Syntaxin-4 mediates exocytosis of pre-docked and newcomer insulin granules underlying biphasic glucose-stimulated insulin secretion in human pancreatic beta cells

Diabetologia

Volumn 58, Issue 6, 2015, Pages 1250-1259

  Xie, Li ^a   Zhu, Dan ^a   Dolai, Subhankar ^a   Liang, Tao ^a   Qin, Tairan ^a   Kang, Youhou ^a   Xie, Huanli ^a   Huang, Ya Chi ^a   Gaisano, Herbert Y ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Exocytosis; Human islets; Newcomer insulin granules; Syntaxin 4

Indexed keywords

BIPHASIC INSULIN; GLUCOSE; INSULIN; MUNC18 PROTEIN; PHOTOPROTEIN; RED FLUORESCENT PROTEIN; SMALL INTERFERING RNA; SYNAPTOBREVIN; SYNAPTOBREVIN 2; SYNTAXIN; SYNTAXIN 4, HUMAN; VAMP2 PROTEIN, HUMAN; VAMP8 PROTEIN, HUMAN;

ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; CONFOCAL MICROSCOPY; CYTOLOGY; EXOCYTOSIS; GENE SILENCING; HUMAN; METABOLISM; MOUSE; PANCREAS ISLET BETA CELL; PATCH CLAMP TECHNIQUE; SECRETION (PROCESS); SINGLE CELL ANALYSIS;

ANIMALS; BIPHASIC INSULINS; CELLS, CULTURED; EXOCYTOSIS; GENE KNOCKDOWN TECHNIQUES; GLUCOSE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; LUMINESCENT PROTEINS; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MUNC18 PROTEINS; PATCH-CLAMP TECHNIQUES; QA-SNARE PROTEINS; R-SNARE PROTEINS; RNA, SMALL INTERFERING; SINGLE-CELL ANALYSIS; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 84939970696     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-015-3545-4     Document Type: Article

References (32)

1. Sudhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323:474–477
2. Burgoyne RD, Barclay JW, Ciufo LF, Graham ME, Handley MT, Morgan A (2009) The functions of Munc18-1 in regulated exocytosis. Ann N Y Acad Sci 1152:76–86
3. Kasai K, Fujita T, Gomi H, Izumi T (2008) Docking is not a prerequisite but a temporal constraint for fusion of secretory granules. Traffic 9:1191–1203
4. 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 U S A 104:19333–19338
5. Gaisano HY (2014) Here come the newcomer granules, better late than never. Trends Endocrinol Metab 945:1–8
6. Kwan EP, Gaisano HY (2005) Glucagon-like peptide 1 regulates sequential and compound exocytosis in pancreatic islet beta-cells. Diabetes 54:2734–2743
7. Hoppa MB, Jones E, Karanauskaite J et al (2012) Multivesicular exocytosis in rat pancreatic beta cells. Diabetologia 55:1001–1012
8. Wheeler MB, Sheu L, Ghai M et al (1996) Characterization of SNARE protein expression in beta-cell lines and pancreatic islets. Endocrinology 137:1340–1348
9. Ohara-Imaizumi M, Fujiwara T, Nakamichi Y et al (2007) Imaging analysis reveals mechanistic differences between first- and second-phase insulin exocytosis. J Cell Biol 177:695–705
10. Zhu D, Koo E, Kwan E et al (2013) Syntaxin-3 regulates newcomer insulin granule exocytosis and compound fusion in pancreatic beta cells. Diabetologia 56:359–369
11. Spurlin BA, Thurmond DC (2006) Syntaxin 4 facilitates biphasic glucose-stimulated insulin secretion from pancreatic beta-cells. Mol Endocrinol 20:183–193
12. Yang C, Coker KJ, Kim JK et al (2001) Syntaxin 4 heterozygous knockout mice develop muscle insulin resistance. J Clin Invest 107:1311–1318
13. Spurlin BA, Park SY, Nevins AK, Kim JK, Thurmond DC (2004) Syntaxin 4 transgenic mice exhibit enhanced insulin-mediated glucose uptake in skeletal muscle. Diabetes 53:2223–2231
14. Jewell JL, Oh E, Thurmond DC (2010) Exocytosis mechanisms underlying insulin release and glucose uptake: conserved roles for Munc18c and syntaxin 4. AJP Regul Integr Comp Physiol 298:R517–R531
15. Oh E, Stull ND, Mirmira RG, Thurmond DC (2014) Syntaxin 4 up-regulation increases efficiency of insulin release in pancreatic islets from humans with and without type 2 diabetes mellitus. J Clin Endocrinol Metab 99:E866–E870
16. Lam P, Ohno M, Dolai S et al (2013) Munc18b is a major mediator of insulin exocytosis in rat pancreatic β-cells. Diabetes 62:2416–2428
17. Zhu D, Zhang Y, Lam PP et al (2012) Dual role of VAMP8 in regulating insulin exocytosis and islet beta cell growth. Cell Metab 16:238–249
18. Xie L, Zhu D, Kang Y, Liang T, He Y, Gaisano HY (2013) Exocyst Sec5 regulates exocytosis of newcomer insulin granules underlying biphasic insulin secretion. PLoS ONE 8:e6756
19. Xie L, Zhu D, Gaisano HY (2012) Role of mammalian homologue of Caenorhabditis elegans unc-13-1 (Munc13-1) in the recruitment of newcomer insulin granules in both first and second phases of glucose-stimulated insulin secretion in mouse islets. Diabetologia 55:2693–2702
20. Rorsman P, Renstrom E (2003) Insulin granule dynamics in pancreatic beta cells. Diabetologia 46:1029–1045
21. Gillis KD, Mossner R, Neher E (1996) Protein kinase C enhances exocytosis from chromaffin cells by increasing the size of the readily releasable pool of secretory granules. Neuron 16:1209–1220
22. Braun M, Ramracheya R, Bengtsson M et al (2008) Voltage-gated ion channels in human pancreatic β-cells: electrophysiological characterization and role in insulin secretion. Diabetes 57:1618–1628
23. Yasuda T, Shibasaki T, Minami K et al (2010) Rim2alpha determines docking and priming states in insulin granule exocytosis. Cell Metab 12:117–129
24. Olofsson CS, Göpel SO, Barg S et al (2002) Fast insulin secretion reflects exocytosis of docked granules in mouse pancreatic B cells. Pflugers Arch 444:43–51
25. Gaisano HY, Lutz MP, Leser J et al (2001) Supramaximal cholecystokinin displaces Munc18c from the pancreatic acinar basal surface, redirecting apical exocytosis to the basal membrane. J Clin Invest 108:1597–1611
26. Cosen-Binker LI, Lam PP, Binker MG, Gaisano HY (2007) Alcohol-induced protein kinase Calpha phosphorylation of Munc18c in carbachol-stimulated acini causes basolateral exocytosis. Gastroenterology 132:1527–1545
27. Cosen-Binker LI, Binker MG, Wang CC, Hong W, Gaisano HY (2008) VAMP8 is the v-SNARE that mediates basolateral exocytosis in a mouse model of alcoholic pancreatitis. J Clin Invest 118:2535–2551
28. Duncan RR, Greaves J, Wiegand UK et al (2003) Functional and spatial segregation of secretory vesicle pools according to vesicle age. Nature 422:176–180
29. Ostenson CG, Gaisano HY, Sheu L, Tibell A, Bartfati T (2006) Impaired gene and protein expression of exocytotic SNARE complex proteins in pancreatic islets of type 2 diabetic patients. Diabetes 55:435–440
30. Gaisano HY, Ostenson CG, Sheu L, Wheeler MB, Efendic S (2002) Abnormal expression of pancreatic islet exocytotic soluble N-ethylmaleimide-sensitive factor attachment protein receptors in Goto–Kakizaki rats is partially restored by phlorizin treatment and accentuated by high glucose treatment. Endocrinology 143:4218–4226
31. Latham CF, Lopez JA, Hu SH et al (2006) Molecular dissection of the Munc18c/syntaxin4 interaction: implications for regulation of membrane trafficking. Traffic 7:1408–1419
32. Oh E, Kalwat MA, Kim MJ, Verhage M, Thurmond DC (2012) Munc18-1 regulates first-phase insulin release by promoting granule docking to multiple syntaxin isoforms. J Biol Chem 287:25821–25833