The insulin secretory granule as a signaling hub

Trends in Endocrinology and Metabolism

Volumn 21, Issue 10, 2010, Pages 599-609

  Suckale, Jakob ^a   Solimena, Michele ^a,b  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; AMYLIN; C PEPTIDE; CALCIUM CHANNEL; GUANINE NUCLEOTIDE BINDING PROTEIN; INSULIN; ION CHANNEL; MEMBRANE PROTEIN; POLYPEPTIDE; POTASSIUM CHANNEL; PROINSULIN; PROTEIN TYROSINE PHOSPHATASE; PROTEOME; RAB PROTEIN; RAB27A PROTEIN; RAB3A PROTEIN; UNCLASSIFIED DRUG;

BRAIN; ENERGY METABOLISM; FEEDBACK SYSTEM; GOLGI COMPLEX; HORMONE RELEASE; HUMAN; INSULIN RELEASE; INSULINOMA; KIDNEY CELL; MEMBRANE TRANSPORT; METABOLIC REGULATION; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEOMICS; REVIEW; SECRETORY GRANULE; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CHROMOGRANINS; HUMANS; INSULIN; MONOMERIC GTP-BINDING PROTEINS; SECRETORY VESICLES; SIGNAL TRANSDUCTION;

EID: 77957235524     PISSN: 10432760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tem.2010.06.003     Document Type: Review

References (117)

1. Fonseca S.G., et al. Endoplasmic reticulum stress in beta-cells and development of diabetes. Curr. Opin. Pharmacol. 2009, 9:763-770.
2. Miaczynska M., et al. Not just a sink: endosomes in control of signal transduction. Curr. Opin. Cell Biol. 2004, 16:400-406.
3. Suckale J., Solimena M. Pancreas islets in metabolic signaling-focus on the beta-cell. Front. Biosci. 2008, 13:7156-7171.
4. Derbinski J., et al. Promiscuous gene expression in medullary thymic epithelial cells mirrors the peripheral self. Nat. Immunol. 2001, 2:1032-1039.
5. Fan Y., et al. Thymus-specific deletion of insulin induces autoimmune diabetes. EMBO J. 2009, 28:2812-2824.
6. Deltour L., et al. Differential expression of the two nonallelic proinsulin genes in the developing mouse embryo. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:527-531.
7. Devaskar S.U., et al. Insulin gene expression and insulin synthesis in mammalian neuronal cells. J. Biol. Chem. 1994, 269:8445-8454.
8. Song J., et al. Axons guided by insulin receptor in Drosophila visual system. Science 2003, 300:502-505.
9. Rajala A., et al. Loss of neuroprotective survival signal in mice lacking insulin receptor gene in rod photoreceptor cells. J. Biol. Chem. 2008, 283:19781-19792.
10. Kojima H., et al. Extrapancreatic insulin-producing cells in multiple organs in diabetes. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2458-2463.
11. Schuit F.C., et al. Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pancreatic beta cells. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:3865-3869.
12. Dean P.M. Ultrastructural morphometry of the pancreatic beta-cell. Diabetologia 1973, 9:115-119.
13. Straub S.G., et al. 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 2004, 53:3179-3183.
14. Howell S.L. The mechanism of insulin secretion. Diabetologia 1984, 26:319-327.
15. Dunn M.F. Zinc-ligand interactions modulate assembly and stability of the insulin hexamer - a review. Biometals 2005, 18:295-303.
16. Yu S.S., Kitbachi A.E. Biological activity of proinsulin and related polypeptides in the fat tissue. J. Biol. Chem. 1973, 248:3753-3761.
17. Galloway J.A., et al. Biosynthetic human proinsulin. Review of chemistry, in vitro and in vivo receptor binding, animal and human pharmacology studies, and clinical trial experience. Diabetes Care 1992, 15:666-692.
18. Steiner D.F., et al. A brief perspective on insulin production. Diabetes. Obes. Metab. 2009, 11(Suppl 4):189-196.
19. Davidson H.W., et al. Intraorganellar calcium and pH control proinsulin cleavage in the pancreatic beta cell via two distinct site-specific endopeptidases. Nature 1988, 333:93-96.
20. Marsh B.J., et al. Regulated autophagy controls hormone content in secretory-deficient pancreatic endocrine beta-cells. Mol. Endocrinol. 2007, 21:2255-2269.
21. Michael D.J., et al. Pancreatic beta-cells secrete insulin in fast- and slow-release forms. Diabetes 2006, 55:600-607.
22. Halban P.A. Differential rates of release of newly synthesized and of stored insulin from pancreatic islets. Endocrinology 1982, 110:1183-1188.
23. Gold G., et al. Evidence that glucose " marks" beta cells resulting in preferential release of newly synthesized insulin. Science 1982, 218:56-58.
24. Hutton J.C., et al. Isolation and characterisation of insulin secretory granules from a rat islet cell tumour. Diabetologia 1982, 23:365-373.
25. Hickey A.J.R., et al. Proteins associated with immunopurified granules from a model pancreatic islet beta-cell system: proteomic snapshot of an endocrine secretory granule. J. Proteome Res. 2009, 8:178-186.
26. Brunner Y., et al. Proteomics analysis of insulin secretory granules. Mol. Cell Proteomics 2007, 6:1007-1017.
27. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26:1367-1372.
28. Saltiel A.R., Kahn C.R. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001, 414:799-806.
29. Pollak M. Insulin and insulin-like growth factor signalling in neoplasia. Nat. Rev. Cancer 2008, 8:915-928.
30. McNay E.C. Insulin and ghrelin: peripheral hormones modulating memory and hippocampal function. Curr. Opin. Pharmacol. 2007, 7:628-632.
31. Leibiger I.B., et al. Insulin signaling in the pancreatic beta-cell. Annu. Rev. Nutr. 2008, 28:233-251.
32. Shafqat J., et al. Proinsulin C-peptide elicits disaggregation of insulin resulting in enhanced physiological insulin effects. Cell Mol. Life Sci. 2006, 63:1805-1811.
33. Bugliani M., et al. Effects of C-peptide on isolated human pancreatic islet cells. Diabetes Metab. Res. Rev. 2007, 23:215-219.
34. Samnegård B., et al. C-peptide prevents glomerular hypertrophy and mesangial matrix expansion in diabetic rats. Nephrol. Dial. Transplant 2005, 20:532-538.
35. Kamiya H., et al. C-Peptide reverses nociceptive neuropathy in type 1 diabetes. Diabetes 2006, 55:3581-3587.
36. Ogawa A., et al. Amylin secretion from the rat pancreas and its selective loss after streptozotocin treatment. J. Clin. Invest. 1990, 85:973-976.
37. Akesson B., et al. Islet amyloid polypeptide inhibits glucagon release and exerts a dual action on insulin release from isolated islets. Regul. Pept. 2003, 111:55-60.
38. Young A.A., et al. Dose-responses for the slowing of gastric emptying in a rodent model by glucagon-like peptide (7-36) NH2, amylin, cholecystokinin, and other possible regulators of nutrient uptake. Metabolism 1996, 45:1-3.
39. Rushing P.A., et al. Amylin: a novel action in the brain to reduce body weight. Endocrinology 2000, 141:850-853.
40. Dacquin R., et al. Amylin inhibits bone resorption while the calcitonin receptor controls bone formation in vivo. J. Cell Biol. 2004, 164:509-514.
41. Lee N.K., et al. Endocrine regulation of energy metabolism by the skeleton. Cell 2007, 130:456-469.
42. Khemtémourian, L. et al. (2008) Recent insights in islet amyloid polypeptide-induced membrane disruption and its role in beta-cell death in type 2 diabetes mellitus. Exp. Diabetes Res. 2008, DOI: doi:10.1155/2008/421287.
43. Cornu M., et al. Glucagon-like peptide-1 protects beta-cells against apoptosis by increasing the activity of an IGF-2/IGF-1 receptor autocrine loop. Diabetes 2009, 58:1816-1825.
44. Cornu M., et al. Glucagon-like peptide-1 increases beta-cell glucose competence and proliferation by translational induction of insulin-like growth factor-1 receptor expression. J. Biol. Chem. 2010, 285:10538-10545.
45. Buchanan C.M., et al. Preptin derived from proinsulin-like growth factor II (proIGF-II) is secreted from pancreatic islet beta-cells and enhances insulin secretion. Biochem. J. 2001, 360:431-439.
46. Cornish J., et al. Preptin, another peptide product of the pancreatic beta-cell, is osteogenic in vitro and in vivo. Am. J. Physiol. Endocrinol. Metab. 2007, 292:E117-122.
47. Waeber G., et al. Insulin secretion is regulated by the glucose-dependent production of islet beta cell macrophage migration inhibitory factor. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:4782-4787.
48. Portela-Gomes G.M., et al. PACAP is expressed in secretory granules of insulin and glucagon cells in human and rodent pancreas. Evidence for generation of cAMP compartments uncoupled from hormone release in diabetic islets. Regul. Pept. 2003, 113:31-39.
49. Kim T., et al. Chromogranin A, an " on/off" switch controlling dense-core secretory granule biogenesis. Cell 2001, 106:499-509.
50. Hendy G.N., et al. Targeted ablation of the chromogranin a (Chga) gene: normal neuroendocrine dense-core secretory granules and increased expression of other granins. Mol. Endocrinol. 2006, 20:1935-1947.
51. Portela-Gomes G.M., et al. The importance of chromogranin A in the development and function of endocrine pancreas. Regul. Pept. 2008, 151:19-25.
52. Obermüller S., et al. Defective secretion of islet hormones in chromogranin-B deficient mice. PLoS ONE 2010, 5:e8936.
53. Udupi V., et al. Prohormone convertase-1 is essential for conversion of chromogranin A to pancreastatin. Regul. Pept. 1999, 83:123-127.
54. Hoflehner J., et al. Processing of secretogranin II by prohormone convertases: importance of PC1 in generation of secretoneurin. FEBS Lett. 1995, 360:294-298.
55. Schmid G.M., et al. Inhibition of insulin secretion by betagranin, an N-terminal chromogranin A fragment. J. Biol. Chem. 2007, 282:12717-12724.
56. Arden S.D., et al. The post-translational processing of chromogranin A in the pancreatic islet: involvement of the eukaryote subtilisin PC2. Biochem. J. 1994, 298:521-528.
57. Tatemoto K., et al. Pancreastatin, a novel pancreatic peptide that inhibits insulin secretion. Nature 1986, 324:476-478.
58. Sánchez-Margalet V., Goberna R. Pancreastatin inhibits insulin-stimulated glycogen synthesis but not glycolysis in rat hepatocytes. Regul. Pept. 1994, 51:215-220.
59. Gayen J.R., et al. A novel pathway of insulin sensitivity in chromogranin A null mice: a crucial role for pancreastatin in glucose homeostasis. J. Biol. Chem. 2009, 284:28498-28509.
60. Ghia J., et al. The effect of a chromogranin A-derived peptide (CgA4-16) in the writhing nociceptive response induced by acetic acid in rats. Life Sci. 2004, 75:1787-1799.
61. Lugardon K., et al. Antibacterial and antifungal activities of vasostatin-1, the N-terminal fragment of chromogranin A. J. Biol. Chem. 2000, 275:10745-10753.
62. Braun M., et al. Corelease and differential exit via the fusion pore of GABA, serotonin, and ATP from LDCV in rat pancreatic beta cells. J. Gen. Physiol. 2007, 129:221-231.
63. Bailey S.J., et al. Glucose-dependent regulation of gamma-aminobutyric acid (GABA A) receptor expression in mouse pancreatic islet alpha-cells. Diabetes 2007, 56:320-327.
64. Petit P., et al. P2 purinergic signalling in the pancreatic beta-cell: control of insulin secretion and pharmacology. Eur. J. Pharm. Sci. 2009, 37:67-75.
65. Richards-Williams C., et al. Extracellular ATP and zinc are co-secreted with insulin and activate multiple P2X purinergic receptor channels expressed by islet beta-cells to potentiate insulin secretion. Purinergic Signal. 2008, 4:393-405.
66. Léon C., et al. The P2Y(1) receptor is involved in the maintenance of glucose homeostasis and in insulin secretion in mice. Purinergic Signal. 2005, 1:145-151.
67. Verspohl E.J., et al. Effect of purinergic agonists and antagonists on insulin secretion from INS-1 cells (insulinoma cell line) and rat pancreatic islets. Can. J. Physiol. Pharmacol. 2002, 80:562-568.
68. Bertrand G., et al. Membrane and intracellular effects of adenosine in mouse pancreatic beta-cells. Am. J. Physiol. 1989, 257:E473-478.
69. Lemaire K., et al. Insulin crystallization depends on zinc transporter ZnT8 expression, but is not required for normal glucose homeostasis in mice. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14872-14877.
70. Nicolson T.J., et al. Insulin storage and glucose homeostasis in mice null for the granule zinc transporter ZnT8 and studies of the type 2 diabetes-associated variants. Diabetes 2009, 58:2070-2083.
71. Ishihara H., et al. Islet beta-cell secretion determines glucagon release from neighbouring alpha-cells. Nat. Cell Biol. 2003, 5:330-335.
72. Slucca M., et al. ATP-sensitive K+ channel mediates the zinc switch-off signal for glucagon response during glucose deprivation. Diabetes 2010, 59:128-134.
73. Ravier M.A., Rutter G.A. Glucose or insulin, but not zinc ions, inhibit glucagon secretion from mouse pancreatic alpha-cells. Diabetes 2005, 54:1789-1797.
74. Jansen J., et al. Zinc and diabetes-clinical links and molecular mechanisms. J. Nutr. Biochem. 2009, 20:399-417.
75. Torii S., et al. Cytoplasmic transport signal is involved in phogrin targeting and localization to secretory granules. Traffic 2005, 6:1213-1224.
76. Wasmeier C., et al. The lumenal domain of the integral membrane protein phogrin mediates targeting to secretory granules. Traffic 2002, 3:654-665.
77. Hosaka M., et al. Interaction between secretogranin III and carboxypeptidase E facilitates prohormone sorting within secretory granules. J. Cell Sci. 2005, 118:4785-4795.
78. Taupenot L., et al. Identification of a novel sorting determinant for the regulated pathway in the secretory protein chromogranin A. J. Cell Sci. 2002, 115:4827-4841.
79. Glombik M.M., et al. The disulfide-bonded loop of chromogranin B mediates membrane binding and directs sorting from the trans-Golgi network to secretory granules. EMBO J. 1999, 18:1059-1070.
80. Dhanvantari S., et al. Carboxypeptidase E, a prohormone sorting receptor, is anchored to secretory granules via a C-terminal transmembrane insertion. Biochemistry 2002, 41:52-60.
81. Arnaoutova I., et al. The prohormone processing enzyme PC3 is a lipid raft-associated transmembrane protein. Biochemistry 2003, 42:10445-10455.
82. Stettler H., et al. Proprotein convertase PC3 is not a transmembrane protein. Biochemistry 2005, 44:5339-5345.
83. Jain R.K., et al. In vitro aggregation of the regulated secretory protein chromogranin A. Biochem. J. 2002, 368:605-610.
84. Hosaka M., et al. Secretogranin III binds to cholesterol in the secretory granule membrane as an adapter for chromogranin A. J. Biol. Chem. 2004, 279:3627-3634.
85. Kuliawat R., et al. Proinsulin endoproteolysis confers enhanced targeting of processed insulin to the regulated secretory pathway. Mol. Biol. Cell 2000, 11:1959-1972.
86. Primo M.E., et al. Structure of the mature ectodomain of the human receptor-type protein-tyrosine phosphatase IA-2. J. Biol. Chem. 2008, 283:4674-4681.
87. Gross S., et al. Multimerization of the protein-tyrosine phosphatase (PTP)-like insulin-dependent diabetes mellitus autoantigens IA-2 and IA-2beta with receptor PTPs (RPTPs). Inhibition of RPTPalpha enzymatic activity. J. Biol. Chem. 2002, 277:48139-48145.
88. Trajkovski M., et al. Regulation of insulin granule turnover in pancreatic beta-cells by cleaved ICA512. J. Biol. Chem. 2008, 283:33719-33729.
89. Orci L., et al. Conversion of proinsulin to insulin occurs coordinately with acidification of maturing secretory vesicles. J. Cell Bio. 1986, 103:2273-2281.
90. Sun-Wada G., et al. The a3 isoform of V-ATPase regulates insulin secretion from pancreatic beta-cells. J. Cell Sci. 2006, 119:4531-4540.
91. Louagie E., et al. Role of furin in granular acidification in the endocrine pancreas: identification of the V-ATPase subunit Ac45 as a candidate substrate. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:12319-12324.
92. Barg S., et al. Priming of insulin granules for exocytosis by granular Cl(-) uptake and acidification. J. Cell Sci. 2001, 114:2145-2154.
93. Deriy L.V., et al. The granular chloride channel ClC-3 is permissive for insulin secretion. Cell Metab. 2009, 10:316-323.
94. Li D., et al. Suppression of sulfonylurea- and glucose-induced insulin secretion in vitro and in vivo in mice lacking the chloride transport protein ClC-3. Cell Metab. 2009, 10:309-315.
95. Yoo S.H., et al. Localization of three types of the inositol 1,4,5-trisphosphate receptor/Ca(2+) channel in the secretory granules and coupling with the Ca(2+) storage proteins chromogranins A and B. J. Biol. Chem. 2001, 276:45806-45812.
96. Thrower E.C., et al. Activation of the inositol 1,4,5-trisphosphate receptor by the calcium storage protein chromogranin A. J. Biol. Chem. 2002, 277:15801-15806.
97. Ravazzola M., et al. Inositol 1,4,5-trisphosphate receptor subtype 3 in pancreatic islet cell secretory granules revisited. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:2745-2748.
98. Mitchell K.J., et al. Dense core secretory vesicles revealed as a dynamic Ca(2+) store in neuroendocrine cells with a vesicle-associated membrane protein aequorin chimaera. J. Cell Biol. 2001, 155:41-51.
99. Mitchell K.J., et al. Ryanodine receptor type I and nicotinic acid adenine dinucleotide phosphate receptors mediate Ca2+ release from insulin-containing vesicles in living pancreatic beta-cells (MIN6). J. Biol. Chem. 2003, 278:11057-11064.
100. Barg S., et al. Fast exocytosis with few Ca(2+) channels in insulin-secreting mouse pancreatic B cells. Biophys. J. 2001, 81:3308-3323.
101. Hoppa M.B., et al. Chronic palmitate exposure inhibits insulin secretion by dissociation of Ca(2+) channels from secretory granules. Cell Metab. 2009, 10:455-465.
102. Collins S.C., et al. Progression of diet-induced diabetes in C57BL6J mice involves functional dissociation of Ca2(+) channels from secretory vesicles. Diabetes 2010, 59:1192-1201.
103. Geng X., et al. The insulin secretory granule is the major site of K(ATP) channels of the endocrine pancreas. Diabetes 2003, 52:767-776.
104. Varadi A., et al. Intracellular ATP-sensitive K+ channels in mouse pancreatic beta cells: against a role in organelle cation homeostasis. Diabetologia 2006, 49:1567-1577.
105. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2001, 2:107-117.
106. Matsumoto M., et al. Noc2 is essential in normal regulation of exocytosis in endocrine and exocrine cells. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:8313-8318.
107. Waselle L., et al. Involvement of the Rab27 binding protein Slac2c/MyRIP in insulin exocytosis. Mol. Biol. Cell 2003, 14:4103-4113.
108. Paulmann N., et al. Intracellular serotonin modulates insulin secretion from pancreatic beta-cells by protein serotonylation. PLoS Biol. 2009, 7:e1000229.
109. Shibasaki T., et al. Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19333-19338.
110. Ort T., et al. The receptor tyrosine phosphatase-like protein ICA512 binds the PDZ domains of beta2-syntrophin and nNOS in pancreatic beta-cells. Eur. J. Cell Biol. 2000, 79:621-630.
111. Mains R.E., et al. Kalirin, a multifunctional PAM COOH-terminal domain interactor protein, affects cytoskeletal organization and ACTH secretion from AtT-20 cells. J. Biol. Chem. 1999, 274:2929-2937.
112. Löbner K., et al. Different regulated expression of the tyrosine phosphatase-like proteins IA-2 and phogrin by glucose and insulin in pancreatic islets: relationship to development of insulin secretory responses in early life. Diabetes 2002, 51:2982-2988.
113. Trajkovski M., et al. Nuclear translocation of an ICA512 cytosolic fragment couples granule exocytosis and insulin expression in {beta}-cells. J. Cell Biol. 2004, 167:1063-1074.
114. Mziaut H., et al. Synergy of glucose and growth hormone signalling in islet cells through ICA512 and STAT5. Nat. Cell Biol. 2006, 8:435-445.
115. Mziaut H., et al. ICA512 signaling enhances pancreatic beta-cell proliferation by regulating cyclins D through STATs. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:674-679.
116. Torii S., et al. Gene silencing of phogrin unveils its essential role in glucose-responsive pancreatic beta-cell growth. Diabetes 2009, 58:682-692.
117. Konstantinova I., et al. EphA-Ephrin-A-mediated beta cell communication regulates insulin secretion from pancreatic islets. Cell 2007, 129:359-370.