Amplification of insulin secretion by acetylcholine or phorbol ester is independent of β-cell microfilaments and distinct from metabolic amplification

Molecular and Cellular Endocrinology

Volumn 367, Issue 1-2, 2013, Pages 11-20

  Mourad, Nizar I ^a   Nenquin, Myriam ^a   Henquin, Jean Claude ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Ca2+ c; Acetylcholine; ACh; Insulin granules; Insulin secretion; IP3; KATP; Microfilaments; Pancreatic islet; Phorbol ester; PKC; PKD1; PMA

Indexed keywords

ACETYLCHOLINE; GLUCOSE; JASPAMIDE; PHORBOL ESTER; PROTEIN KINASE C; TOLBUTAMIDE;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLYMERIZATION; EXOCYTOSIS; FEMALE; GENE AMPLIFICATION; GLUCOSE METABOLISM; INSULIN RELEASE; MICROFILAMENT; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ACETYLCHOLINE; ACTIN CYTOSKELETON; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; CALCIUM; DEPSIPEPTIDES; FEMALE; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; PHORBOL ESTERS; POLYMERIZATION; THIAZOLIDINES; TOLBUTAMIDE;

EID: 84873525593     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.12.002     Document Type: Article

References (67)

1. Ahrén B. Islet G protein-coupled receptors as potential targets for treatment of type 2 diabetes. Nat. Rev. Drug Discov. 2009, 8:369-385.
2. Ammälä C., Eliasson L., Bokvist K., Berggren P.O., Honkanen R.E., Sjöholm A., Rorsman P. Activation of protein kinases and inhibition of protein phosphatases play a central role in the regulation of exocytosis in mouse pancreatic β-cells. Proc. Natl. Acad. Sci. USA 1994, 91:4343-4347.
3. Biden T.J., Prugue M.L., Davison A.G. Evidence for phosphatidylinositol hydrolysis in pancreatic islets stimulated with carbamoylcholine. Kinetic analysis of inositol polyphosphate metabolism. Biochem. J. 1992, 285:541-549.
4. Brose N., Rosenmund C. Move over protein kinase C, you've got company: alternative cellular effectors of diacylglycerol and phorbol esters. J. Cell Sci. 2002, 115:4399-4411.
5. Cantley J., Burchfield J.G., Pearson G.L., Schmitz-Peiffer C., Leitges M., Biden T.J. Deletion of PKC-epsilon selectively enhances the amplifying pathways of glucose-stimulated insulin secretion via increased lipolysis in mouse β-cells. Diabetes 2009, 58:1826-1834.
6. Eliasson L., Ma X., Renström E., Barg S., Berggren P.O., Galvanovskis J., Gromada J., Jing X., Lundquist I., Salehi A., Sewing S., Rorsman P. SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J. Gen. Physiol. 2003, 121:181-197.
7. Eliasson L., Abdulkader F., Braun M., Galvanovskis J., Hoppa M.B., Rorsman P. Novel aspects of the molecular mechanisms controlling insulin secretion. J. Physiol. 2008, 586:3313-3324.
8. Gao Z.Y., Gilon P., Henquin J.C. The role of protein kinase-C in signal transduction through vasopressin and acetylcholine receptors in pancreatic B-cells from normal mouse. Endocrinology 1994, 135:191-199.
9. Gautam D., Han S.J., Duttaroy A., Mears D., Hamdan F.F., Li J.H., Cui Y., Jeon J., Wess J. Role of the M3 muscarinic acetylcholine receptor in β-cell function and glucose homeostasis. Diabetes Obes. Metab. 2007, 9(Suppl 2):158-169.
10. + channels in mouse β-cells. J. Clin. Invest. 1993, 91:871-880.
11. Gillis K.D., Mossner R., Neher E. Protein kinase C enhances exocytosis from chromaffin cells by increasing the size of the readily releasable pool of secretory granules. Neuron 1996, 16:1209-1220.
12. Gilon P., Henquin J.C. Mechanisms and physiological significance of the cholinergic control of pancreatic beta-cell function. Endocr. Rev. 2001, 22:565-604.
13. Gonelle-Gispert C., Costa M., Takahashi M., Sadoul K., Halban P. Phosphorylation of SNAP-25 on serine-187 is induced by secretagogues in insulin-secreting cells, but is not correlated with insulin secretion. Biochem. J. 2002, 368:223-232.
14. 2+. Cell Calcium 1992, 13:219-226.
15. Henquin J.C. Regulation of insulin secretion: a matter of phase control and amplitude modulation. Diabetologia 2009, 52:739-751.
16. Henquin J.C., Nenquin M. The muscarinic receptor subtype in mouse pancreatic B-cells. FEBS Lett. 1988, 236:89-92.
17. Henquin J.C., Garcia M.C., Bozem M., Hermans M.P., Nenquin M. Muscarinic control of pancreatic B cell function involves sodium-dependent depolarization and calcium influx. Endocrinology 1988, 122:2134-2142.
18. 2+ entry. FEBS Lett. 2012, 586:89-95.
19. Jones P.M., Persaud S.J. Protein kinases, protein phosphorylation, and the regulation of insulin secretion from pancreatic β-cells. Endocr. Rev. 1998, 19:429-461.
20. 2+ and a phorbol ester on insulin secretion from islets of Langerhans permeabilised by high-voltage discharge. FEBS Lett. 1985, 191:102-106.
21. Kang L., He Z., Xu P., Fan J., Betz A., Brose N., Xu T. Munc13-1 is required for the sustained release of insulin from pancreatic beta cells. Cell Metab. 2006, 3:463-468.
22. Kasai K., Fujita T., Gomi H., Izumi T. Docking is not a prerequisite but a temporal constraint for fusion of secretory granules. Traffic 2008, 9:1191-1203.
23. 2+ in the pancreatic B-cell. FEBS Lett. 1992, 303:85-90.
24. Kong K.C., Butcher A.J., McWilliams P., Jones D., Wess J., Hamdan F.F., Werry T., Rosethorne E.M., Charlton S.J., Munson S.E., Cragg H.A., Smart A.D., Tobin A.B. M3-muscarinic receptor promotes insulin release via receptor phosphorylation/arrestin-dependent activation of protein kinase D1. Proc. Natl. Acad. Sci. USA 2010, 107:21181-21186.
25. Kwan E.P., Xie L., Sheu L., Nolan C.J., Prentki M., Betz A., Brose N., Gaisano H.Y. Munc13-1 deficiency reduces insulin secretion and causes abnormal glucose tolerance. Diabetes 2006, 55:1421-1429.
26. Kwan E.P., Xie L., Sheu L., Ohtsuka T., Gaisano H.Y. Interaction between Munc13-1 and RIM is critical for glucagon-like peptide-1 mediated rescue of exocytotic defects in Munc13-1 deficient pancreatic β-cells. Diabetes 2007, 56:2579-2588.
27. Leech C.A., Dzhura I., Chepurny O.G., Kang G., Schwede F., Genieser H.G., Holz G.G. Molecular physiology of glucagon-like peptide-1 insulin secretagogue action in pancreatic β cells. Prog. Biophys. Mol. Biol. 2011, 107:236-247.
28. Li G., Rungger-Brändle E., Just I., Jonas J.C., Aktories K., Wollheim C.B. Effect of disruption of actin filaments by Clostridium botulinum C2 toxin on insulin secretion in HIT-T15 cells and pancreatic islets. Mol. Biol. Cell 1994, 5:1199-1213.
29. 2+ entry in insulin-releasing pancreatic β-cells. Cell Calcium 1997, 22:277-286.
30. 2+ entry in mouse pancreatic β-cells by both direct and indirect mechanisms. J. Physiol. 1997, 503:387-398.
31. Mourad N.I., Nenquin M., Henquin J.C. Metabolic amplifying pathway increases both phases of insulin secretion independently of β-cell actin microfilaments. Am. J. Physiol. Cell Physiol. 2010, 299:C389-398.
32. Mourad N.I., Nenquin M., Henquin J.C. Metabolic amplification of insulin secretion by glucose is independent of β-cell microtubules. Am. J. Physiol. Cell Physiol. 2011, 300:C697-706.
33. Mourad N.I., Nenquin M., Henquin J.C. CAMP-mediated and metabolic amplification of insulin secretion are distinct pathways sharing independence of β-cell microfilaments. Endocrinology 2012, 153:4644-4654.
34. Nagamatsu S., Ohara-Imaizumi M., Nakamichi Y., Kikuta T., Nishiwaki C. Imaging docking and fusion of insulin granules induced by antidiabetes agents: sulfonylurea and glinide drugs preferentially mediate the fusion of newcomer, but not previously docked, insulin granules. Diabetes 2006, 55:2819-2825.
35. 2+ influx by phorbol ester in rat pancreatic β-cells. Cell Signal. 2001, 13:199-205.
36. Nenquin M., Szollosi A., Aguilar-Bryan L., Bryan J., Henquin J.C. Both triggering and amplifying pathways contribute to fuel-induced insulin secretion in the absence of sulfonylurea receptor-1 in pancreatic β-cells. J. Biol. Chem. 2004, 279:32316-32324.
37. Nesher R., Anteby E., Yedovizky M., Warwar N., Kaiser N., Cerasi E. β-cell protein kinases and the dynamics of the insulin response to glucose. Diabetes 2002, 51(Suppl 1):S68-S73.
38. Nevins A.K., Thurmond D.C. Glucose regulates the cortical actin network through modulation of Cdc42 cycling to stimulate insulin secretion. Am. J. Physiol. Cell Physiol. 2003, 285:C698-710.
39. 2+. Diabetes 1998, 47:1699-1706.
40. 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.
41. Pedersen M.G., Sherman A. Newcomer insulin secretory granules as a highly calcium-sensitive pool. Proc. Natl. Acad. Sci. USA 2009, 106:7432-7436.
42. 2+, cAMP, and phospholipid-derived messengers in coupling mechanisms of insulin secretion. Physiol. Rev. 1987, 67:1185-1248.
43. 2+ measurements in mouse pancreatic beta cells support the existence of an amplifying effect of glucose on insulin secretion. Diabetologia 2010, 53:1947-1957.
44. + current by muscarinic receptors in mouse pancreatic β-cells. J. Biol. Chem. 2002, 277:38373-38380.
45. ATP channel-independent pathway of regulation of insulin secretion by glucose: in search of the underlying mechanism. Diabetes 1998, 47:1713-1721.
46. + channels in β-cells. Endocrinology 1999, 140:2252-2257.
47. Schmitz-Peiffer C., Biden T.J. Protein kinase C function in muscle, liver, and β-cells and its therapeutic implications for type 2 diabetes. Diabetes 2008, 57:1774-1783.
48. Seino S. Cell signalling in insulin secretion: the molecular targets of ATP, cAMP and sulfonylurea. Diabetologia 2012, 55:2096-2108.
49. 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. USA 2007, 104:19333-19338.
50. Shu Y., Liu X., Yang Y., Takahashi M., Gillis K.D. Phosphorylation of SNAP-25 at Ser187 mediates enhancement of exocytosis by a phorbol ester in INS-1 cells. J. Neurosci. 2008, 28:21-30.
51. Straub S.G., Sharp G.W. Glucose-stimulated signaling pathways in biphasic insulin secretion. Diabetes Metab. Res. Rev. 2002, 18:451-463.
52. Sumara G., Formentini I., Collins S., Sumara I., Windak R., Bodenmiller B., Ramracheya R., Caille D., Jiang H., Platt K.A., Meda P., Aebersold R., Rorsman P., Ricci R. Regulation of PKD by the MAPK p38delta in insulin secretion and glucose homeostasis. Cell 2009, 136:235-248.
53. Swayne L.A., Mezghrani A., Varrault A., Chemin J., Bertrand G., Dalle S., Bourinet E., Lory P., Miller R.J., Nargeot J., Monteil A. The NALCN ion channel is activated by M3 muscarinic receptors in a pancreatic β-cell line. EMBO Rep. 2009, 10:873-880.
54. 2+ by forskolin and phorbol ester. FEBS Lett. 1985, 183:430-432.
55. Taneera J., Lang S., Sharma A., Fadista J., Zhou Y., Ahlqvist E., Jonsson A., Lyssenko V., Vikman P., Hansson O., Parikh H., Korsgren O., Soni A., Krus U., Zhang E., Jing X.J., Esguerra J.L., Wollheim C.B., Salehi A., Rosengren A., Renström E., Groop L. A systems genetics approach identifies genes and pathways for type 2 diabetes in human islets. Cell Metab. 2012, 16:122-134.
56. Tsuboi T., Kikuta T., Warashina A., Terakawa S. Protein kinase C-dependent supply of secretory granules to the plasma membrane. Biochem. Biophys. Res. Commun. 2001, 282:621-628.
57. Uchida T., Iwashita N., Ohara-Imaizumi M., Ogihara T., Nagai S., Choi J.B., Tamura Y., Tada N., Kawamori R., Nakayama K.I., Nagamatsu S., Watada H. Protein kinase C delta plays a non-redundant role in insulin secretion in pancreatic β-cells. J. Biol. Chem. 2007, 282:2707-2716.
58. van Obberghen E., Somers G., Devis G., Vaughan G.D., Malaisse-Lagae F., Orci L., Malaisse W.J. Dynamics of insulin release and microtubular-microfilamentous system. Effect of cytochalasin B. J. Clin. Invest. 1973, 52:1041-1051.
59. Vitale M.L., Seward E.P., Trifaró J.M. Chromaffin cell cortical actin network dynamics control the size of the release-ready vesicle pool and the initial rate of exocytosis. Neuron 1995, 14:353-363.
60. 2+. J. Gen. Physiol. 2004, 124:653-662.
61. Wang Z., Thurmond D.C. Mechanisms of biphasic insulin-granule exocytosis - roles of the cytoskeleton, small GTPases and SNARE proteins. J. Cell Sci. 2009, 122:893-903.
62. Xie L., Zhu D., Gaisano H.Y. 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 2012, 55:2693-2702.
63. Yaney G.C., Corkey B.E. Fatty acid metabolism and insulin secretion in pancreatic beta cells. Diabetologia 2003, 46:1297-1312.
64. 2+-sensitive pool of granules is regulated by glucose and protein kinases in insulin-secreting INS-1 cells. J. Gen. Physiol. 2004, 124:641-651.
65. Yu W., Niwa T., Fukasawa T., Hidaka H., Senda T., Sasaki Y., Niki I. Synergism of protein kinase A, protein kinase C, and myosin light-chain kinase in the secretory cascade of the pancreatic β-cell. Diabetes 2000, 49:945-952.
66. Zawalich W.S., Zawalich K.C. Effects of protein kinase C inhibitors on insulin secretory responses from rodent pancreatic islets. Mol. Cell. Endocrinol. 2001, 177:95-105.
67. Zhang H., Nagasawa M., Yamada S., Mogami H., Suzuki Y., Kojima I. Bimodal role of conventional protein kinase C in insulin secretion from rat pancreatic β-cells. J. Physiol. 2004, 561:133-147.