structurally related to the exocyst subunit Sec6, in insulin secretion. Biomed Res 29:85–91PubMedCrossRef Saito T, Shibasaki T, Seino S (2008) Involvement of Exoc3l, a protein structurally related to the exocyst subunit Sec6, in insulin secretion. Biomed Res 29:85–91PubMedCrossRef
46.
go back to reference Weir GC, Mojsov S, Hendrick GK, Habener JF (1989) Glucagonlike peptide I (7–37) actions on endocrine pancreas. Diabetes 38:338–342PubMedCrossRef Weir GC, Mojsov S, Hendrick GK, Habener JF (1989) Glucagonlike peptide I (7–37) actions on endocrine pancreas. Diabetes 38:338–342PubMedCrossRef
47.
go back to reference Gembal M, Detimary P, Gilon P, Gao ZY, Henquin JC (1993) Mechanisms by which glucose can control insulin release independently from its action on adenosine triphosphate-sensitive K+ channels in mouse B cells. J Clin Invest 91:871–880PubMedCrossRef Gembal M, Detimary P, Gilon P, Gao ZY, Henquin JC (1993) Mechanisms by which glucose can control insulin release independently from its action on adenosine triphosphate-sensitive K+ channels in mouse B cells. J Clin Invest 91:871–880PubMedCrossRef
48.
go back to reference Holz GG 4th, Kuhtreiber WM, Habener JF (1993) Pancreatic β-cells are rendered glucose-competent by the insulinotropic hormone glucagon-like peptide-1(7–37). Nature 361:362–365PubMedCrossRef Holz GG 4th, Kuhtreiber WM, Habener JF (1993) Pancreatic β-cells are rendered glucose-competent by the insulinotropic hormone glucagon-like peptide-1(7–37). Nature 361:362–365PubMedCrossRef
49.
go back to reference Miki T, Minami K, Shinozaki H et al (2005) Distinct effects of glucose-dependent insulinotropic polypeptide and glucagon-like peptide-1 on insulin secretion and gut motility. Diabetes 54:1056–1063PubMedCrossRef Miki T, Minami K, Shinozaki H et al (2005) Distinct effects of glucose-dependent insulinotropic polypeptide and glucagon-like peptide-1 on insulin secretion and gut motility. Diabetes 54:1056–1063PubMedCrossRef
50.
go back to reference Fujimoto W, Miki T, Ogura T et al (2009) Niflumic acid-sensitive ion channels play an important role in the induction of glucose-stimulated insulin secretion by cyclic AMP in mice. Diabetologia 52:863–872PubMedCrossRef Fujimoto W, Miki T, Ogura T et al (2009) Niflumic acid-sensitive ion channels play an important role in the induction of glucose-stimulated insulin secretion by cyclic AMP in mice. Diabetologia 52:863–872PubMedCrossRef
51.
go back to reference Sturgess NC, Ashford ML, Cook DL, Hales CN (1985) The sulphonylurea receptor may be an ATP-sensitive potassium channel. Lancet 2:474–475PubMedCrossRef Sturgess NC, Ashford ML, Cook DL, Hales CN (1985) The sulphonylurea receptor may be an ATP-sensitive potassium channel. Lancet 2:474–475PubMedCrossRef
52.
go back to reference Aguilar-Bryan L, Nichols CG, Wechsler SW et al (1995) Cloning of the β cell high-affinity sulfonylurea receptor: a regulator of insulin secretion. Science 268:423–426PubMedCrossRef Aguilar-Bryan L, Nichols CG, Wechsler SW et al (1995) Cloning of the β cell high-affinity sulfonylurea receptor: a regulator of insulin secretion. Science 268:423–426PubMedCrossRef
53.
go back to reference Inagaki N, Gonoi T, Clement JP 4th et al (1995) Reconstitution of I KATP: an inward rectifier subunit plus the sulfonylurea receptor. Science 270:1166–1170PubMedCrossRef Inagaki N, Gonoi T, Clement JP 4th et al (1995) Reconstitution of I KATP: an inward rectifier subunit plus the sulfonylurea receptor. Science 270:1166–1170PubMedCrossRef
54.
go back to reference Sakura H, Ammala C, Smith PA, Gribble FM, Ashcroft FM (1995) Cloning and functional expression of the cDNA encoding a novel ATP-sensitive potassium channel subunit expressed in pancreatic β-cells, brain, heart and skeletal muscle. FEBS Letters 377:338–344PubMedCrossRef Sakura H, Ammala C, Smith PA, Gribble FM, Ashcroft FM (1995) Cloning and functional expression of the cDNA encoding a novel ATP-sensitive potassium channel subunit expressed in pancreatic β-cells, brain, heart and skeletal muscle. FEBS Letters 377:338–344PubMedCrossRef
55.
go back to reference Aguilar-Bryan L, Bryan J (1999) Molecular biology of adenosine triphosphate-sensitive potassium channels. Endocrine reviews 20:101–135PubMedCrossRef Aguilar-Bryan L, Bryan J (1999) Molecular biology of adenosine triphosphate-sensitive potassium channels. Endocrine reviews 20:101–135PubMedCrossRef
56.
go back to reference Seino S (1999) ATP-sensitive potassium channels: a model of heteromultimeric potassium channel/receptor assemblies. Annu Rev Physiol 61:337–362PubMedCrossRef Seino S (1999) ATP-sensitive potassium channels: a model of heteromultimeric potassium channel/receptor assemblies. Annu Rev Physiol 61:337–362PubMedCrossRef
57.
go back to reference Seino S, Miki T (2003) Physiological and pathophysiological roles of ATP-sensitive K+ channels. Prog Biophys Mol Biol 81:133–176PubMedCrossRef Seino S, Miki T (2003) Physiological and pathophysiological roles of ATP-sensitive K+ channels. Prog Biophys Mol Biol 81:133–176PubMedCrossRef
58.
go back to reference Gribble FM, Reimann F (2003) Sulphonylurea action revisited: the post-cloning era. Diabetologia 46:875–891PubMedCrossRef Gribble FM, Reimann F (2003) Sulphonylurea action revisited: the post-cloning era. Diabetologia 46:875–891PubMedCrossRef
59.
go back to reference Winkler M, Stephan D, Bieger S, Kuhner P, Wolff F, Quast U (2007) Testing the bipartite model of the sulfonylurea receptor binding site: binding of A-, B-, and A + B-site ligands. J Pharmacol Exp Ther 322:701–708PubMedCrossRef Winkler M, Stephan D, Bieger S, Kuhner P, Wolff F, Quast U (2007) Testing the bipartite model of the sulfonylurea receptor binding site: binding of A-, B-, and A + B-site ligands. J Pharmacol Exp Ther 322:701–708PubMedCrossRef
60.
go back to reference Proks P, Ashcroft FM (2009) Modeling KATP channel gating and its regulation. Prog Biophys Mol Biol 99:7–19PubMedCrossRef Proks P, Ashcroft FM (2009) Modeling KATP channel gating and its regulation. Prog Biophys Mol Biol 99:7–19PubMedCrossRef
61.
go back to reference Miki T, Tashiro F, Iwanaga T et al (1997) Abnormalities of pancreatic islets by targeted expression of a dominant-negative KATP channel. Proc Natl Acad Sci USA 94:11969–11973PubMedCrossRef Miki T, Tashiro F, Iwanaga T et al (1997) Abnormalities of pancreatic islets by targeted expression of a dominant-negative KATP channel. Proc Natl Acad Sci USA 94:11969–11973PubMedCrossRef
62.
go back to reference Miki T, Nagashima K, Tashiro F et al (1998) Defective insulin secretion and enhanced insulin action in KATP channel-deficient mice. Proc Natl Acad Sci USA 95:10402–10406PubMedCrossRef Miki T, Nagashima K, Tashiro F et al (1998) Defective insulin secretion and enhanced insulin action in KATP channel-deficient mice. Proc Natl Acad Sci USA 95:10402–10406PubMedCrossRef
63.
go back to reference Seghers V, Nakazaki M, DeMayo F, Aguilar-Bryan L, Bryan J (2000) Sur1 knockout mice. A model for KATP channel-independent regulation of insulin secretion. J Biol Chem 275:9270–9277PubMedCrossRef Seghers V, Nakazaki M, DeMayo F, Aguilar-Bryan L, Bryan J (2000) Sur1 knockout mice. A model for KATP channel-independent regulation of insulin secretion. J Biol Chem 275:9270–9277PubMedCrossRef
64.
go back to reference Shiota C, Larsson O, Shelton KD et al (2002) Sulfonylurea receptor type 1 knock-out mice have intact feeding-stimulated insulin secretion despite marked impairment in their response to glucose. J Biol Chem 277:37176–37183PubMedCrossRef Shiota C, Larsson O, Shelton KD et al (2002) Sulfonylurea receptor type 1 knock-out mice have intact feeding-stimulated insulin secretion despite marked impairment in their response to glucose. J Biol Chem 277:37176–37183PubMedCrossRef
65.
go back to reference Ravier MA, Nenquin M, Miki T, Seino S, Henquin JC (2009) Glucose controls cytosolic Ca2+ and insulin secretion in mouse islets lacking adenosine triphosphate-sensitive K+ channels owing to a knockout of the pore-forming subunit Kir6.2. Endocrinology 150:33–45PubMedCrossRef Ravier MA, Nenquin M, Miki T, Seino S, Henquin JC (2009) Glucose controls cytosolic Ca2+ and insulin secretion in mouse islets lacking adenosine triphosphate-sensitive K+ channels owing to a knockout of the pore-forming subunit Kir6.2. Endocrinology 150:33–45PubMedCrossRef
66.
go back to reference Gloyn AL, Pearson ER, Antcliff JF et al (2004) Activating mutations in the gene encoding the ATP-sensitive potassium-channel subunit Kir6.2 and permanent neonatal diabetes. N Engl J Med 350:1838–1849PubMedCrossRef Gloyn AL, Pearson ER, Antcliff JF et al (2004) Activating mutations in the gene encoding the ATP-sensitive potassium-channel subunit Kir6.2 and permanent neonatal diabetes. N Engl J Med 350:1838–1849PubMedCrossRef
67.
go back to reference Remedi MS, Nichols CG (2009) Hyperinsulinism and diabetes: genetic dissection of β cell metabolism–excitation coupling in mice. Cell Metab 10:442–453PubMedCrossRef Remedi MS, Nichols CG (2009) Hyperinsulinism and diabetes: genetic dissection of β cell metabolism–excitation coupling in mice. Cell Metab 10:442–453PubMedCrossRef
68.
go back to reference Ashcroft FM (2010) New uses for old drugs: neonatal diabetes and sulphonylureas. Cell Metab 11:179–181PubMedCrossRef Ashcroft FM (2010) New uses for old drugs: neonatal diabetes and sulphonylureas. Cell Metab 11:179–181PubMedCrossRef
69.
go back to reference Borg WP, During MJ, Sherwin RS, Borg MA, Brines ML, Shulman GI (1994) Ventromedial hypothalamic lesions in rats suppress counterregulatory responses to hypoglycemia. J Clin Invest 93:1677–1682PubMedCrossRef Borg WP, During MJ, Sherwin RS, Borg MA, Brines ML, Shulman GI (1994) Ventromedial hypothalamic lesions in rats suppress counterregulatory responses to hypoglycemia. J Clin Invest 93:1677–1682PubMedCrossRef
70.
go back to reference Miki T, Liss B, Minami K et al (2001) ATP-sensitive K+ channels in the hypothalamus are essential for the maintenance of glucose homeostasis. Nat Neurosci 4:507–512PubMed Miki T, Liss B, Minami K et al (2001) ATP-sensitive K+ channels in the hypothalamus are essential for the maintenance of glucose homeostasis. Nat Neurosci 4:507–512PubMed
71.
go back to reference MacDonald PE, de Marinis YZ, Ramracheya R et al (2007) A KATP channel-dependent pathway within α cells regulates glucagon release from both rodent and human islets of Langerhans. PLoS Biol 5:e143PubMedCrossRef MacDonald PE, de Marinis YZ, Ramracheya R et al (2007) A KATP channel-dependent pathway within α cells regulates glucagon release from both rodent and human islets of Langerhans. PLoS Biol 5:e143PubMedCrossRef
72.
go back to reference Wang PH, Moller D, Flier JS, Nayak RC, Smith RJ (1989) Coordinate regulation of glucose transporter function, number, and gene expression by insulin and sulfonylureas in L6 rat skeletal muscle cells. J Clin Invest 84:62–67PubMedCrossRef Wang PH, Moller D, Flier JS, Nayak RC, Smith RJ (1989) Coordinate regulation of glucose transporter function, number, and gene expression by insulin and sulfonylureas in L6 rat skeletal muscle cells. J Clin Invest 84:62–67PubMedCrossRef
73.
go back to reference Pulido N, Casla A, Suarez A, Casanova B, Arrieta FJ, Rovira A (1996) Sulphonylurea stimulates glucose uptake in rats through an ATP-sensitive K+ channel dependent mechanism. Diabetologia 39:22–27PubMed Pulido N, Casla A, Suarez A, Casanova B, Arrieta FJ, Rovira A (1996) Sulphonylurea stimulates glucose uptake in rats through an ATP-sensitive K+ channel dependent mechanism. Diabetologia 39:22–27PubMed
74.
go back to reference Minami K, Morita M, Saraya A et al (2003) ATP-sensitive K+ channel-mediated glucose uptake is independent of IRS-1/phosphatidylinositol 3-kinase signaling. Am J Physiol Endocrinol Metab 285:E1289–E1296PubMed Minami K, Morita M, Saraya A et al (2003) ATP-sensitive K+ channel-mediated glucose uptake is independent of IRS-1/phosphatidylinositol 3-kinase signaling. Am J Physiol Endocrinol Metab 285:E1289–E1296PubMed
75.
go back to reference Chutkow WA, Samuel V, Hansen PA et al (2001) Disruption of Sur2-containing KATP channels enhances insulin-stimulated glucose uptake in skeletal muscle. Proc Natl Acad Sci USA 98:11760–11764PubMedCrossRef Chutkow WA, Samuel V, Hansen PA et al (2001) Disruption of Sur2-containing KATP channels enhances insulin-stimulated glucose uptake in skeletal muscle. Proc Natl Acad Sci USA 98:11760–11764PubMedCrossRef
76.
go back to reference Minami K, Miki T, Kadowaki T, Seino S (2004) Roles of ATP-sensitive K+ channels as metabolic sensors: studies of Kir6.x null mice. Diabetes 53(Suppl 3):S176–S180PubMedCrossRef Minami K, Miki T, Kadowaki T, Seino S (2004) Roles of ATP-sensitive K+ channels as metabolic sensors: studies of Kir6.x null mice. Diabetes 53(Suppl 3):S176–S180PubMedCrossRef
80.
81.
go back to reference Delmeire D, Flamez D, Hinke SA, Cali JJ, Pipeleers D, Schuit F (2003) Type VIII adenylyl cyclase in rat β cells: coincidence signal detector/generator for glucose and GLP-1. Diabetologia 46:1383–1393PubMedCrossRef Delmeire D, Flamez D, Hinke SA, Cali JJ, Pipeleers D, Schuit F (2003) Type VIII adenylyl cyclase in rat β cells: coincidence signal detector/generator for glucose and GLP-1. Diabetologia 46:1383–1393PubMedCrossRef
82.
go back to reference Guenifi A, Portela-Gomes GM, Grimelius L, Efendic S, Abdel-Halim SM (2000) Adenylyl cyclase isoform expression in non-diabetic and diabetic Goto–Kakizaki (GK) rat pancreas. Evidence for distinct overexpression of type-8 adenylyl cyclase in diabetic GK rat islets. Histochem Cell Biol 113:81–89PubMedCrossRef Guenifi A, Portela-Gomes GM, Grimelius L, Efendic S, Abdel-Halim SM (2000) Adenylyl cyclase isoform expression in non-diabetic and diabetic Goto–Kakizaki (GK) rat pancreas. Evidence for distinct overexpression of type-8 adenylyl cyclase in diabetic GK rat islets. Histochem Cell Biol 113:81–89PubMedCrossRef
83.
go back to reference Kashima Y, Miki T, Shibasaki T et al (2001) Critical role of cAMP–GEFII–Rim2 complex in incretin-potentiated insulin secretion. J Biol Chem 276:46046–46053PubMedCrossRef Kashima Y, Miki T, Shibasaki T et al (2001) Critical role of cAMP–GEFII–Rim2 complex in incretin-potentiated insulin secretion. J Biol Chem 276:46046–46053PubMedCrossRef
84.
go back to reference Seino S, Shibasaki T (2005) PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol Rev 85:1303–1342PubMedCrossRef Seino S, Shibasaki T (2005) PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol Rev 85:1303–1342PubMedCrossRef
85.
go back to reference Leiser M, Fleischer N (1996) cAMP-dependent phosphorylation of the cardiac-type α1 subunit of the voltage-dependent Ca2+ channel in a murine pancreatic β-cell line. Diabetes 45:1412–1418PubMedCrossRef Leiser M, Fleischer N (1996) cAMP-dependent phosphorylation of the cardiac-type α1 subunit of the voltage-dependent Ca2+ channel in a murine pancreatic β-cell line. Diabetes 45:1412–1418PubMedCrossRef
86.
go back to reference Safayhi H, Haase H, Kramer U et al (1997) L-type calcium channels in insulin-secreting cells: biochemical characterization and phosphorylation in RINm5F cells. Mol Endocrinol 11:619–629PubMedCrossRef Safayhi H, Haase H, Kramer U et al (1997) L-type calcium channels in insulin-secreting cells: biochemical characterization and phosphorylation in RINm5F cells. Mol Endocrinol 11:619–629PubMedCrossRef
87.
go back to reference Thorens B, Deriaz N, Bosco D et al (1996) Protein kinase A-dependent phosphorylation of GLUT2 in pancreatic β cells. J Biol Chem 271:8075–8081PubMedCrossRef Thorens B, Deriaz N, Bosco D et al (1996) Protein kinase A-dependent phosphorylation of GLUT2 in pancreatic β cells. J Biol Chem 271:8075–8081PubMedCrossRef
88.
go back to reference Sugawara K, Shibasaki T, Mizoguchi A, Saito T, Seino S (2009) Rab11 and its effector Rip11 participate in regulation of insulin granule exocytosis. Genes Cells 14:445–456PubMedCrossRef Sugawara K, Shibasaki T, Mizoguchi A, Saito T, Seino S (2009) Rab11 and its effector Rip11 participate in regulation of insulin granule exocytosis. Genes Cells 14:445–456PubMedCrossRef
89.
go back to reference de Rooij J, Zwartkruis FJ, Verheijen MH et al (1998) Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396:474–477PubMedCrossRef de Rooij J, Zwartkruis FJ, Verheijen MH et al (1998) Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396:474–477PubMedCrossRef
90.
go back to reference Kawasaki H, Springett GM, Mochizuki N et al (1998) A family of cAMP-binding proteins that directly activate Rap1. Science 282:2275–2279PubMedCrossRef Kawasaki H, Springett GM, Mochizuki N et al (1998) A family of cAMP-binding proteins that directly activate Rap1. Science 282:2275–2279PubMedCrossRef
91.
go back to reference de Rooij J, Rehmann H, van Triest M, Cool RH, Wittinghofer A, Bos JL (2000) Mechanism of regulation of the Epac family of cAMP-dependent RapGEFs. J Biol Chem 275:20829–20836PubMedCrossRef de Rooij J, Rehmann H, van Triest M, Cool RH, Wittinghofer A, Bos JL (2000) Mechanism of regulation of the Epac family of cAMP-dependent RapGEFs. J Biol Chem 275:20829–20836PubMedCrossRef
92.
go back to reference Gloerich M, Bos JL (2010) Epac: defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol 50:355–375PubMedCrossRef Gloerich M, Bos JL (2010) Epac: defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol 50:355–375PubMedCrossRef
93.
go back to reference Niimura M, Miki T, Shibasaki T, Fujimoto W, Iwanaga T, Seino S (2009) Critical role of the N-terminal cyclic AMP-binding domain of Epac2 in its subcellular localization and function. J Cell Physiol 219:652–658PubMedCrossRef Niimura M, Miki T, Shibasaki T, Fujimoto W, Iwanaga T, Seino S (2009) Critical role of the N-terminal cyclic AMP-binding domain of Epac2 in its subcellular localization and function. J Cell Physiol 219:652–658PubMedCrossRef
94.
go back to reference Ueno H, Shibasaki T, Iwanaga T et al (2001) Characterization of the gene EPAC2: structure, chromosomal localization, tissue expression, and identification of the liver-specific isoform. Genomics 78:91–98PubMedCrossRef Ueno H, Shibasaki T, Iwanaga T et al (2001) Characterization of the gene EPAC2: structure, chromosomal localization, tissue expression, and identification of the liver-specific isoform. Genomics 78:91–98PubMedCrossRef
95.
go back to reference Ponsioen B, Gloerich M, Ritsma L, Rehmann H, Bos JL, Jalink K (2009) Direct spatial control of Epac1 by cyclic AMP. Mol Cell Biol 29:2521–2531PubMedCrossRef Ponsioen B, Gloerich M, Ritsma L, Rehmann H, Bos JL, Jalink K (2009) Direct spatial control of Epac1 by cyclic AMP. Mol Cell Biol 29:2521–2531PubMedCrossRef
96.
go back to reference Li Y, Asuri S, Rebhun JF, Castro AF, Paranavitana NC, Quilliam LA (2006) The RAP1 guanine nucleotide exchange factor Epac2 couples cyclic AMP and Ras signals at the plasma membrane. J Biol Chem 281:2506–2514PubMedCrossRef Li Y, Asuri S, Rebhun JF, Castro AF, Paranavitana NC, Quilliam LA (2006) The RAP1 guanine nucleotide exchange factor Epac2 couples cyclic AMP and Ras signals at the plasma membrane. J Biol Chem 281:2506–2514PubMedCrossRef
97.
go back to reference Liu C, Takahashi M, Li Y et al (2008) Ras is required for the cyclic AMP-dependent activation of Rap1 via Epac2. Mol Cell Biol 28:7109–7125PubMedCrossRef Liu C, Takahashi M, Li Y et al (2008) Ras is required for the cyclic AMP-dependent activation of Rap1 via Epac2. Mol Cell Biol 28:7109–7125PubMedCrossRef
98.
go back to reference Leech CA, Dzhura I, Chepurny OG et al (2011) Molecular physiology of glucagon-like peptide-1 insulin secretagogue action in pancreatic β cells. Prog Biophys Mol Biol 107:236–247PubMedCrossRef Leech CA, Dzhura I, Chepurny OG et al (2011) Molecular physiology of glucagon-like peptide-1 insulin secretagogue action in pancreatic β cells. Prog Biophys Mol Biol 107:236–247PubMedCrossRef
99.
go back to reference Vandecasteele G, Rochais F, Abi-Gerges A, Fischmeister R (2006) Functional localization of cAMP signalling in cardiac myocytes. Biochem Soc Trans 34:484–488PubMedCrossRef Vandecasteele G, Rochais F, Abi-Gerges A, Fischmeister R (2006) Functional localization of cAMP signalling in cardiac myocytes. Biochem Soc Trans 34:484–488PubMedCrossRef
100.
go back to reference Ozanne SE, Guest PC, Hutton JC, Hales CN (1995) Intracellular localization and molecular heterogeneity of the sulphonylurea receptor in insulin-secreting cells. Diabetologia 38:277–282PubMedCrossRef Ozanne SE, Guest PC, Hutton JC, Hales CN (1995) Intracellular localization and molecular heterogeneity of the sulphonylurea receptor in insulin-secreting cells. Diabetologia 38:277–282PubMedCrossRef
101.
go back to reference Eliasson L, Renstrom E, Ammala C et al (1996) PKC-dependent stimulation of exocytosis by sulfonylureas in pancreatic β cells. Science 271:813–815PubMedCrossRef Eliasson L, Renstrom E, Ammala C et al (1996) PKC-dependent stimulation of exocytosis by sulfonylureas in pancreatic β cells. Science 271:813–815PubMedCrossRef
102.
go back to reference Eliasson L, Ma X, Renstrom E et al (2003) SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B cells. J Gen Physiol 121:181–197PubMedCrossRef Eliasson L, Ma X, Renstrom E et al (2003) SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B cells. J Gen Physiol 121:181–197PubMedCrossRef
103.
go back to reference Zhang CL, Katoh M, Shibasaki T et al (2009) The cAMP sensor Epac2 is a direct target of antidiabetic sulfonylurea drugs. Science 325:607–610PubMedCrossRef Zhang CL, Katoh M, Shibasaki T et al (2009) The cAMP sensor Epac2 is a direct target of antidiabetic sulfonylurea drugs. Science 325:607–610PubMedCrossRef
104.
go back to reference Lakowicz JR (1999) Energy transfer. In: Lakowicz JR (ed) Principles of fluorescence spectroscopy. Kluwer Academic, New York, pp 368–391 Lakowicz JR (1999) Energy transfer. In: Lakowicz JR (ed) Principles of fluorescence spectroscopy. Kluwer Academic, New York, pp 368–391
105.
go back to reference Miyawaki A, Tsien RY (2000) Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol 327:472–500PubMedCrossRef Miyawaki A, Tsien RY (2000) Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol 327:472–500PubMedCrossRef
106.
go back to reference Seino S, Zhang CL, Shibasaki T (2010) Sulfonylurea action re-revisited. J Diabetes Invest 1:37–39CrossRef Seino S, Zhang CL, Shibasaki T (2010) Sulfonylurea action re-revisited. J Diabetes Invest 1:37–39CrossRef
107.
go back to reference Renold AE (1970) Insulin biosynthesis and secretion—a still unsettled topic. N Engl J Med 282:173–182PubMedCrossRef Renold AE (1970) Insulin biosynthesis and secretion—a still unsettled topic. N Engl J Med 282:173–182PubMedCrossRef
Metadata
Title
Cell signalling in insulin secretion: the molecular targets of ATP, cAMP and sulfonylurea
Author
S. Seino
Publication date
01-08-2012
Publisher
Springer-Verlag
Published in
Diabetologia / Issue 8/2012
Print ISSN: 0012-186X
Electronic ISSN: 1432-0428
DOI
https://doi.org/10.1007/s00125-012-2562-9

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