Novel aspects of the molecular mechanisms controlling insulin secretion

Journal of Physiology

Volumn 586, Issue 14, 2008, Pages 3313-3324

  Eliasson, Lena ^a   Abdulkader, Fernando ^b,c   Braun, Matthias ^b   Galvanovskis, Juris ^b   Hoppa, Michael B ^b   Rorsman, Patrik ^b  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ADENOSINE TRIPHOSPHATE; BIPHASIC INSULIN; CALCIUM CHANNEL; CALCIUM CHANNEL L TYPE; CALCIUM ION; GLIBENCLAMIDE; GLUCOSE; LIPID; PALMITIC ACID; SNARE PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN; SYNTAXIN; AMYLIN; CYTOCHALASIN B; DELAYED RECTIFIER POTASSIUM CHANNEL; NERVE CELL ADHESION MOLECULE; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN; SYNTAXIN 1; ZINC ION;

CELL ULTRASTRUCTURE; EXOCYTOSIS; FEEDBACK SYSTEM; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; HYPERLIPIDEMIA; INSULIN RELEASE; LONG TERM EXPOSURE; MEMBRANE FUSION; MOLECULAR DOCKING; MOLECULAR SIZE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SECRETORY GRANULE; CELL FUNCTION; CELL GRANULE; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE POTENTIAL; CELLULAR PARAMETERS; CELLULAR SECRETION; ELECTRIC ACTIVITY; ENZYME RELEASE; GLUCOSE METABOLISM; HOMEOSTASIS; HUMAN; NEUROTRANSMITTER RELEASE; PHYSIOLOGICAL PROCESS; PROTEIN AGGREGATION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SYNAPSE VESICLE;

ANIMALS; CALCIUM; EXOCYTOSIS; INSULIN; INSULIN-SECRETING CELLS; MICE;

EID: 48949120517     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2008.155317     Document Type: Review

References (90)

1. Ammala C, Eliasson L, Bokvist K, Larsson O, Ashcroft FM & Rorsman P (1993). Exocytosis elicited by action potentials and voltage-clamp calcium currents in individual mouse pancreatic B-cells. J Physiol 472, 665-688.
2. Ashcroft FM & Rorsman P (1989). Electrophysiology of the pancreatic β-cell. Prog Biophys Mol Biol 54, 87-143.
3. A) receptor expression in mouse pancreatic islet α-cells. Diabetes 56, 320-327.
4. Baillyes EM, Guest PC & Hutton JC (1992). Insulin synthesis. In Insulin: Molecular Biology to Pathology, ed. Ashcroft FM & Ashcroft SJH, pp. 64-96. IRL Press, Oxford.
5. 2+ channels in insulin-secreting mouse pancreatic B cells. Biophys J 81, 3308-3323.
6. Barg S, Olofsson CS Schriever-Abeln J, Wendt A, Gebre-Medhin S, Renström E & Rorsman P (2002). Delay between fusion pore opening and peptide release from large dense-core vesicles in neuroendocrine cells. Neuron 33, 287-299.
7. 2+ sensor after all? J Gen Physiol 124, 623-625.
8. Barnard RJ, Morgan A & Burgoyne RD (1997). Stimulation of NSF ATPase activity by α-SNAP is required for SNARE complex disassembly and exocytosis. J Cell Biol 139, 875-883.
9. Bokvist K, Holmqvist M, Gromada J & Rorsman P (2000). Compound exocytosis in voltage-clamped mouse pancreatic β-cells revealed by carbon fibre amperometry. Pflugers Arch 439, 634-645.
10. Braun M, Ramracheya R, Bengtsson M, Zhang Q, Karanauskaite J, Partridge C, Johnson PR & Rorsman P (2008). Voltage-gated ion channels in human pancreatic β-cells. Electrophysiological characterization and role in insulin secretion. Diabetes 57, 1618-1628.
11. Braun M, Wendt A, Birnir B, Broman J, Eliasson L, Galvanovskis J, Gromada J, Mulder H & Rorsman P (2004). Regulated exocytosis of GABA-containing synaptic-like microvesicles in pancreatic β-cells. J Gen Physiol 123, 191-204.
12. Braun M, Wendt A, Karanauskaite J, Galvanovskis J, Clark A, Macdonald PE & Rorsman P (2007). Corelease and differential exit via the fusion pore of GABA, serotonin, and ATP from LDCV in rat pancreatic β cells. J Gen Physiol 129, 221-231.
13. Chow RH, von Ruden L & Neher E (1992). Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature 356, 60-63.
14. Collins SC, Salehi A, Eliasson L, Olofsson CS & Rorsman P (2008). Long-term exposure of mouse pancreatic islets to oleate or palmitate results in reduced glucose-induced somatostatin and oversecretion of glucagon. Diabetologia in press.
15. Curry DL, Bennett LL & Grodsky GM (1968). Dynamics of insulin secretion by the perfused rat pancreas. Endocrinology 83, 572-584.
16. Daniel S, Noda M, Straub SG & Sharp GW (1999). Identification of the docked granule pool responsible for the first phase of glucose-stimulated insulin secretion. Diabetes 48, 1686-1690.
17. Dean PM (1973). Ultrastructural morphometry of the pancreatic β-cell. Diabetologia 9, 115-119.
18. Dulubova I, Khvotchev M, Liu S, Huryeva I, Sudhof TC & Rizo J (2007). Munc18-1 binds directly to the neuronal SNARE complex. Proc Natl Acad Sci U S A 104, 2697-2702.
19. Duncan RR, Greaves J, Wiegand UK, Matskevich I, Bodammer G, Apps DK, Shipston MJ & Chow RH (2003). Functional and spatial segregation of secretory vesicle pools according to vesicle age. Nature 422, 176-180.
20. Elhamdani A, Azizi F & Artalejo CR (2006). Double patch clamp reveals that transient fusion (kiss-and-run) is a major mechanism of secretion in calf adrenal chromaffin cells: High calcium shifts the mechanism from kiss-and-run to complete fusion. J Neurosci 26, 3030-3036.
21. Eliasson L, Gaisano H & Vikman J (2005). Reduced stimulation by cAMP in insulin-secreting cells overexpressing truncated SNAP-25. Diabetologia 48, A172.
22. Eliasson L, Ma X, Renström E, Barg S, Berggren PO, Galvanovskis J, Gromada J, Jing X, Lundquist I, Salehi A, Sewing S & Rorsman P (2003). SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J Gen Physiol 121, 181-197.
23. Esni F, Taljedal IB, Perl AK, Cremer H, Christofori G & Semb H (1999). Neural cell adhesion molecule (N-CAM) is required for cell type segregation and normal ultrastructure in pancreatic islets. J Cell Biol 144, 325-337.
24. Fukuda M, Imai A, Nashida T & Shimomura H (2005). Slp4-a/ granuphilin-a interacts with syntaxin-2/3 in a Munc18-2-dependent manner. J Biol Chem 280, 39175-39184.
25. Gauthier BR, Duhamel DL, Iezzi M, Theander S, Saltel F, Fukuda M, Wehrle-Haller B & Wollheim CB (2007). Synaptotagmin VII splice variants α, β, and δ are expressed in pancreatic β-cells and regulate insulin exocytosis. FASEB J 22, 194-206.
26. Gauthier BR & Wollheim CB (2006). MicroRNAs: 'ribo-regulators'of glucose homeostasis. Nat Med 12, 36-38.
27. Gerber SH & Sudhof TC (2002). Molecular determinants of regulated exocytosis. Diabetes 51, S3-S11.
28. Gold G, Gishizky ML & Grodsky GM (1982). Evidence that glucose 'marks'beta cells resulting in preferential release of newly synthesized insulin. Science 218, 56-58.
29. Goodge KA & Hutton JC (2000). Translational regulation of proinsulin biosynthesis and proinsulin conversion in the pancreatic β-cell. Semin Cell Dev Biol 11, 235-242.
30. Göpel S, Zhang Q, Eliasson L, Ma XS, Galvanovskis J, Kanno T, Salehi A & Rorsman P (2004). Capacitance measurements of exocytosis in mouse pancreatic α-, β- and δ-cells within intact islets of Langerhans. J Physiol 556, 711-726.
31. 2+ sensor synaptotagmin 9 in endocrine β-cells. Biochem J 403, 483-492.
32. Gromada J, Bokvist K, Ding WG, Holst JJ, Nielsen JH & Rorsman P (1998). Glucagon-like peptide 1 (7-36) amide stimulates exocytosis in human pancreatic β-cells by both proximal and distal regulatory steps in stimulus-secretion coupling. Diabetes 47, 57-65.
33. Gromada J, Høy M, Renström E, Bokvist K, Eliasson L, Göpel S & Rorsman P (1999). CaM kinase II-dependent mobilization of secretory granules underlies acetylcholine-induced stimulation of exocytosis in mouse pancreatic B-cells. J Physiol 518, 745-759.
34. Gustavsson N, Lao Y, Maximov A, Chuang JC, Kostromina E, Repa JJ, Li C, Radda GK, Sudhof TC & Han W (2008). Impaired insulin secretion and glucose intolerance in synaptotagmin-7 null mutant mice. Proc Natl Acad Sci U S A 105, 3992-3997.
35. Henquin JC (2000). Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 49, 1751-1760.
36. Henquin JC, Dufrane D & Nenquin M (2006). Nutrient control of insulin secretion in isolated normal human islets. Diabetes 55, 3470-3477.
37. Hosker JP, Rudenski AS, Burnett MA, Matthews DR & Turner RC (1989). Similar reduction of first- and second-phase B-cell responses at three different glucose levels in type II diabetes and the effect of gliclazide therapy. Metabolism 38, 767-772.
38. Hutton JC, Penn EJ & Peshavaria M (1983). Low-molecular weight constituents of isolated insulin-secretory granules. Bivalent cations, adenine nucleotides and inorganic phosphate. Biochem J 210, 297-305.
39. 2+ -dependent insulin secretion in islets. FEBS Lett 579, 5241-5246.
40. 2+ -dependent insulin exocytosis. J Cell Sci 117, 3119-3127.
41. Ivarsson R, Obermüller S, Rutter GA, Galvanovskis J & Renström E (2004). Temperature-sensitive random insulin granule diffusion is a prerequisite for recruiting granules for release. Traffic 5, 750-762.
42. Jeans AF, Oliver PL, Johnson R, Capogna M, Vikman J, Molnar Z, Babbs A, Partridge CJ, Salehi A, Bengtsson M, Eliasson L, Rorsman P & Davies KE (2007). A dominant mutation in Snap25 causes impaired vesicle trafficking, sensorimotor gating, and ataxia in the blind-drunk mouse. Proc Natl Acad Sci U S A 104, 2431-2436.
43. Jewell JL, Luo W, Oh E, Wang Z & Thurmond DC (2008). Filamentous actin regulates insulin exocytosis through direct interaction with syntaxin 4. J Biol Chem 283, 10716-10726.
44. Kang L, He Z, Xu P, Fan J, Betz A, Brose N & Xu T (2006). Munc13-1 is required for the sustained release of insulin from pancreatic β cells. Cell Metab 3, 463-468.
45. Kato T, Shimano H, Yamamoto T, Yokoo T, Endo Y, Ishikawa M, Matsuzaka T, Nakagawa Y, Kumadaki S, Yahagi N, Takahashi A, Sone H, Suzuki H, Toyoshima H, Hasty AH, Takahashi S, Gomi H, Izumi T & Yamada N (2006). Granuphilin is activated by SREBP-1c and involved in impaired insulin secretion in diabetic mice. Cell Metab 4, 143-154.
46. Lang J (1999). Molecular mechanisms and regulation of insulin exocytosis as a paradigm of endocrine secretion. Eur J Biochem 259, 3-17.
47. + channels: tuning β-cell excitability with syntaxin-1A and other exocytotic proteins. Endocr Rev 28, 653-663.
48. Lovis P, Gattesco S & Regazzi R (2008). Regulation of the expression of components of the machinery of exocytosis of insulin-secreting cells by microRNAs. Biol Chem 389, 305-312.
49. MacDonald PE, Braun M, Galvanovskis J & Rorsman P (2006). Release of small transmitters through kiss-and-run fusion pores in rat pancreatic β cells. Cell Metab 4, 283-290.
50. Meissner HP (1976). Electrical characteristics of the β-cells in pancreatic islets. J Physiol (Paris) 72, 757-767.
51. Meissner HP & Atwater IJ (1976). The kinetics of electrical activity of β cells in response to a 'square wave'stimulation with glucose or glibenclamide. Horm Metab Res 8, 11-16.
52. Nagy G, Matti U, Nehring RB, Binz T, Rettig J, Neher E & Sorensen JB (2002). Protein kinase C-dependent phosphorylation of synaptosome-associated protein of 25 kDa at Ser 187 potentiates vesicle recruitment. J Neurosci 22, 9278-9286.
53. Nagy G, Reim K, Matti U, Brose N, Binz T, Rettig J, Neher E & Sorensen JB (2004). Regulation of releasable vesicle pool sizes by protein kinase A-dependent phosphorylation of SNAP-25. Neuron 41, 417-429.
54. 2+ microdomains: New tools for understanding their roles in neurotransmitter release. Neuron 20, 389-399.
55. Obermüller S, Lindqvist A, Karanauskaite J, Galvanovskis J, Rorsman P & Barg S (2005). Selective nucleotide-release from dense-core granules in insulin-secreting cells. J Cell Sci 118, 4271-4282.
56. Ohara-Imaizumi M, Fujiwara T, Nakamichi Y, Okamura T, Akimoto Y, Kawai J, Matsushima S, Kawakami H, Watanabe T, Akagawa K & Nagamatsu S (2007). Imaging analysis reveals mechanistic differences between first- and second-phase insulin exocytosis. J Cell Biol 177, 695-705.
57. Ohara-Imaizumi M, Nishiwaki C, Kikuta T, Kumakura K, Nakamichi Y & Nagamatsu S (2004). Site of docking and fusion of insulin secretory granules in live MIN6 beta cells analyzed by TAT-conjugated anti-syntaxin 1 antibody and total internal reflection fluorescence microscopy. J Biol Chem 279, 8403-8408.
58. Olofsson CS, Göpel SO, Barg S, Galvanovskis J, Ma X, Salehi A, Rorsman P & Eliasson L (2002). Fast insulin secretion reflects exocytosis of docked granules in mouse pancreatic B-cells. Pflugers Arch 444, 43-51.
59. Olsen HL, Hoy M, Zhang W, Bertorello AM, Bokvist K, Capito K, Efanov AM, Meister B, Thams P, Yang SN, Rorsman P, Berggren PO & Gromada J (2003). Phosphatidylinositol 4-kinase serves as a metabolic sensor and regulates priming of secretory granules in pancreatic β cells. Proc Natl Acad Sci U S A 100, 5187-5192.
60. Orci L, Gabbay KH & Malaisse WJ (1972). Pancreatic β-cell web: its possible role in insulin secretion. Science 175, 1128-1130.
61. Ostenson CG, Gaisano H, Sheu L, Tibell A & Bartfai T (2006). Impaired gene and protein expression of exocytotic soluble N -ethylmaleimide attachment protein receptor complex proteins in pancreatic islets of type 2 diabetic patients. Diabetes 55, 435-440.
62. Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, Macdonald PE, Pfeffer S, Tuschl T, Rajewsky N, Rorsman P & Stoffel M (2004). A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432, 226-230.
63. Renström E, Ding WG, Bokvist K & Rorsman P (1996). Neurotransmitter-induced inhibition of exocytosis in insulin-secreting β cells by activation of calcineurin. Neuron 17, 513-522.
64. Rorsman P & Renström E (2003). Insulin granule dynamics in pancreatic β cells. Diabetologia 46, 1029-1045.
65. Sánchez-Andrés JV, Gomis A & Valdeolmillos M (1995). The electrical activity of mouse pancreatic β-cells recorded in vivo shows glucose-dependent oscillations. J Physiol 486, 223-228.
66. Schnell AH, Swenne I & Borg LA (1988). Lysosomes and pancreatic islet function. A quantitative estimation of crinophagy in the mouse pancreatic B-cell. Cell Tissue Res 252, 9-15.
67. Seino S & Shibasaki T (2005). PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol Rev 85, 1303-1342.
68. Shibasaki T, Takahashi H, Miki T, Sunaga Y, Matsumura K, Yamanaka M, Zhang C, Tamamoto A, Satoh T, Miyazaki JI & Seino S (2007). Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci U S A 104, 19333-19338.
69. Shu Y, Liu X, Yang Y, Takahashi M & Gillis KD (2008). Phosphorylation of SNAP-25 at Ser 187 mediates enhancement of exocytosis by a phorbol ester in INS-1 cells. J Neurosci 28, 21-30.
70. Speidel D, Salehi A, Obermueller S, Lundquist I, Brose N, Renström E & Rorsman P (2008). CAPS1 and CAPS2 regulate stability and recruitment of insulin granules in mouse pancreatic β cells. Cell Metab 7, 57-67.
71. Speier S & Rupnik M (2003). A novel approach to in situ characterization of pancreatic β-cells. Pflugers Arch 446, 553-558.
72. Spurlin BA & Thurmond DC (2006). Syntaxin 4 facilitates biphasic glucose-stimulated insulin secretion from pancreatic β-cells. Mol Endocrinol 20, 183-193.
73. Steyer JA, Horstmann H & Almers W (1997). Transport, docking and exocytosis of single secretory granules in live chromaffin cells. Nature 388, 474-478.
74. 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, 3179-3183.
75. Torii S, Zhao S, Yi Z, Takeuchi T & Izumi T (2002). Granuphilin modulates the exocytosis of secretory granules through interaction with syntaxin 1a. Mol Cell Biol 22, 5518-5526.
76. Tsuboi T, Ravier MA, Parton LE & Rutter GA (2006). Sustained exposure to high glucose concentrations modifies glucose signaling and the mechanics of secretory vesicle fusion in primary rat pancreatic β-cells. Diabetes 55, 1057-1065.
77. Tsuboi T & Rutter GA (2003). Insulin secretion by 'kiss-and-run'exocytosis in clonal pancreatic islet β-cells. Biochem Soc Trans 31, 833-836.
78. Valdeolmillos M, Gomis A & Sánchez-Andrés JV (1996). In vivo synchronous membrane potential oscillations in mouse pancreatic β-cells: Lack of co-ordination between islets. J Physiol 493, 9-18.
79. Vikman J & Eliasson L (2005). Depletion of cholesterol using a low concentration of methyl-betacyclodextrin reduces the exocytotic response in single mouse pancreatic B-cells. Diabetologia 48, A66.
80. Vikman J, Ma X, Hockerman GH, Rorsman P & Eliasson L (2006). Antibody inhibition of synaptosomal protein of 25 kDa (SNAP-25) and syntaxin 1 reduces rapid exocytosis in insulin-secreting cells. J Mol Endocrinol 36, 503-515.
81. Vikman J, Ma X, Tagaya M & Eliasson L (2003). Requirement for N -ethylmaleimide-sensitive factor for exocytosis of insulin-containing secretory granules in pancreatic β-cells. Biochem Soc Trans 31, 842-847.
82. Vitale ML, Seward EP & Trifaro JM (1995). Chromaffin cell cortical actin network dynamics control the size of the release-ready vesicle pool and the initial rate of exocytosis. Neuron 14, 353-363.
83. Wang J, Takeuchi T, Yokota H & Izumi T (1999). Novel rabphilin-3-like protein associates with insulin-containing granules in pancreatic β cells. J Biol Chem 274, 28542-28548.
84. Wendt A, Birnir B, Buschard K, Gromada J, Salehi A, Sewing S, Rorsman P & Braun M (2004). Glucose inhibition of glucagon secretion from rat α-cells is mediated by GABA released from neighboring β-cells. Diabetes 53, 1038-1045.
85. Wightman RM, Jankowski JA, Kennedy RT, Kawagoe KT, Schroeder TJ, Leszczyszyn DJ, Near JA, Diliberto EJ Jr & Viveros OH (1991). Temporally resolved catecholamine spikes correspond to single vesicle release from individual chromaffin cells. Proc Natl Acad Sci U S A 88, 10754-10758.
86. 2+ channel is functionally coupled to the exocytotic machinery. Proc Natl Acad Sci U S A 96, 248-253.
87. 2+ sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54, 567-581.
88. Yang B, Steegmaier M, Gonzalez LC Jr & Scheller RH (2000). nSec1 binds a closed conformation of syntaxin1A. J Cell Biol 148, 247-252.
89. 2+ -sensitive pool of granules is regulated by glucose and protein kinases in insulin-secreting INS-1 cells. J Gen Physiol 124, 641-651.
90. Zawalich WS, Tesz GJ & Zawalich KC (2001). Are 5-hydroxytryptamine-preloaded β-cells an appropriate physiologic model system for establishing that insulin stimulates insulin secretion? J Biol Chem 276, 37120-37123.