Regulation of resident and newcomer insulin granules by calcium and SNARE proteins

Frontiers in Bioscience

Volumn 16, Issue 4, 2011, Pages 1197-1210

  Aoyagi, Kyota ^a   Ohara Imaizumi, Mica ^a   Nagamatsu, Shinya ^a  

^a KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Insulin secretion; Pancreatic beta cell; TIRF microscopy

Indexed keywords

MUS;

CALCIUM; INSULIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAC1 PROTEIN; SNARE PROTEIN;

CELL GRANULE; EXOCYTOSIS; FLUORESCENCE MICROSCOPY; METABOLISM; PHYSIOLOGY; REVIEW; SECRETION; SECRETORY VESICLE;

CALCIUM; CYTOPLASMIC GRANULES; EXOCYTOSIS; INSULIN; MICROSCOPY, FLUORESCENCE; PHOSPHATIDYLINOSITOL 3-KINASE; RAC1 GTP-BINDING PROTEIN; SECRETORY VESICLES; SNARE PROTEINS;

EID: 79955013713     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3784     Document Type: Article

References (136)

1. Polonsky KS: Lilly Lecture 1994. The beta-cell in diabetes: from molecular genetics to clinical research. Diabetes 44, 705-717 (1995)
2. Taylor SI, Accili D, Imai Y: Insulin resistance or insulin deficiency. Which is the primary cause of NIDDM? Diabetes 43, 735-740 (1994)
3. Turner RC, Hattersley AT, Shaw JT, Levy JC: Type II diabetes: clinical aspects of molecular biological studies. Diabetes 44, 1-10 (1995)
4. Sudhof TC: The synaptic vesicle cycle. Annu Rev Neurosci 27, 509-547 (2004) (Pubitemid 39050412)
5. Jahn R, Lang T, Sudhof TC: Membrane fusion. Cell 112, 519-533 (2003) (Pubitemid 36263084)
6. Klenchin VA, Martin TF: Priming in exocytosis: attaining fusion-competence after vesicle docking. Biochimie 82, 399-407 (2000) (Pubitemid 30391896)
7. Johnson JH, Newgard CB, Milburn JL, Lodish HF, Thorens B: The high Km glucose transporter of islets of Langerhans is functionally similar to the low affinity transporter of liver and has an identical primary sequence. J Biol Chem 265, 6548-6551 (1990)
8. Ghosh A, Ronner P, Cheong E, Khalid P, Matschinsky FM: The role of ATP and free ADP in metabolic coupling during fuel-stimulated insulin release from islet beta-cells in the isolated perfused rat pancreas. J Biol Chem 266, 22887-22892 (1991) (Pubitemid 21908734)
9. Detimary P, Jonas JC, Henquin JC: Possible links between glucose-induced changes in the energy state of pancreatic B cells and insulin release. Unmasking by decreasing a stable pool of adenine nucleotides in mouse islets. J Clin Invest 96, 1738-1745 (1995)
10. Ashcroft FM: K(ATP) channels and insulin secretion: a key role in health and disease. Biochem Soc Trans 34, 243-246 (2006)
11. Rorsman P: The pancreatic beta-cell as a fuel sensor: an electrophysiologist's viewpoint. Diabetologia 40, 487-495 (1997) (Pubitemid 27186783)
12. Gembal M, Gilon P, Henquin JC: Evidence that glucose can control insulin release independently from its action on ATP-sensitive K+ channels in mouse B cells. J Clin Invest 89, 1288-1295 (1992)
13. Li G, Regazzi R, Balch WE, Wollheim CB: Stimulation of insulin release from permeabilized HIT-T15 cells by a synthetic peptiDe corresponding to the effector domain of the small GTP-binding protein rab3. FEBS Lett 327, 145-149 (1993) (Pubitemid 23211178)
14. Baffy G, Yang L, Wolf BA, Williamson JR: G-protein specificity in signaling pathways that mobilize calcium in insulin-secreting beta-TC3 cells. Diabetes 42, 1878-1882 (1993) (Pubitemid 23346426)
15. Ashcroft FM, Proks P, Smith PA, Ammala C, Bokvist K, Rorsman P: Stimulus-secretion coupling in pancreatic beta cells. J Cell Biochem 55 Suppl, 54-65 (1994) (Pubitemid 24199285)
16. Prentki M, Corkey BE: Are the beta-cell signaling molecules malonyl-CoA and cystolic long-chain acyl-CoA implicated in multiple tissue defects of obesity and NIDDM? Diabetes 45, 273-283 (1996) (Pubitemid 26069039)
17. Sorenson RL, Brelje TC, Roth C: Effect of tyrosine kinase inhibitors on islets of Langerhans: evidence for tyrosine kinases in the regulation of insulin secretion. Endocrinology 134, 1975-1978 (1994) (Pubitemid 24110766)
18. Ratcliff H, Jones PM: Effects of okadaic acid on insulin secretion from rat islets of Langerhans. Biochim Biophys Acta 1175, 188-191 (1993) (Pubitemid 23024890)
19. O'Connor MD, Landahl H, Grodsky GM: Comparison of storage- and signal-limited models of pancreatic insulin secretion. Am J Physiol 238, R378-R389 (1980)
20. Ma YH, Wang J, Rodd GG, Bolaffi JL, Grodsky GM: Differences in insulin secretion between the rat and mouse: role of cAMP. Eur J Endocrinol 132, 370-376 (1995)
21. Sudhof TC, Rothman JE: Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477 (2009)
22. Sollner T, Bennett MK, Whiteheart SW, Scheller RH, Rothman JE: A protein assembly-disassembly pathway invitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409-418 (1993) (Pubitemid 23335067)
23. Humeau Y, Doussau F, Grant NJ, Poulain B: How botulinum and tetanus neurotoxins block neurotransmitter release. Biochimie 82, 427-446 (2000) (Pubitemid 30391899)
24. Sorensen JB, Nagy G, Varoqueaux F, Nehring RB, Brose N, Wilson MC, Neher E: Differential control of the releasable vesicle pools by SNAP-25 splice variants and SNAP-23. Cell 114, 75-86 (2003) (Pubitemid 36859842)
25. Schoch S, Deak F, Konigstorfer A, Mozhayeva M, Sara Y, Sudhof TC, Kavalali ET: SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294, 1117-1122 (2001) (Pubitemid 33041870)
26. Borisovska M, Zhao Y, Tsytsyura Y, Glyvuk N, Takamori S, Matti U, Rettig J, Sudhof T, Bruns D: v- SNAREs control exocytosis of vesicles from priming to fusion. EMBO J 24, 2114-2126 (2005) (Pubitemid 40961796)
27. Washbourne P, Thompson PM, Carta M, Costa ET, Mathews JR, Lopez-Benditó G, Molnar Z, Becher MW, Valenzuela CF, Partridge LD, Wilson MC: Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 5, 19-26 (2002) (Pubitemid 34038778)
28. Olofsson CS, Gopel SO, Barg S, Galvanovskis J, Ma X, Salehi A, Rorsman P, Eliasson L: Fast insulin secretion reflects exocytosis of docked granules in mouse pancreatic B-cells. Pflugers Arch 444, 43-51 (2002) (Pubitemid 34499244)
29. Straub SG, Shanmugam G, Sharp GW: Stimulation of insulin release by glucose is associated with an increase in the number of docked granules in the beta-cells of rat pancreatic islets. Diabetes 53, 3179-3183 (2004) (Pubitemid 39564493)
30. 2+-but not for GTP gamma S-induced insulin secretion. EMBO J 14, 2723-2730 (1995)
31. 2+-induced exocytosis in mouse pancreatic Bcells. J Physiol 503, 399-412 (1997) (Pubitemid 27423364)
32. Renstom E, Eliasson L, Bokvist K, Rorsman P: Cooling inhibits exocytosis in single mouse pancreatic B-cells by suppression of granule mobilization. J Physiol 494, 41-52 (1996) (Pubitemid 26238000)
33. Nagamatsu S, Fujiwara T, Nakamichi Y, Watanabe T, Katahira H, Sawa H, Akagawa K: Expression and functional role of syntaxin 1/HPC-1 in pancreatic beta cells. Syntaxin 1A, but not 1B, plays a negative role in regulatory insulin release pathway. J Biol Chem 271, 1160-1165 (1996)
34. Sadoul K, Lang J, Montecucco C, Weller U, Regazzi R, Catsicas S, Wollheim CB, Halban PA: SNAP-25 is expressed in islets of Langerhans and is involved in insulin release. J Cell Biol 128, 1019-1028 (1995)
35. Sadoul K, Berger A, Niemann H, Weller U, Roche PA, Klip A, Trimble WS, Regazzi R, Catsicas S, Halban PA: SNAP-23 is not cleaved by botulinum neurotoxin E and can replace SNAP-25 in the process of insulin secretion. J Biol Chem 272, 33023-33027 (1997) (Pubitemid 28023642)
36. Jacobsson G, Bean AJ, Scheller RH, Juntti-Berggren L, Deeney JT, Berggren PO, Meister B: Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells. Proc Natl Acad Soc U S A 91, 12487-12491 (1994)
37. Wheeler MB, Sheu L, Ghai M, Bouquillon A, Grondin G, Weller U, Beaudoin AR, Bennett MK, Trimble WS, Gaisano HY: Characterization of SNARE protein expression in beta cell lines and pancreatic islets. Endocrinology 137, 1340-1348 (1996) (Pubitemid 26095251)
38. Nagamatsu S, Sawa H, Nakamichi Y, Kondo Y, Matsushima S, Watanabe T: Non-functional role of syntaxin 2 in insulin exocytosis by pancreatic beta cells. Cell Biochem Funct 15, 237-242 (1997) (Pubitemid 27507595)
39. 2+- but not for guanosine 5′-[gammathio] triphosphate-induced secretion. Biochem J 320, 201-205 (1996)
40. Martín F, Moya F, Gutierrez LM, Reig JA, Soria B: Role of syntaxin in mouse pancreatic beta cells. Diabetologia 38, 860-863 (1995)
41. Kawai J, Ohara-Imaizumi M, Nakamichi Y, Okamura T, Akimoto Y, Matsushima S, Aoyagi K, Kawakami H, Watanabe T, Watada H, Kawamori R, Nagamatsu S: Insulin exocytosis in Goto-Kakizaki rat beta-cells subjected to long-term gliniDe or sulfonylurea treatment. Biochem J 412, 93-101 (2008) (Pubitemid 351678339)
42. Ohara-Imaizumi M, Nishiwaki C, Nakamichi Y, Kikuta T, Nagai S, Nagamatsu S: Correlation of syntaxin-1 and SNAP-25 clusters with docking and fusion of insulin granules analysed by total internal reflection fluorescence microscopy. Diabetologia 47, 2200-2207 (2004) (Pubitemid 40174693)
43. Nagamatsu S, Nakamichi Y, Yamamura C, Matsushima S, Watanabe T, Ozawa S, Furukawa H, Ishida H: Decreased expression of t-SNARE, syntaxin 1, and SNAP-25 in pancreatic beta-cells is involved in impaired insulin secretion from diabetic GK rat islets: restoration of decreased t-SNARE proteins improves impaired insulin secretion. Diabetes 48, 2367-2373 (1999) (Pubitemid 30395428)
44. Vikman J, Ma X, Hockerman GH, Rorsman P, Eliasson L: 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 (2006) (Pubitemid 43904943)
45. Land J, Zhang H, Vaidyanathan VV, Sadoul K, Niemann H, Wollheim CB: Transient expression of botulinum neurotoxin C1 light chain differentially inhibits calcium and glucose induced insulin secretion in clonal beta-cells. FEBS Lett 419, 13-17 (1997) (Pubitemid 28011207)
46. Rorsman P, Eliasson L, Renstom E, Gromada J, Barg S, Gopel S: The Cell Physiology of Biphasic Insulin Secretion. News Physiol Sci 15, 72-77 (2000)
47. Eliasson L, Abdulkader F, Braun M, Galvanovskis J, Hoppa MB, Rorsman P: Novel aspects of the molecular mechanisms controlling insulin secretion. J Physiol 586, 3313-3324 (2008) (Pubitemid 352003868)
48. Eliasson L, Proks P, Ammala C, Ashcroft FM, Bokvist K, Renstom E, Rorsman P, Smith PA: Endocytosis of secretory granules in mouse pancreatic beta-cells evoked by transient elevation of cytosolic calcium. J Physiol 493, 755-767 (1996) (Pubitemid 26232111)
49. Renstom E, Eliasson L, Rorsman P: Protein kinase Adependent and -independent stimulation of exocytosis by cAMP in mouse pancreatic B-cells. J Physiol 502, 105-118 (1997) (Pubitemid 27322979)
50. 2+ channels accounts for first-phase insulin secretion in mouse beta-cells. Diabetes 511, S74-S82 (2002) (Pubitemid 34761498)
51. Gromada J, Hoy M, Renstom E, Bokvist K, Eliasson L, Gopel S, Rorsman P: CaM kinase II-dependent mobilization of secretory granules underlies acetylcholineinduced stimulation of exocytosis in mouse pancreatic Bcells. J Physiol 518, 745-759 (1999) (Pubitemid 29387244)
52. Rorsman P, Renstom E: Insulin granule dynamics in pancreatic beta cells. Diabetologia 46, 1029-1045 (2003) (Pubitemid 37041234)
53. Barg S, Lindqvist A, Obermüller S: Granule docking and cargo release in pancreatic beta-cells. Biochem Soc Trans 36, 294-299 (2008) (Pubitemid 351839319)
54. Straub SG, Sharp GW: Glucose-stimulated signaling pathways in biphasic insulin secretion. Diabetes Metab Res Rev 18, 451-463 (2002) (Pubitemid 36041600)
55. Bratanova-Tochkova TK, Cheng H, Daniel S, Gunawardana S, Liu YJ, Mulvaney-Musa J, Schermerhorn T, Straub SG, Yajima H, Sharp GW: Triggering and augmentation mechanisms, granule pools, and biphasic insulin secretion. Diabetes 511, S83-S90 (2002) (Pubitemid 34761499)
56. Fredj NB, Burrone J: A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat Neurosci 12, 751-758 (2009)
57. Mathew SS, Pozzo-Miller L, Hablitz JJ: Kainate modulates presynaptic GABA release from two vesicle pools. J Neurosci 28, 725-731 (2008) (Pubitemid 351159023)
58. Sara Y, Virmani T, Deak F, Liu X, Kavalali ET: An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 45, 563-573 (2005) (Pubitemid 40249868)
59. Axerlod D: Total internal reflection fluorescence microscopy in cell biology. Traffic 2, 764-774 (2001)
60. Steyer JA, Almers W: A real-time view of life within 100 nm of the plasma membrane. Nat Rev Mol Cell Biol 2, 268-275 (2001) (Pubitemid 33676969)
61. Axelrod D: Cell-substrate contacts illuminated by total internal reflection fluorescence. J Cell Biol 89, 141-145 (1981) (Pubitemid 11066139)
62. Truskey GA, Burmeister JS, Grapa E, Reichert WM: Total internal reflection fluorescence microscopy (TIRFM). II. Topographical mapping of relative cell/substratum separation distances. J Cell Sci 103, 491-499 (1992)
63. Vale RD, Funatsu T, Pierce DW, Romberg L, Harada Y, Yanagida T: Direct observation of single kinesin molecules moving along microtubules. Nature 380, 451-453 (1996) (Pubitemid 26102723)
64. Sund SE, Axelrod D: Actin dynamics at the living cell submembrane imaged by total internal reflection fluorescence photobleaching. Biophys J 79, 1655-1669 (2000)
65. Dickson RM, Norris DJ, Tzeng YL, Moerner WE: Three-dimensional imaging of single molecules solvated in pores of poly(acrylamide) gels. Science 274, 966-969 (1996) (Pubitemid 26398415)
66. Oheim M, Loerke D, Stühmer 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 27, 83-98 (1998) (Pubitemid 28123529)
67. Sako Y, Minoghchi S, Yanagida T: Single-molecule imaging of EGFR signalling on the surface of living cells. Nat Cell Biol 2, 168-172 (2000)
68. Tsuboi T, Zhao C, Terakawa S, Rutter GA: Simultaneous evanescent wave imaging of insulin vesicle membrane and cargo during a single exocytotic event. Curr Biol 10, 1307-1310 (2000)
69. Pouli AE, Emmanouilidou E, Zhao C, Wasmeier C, Hutton JC, Rutter GA: Secretory-granule dynamics visualized in vivo with a phogrin-green fluorescent protein chimaera. Biochem J 333, 193-199 (1998) (Pubitemid 28342509)
70. Tsuboi T, Rutter GA: Multiple forms of "kiss-and-run" exocytosis revealed by evanescent wave microscopy. Curr Biol 13, 563-567 (2003) (Pubitemid 36391933)
71. 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 279, 47115-47124 (2004) (Pubitemid 39518368)
72. Gridley S, Lane WS, Garner CW, Lienhard GE: Novel insulin-elicited phosphoproteins in adipocytes. Cell Signal 17, 59-66 (2005) (Pubitemid 39286780)
73. Ohara-Imaizumi M, Nakamichi Y, Tanaka T, Ishida H, Nagamatsu S: Imaging exocytosis of single insulin secretory granules with evanescent wave microscopy: distinct behavior of granule motion in biphasic insulin release. J Biol chem. 277, 3805-3808 (2001) (Pubitemid 34968628)
74. Ohara-Imaizumi M, Nishiwaki C, Kikuta T, Nagai S, Nakamichi Y, Nagamatsu S: TIRF imaging of docking and fusion of single insulin granule motion in primary rat pancreatic beta-cells: different behaviour of granule motion between normal and Goto-Kakizaki diabetic rat beta-cells. Biochem J 381, 13-18 (2004) (Pubitemid 38932205)
75. 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 secondphase insulin exocytosis. J Cell Biol 177, 695-705 (2007) (Pubitemid 46799840)
76. 2+ as evidences in single pancreatic islets. J Biol Chem 268, 22265-22268 (1993) (Pubitemid 23318266)
77. Michael DJ, Xiong W, Geng X, Drain P, Chow RH: Human insulin vesicle dynamics during pulsatile secretion. Diabetes 56, 1277-1288 (2007) (Pubitemid 46715608)
78. Dyachok O, Idevall-Hagren O, Sagetorp J, Tian G, Wuttke A, Arrieumerlou C, Akusjärvi G, Gylfe E, Tengholm A: Glucose-induced cyclic AMP oscillations regulate pulsatile insulin secretion. Cell Metab 8, 26-37 (2008) (Pubitemid 351859229)
79. Oh E, Thurmond DC: Munc18c depletion selectively impairs the sustained phase of insulin release. Diabetes 58, 1165-1174 (2009)
80. Fujimoto W, Miki T, Ogura T, Zhang M, Seino Y, Satin LS, Nakaya H, Seino S: Niflumic acid-sensitive ion channels play an important role in the induction of glucosestimulated insulin secretion by cyclic AMP in mice. Diabetologia 52, 863-872 (2009)
81. Wijesekara N, Dai FF, Hardy AB, Giglou PR, Bhattacharjee A, Koshkin V, Chimienti F, Gaisano HY, Rutter GA, Wheeler MB: Beta cell-specific Znt8 deletion in mice causes marked defects in insulin processing, crystallization and secretion. Diabetologia 53, 1656-1668 (2010)
82. 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 283, 17939-17945 (2008)
83. Gomi H, Mizutani S, Kasai K, Itohara S, Izumi T: Granuphilin molecularly dockes insulin granules to the fusion machinery. J Cell Biol 171, 99-109 (2005) (Pubitemid 41434605)
84. De Wit H, Walter AM, Milosevic I, Gulyas-Kovacs A, Riedel D, Sørensen JB, Verhage M: Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes. Cell 138, 935-946 (2009)
85. De Wit H, Cornelisse LN, Toonen RF, Verhage M: Docking of secretory vesicles is syntaxin dependent. PLoS One 1, e126 (2006)
86. Verhage M, Sørensen JB: Vesicle docking in regulated exocytosis. Traffic 9, 1414-1424 (2008)
87. Lang T, Bruns D, Wenzel D, Riedel D, Holroyd P, Thiele C, Jahn R: SNAREs are concentrated in cholesteroldependent clusters that define docking and fusion sites for exocytosis. EMBO J 20, 2202-2213 (2001) (Pubitemid 32410590)
88. Lang T, Margittai M, Holzler H, Jahn R: SNAREs in native plasma membranes are active and readily form core complexes with endogenous and exogenous SNAREs. J Cell Biol 158, 751-760 (2002) (Pubitemid 34920113)
89. Aoyagi K, Sugaya T, Umeda M, Yamamoto S, Terakawa S, Takahashi M: The activation of exocytotic sites by the formation of phosphatidylinositol 4,5-bisphosphate microdomains at syntaxin clusters. J Biol Chem 280, 17346-17352 (2005) (Pubitemid 41389204)
90. Stein S, Weiss A, Adermann K, Lazarovici P, Hochman J, Wellhoner H: A disulfiDe conjugate between anti-tetanus antibodies and HIV (37-72)Tat neutralizes tetanus toxin insiDe chromaffin cells. FEBS Lett 458, 383-386 (1996) (Pubitemid 29433840)
91. Steffen W: Tat-mediated delivery of antibodies into cultured cells. Methods Mol Biol 161, 141-148 (2001)
92. Niesner U, Halin C, Lozzi L, Günthert M, Neri P, Wunderli-Allenspach H, Zardi L, Neri D: Quantitation of the tumor-targeting properties of antibody fragments conjugated to cell-permeating HIV-1 TAT peptides. Bioconjug Chem 13, 729-736 (2002) (Pubitemid 34801114)
93. Ohara-Imaizumi M, Nishiwaki C, Kikuta T, Kumakura K, Nakamichi Y, Nagamatsu S: 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 (2004) (Pubitemid 38294733)
94. Deguchi-Tawarada M, Inoue E, Takao-Rikitsu E, Inoue M, Ohtsuka T, Takai Y: CAST2: identification and characterization of a protein structurally related to the presynaptic cytomatrix protein CAST. Genes Cells 9, 15-23 (2004) (Pubitemid 38180878)
95. Wang Y, Liu X, Biederer T, Sudhof TC: A family of RIM-binding proteins regulated by alternative splicing: Implications for the genesis of synaptic active zones. Proc Natl Acad Sci U S A 99, 14464-14469 (2002) (Pubitemid 35257694)
96. Monier S, Jollivet F, Janoueix-Lerosey I, Johannes L, Goud B: Characterization of novel Rab6-interacting proteins involved in endosome-to-TGN transport. Traffic 3, 289-297 (2002) (Pubitemid 34303261)
97. Ohara-Imaizumi M, Ohtsuka T, Matsushima S, Akimoto Y, Nishiwaki C, Nakamichi Y, Kikuta T, Nagai S, Kawakami H, Watanabe T, Nagamatsu S: ELKS, a protein structurally related to the active zone-associated protein CAST, is expressed in pancreatic beta cells and functions in insulin exocytosis: interaction of ELKS with exocytotic machinery analyzed by total internal reflection fluorescence microscopy. Mol Biol Cell 16, 3289-3300 (2005) (Pubitemid 40962598)
98. Ohara-Imaizumi M, Cardozo AK, Kikuta T, Eizirik DL, Nagamatsu S: The cytokine interleukin-1beta reduces the docking and fusion of insulin granules in pancreatic betacells, preferentially decreasing the first phase of exocytosis. J Biol Chem 279, 41271-41274 (2004) (Pubitemid 39313564)
99. Daniel S, Noda M, Straub SG, Sharp GW: Identification of the docked granule pool responsible for the first phase of glucose-stimulated insulin secretion. Diabetes 48, 1686-1690 (1999) (Pubitemid 29415184)
100. Barg S, Huang P, Eliasson L, Nelson DJ, Obermuller S, Rorsman P, Thevenod F, Renstom E: Priming of insulin granules for exocytosis by granular Cl- uptake and acidification. J. Cell Sci. 114, 2145-2154 (2001)
101. Barg S: Mechanisms of exocytosis in insulin-secreting B-cells and glucagon-secreting A-cells. Pharmacol. Toxicol. 92, 3-13 (2003) (Pubitemid 36238071)
102. 2+ concentration determines type of fusing insulin granules in pancreatic beta cells. Biochem Biophys Res Commun 385, 291-295 (2009)
103. Pedersen MG, Sherman A: Newcomer insulin secretory granules as a highly calcium-sensitive pool. Proc Natl Acad Sci U S A 106, 7432-7436 (2009)
104. 2+ channel null mice. EMBO J 22, 3844-3854 (2003) (Pubitemid 36980594)
105. Jing X, Li DQ, Olofsson CS, Salehi A, Surve VV, Caballero J, Ivarsson R, Lundquist I, Pereverzev A, Schneider T, Rorsman P, Renstom E: CaV2.3 calcium channels control second-phase insulin release. J Clin Invest 115, 146-154 (2005) (Pubitemid 40385515)
106. 2+-dependent insulin secretion in islets. FEBS Lett 579, 5241-5246 (2005) (Pubitemid 41318098)
107. 2+ -dependent insulin exocytosis. J Cell Sci 117, 3119-3127 (2004) (Pubitemid 39139899)
108. Gauthier BR, Duhamel DL, Iezzi M, Theander S, Saltel F, Fukuda M, Wehrle-Haller B, Wollheim CB: Synaptotagmin VII splice variants alpha, beta, and delta are expressed in pancreatic beta-cells and regulate insulin exocytosis. FASEB J 22, 194-206 (2008)
109. Gustavsson N, Lao Y, Maximov A, Chuang JC, Kostromina E, Repa JJ, Li C, Radda GK, Sudhof TC, Han W: Impaired insulin secretion and glucose intolerance in synaptotagmin-7 null mutant mice. Proc Natl Acad Sci U S A 105, 3992-3997 (2008) (Pubitemid 351723512)
110. Krementsov DN, Krementsova EB, Trybus KM: Myosin V: regulation by calcium, calmodulin, and the tail domain. J Cell Biol 164, 877-886 (2004) (Pubitemid 38366899)
111. Ivarsson R, Jing X, Waselle L, Regazzi R, Renstom E: Myosin 5a controls insulin granule recruitment during latephase secretion. Traffic 6, 1027-1035 (2005) (Pubitemid 41472461)
112. Leibiger IB, Leibiger B, Berggren PO: Insulin feedback action on pancreatic beta-cell function. FEBS Lett 532, 1-6 (2002) (Pubitemid 35375856)
113. Cantley LC: The phosphoinositiDe 3-kinase pathway. Science 296, 1655-1657 (2002) (Pubitemid 34579158)
114. 2+] elevation signals. Diabetes 51, 87-97 (2002) (Pubitemid 34517984)
115. Hagiwara S, Sakurai T, Tashiro F, Hashimoto Y, Matsuda Y, Nonomura Y, Miyazaki J: An inhibitory role for phosphatidylinositol 3-kinase in insulin secretion from pancreatic B cell line MIN6. Biochem Biophys Res Commun 214, 51-59 (1995)
116. Zawalich WS, Zawalich KC: A link between insulin resistance and hyperinsulinemia: inhibitors of phosphatidylinositol 3-kinase augment glucose-induced insulin secretion from islets of lean, but not obese, rats. Endocrinology 141, 3287-3295 (2000) (Pubitemid 32269017)
117. Zawalich WS, Tesz GJ, Zawalich KC: Inhibitors of phosphatidylinositol 3-kinase amplify insulin release from islets of lean but not obese mice. J Endocrinol 174, 247-258 (2002) (Pubitemid 34965763)
118. Pigeau GM, Kolic J, Ball BJ, Hoppa MB, Wang YW, Ruckle T, Woo M, Manning Fox JE, MacDonald PE: Insulin granule recruitment and exocytosis is dependent on p110γ in insulinoma and human beta-cells. Diabetes 58, 2084-2092 (2009)
119. Lindmo K, Stenmark H: Regulation of membrane traffic by phosphoinositiDe 3-kinases. J Cell Sci 119, 605-614 (2006)
120. Itakura M, Yamamori S, Kuwahara R, Sekiguchi M, Takahashi M: Two distinct regulatory mechanisms of neurotransmitter release by phosphatidylinositol 3-kinase. J Neurochem 94, 502-509 (2005) (Pubitemid 40995265)
121. Kwon T, Kwon DY, Chun J, Kim JH, Kang SS: Akt protein kinase inhibits Rac1-GTP binding through phosphorylation at serine 71 of Rac1. J Biol Chem 275, 423-428 (2000) (Pubitemid 30039001)
122. Zhou GL, Zhuo Y, King CC, Fryer BH, Bokoch GM, Field J: Akt phosphorylation of serine 21 on Pak1 modulates Nck binding and cell migration. Mol Cell Biol 23, 8058-8069 (2003) (Pubitemid 37377498)
123. Evans GJ, Barclay JW, Prescott GR, Jo SR, Burgoyne RD, Birnbaum MJ, Morgan A: Protein kinase B/Akt is a novel cysteine string protein kinase that regulates exocytosis release kinetics and quantal size. J Biol Chem 281, 1564-1572 (2006)
124. Kane S, Sano H, Liu SC, Asara JM, Lane WS, Garner CC, Lienhard GE: A method to identify serine kinase substrates. Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain. J Biol Chem 277, 22115-22118 (2002) (Pubitemid 34967174)
125. Sano H, Kane S, Sano E, Mîinea CP, Asara JM, Lane WS, Garner CW, Lienhard GE: Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J Biol Chem 278, 14599-14602 (2003) (Pubitemid 36799780)
126. Wang Z, Oh E, Thurmond DC: Glucose-stimulated Cdc42 signaling is essential for the second phase of insulin secretion. J Biol Chem 282, 9536-9546 (2007) (Pubitemid 47104622)
127. Li J, Luo R, Kowluru A, Li G: Novel regulation by Rac1 of glucose- and forskolin-induced insulin secretion in INS-1 beta-cells. Am J Physiol Endocrinol Metab 286, E818-E827 (2004) (Pubitemid 38514676)
128. Evans GJ, Morgan A, Burgoyne RD: Tying everything together: the multiple roles of cysteine string protein (CSP) in regulated exocytosis. Traffic 4, 653-659 (2003) (Pubitemid 37168587)
129. Buchner E, Gundersen CB: The DnaJ-like cysteine string protein and exocytotic neurotransmitter release. Trends Neurosci 20, 223-227 (1997) (Pubitemid 27158052)
130. Zhang H, Kelley WL, Chamberlain LH, Burgoyne RD, Wollheim CB, Lang J: Cysteine-string proteins regulate exocytosis of insulin independent from transmembrane ion fluxes. FEBS Lett 437, 267-272 (1998) (Pubitemid 28511172)
131. Brown H, Larsson O, Bränström R, Yang SN, Leibiger B, Leibiger I, Fried G, MoeDe T, Deeney JT, Brown GR, Jacobsson G, Rhodes CJ, Braun JE, Scheller RH, Corkey BE, Berggren PO, Meister B: Cysteine string protein (CSP) is an insulin secretory granule-associated protein regulating beta-cell exocytosis. EMBO J 17, 5048-5058 (1998) (Pubitemid 28408470)
132. Evans GJ, Morgan A: Phosphorylation-dependent interaction of the synaptic vesicle proteins cysteine string protein and synaptotagmin I. Biochem J 364, 343-347 (2002) (Pubitemid 34620793)
133. Nie Z, Ranjan R, Wenniger JJ, Hong SN, Bronk P, Zinsmaier KE: Overexpression of cysteine-string proteins in Drosophila reveals interactions with syntaxin. J Neurosci 19, 10270-10279 (1999) (Pubitemid 30228034)
134. Evans GJ, Wilkinson MC, Graham ME, Turner KM, Chamberlain LH, Burgoyne RD, Morgan A: Phosphorylation of cysteine string protein by protein kinase A. Implications for the modulation of exocytosis. J BiolChem 276, 47877-47885 (2001)
135. Bouzakri K, Ribaux P, Tomas A, Parnaud G, Rickenbach K, Halban PA: Rab GTPase-activating protein AS160 is a major downstream effector of protein kinase B/Akt signaling in pancreatic beta-cells. Diabetes 57, 1195-1204 (2008)
136. 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 115, 388-396 (2005) (Pubitemid 40385480)