Exocytosis in islet β-cells

Advances in Experimental Medicine and Biology

Volumn 654, Issue , 2010, Pages 305-338

  Kasai, Haruo ^a   Hatakeyama, Hiroyasu ^b   Ohno, Mitsuyo ^b   Takahashi, Noriko ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b NONE

Author keywords

Insulin secretion; Pancreatic islet; Sequential exocytosis; Two photon microscopy

Indexed keywords

4 AMINOBUTYRIC ACID; ADENOSINE TRIPHOSPHATE; BIPHASIC INSULIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUCOSE; KT 5720; MICRORNA; MICRORNA 375; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; NEUROTRANSMITTER; PROTEIN KINASE INHIBITOR; SEROTONIN; SNARE PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; UNCLASSIFIED DRUG; CALCIUM; INSULIN;

ARTICLE; CELL COMPOSITION; CELL GRANULE; CELL VACUOLE; CROSS PRESENTATION; DIFFUSION; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; ENZYME REGULATION; EXOCYTOSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; FUSION PORE; INSULIN RELEASE; KINETICS; LARGE DENSE CORE VESICLE; MICROSCOPY; MOLECULAR BIOLOGY; MOLECULAR DOCKING; NONHUMAN; NUCLEAR PORE; OPTICAL TOMOGRAPHY; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN FUNCTION; SYNAPTIC LIKE MICROVESICLE; TOTAL INTERNAL REFLECTION FIELD MICROSCOPY; TWO PHOTON EXTRACELLULAR POLAR TRACER IMAGING; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; CYTOSOL; HUMAN; METABOLISM; METHODOLOGY; PHOTON; REVIEW; SECRETION; TIME;

ANIMALS; CALCIUM; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOSOL; ELECTROPHYSIOLOGY; EXOCYTOSIS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; KINETICS; MICROSCOPY; MODELS, BIOLOGICAL; PHOTONS; TIME FACTORS;

EID: 77953954950     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-90-481-3271-3_14     Document Type: Article

References (157)

1. Dean PM. Ultrastructural morphometry of the pancreatic beta-cell. Diabetologia 1973;9:115-9.
2. Takahashi N, Hatakeyama H, Okado H, Miwa A, Kishimoto T, Kojima T, Abe T, Kasai H. Sequential exocytosis of insulin granules is associated with redistribution of SNAP25. J Cell Biol 2004;165:255-62. (Pubitemid 38544528)
3. Kasai H, Hatakeyama H, Kishimoto T, Liu T-T, Nemoto T, Takahashi N. A new quantitative (two-photon extracellular polar-tracer imaging-based quantification (TEPIQ)) analysis for diameters of exocytic vesicles and its application to mouse pancreatic islets. J Physiol 2005;568:891-903. (Pubitemid 41646029)
4. Dudek RW, Boyne AF. An excursion through the ultrastructural world of quick-frozen pancreatic islets. Am J Anat 1986;175:217-43, 354. (Pubitemid 16128875)
5. Plattner H, Artalejo AR, Neher E. Ultrastructural organization of bovine chromaffin cell cortex-analysis by cryofixation and morphometry of aspects pertinent to exocytosis. J Cell Biol 1997;139:1709-17. (Pubitemid 28079236)
6. Kahn CR. Joslin's Diabetes Mellitus. Lippincott Williams 2004; & Wilkins, Philadelphia,.
7. Henquin JC (2000) Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 49:1751-60.
8. Vaag A, Henriksen JE, Madsbad S, Holm N, Beck-Nielsen H. Insulin secretion, insulin action, and hepatic glucose production in identical twins discordant for non-insulindependent diabetes mellitus. J Clin Invest 1995;95:690-8.
9. Thomas-Reetz AC, De Camilli P. A role for synaptic vesicles in non-neuronal cells: clues from pancreatic β cells and from chromaffin cells. FASEB J 1994;8:209-16.
10. Hatakeyama H, Takahashi N, Kishimoto T, Nemoto T, Kasai H. Two cAMP-dependent pathways differentially regulate exocytosis of large dense-core and small vesicles in mouse beta-cells. J Physiol 2007;582:1087-98. (Pubitemid 47104342)
11. Dan Y, Poo M. Quantal transmitter secretion from myocytes loaded with acetylcholine. Nature 1992;359:733-6.
12. Borgonovo B, Cocucci E, Racchetti G, Podini P, Bachi A,Meldolesi J. Regulated exocytosis: a novel, widely expressed system. Nat Cell Biol 2002;4:955-62. (Pubitemid 35469425)
13. Kasai H. Comparative biology of exocytosis: Implications of kinetic diversity for secretory function. Trends Neurosci 1999;22:88-93. (Pubitemid 29125556)
14. McNeil PL, Steinhardt RA. Plasma membrane disruption: repair, prevention, adaptation. Annu Rev Cell Dev Biol 2003;19:697-731. (Pubitemid 37487366)
15. Steinhardt RA, Bi G, Alderton JM. Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release. Science 1994;263:390-3. (Pubitemid 24067947)
16. Maritzen T, Keating DJ, Neagoe I, Zdebik AA, Jentsch TJ. Role of the vesicular chloride transporter ClC-3 in neuroendocrine tissue. J Neurosci 2008;28:10587-98.
17. Rothman JE. Mechanisms of intracellular protein transport. Nature 1994;372:55-63. (Pubitemid 24339484)
18. Sudhof TC. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 1995;375:645-53.
19. Mochida S. Protein-protein interactions in neurotransmitter release. Neurosci Res 2000;36:175-82. (Pubitemid 30100582)
20. Jahn R, Lang T, Sudhof TC. Membrane fusion. Cell 2003;112:519-33. (Pubitemid 36263084)
21. Lang J. Molecular mechanisms and regulation of insulin exocytosis as a paradigm of endocrine secretion. Eur J Biochem 1999;259:3-17. (Pubitemid 29030812)
22. Gerber SH, Sudhof TC. Molecular determinants of regulated exocytosis. Diabetes 51 Suppl 2002;1:S3-11. (Pubitemid 34761486)
23. Gomi H, Mizutani S, Kasai K, Itohara S, Izumi T. Granuphilin molecularly docks insulin granules to the fusion machinery. J Cell Biol 2005;171:99-109. (Pubitemid 41434605)
24. Kasai K, Ohara-Imaizumi M, Takahashi N, Mizutani S, Zhao S, Kikuta T, Kasai H, Nagamatsu S, Gomi H, Izumi T. Rab27a mediates the tight docking of insulin granules onto the plasma membrane during glucose stimulation. J Clin Invest 2005;115:388-96. (Pubitemid 40385480)
25. Nemoto T, Kimura R, Ito K, Tachikawa A, Miyashita Y, Iino M, Kasai H. Sequentialreplenishment mechanism of exocytosis in pancreatic acini. Nat Cell Biol 2001;3:253-8. (Pubitemid 32201320)
26. Takahashi N, Kishimoto T, Nemoto T, Kadowaki T, Kasai H. Fusion pore dynamics and insulin granule exocytosis in the pancreatic islet. Science 2002;297:1349-52. (Pubitemid 34913173)
27. Nemoto T, Kojima T, Oshima A, Bito H, Kasai H. Stabilization of exocytosis by dynamic F-actin coating of zymogen granules in pancreatic acini. J Biol Chem 2004;279:37544-50. (Pubitemid 39195467)
28. Oshima A, Kojima T, Dejima K, Hisa I, Kasai H, Nemoto T. Two-photon microscopic analysis of acetylcholine-induced mucus secretion in guinea pig nasal glands. Cell Calcium 2005;37:349-57. (Pubitemid 40331453)
29. Kishimoto T, Liu TT, Hatakeyama H, Nemoto T, Takahashi N, Kasai H. Sequential compound exocytosis of large dense-core vesicles in PC12 cells studied with TEPIQ analysis. J Physiol 2005;568:905-15.
30. Liu TT, Kishimoto T, Hatakeyama H, Nemoto T, Takahashi N, Kasai H. Exocytosis and endocytosis of small vesicles in PC12 cells studied with TEPIQ analysis. J Physiol 2005;568:917-29.
31. Hatakeyama H, Kishimoto T, Nemoto T, Kasai H, Takahashi N. Rapid glucose sensing by protein kinase A for insulin exocytosis in mouse pancreatic islets. J Physiol 2006;570: 271-82.
32. Kishimoto T, Kimura R, Liu T-T, Nemoto T, Takahashi N, Kasai H. Vacuolar sequential exocytosis of large dense-core vesicles in adrenal medulla. EMBO J 2006;25:673-82. (Pubitemid 43292430)
33. Neher E, Marty A. Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc Natl Acad Sci USA 1982;79:6712-16. (Pubitemid 13220246)
34. Klyachko VA, Jackson MB. Capacitance steps and fusion pores of small and large-densecore vesicles in nerve terminals. Nature 2002;418:89-92. (Pubitemid 34742576)
35. MacDonald PE, Obermuller S, Vikman J, Galvanovskis J, Rorsman P, Eliasson L. Regulated exocytosis and kiss-and-run of synaptic-like microvesicles in INS-1 and primary rat betacells. Diabetes 2005;54:736-43. (Pubitemid 40322076)
36. Alvarez De Toledo G, Fernadez-Chacon R, Fernandez JM. Release of secretory products during transient vesicle fusion. Nature 1993;363:554-8. (Pubitemid 23186644)
37. Albillos A, Dernick G, Horstmann H, Almers W, Alvarez de Toledo G, Lindau M. The exocytotic event in chromaffin cells revealed by patch amperometry. Nature 1997;389: 509-12. (Pubitemid 27435328)
38. Takahashi N, Kadowaki T, Yazaki Y, Miyashita Y, Kasai H. Multiple exocytotic pathways in pancreatic β cells. J Cell Biol 1997;138:55-64. (Pubitemid 27337452)
39. Smith CB, Betz WJ. Simultaneous independent measurement of endocytosis and exocytosis. Nature 1996;380:531-4. (Pubitemid 26110642)
40. 2+ compounds. J Physiol (Lond 1996;) 494:53-65. (Pubitemid 26238001)
41. Zhou Z, Misler S. Amperometric detection of quantal secretion from patch-clamped rat pancreatic β-cells. J Biol Chem 1996;270:270-7. (Pubitemid 26026589)
42. Kirillova J, Thomas P, Almers W. Two independently regulated secretory pathways in mast cells. J Physiol 1993);(Paris) 87:203-8. (Pubitemid 23263505)
43. Oberhauser AF, Robinson I, Fernandez JM. Simultaneous capacitance and amperometric measurements of exocytosis: A comparison. Biophys J 1996;71:1131-9. (Pubitemid 26289195)
44. Ninomiya Y, Kishimoto T, Yamazawa T, Ikeda H, Miyashita Y, Kasai H. Kinetic diversity in the fusion of exocytotic vesicles. EMBO J 1997;16:929-34. (Pubitemid 27113172)
45. Haller M, Heinemann C, Chow RH, Heidelberger R, Neher E. Comparison of secretory responses as measured by membrane capacitance and by amperometry. Biophys J 1998;74:2100-13. (Pubitemid 28157945)
46. Karanauskaite J, Hoppa MB, Braun M, Galvanovskis J, Rorsman P. Quantal ATP release in rat beta-cells by exocytosis of insulin-containing LDCVs. Pflugers Arch 2009; 458: 389-401.
47. Hollins B, Ikeda SR (1997) Heterologous expression of a P2x-purinoceptor in rat chromaffin cells detects vesicular ATP release. J Neurophysiol 78:3069-76 (Pubitemid 28098815)
48. Obermuller S, Lindqvist A, Karanauskaite J, Galvanovskis J, Rorsman P, Barg S. Selective nucleotide-release from dense-core granules in insulin-secreting cells. J Cell Sci 2005;118:4271-82. (Pubitemid 41488964)
49. Braun M, Wendt A, Birnir B, Broman J, Eliasson L, Galvanovskis J, Gromada J, Mulder H, Rorsman P. Regulated exocytosis of GABA-containing synaptic-like microvesicles in pancreatic beta-cells. J Gen Physiol 2004;123:191-204. (Pubitemid 38282970)
50. Braun M, Wendt A, Karanauskaite J, Galvanovskis J, Clark A, MacDonald PE, Rorsman P. Corelease and differential exit via the fusion pore of GABA, serotonin, and ATP from LDCV in rat pancreatic beta cells. J Gen Physiol 2007;129:221-31. (Pubitemid 46333924)
51. Steyer JA, Horstmann H, Almers W. Transport, docking and exocytosis of single secretory granules in live chromaffin cells. Nature 1997;388:474-8. (Pubitemid 27328925)
52. Oheim M, Loerke D, Stuhmer W, Chow RH. The last few milliseconds in the life of a secretory granule. Docking, dynamics and fusion visualized by total internal reflection fluorescence microscopy (TIRFM). Eur Biophys J 1998;27:83-98. (Pubitemid 28123529)
53. Tsuboi T, Terakawa S, Scalettar BA, Fantus C, Roder J, Jeromin A. Sweeping model of dynamin activity. Visualization of coupling between exocytosis and endocytosis under an evanescent wave microscope with green fluorescent proteins. J Biol Chem 2002;277: 15957-61. (Pubitemid 34967877)
54. Ohara-Imaizumi M, Fujiwara T, Nakamichi Y, Okamura T, Akimoto Y, Kawai J, Matsushima S, Kawakami H, Watanabe T, Akagawa K, Nagamatsu S. Imaging analysis reveals mechanistic differences between first- and second-phase insulin exocytosis. J Cell Biol 2007;177:695-705. (Pubitemid 46799840)
55. Kasai K, Fujita T, Gomi H, Izumi T. Docking is not a prerequisite but a temporal constraint for fusion of secretory granules. Traffic 2008;9:1191-203. (Pubitemid 351916892)
56. Shibasaki T, Takahashi H, Miki T, Sunaga Y, Matsumura K, Yamanaka M, Zhang C, Tamamoto A, Satoh T, Miyazaki J, Seino S. Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci U S A 2007;104:19333-8.
57. Allersma MW, Wang L, Axelrod D, Holz RW. Visualization of regulated exocytosis with a granule-membrane probe using total internal reflection microscopy. Mol Biol Cell 2004;15:4658-68. (Pubitemid 39299112)
58. Toonen RF, Kochubey O, de WH, Gulyas-Kovacs A, Konijnenburg B, Sorensen JB, Klingauf J, Verhage M. Dissecting docking and tethering of secretory vesicles at the target membrane. EMBO J 2006;25:3725-37. (Pubitemid 44300259)
59. Verhage M, Sorensen JB. Vesicle docking in regulated exocytosis. Traffic 2008;9:1414-24.
60. Michael DJ, Geng X, Cawley NX, Loh YP, Rhodes CJ, Drain P, Chow RH. Fluorescent cargo proteins in pancreatic beta-cells: design determines secretion kinetics at exocytosis. Biophys J 2004;87:L03-5. (Pubitemid 39602872)
61. Kasai H, Kishimoto T, Nemoto T, Hatakeyama H, Liu TT, Takahashi N. Two-photon excitation imaging of exocytosis and endocytosis and determination of their spatial organization. Adv Drug Deliv Rev 2006;58:850-77. (Pubitemid 44709259)
62. Fukui K, Yang Q, Cao Y, Takahashi N, Hatakeyama H, Wang H, Wada J, Zhang Y, Marselli L, Nammo T, Yoneda K, Onishi M, Higashiyama S, Matsuzawa Y, Gonzalez FJ, Weir GC, Kasai H, Shimomura I, Miyagawa J, Wollheim CB, Yamagata K. The HNF- 1 target collectrin controls insulin exocytosis by SNARE complex formation. Cell Metab 2005;2:373-84.
63. Miura A, Yamagata K, Kakei M, Hatakeyama H, Takahashi N, Fukui K, Nammo T, Yoneda K, Inoue Y, Sladek FM, Magnuson MA, Kasai H, Miyagawa J, Gonzalez FJ, Shimomura I. Hepatocyte nuclear factor-4alpha is essential for glucose-stimulated insulin secretion by pancreatic beta-cells. J Biol Chem 2006;281:5246-57. (Pubitemid 43847789)
64. Speidel D, Salehi A, Obermueller S, Lundquist I, Brose N, Renstrom E, Rorsman P. CAPS1 and CAPS2 regulate stability and recruitment of insulin granules in mouse pancreatic beta cells. Cell Metab 2008;7:57-67.
65. Ma L, Bindokas VP, Kuznetsov A, Rhodes C, Hays L, Edwardson JM, Ueda K, Steiner DF, Philipson LH. Direct imaging shows that insulin granule exocytosis occurs by complete vesicle fusion. Proc Natl Acad Sci U S A 2004;101:9266-71. (Pubitemid 38812864)
66. Michael DJ, Ritzel RA, Haataja L, Chow RH. Pancreatic beta-cells secrete insulin in fastand slow-release forms. Diabetes 2006;55:600-7. (Pubitemid 43343215)
67. Scepek S, Lindau M. Focal exocytosis by eosinophils - compound exocytosis and cumulative fusion. EMBO J 1993;12:1811-7. (Pubitemid 23157696)
68. Hafez I, Stolpe A, Lindau M. Compound exocytosis and cumulative fusion in eosinophils. J Biol Chem 2003;278:44921-8. (Pubitemid 37377251)
69. Alvarez de Toledo G, Fernandez JM. Compound versus multigranular exocytosis in peritoneal mast cells. J Gen Physiol 1990;95:397-409. (Pubitemid 20109756)
70. Klenchin VA, Martin TF. Priming in exocytosis: attaining fusion-competence after vesicle docking. Biochimie 2000;82:399-407. (Pubitemid 30391896)
71. Rizzoli SO, Betz WJ. The structural organization of the readily releasable pool of synaptic vesicles. Science 2004;303:2037-9. (Pubitemid 38393282)
72. Bonner-Weir S. Morphological evidence for pancreatic polarity of β-cell within islets of Langerhans. Diabetes 1988;37:616-21.
73. In't VP, Pipeleers DG, Gepts W. Evidence against the presence of tight junctions in normal endocrine pancreas. Diabetes 1984;33:101-4. (Pubitemid 14187212)
74. Heuser JE, Reese TS. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 1973;57:315-44.
75. Kwan EP, Gaisano HY. Glucagon-like peptide 1 regulates sequential and compound exocytosis in pancreatic islet beta-cells. Diabetes 2005;54:2734-43. (Pubitemid 41233597)
76. Breckenridge LJ, Almers W. Currents through the fusion pore that forms during exocytosis of a secretory vesicle. Nature 1987;328:814-7. (Pubitemid 17125959)
77. Zhou Z, Misler S, Chow RH. Rapid fluctuations in transmitter release from single vesicles in bovine adrenal chromaffin cells. Biophys J 1996;70:1543-52. (Pubitemid 26073067)
78. Dodson G, Steiner D. The role of assembly in insulin's biosynthesis. Curr Opin Struct Biol 1998;8:189-94. (Pubitemid 28221050)
79. Barg S, Olofsson CS, Schriever-Abeln J, Wendt A, Gebre-Medhin S, Renstrom E, Rorsman P. Delay between fusion pore opening and peptide release from large dense-core vesicles in neuroendocrine cells. Neuron 2002;33:287-99. (Pubitemid 34127760)
80. Tsuboi T, McMahon HT, Rutter GA. Mechanisms of dense core vesicle recapture following "kiss and run" ("cavicapture") exocytosis in insulin-secreting cells. J Biol Chem 2004;279:47115-24. (Pubitemid 39518368)
81. Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol 2002;157:1071-82.
82. Taraska JW, Perrais D, Ohara-Imaizumi M, Nagamatsu S, Almers W. Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc Natl Acad Sci U S A 2003;100:2070-5. (Pubitemid 36254575)
83. Chernomordik LV, Kozlov MM. Membrane hemifusion: crossing a chasm in two leaps. Cell 2005;123:375-82. (Pubitemid 41546669)
84. Thorn P, Fogarty KE, Parker I. Zymogen granule exocytosis is characterized by long fusion pore openings and preservation of vesicle lipid identity. Proc Natl Acad Sci U S A 2004;101:6774-9. (Pubitemid 38586050)
85. Han X, Wang CT, Bai J, Chapman ER, Jackson MB. Transmembrane segments of syntaxin line the fusion pore of Ca2+-triggered exocytosis. Science 2004;304:289-92. (Pubitemid 38452181)
86. Pickett JA, Thorn P, Edwardson JM. The plasma membrane Q-SNARE syntaxin 2 enters the zymogen granule membrane during exocytosis in the pancreatic acinar cell. J Biol Chem 2005;280:1506-11.
87. Persaud SJ, Jones PM, Howell SL. Glucose-stimulated insulin secretion is not dependent on activation of protein kinase A. Biochem Biophys Res Com 1990;173:833-9.
88. Lester LB, Langeberg LK, Scott JD. Anchoring of protein kinase A facilitates hormonemediated insulin secretion. Proc Natl Acad Sci U S A 1997;94:14942-7. (Pubitemid 28041479)
89. Harris TE, Persaud SJ, Jones PM. Pseudosubstrate inhibition of cyclic AMP-dependent protein kinase in intact pancreatic islets: effects on cyclic AMP-dependent and glucosedependent insulin secretion. Biochem Biophys Res Com 1997;232:648-51. (Pubitemid 27214051)
90. Takahashi N, Nemoto T, Kiumra R, Tachikawa A, Miwa A, Okado H, Miyashita Y, Iino M, Kadowaki T, Kasai H. Two-photon excitation imaging of pancreatic islets with various fluorescent probes. Diabetes 2002;51 Suppl. 1:S25-8. (Pubitemid 34761489)
91. 2+ dependent exocytosis in pancreatic β-cells. Proc Natl Acad Sci, U S A 1999;96:760-5. (Pubitemid 29061282)
92. Gembal M, Gilon P, Henquin J. Evidence that glucose can control insulin release independently from its action on ATP-sensitive K+ channels in mouse B cells. J Clin Invest 1992;89:1288-95.
93. Aizawa T, Sato Y, Ishihara F, Taguchi N, Komatsu M, Suzuki N, Hashizume K, Yamada T. ATP-sensitive K+ channel-independent glucose action in rat pancreatic β-cell. Am J Physiol 1994;266:C622-7.
94. 2+ and insulin secretion in mouse islets lacking adenosine triphosphate-sensitive K+ channels owing to a knockout of the pore-forming subunit Kir6.2. Endocrinology 2009;150:33-45.
95. 2+-dependent insulin exocytosis in pancreatic β-cells. Diabetes 2001;51:S19-24.
96. Charles MA, Fanska R, Schmid FG, Forsham PH, Grodsky GM. Adenosine 3',5'- monophosphate in pancreatic islets: glucose-induced insulin release. Science 1973;179: 569-71.
97. Valverde I, Vandermeers A, Anjaneyulu R,Malaisse WJ. Calmodulin activation of adenylate cyclase in pancreatic islets. Science 1979;206:225-27.
98. Hellman B, Idahl LA, Lernmark A, Taljedal IB. The pancreatic beta-cell recognition of insulin secretagogues: does cyclic AMP mediate the effect of glucose? Proc Natl Acad Sci U S A 1974;71:3405-9.
99. Dyachok O, Idevall-Hagren O, Sagetorp J, Tian G, Wuttke A, Arrieumerlou C, Akusjarvi G, Gylfe E, Tengholm A. Glucose-induced cyclic AMP oscillations regulate pulsatile insulin secretion. Cell Metab 2008;8:26-37. (Pubitemid 351859229)
100. Tengholm A, Gylfe E. Oscillatory control of insulin secretion. Mol Cell Endocrinol 2009;297:58-72.
101. Enserink JM, Christensen AE, de RJ, van TM, Schwede F, Genieser HG, Doskeland SO, Blank JL, Bos JL. A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat Cell Biol 2002;4:901-6. (Pubitemid 35331366)
102. 2+ in rat pancreatic β-cells. Diabetes 1996;45:295-301.
103. 2+-induced Ca2+ release in mouse pancreatic beta cells. J Physiol 2005;566:173-88. (Pubitemid 40984212)
104. Islam MS. The ryanodine receptor calcium channel of beta-cells: molecular regulation and physiological significance. Diabetes 2002;51:1299-309.
105. MacDonald PE, Braun M, Galvanovskis J, Rorsman P. Release of small transmitters through kiss-and-run fusion pores in rat pancreatic beta cells. Cell Metab 2006;4:283-90. (Pubitemid 44430913)
106. Gustavsson N, Wei SH, Hoang DN, Lao Y, Zhang Q, Radda GK, Rorsman P, Sudhof TC, Han W. Synaptotagmin-7 is a principal Ca2+-sensor for Ca2+-induced glucagon exocytosis in pancreas. J Physiol 2009;
107. Gauthier BR, Wollheim CB (2008) Synaptotagmins bind calcium to release insulin. Am J Physiol Endocrinol Metab 295:E1279-86
108. Monterrat C, Grise F, Benassy MN, Hemar A, Lang J. The calcium-sensing protein synaptotagmin 7 is expressed on different endosomal compartments in endocrine, neuroendocrine cells or neurons but not on large dense core vesicles. Histochem Cell Biol 2007;127:625-32. (Pubitemid 46879055)
109. Grise F, Taib N, Monterrat C, Lagree V, Lang J. Distinct roles of the C2A and the C2B domain of the vesicular Ca2+ sensor synaptotagmin 9 in endocrine beta-cells. Biochem J 2007;403:483-92. (Pubitemid 46706976)
110. Nagy G, Reim K, Matti U, Brose N, Binz T, Rettig J, Neher E, Sorensen JB. Regulation of releasable vesicle pool sizes by protein kinase A-dependent phosphorylation of SNAP-25. Neuron 2004;41:417-29. (Pubitemid 38228352)
111. Chheda MG, Ashery U, Thakur P, Rettig J, Sheng ZH. Phosphorylation of Snapin by PKA modulates its interaction with the SNARE complex. Nat Cell Biol 2001;3:331-8. (Pubitemid 32288439)
112. Kashima Y, Miki T, Shibasaki T, Ozaki N, Miyazaki M, Yano H, Seino S. Critical role of cAMP-GEFII-Rim2 complex in incretin-potentiated insulin secretion. J Biol Chem 2001;276:46046-53.
113. Ozaki N, Shibasaki T, Kashima Y, Miki T, Takahashi K, Ueno H, Sunaga Y, Yano H, Matsuura Y, Iwanaga T, Takai Y, Seino S. cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat Cell Biol 2000;2:805-11.
114. Kwan EP, Xie L, Sheu L, Ohtsuka T, Gaisano HY. Interaction between Munc13-1 and RIM is critical for glucagon-like peptide-1 mediated rescue of exocytotic defects in Munc13-1 deficient pancreatic beta-cells. Diabetes 2007;56:2579-88. (Pubitemid 47523266)
115. Lonart G, Schoch S, Kaeser PS, Larkin CJ, Sudhof TC, Linden DJ. Phosphorylation of RIM1alpha by PKA triggers presynaptic long-term potentiation at cerebellar parallel fiber synapses. Cell 2003;115:49-60. (Pubitemid 37255317)
116. Ivarsson R, Jing X, Waselle L, Regazzi R, Renstrom E. Myosin 5a controls insulin granule recruitment during late-phase secretion. Traffic 2005;6:1027-35. (Pubitemid 41472461)
117. Wang Z, Oh E, Thurmond DC. Glucose-stimulated Cdc42 signaling is essential for the second phase of insulin secretion. J Biol Chem 2007;282:9536-46. (Pubitemid 47104622)
118. Nevins AK, Thurmond DC. A direct interaction between Cdc42 and vesicle-associated membrane protein 2 regulates SNARE-dependent insulin exocytosis. J Biol Chem 2005;280:1944-52.
119. Jing X, Li DQ, Olofsson CS, Salehi A, Surve VV, Caballero J, Ivarsson R, Lundquist I, Pereverzev A, Schneider T, Rorsman P, Renstrom E. CaV2.3 calcium channels control second-phase insulin release. J Clin Invest 2005;115:146-54. (Pubitemid 40385515)
120. Knoch KP, Meisterfeld R, Kersting S, Bergert H, Altkruger A, Wegbrod C, Jager M, Saeger HD, Solimena M. cAMP-dependent phosphorylation of PTB1 promotes the expression of insulin secretory granule proteins in beta cells. Cell Metab 2006;3:123-34.
121. Henquin JC, Nenquin M, Szollosi A, Kubosaki A, Louis NA. Insulin secretion in islets from mice with a double knockout for the dense core vesicle proteins islet antigen-2 (IA-2) and IA-2beta. J Endocrinol 2008;196:573-81. (Pubitemid 351425513)
122. Varadi A, Tsuboi T, Rutter GA. Myosin Va transports dense core secretory vesicles in pancreatic MIN6 beta-cells. Mol Biol Cell 2005;16:2670-80. (Pubitemid 40741215)
123. Tomas A, Meda P, Regazzi R, Pessin JE, Halban PA. Munc 18-1 and granuphilin collaborate during insulin granule exocytosis. Traffic 2008;9:813-32. (Pubitemid 351494309)
124. Cheviet S, Coppola T, Haynes LP, Burgoyne RD, Regazzi R. The Rab-binding protein Noc2 is associated with insulin-containing secretory granules and is essential for pancreatic betacell exocytosis. Mol Endocrinol 2004;18:117-26. (Pubitemid 38073159)
125. Matsumoto M, Miki T, Shibasaki T, Kawaguchi M, Shinozaki H, Nio J, Saraya A, Koseki H, Miyazaki M, Iwanaga T, Seino S. Noc2 is essential in normal regulation of exocytosis in endocrine and exocrine cells. Proc Natl Acad Sci U S A 2004;101:8313-8. (Pubitemid 38736572)
126. Lopez JA, Kwan EP, Xie L, He Y, James DE, Gaisano HY. The RalA GTPase is a central regulator of insulin exocytosis from pancreatic islet beta cells. J Biol Chem 2008;283:17939-45.
127. Sumara G, Formentini I, Collins S, Sumara I, Windak R, Bodenmiller B, Ramracheya R, Caille D, Jiang H, Platt KA, Meda P, Aebersold R, Rorsman P, Ricci R. Regulation of PKD by theMAPK p38delta in insulin secretion and glucose homeostasis. Cell 2009;136:235-48.
128. Illies C, Gromada J, Fiume R, Leibiger B, Yu J, Juhl K, Yang SN, Barma DK, Falck JR, Saiardi A, Barker CJ, Berggren PO. Requirement of inositol pyrophosphates for full exocytotic capacity in pancreatic beta cells. Science 2007;318:1299-302. (Pubitemid 350172894)
129. Reese C, Heise F, Mayer A. Trans-SNARE pairing can precede a hemifusion intermediate in intracellular membrane fusion. Nature 2005;436:410-4. (Pubitemid 41059052)
130. Larsson S, Wierup N, Sundler F, Eliasson L, Holm C. Lack of cholesterol mobilization in islets of hormone-sensitive lipase deficient mice impairs insulin secretion. Biochem Biophys Res Commun 2008;376:558-62.
131. Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, Macdonald PE, Pfeffer S, Tuschl T, Rajewsky N, Rorsman P, Stoffel M. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004;432:226-30. (Pubitemid 39545853)
132. Poy MN, Hausser J , Trajkovski M, Braun M, Collins S, Rorsman P, Zavolan M, Stoffel M. miR-375 maintains normal pancreatic {alpha}- and {beta}-cell mass. Proc Natl Acad Sci U S 2009;A.
133. Lovis P, Gattesco S, Regazzi R (2008) Regulation of the expression of components of the exocytotic machinery of insulin-secreting cells by microRNAs. Biol Chem 389:305-12 (Pubitemid 351329024)
134. Gao N, White P, Doliba N, Golson ML, Matschinsky FM, Kaestner KH. Foxa2 controls vesicle docking and insulin secretion in mature Beta cells. Cell Metab 2007;6:267-79. (Pubitemid 47450186)
135. Plaisance V, Abderrahmani A, Perret-Menoud V, Jacquemin P, Lemaigre F, Regazzi R. MicroRNA-9 controls the expression of Granuphilin/Slp4 and the secretory response of insulin-producing cells. J Biol Chem 2006;281:26932-42. (Pubitemid 44401722)
136. Lovis P, Roggli E, Laybutt DR, Gattesco S, Yang JY,Widmann C, Abderrahmani A, Regazzi R. Alterations in microRNA expression contribute to fatty acid-induced pancreatic beta-cell dysfunction. Diabetes 2008;57:2728-36.
137. Rebois RV, Reynolds EE, Toll L, Howard BD. Storage of dopamine and acetylcholine in granules of PC12, a clonal pheochromocytoma cell line. Biochemistry 1980;19:1240-8. (Pubitemid 10033206)
138. Harata N, Ryan TA, Smith SJ, Buchanan J, Tsien RW. Visualizing recycling synaptic vesicles in hippocampal neurons by FM 1-43 photoconversion. Proc Natl Acad Sci USA 2001;98:12748-53. (Pubitemid 33020017)
139. Brumback AC, Lieber JL, Angleson JK, Betz WJ. Using FM1-43 to study neuropeptide granule dynamics and exocytosis. Methods 2004;33:287-94. (Pubitemid 38746616)
140. Orci L, Malaisse-Lagae F, Ravazzola M, Amherdt M, Renold AE. Exocytosis-endocytosis coupling in the pancreatic beta cell. Science 1973;181:561-2.
141. 2+ triggered massive exocytosis in Chinese hamster ovary cells. EMBO J 1996;15:3787-91. (Pubitemid 26289788)
142. 2+ compound. J Biol Chem 1996;271:17751-4. (Pubitemid 26250748)
143. Ito K, Miyashita Y, Kasai H. Micromolar and submicromolar Ca2+ spikes regulating distinct cellular functions in pancreatic acinar cells. EMBO J 1997;16:242-51. (Pubitemid 27049382)
144. McNeil PL, Steinhardt RA. Loss, restoration, and maintenance of plasma membrane integrity. J Cell Biol 1997;137:1-4. (Pubitemid 27167290)
145. Renstrom E, Eliasson L, Rorsman P. Protein kinase A-dependent and -independent stimulation of exocytosis by cAMP in mouse pancreatic B-cells. J Physiol 1997;502:105-18. (Pubitemid 27322979)
146. Eliasson L, Ma X, Renstrom E, Barg S, Berggren PO, Galvanovskis J, Gromada J, Jing X, Lundquist I, Salehi A, Sewing S, Rorsman P. SUR1 regulates PKA-independent cAMPinduced granule priming in mouse pancreatic B-cells. J Gen Physiol 2003;121:181-97. (Pubitemid 36292989)
147. Sedej S, Rose T, Rupnik M. cAMP increases Ca2+-dependent exocytosis through both PKA and Epac2 in mouse melanotrophs from pituitary tissue slices. J Physiol 2005;567:799-813. (Pubitemid 41387827)
148. John J, Sohmen R, Feuerstein J, Linke R,Wittinghofer A, Goody RS. Kinetics of interaction of nucleotides with nucleotide-free H-ras p21. Biochemistry 1990;29:6058-65. (Pubitemid 20201412)
149. Itzen A, Rak A, Goody RS. Sec2 is a highly efficient exchange factor for the Rab protein Sec4. J Mol Biol 2007;365:1359-67. (Pubitemid 46048839)
150. Ozaki N, Shibasaki T, Kashima Y, Miki T, Takahashi K, Ueno H, Sunaga Y, Yano H, Matsuura Y, Iwanaga T, Takai Y, Seino S. cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat Cell Biol 2000;2:805-11.
151. Wang Y, Okamoto M, Schmitz F, Hofmann K, Sudhof TC. Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 1997;388:593-8. (Pubitemid 27340010)
152. Bernard-Kargar C, Kassis N, Berthault MF, Pralong W, Ktorza A. Sialylated form of the neural cell adhesion molecule (NCAM): a new tool for the identification and sorting of betacell subpopulations with different functional activity. Diabetes 50 Suppl 2001;1:S125-30. (Pubitemid 32148234)
153. Langley OK, etsee-Ufrecht MC, Grant NJ, Gratzl M. Expression of the neural cell adhesion molecule NCAM in endocrine cells. J Histochem Cytochem 1989;37:781-91. (Pubitemid 19156460)
154. Esni F, Taljedal IB, Perl AK, Cremer H, Christofori G, Semb H. Neural cell adhesion molecule (N-CAM) is required for cell type segregation and normal ultrastructure in pancreatic islets. J Cell Biol 1999;144:325-37. (Pubitemid 29066035)
155. Hutton JC, Peshavaria M, Tooke NE. 5-Hydroxytryptamine transport in cells and secretory granules from a transplantable rat insulinoma. Biochem J 1983;210:803-10. (Pubitemid 13092017)
156. Hutton JC. The insulin secretory granule. Diabetologia 1989;32:271-81. (Pubitemid 19166479)
157. Gammelsaeter R, Froyland M, Aragon C, Danbolt NC, Fortin D, Storm-Mathisen J, Davanger S, Gundersen V. Glycine, GABA and their transporters