Gelsolin associates with the N terminus of syntaxin 4 to regulate insulin granule exocytosis

Molecular Endocrinology

Volumn 26, Issue 1, 2012, Pages 128-141

  Kalwat, Michael A ^a   Wiseman, Dean A ^a   Luo, Wei ^b   Wang, Zhanxiang ^a   Thurmond, Debbie C ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GenScript Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELSOLIN; GLUCOSE; GREEN FLUORESCENT PROTEIN; INSULIN; NIFEDIPINE; POTASSIUM CHLORIDE; SNARE PROTEIN; SYNTAXIN 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DISSOCIATION; EXOCYTOSIS; IN VITRO STUDY; INSULIN RELEASE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY MECHANISM;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; CELL LINE; CELL MEMBRANE; EXOCYTOSIS; GELSOLIN; GLUCOSE; GREEN FLUORESCENT PROTEINS; INSULIN; INSULIN-SECRETING CELLS; MICE; NIFEDIPINE; POTASSIUM CHLORIDE; QA-SNARE PROTEINS; SECRETORY VESICLES; SNARE PROTEINS;

EID: 84855213751     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2011-1112     Document Type: Article

References (75)

1. Grodsky GM 2000 Kinetics of insulin secretion: underlying metabolic events. In: LeRoith D, Taylor S, Olefsky J, eds. Diabetes mellitus: a fundamental and clinical text. Philadelphia: Lippincott Williams & Wilkins
2. Rorsman P, Eliasson L, Renström E, Gromada J, Barg S, Göpel S 2000 The cell physiology of biphasic insulin secretion. News Physiol Sci 15:72-77
3. Regazzi R, Wollheim CB, Lang J, Theler JM, Rossetto O, Montecucco C, Sadoul K, Weller U, Palmer M, Thorens B 1995 VAMP-2 and cellubrevin are expressed in pancreatic β-cells and are essential for Ca(2+)-but not for GTP γ S-induced insulin secretion. EMBO J 14:2723-2730
4. Sadoul K, Lang J, Montecucco C, Weller U, Regazzi R, Catsicas S, Wollheim CB, Halban PA 1995 SNAP-25 is expressed in islets of Langerhans and is involved in insulin release. J Cell Biol 128:1019-1028
5. Kiraly-Borri CE, Morgan A, Burgoyne RD, Weller U, Wollheim CB, Lang J 1996 Soluble N-ethylmaleimide-sensitive-factor attachment protein and N-ethylmaleimide-insensitive factors are required for Ca2+-stimulated exocytosis of insulin. Biochem J 314:199-203
6. Jacobsson G, Bean AJ, Scheller RH, Juntti-Berggren L, Deeney JT, Berggren PO, Meister B 1994 Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells. Proc Natl Acad Sci USA 91:12487-12491
7. Spurlin BA, Thurmond DC 2006 Syntaxin 4 facilitates biphasic glucose-stimulated insulin secretion from pancreatic β-cells. Mol Endocrinol 20:183-193
8. 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
9. Thurmond DC, Gonelle-Gispert C, Furukawa M, Halban PA, Pessin JE 2003 Glucose-stimulated insulin secretion is coupled to the interaction of actin with the t-SNARE (target membrane soluble N-ethylmaleimide-sensitive factor attachment protein receptor protein) complex. Mol Endocrinol 17:732-742
10. 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
11. Wheeler MB, Sheu L, Ghai M, Bouquillon A, Grondin G, Weller U, Beaudoin AR, Bennett MK, Trimble WS, Gaisano HY 1996 Characterization of SNARE protein expression in β cell lines and pancreatic islets. Endocrinology 137:1340-1348
12. Jahn R, Scheller RH 2006 SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 7:631-643
13. Chen YA, Scheller RH 2001 SNARE-mediated membrane fusion. Nat Rev Mol Cell Biol 2:98-106
14. Leahy JL, Fineman MS 1998 Impaired phasic insulin and amylin secretion in diabetic rats. Am J Physiol 275:E457-E462
15. Varadi A, Tsuboi T, Rutter GA 2005 Myosin Va transports dense core secretory vesicles in pancreatic MIN6 β-cells. Mol Biol Cell 16:2670-2680
16. Nevins AK, Thurmond DC 2003 Glucose regulates the cortical actin network through modulation of Cdc42 cycling to stimulate insulin secretion. Am J Physiol Cell Physiol 285:C698-C710
17. Orci L, Gabbay KH, Malaisse WJ 1972 Pancreatic β-cell web: its possible role in insulin secretion. Science 175:1128-1130
18. Aunis D, Bader MF 1988 The cytoskeleton as a barrier to exocytosis in secretory cells. J Exp Biol 139:253-266
19. Mourad NI, Nenquin M, Henquin JC 2010 Metabolic amplifying pathway increases both phases of insulin secretion independently of β-cell actin microfilaments. Am J Physiol Cell Physiol 299:C389-C398
20. Schubert S, Knoch KP, Ouwendijk J, Mohammed S, Bodrov Y, Jäger M, Altkrüger A, Wegbrod C, Adams ME, Kim Y, Froehner SC, Jensen ON, Kalaidzidis Y, Solimena M 2010 β2-Syntrophin is a Cdk5 substrate that restrains the motility of insulin secretory granules. PLoS One 5:e12929
21. Snabes MC, Boyd 3rd AE 1982 Increased filamentous actin in islets of Langerhans from fasted hamsters. Biochem Biophys Res Commun 104:207-211
22. Swanston-Flatt SK, Carlsson L, Gylfe E 1980 Actin filament formation in pancreatic β-cells during glucose stimulation of insulin secretion. FEBS Lett 117:299-302
23. Konstantinova I, Nikolova G, Ohara-Imaizumi M, Meda P, Kucera T, Zarbalis K, Wurst W, Nagamatsu S, Lammert E 2007 EphAephrin-A-mediatedβ cell communication regulates insulin secretion from pancreatic islets. Cell 129:359-370
24. Howell SL, Tyhurst M 1980 The role of actin in the secretory cycle. Horm Metab Res Suppl 10(Suppl):168-171
25. Lacy PE, Walker MM, Fink CJ 1972 Perifusion of isolated rat islets in vitro. Participation of the microtubular system in the biphasic release of insulin. Diabetes 21:987-998
26. Langford GM 2002 Myosin-V, a versatile motor for short-range vesicle transport. Traffic 3:859-865
27. Eitzen G 2003 Actin remodeling to facilitate membrane fusion. Biochim Biophys Acta 1641:175-181
28. Woronowicz K, Dilks JR, Rozenvayn N, Dowal L, Blair PS, Peters CG, Woronowicz L, Flaumenhaft R 2010 The platelet actin cytoskeleton associates with SNAREs and participates in α-granule secretion. Biochemistry 49:4533-4542
29. Lang T, Wacker I, Wunderlich I, Rohrbach A, Giese G, Soldati T, Almers W 2000 Role of actin cortex in the subplasmalemmal transport of secretory granules in PC-12 cells. Biophys J 78:2863-2877
30. Torregrosa-Hetland CJ, Villanueva J, Giner D, Lopez-Font I, Nadal A, Quesada I, Viniegra S, Expósito-Romero G, Gil A, Gonzalez-Velez V, Segura J, Gutiérrez LM 2011 The F-actin cortical network is a major factor influencing the organization of the secretory machinery in chromaffin cells. J Cell Sci 124:727-734
31. Rondas D, Tomas A, Halban PA 2011 Focal adhesion remodeling is crucial for glucose-stimulated insulin secretion and involves activation of focal adhesion kinase and paxillin. Diabetes 60:1146-1157
32. Jaques F, Jousset H, Tomas A, Prost AL, Wollheim CB, Irminger JC, Demaurex N, Halban PA 2008 Dual effect of cell-cell contact disruption on cytosolic calcium and insulin secretion. Endocrinology 149:2494-2505
33. Band AM, Ali H, Vartiainen MK, Welti S, Lappalainen P, Olkkonen VM, Kuismanen E 2002 Endogenous plasma membrane t-SNARE syntaxin 4 is present in rab11 positive endosomal membranes and associates with cortical actin cytoskeleton. FEBS Lett 531:513-519
34. Wang Z, Thurmond DC 2010 Differential phosphorylation of RhoGDI mediates the distinct cycling of Cdc42 and Rac1 to regulate second-phase insulin secretion. J Biol Chem 285:6186-6197
35. Wang Z, Oh E, Thurmond DC 2007 Glucose-stimulated Cdc42 signaling is essential for the second phase of insulin secretion. J Biol Chem 282:9536-9546
36. Tomas A, Yermen B, Min L, Pessin JE, Halban PA 2006 Regulation of pancreatic _-cell insulin secretion by actin cytoskeleton remodelling: role of gelsolin and cooperation with the MAPK signalling pathway. J Cell Sci 119:2156-2167
37. Nelson TY, Boyd 3rd AE 1985 Gelsolin, a Ca2+-dependent actinbinding protein in a hamster insulin-secreting cell line. J Clin Invest 75:1015-1022
38. Jewell JL, Oh E, Bennett SM, Meroueh SO, Thurmond DC 2008 The tyrosine phosphorylation of Munc18c induces a switch in binding specificity from syntaxin 4 to Doc2β. J Biol Chem 283:21734-21746
39. Yermen B, Tomas A, Halban PA 2007 Pro-survival role of gelsolin in mouse β-cells. Diabetes 56:80-87
40. Witke W, Sharpe AH, Hartwig JH, Azuma T, Stossel TP, Kwiatkowski DJ 1995 Hemostatic, inflammatory, and fibroblast responses are blunted in mice lacking gelsolin. Cell 81:41-51
41. Wiseman DA, Kalwat MA, Thurmond DC 2011 Stimulus-induced S-nitrosylation of syntaxin 4 impacts insulin granule exocytosis. J Biol Chem 286:16344-16354
42. Nevins AK, Thurmond DC 2006 Caveolin-1 functions as a novel Cdc42 guanine nucleotide dissociation inhibitor in pancreatic β-cells. J Biol Chem 281:18961-18972
43. Ishihara H, Asano T, Tsukuda K, Katagiri H, Inukai K, Anai M, Kikuchi M, Yazaki Y, Miyazaki JI, Oka Y 1993 Pancreatic β cell line MIN6 exhibits characteristics of glucose metabolism and glucose-stimulated insulin secretion similar to those of normal islets. Diabetologia 36:1139-1145
44. Henquin JC 2000 Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 49:1751-1760
45. Bratanova-Tochkova TK, Cheng H, Daniel S, Gunawardana S, Liu YJ, Mulvaney-Musa J, Schermerhorn T, Straub SG, Yajima H, Sharp GW 2002 Triggering and augmentation mechanisms, granule pools, and biphasic insulin secretion. Diabetes 51:S83-90
46. Straub SG, Sharp GW 2002 Glucose-stimulated signaling pathways in biphasic insulin secretion. Diabetes Metab Res Rev 18:451-463
47. 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 277:3805-3808
48. Gembal M, Gilon P, Henquin JC 1992 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
49. Henquin JC, Ishiyama N, Nenquin M, Ravier MA, Jonas JC 2002 Signals and pools underlying biphasic insulin secretion. Diabetes 51:S60-S67
50. Spinardi L, Witke W 2007 Gelsolin and diseases. Subcell Biochem 45:55-69
51. Rutter GA, Tsuboi T, Ravier MA 2006 Ca2+ microdomains and the control of insulin secretion. Cell Calcium 40:539-551
52. Nightingale TD, White IJ, Doyle EL, Turmaine M, Harrison-Lavoie KJ, Webb KF, Cramer LP, Cutler DF 2011 Actomyosin II contractility expels von Willebrand factor from Weibel-Palade bodies during exocytosis. J Cell Biol 194:613-629
53. Yin HL, Stossel TP 1979 Control of cytoplasmic actin gel-sol transformation by gelsolin, a calcium-dependent regulatory protein. Nature 281:583-586
54. Choe H, Burtnick LD, Mejillano M, Yin HL, Robinson RC, Choe S 2002 The calcium activation of gelsolin: insights from the 3A structure of the G4-G6/actin complex. J Mol Biol 324:691-702
55. Burtnick LD, Koepf EK, Grimes J, Jones EY, Stuart DI, McLaughlin PJ, Robinson RC 1997 The crystal structure of plasma gelsolin: implications for actin severing, capping, and nucleation. Cell 90: 661-670
56. Casimir M, Dai XQ, Hajmrle C, Kolic J, Guo D, Oudit G, MacDonald PE 2011 Gelsolin knockout impairs insulin secretion independently of actin polymerization. Diabetes 60:A351
57. Azuma T, Witke W, Stossel TP, Hartwig JH, Kwiatkowski DJ 1998 Gelsolin is a downstream effector of rac for fibroblast motility. EMBO J 17:1362-1370
58. Furukawa K, Fu W, Li Y, Witke W, Kwiatkowski DJ, Mattson MP 1997 The actin-severing protein gelsolin modulates calcium channel and NMDA receptor activities and vulnerability to excitotoxicity in hippocampal neurons. J Neurosci 17:8178-8186
59. Janmey PA, Stossel TP 1987 Modulation of gelsolin function by phosphatidylinositol 4,5-bisphosphate. Nature 325:362-364
60. Tomas A, Yermen B, Regazzi R, Pessin JE, Halban PA 2010 Regulation of insulin secretion by phosphatidylinositol-4,5-bisphosphate. Traffic 11:123-137
61. El Sayegh TY, Arora PD, Ling K, Laschinger C, Janmey PA, Anderson RA, McCulloch CA 2007 Phosphatidylinositol-4,5 bisphosphate produced by PIP5KIγ regulates gelsolin, actin assembly, and adhesion strength of N-cadherin junctions. Mol Biol Cell 18:3026-3038
62. Lueck A, Brown D, Kwiatkowski DJ 1998 The actin-binding proteins adseverin and gelsolin are both highly expressed but differentially localized in kidney and intestine. J Cell Sci 111(Pt 24):3633-3643
63. Bruun TZ, Høy M, Gromada J 2000 Scinderin-derived actin-binding peptides inhibit Ca(2+)-and GTPγS-dependent exocytosis in mouse pancreatic β-cells. Eur J Pharmacol 403:221-224
64. Sørensen JB, Matti U, Wei SH, Nehring RB, Voets T, Ashery U, Binz T, Neher E, Rettig J 2002 The SNARE protein SNAP-25 is linked to fast calcium triggering of exocytosis. Proc Natl Acad Sci USA 99:1627-1632
65. Wiser O, Trus M, Hernández A, Renström E, Barg S, Rorsman P, Atlas D 1999 The voltage sensitive Lc-type Ca2+ channel is functionally coupled to the exocytotic machinery. Proc Natl Acad Sci USA 96:248-253
66. Yang SN, Larsson O, Bränström R, Bertorello AM, Leibiger B, Leibiger IB, Moede T, Köhler M, Meister B, Berggren PO 1999 Syntaxin 1 interacts with the L(D) subtype of voltage-gated Ca(2+) channels in pancreatic β cells. Proc Natl Acad Sci USA 96:10164-10169
67. Gustavsson N, Lao Y, Maximov A, Chuang JC, Kostromina E, Repa JJ, Li C, Radda GK, Südhof TC, Han W 2008 Impaired insulin secretion and glucose intolerance in synaptotagmin-7 null mutant mice. Proc Natl Acad Sci USA 105:3992-3997
68. Gauthier BR, Duhamel DL, Iezzi M, Theander S, Saltel F, Fukuda M, Wehrle-Haller B, Wollheim CB 2008 Synaptotagmin VII splice variants α, β, and δ are expressed in pancreatic β-cells and regulate insulin exocytosis. FASEB J 22:194-206
69. Ke B, Oh E, Thurmond DC 2007 Doc2_ is a novel Munc18cinteracting partner and positive effector of syntaxin 4-mediated exocytosis. J Biol Chem 282:21786-21797
70. Verhage M, de Vries KJ, Røshol H, Burbach JP, Gispen WH, Südhof TC 1997 DOC2 proteins in rat brain: complementary distribution and proposed function as vesicular adapter proteins in early stages of secretion. Neuron 18:453-461
71. Oh E, Thurmond DC 2006 The stimulus-induced tyrosine phosphorylation of Munc18c facilitates vesicle exocytosis. J Biol Chem 281:17624-17634
72. Lopez JP, Turner JR, Philipson LH 2010 Glucose-induced ERM protein activation and translocation regulates insulin secretion. Am J Physiol Endocrinol Metab 299:E772-E785
73. Yaekura K, Julyan R, Wicksteed BL, Hays LB, Alarcon C, Sommers S, Poitout V, Baskin DG, Wang Y, Philipson LH, Rhodes CJ 2003 Insulin secretory deficiency and glucose intolerance in Rab3A null mice. J Biol Chem 278:9715-9721
74. Billing-Marczak K, Przybyszewska M, Kuźnicki J 1999 Measurements of [Ca2+] using fura-2 in glioma C6 cells expressing calretinin with GFP as a marker of transfection: no Ca2+-buffering provided by calretinin. Biochim Biophys Acta 1449:169-177
75. Oh E, Thurmond DC 2009 Munc18c depletion selectively impairs the sustained phase of insulin release. Diabetes 58:1165-1174