Insulin secretion from beta cells in intact mouse islets is targeted towards the vasculature

Diabetologia

Volumn 57, Issue 8, 2014, Pages 1655-1663

  Low, Jiun T ^a   Zavortink, Michael ^a   Mitchell, Justin M ^a   Gan, Wan J ^a   Do, Oanh Hoang ^a   Schwiening, Christof J ^b   Gaisano, Herbert Y ^c   Thorn, Peter ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Beta cell; Exocytosis; Insulin; Islets; Secretion; Synapse; Vasculature

Indexed keywords

GLUCOSE; INSULIN; LIPRIN; PICCOLO PROTEIN; RAB2 INTERACTING MOLECULE; STRUCTURAL PROTEIN; SULFORHODAMINE B; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN 1A; UNCLASSIFIED DRUG; SNAP25 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; EXOCYTOSIS; IMMUNOFLUORESCENCE; INSULIN RELEASE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; POLARIZATION; PRIORITY JOURNAL; SYNAPSE; VASCULARIZATION; ANIMAL; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS);

ANIMALS; EXOCYTOSIS; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; MICE; SYNAPSES; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25;

EID: 84904768909     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-014-3252-6     Document Type: Article

References (50)

1. Bonner-Weir S (1988) Morphological evidence for pancreatic polarity of beta cell within islets of Langerhans. Diabetes 37:616-621
2. 2+ channels and insulin-containing secretory granules and its significance for the initiation of exocytosis in mouse pancreatic B cells. EMBO J 14:50-57
3. Paras CD, Qian WJ, Lakey JR, Tan WH, Kennedy RT (2000) Localized exocytosis detected by spatially resolved amperometry in single pancreatic beta-cells. Cell Biochem Biophys 33:227-240
4. Rutter GA, Loder MK, Ravier MA (2006) Rapid three-dimensional imaging of individual insulin release events by Nipkow disc confocal microscopy. Biochem Soc Trans 34:675-678 (Pubitemid 44796396)
5. Oberg-Welsh C (2001) Long-term culture in matrigel enhances the insulin secretion of fetal porcine islet-like cell clusters in vitro. Pancreas 22:157-163
6. Takahashi N, Kishimoto T, Nemoto T, Kadowaki T, Kasai H (2002) Fusion pore dynamics and insulin granule exocytosis in the pancreatic islet. Science 297:1349-1352 (Pubitemid 34913173)
7. Yang L, Ji W, Xue Y, Chen L (2013) Imaging beta-cell mass and function in situ and in vivo. J Mol Med 91:929-938
8. Yasuda T, Shibasaki T, Minami K et al (2010) RIM2 alpha determines docking and priming states in insulin granule exocytosis. Cell Metab 12:117-129
9. Takahashi N, Hatakeyama H, OkadoH, Noguchi J, Ohno M, KasaiH (2010) Snare conformational changes that prepare vesicles for exocytosis. Cell Metab 12:19-29
10. 2+ channel in insulin granule exocytosis. J Biol Chem 279:7956-7961
11. Suckow AT, Comoletti D, Waldrop MA et al (2008) Expression of neurexin, neuroligin, and their cytoplasmic binding partners in the pancreatic beta-cells and the involvement of neuroligin in insulin secretion. Endocrinology 149:6006-6017
12. Ohara-Imaizumi M, Ohtsuka T, Matsushima S et al (2005) 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 (Pubitemid 40962598)
13. Deguchi-Tawarada M, Inoue E, Takao-Rikitsu E, Inoue M, Ohtsuka T, Takai Y (2004) CAST2: identification and characterization of a protein structurally related to the presynaptic cytomatrix protein cast. Genes Cells 9:15-23 (Pubitemid 38180878)
14. Moser T, Neher E (1997) Rapid exocytosis in single chromaffin cells recorded from mouse adrenal slices. J Neurosci 17:2314-2323 (Pubitemid 27137398)
15. 2+ concentration triggering exocytosis in neuroendocrine cells. Proc Natl Acad Sci U S A 91:12765 -12769
16. Gopel S, ZhangQ, Eliasson L et al (2004) Capacitance measurements of exocytosis in mouse pancreatic alpha-, beta- and delta-cells within intact islets of langerhans. J Physiol Lond 556:711-726 (Pubitemid 38660309)
17. Olofsson CS, Collins S, Bengtsson M et al (2007) Long-term exposure to glucose and lipids inhibits glucose-induced insulin secretion downstream of granule fusion with plasma membrane. Diabetes 56:1888-1897 (Pubitemid 47025450)
18. 2+ channels from secretory granules. Cell Metab 10:455-465
19. Huang YC, Rupnik M, Gaisano HY (2011) Unperturbed islet alphacell function examined in mouse pancreas tissue slices. J Physiol Lond 589:395-408
20. Hoppa MB, Jones E, Karanauskaite J et al (2012) Multivesicular exocytosis in rat pancreatic beta cells. Diabetologia 55:1001-1012
21. Low JT, Mitchell JM, Do OH et al (2013) Glucose principally regulates insulin secretion in islets by controlling the numbers of granule fusion events per cell. Diabetologia 56:2629-2637
22. Peters BP, Goldstein IJ (1979) The use of fluorescein-conjugated Bandeiraea simplicifolia B4-isolectin as a histochemical reagent for the detection of alpha-D-galactopyranosyl groups. Their occurrence in basement membranes. Exp Cell Res 120:321-334 (Pubitemid 9216488)
23. Nikolova G, Jabs N, Konstantinova I et al (2006) The vascular basement membrane: a niche for insulin gene expression and beta cell proliferation. Dev Cell 10:397-405
24. Lukinius A, Jansson L, Korsgren O (1995) Ultrastructural evidence for blood microvessels devoid of an endothelial-cell lining in transplanted pancreatic-islets. Am J Physiol 146:429-435
25. Meneghel-Rozzo T, Rozzo A, Poppi L, Rupnik M (2004) In vivo and in vitro development of mouse pancreatic beta-cells in organotypic slices. Cell Tissue Res 316:295-303 (Pubitemid 38823996)
26. Sato Y, Ito T, Udaka N et al (1996) Immunohistochemical localization of facilitated-diffusion glucose transporters in rat pancreatic islets. Tissue Cell 28:637-643 (Pubitemid 27011027)
27. Takahashi N, Hatakeyama H, Kasai H (2004) Sequential insulin exocytosis and redistribution of snap25 analyzed with two-photon imaging. Diabetologia 47:205
28. Nagamatsu S, Fujiwara T, Nakamichi Yet al (1996) 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
29. Granot Z, Swisa A, Magenheim J et al (2009) Lkb1 regulates pancreatic beta cell size, polarity, and function. Cell Metab 10:296-308
30. Nyqvist D, Speier S, Rodriguez-Diaz R et al (2011) Donor islet endothelial cells in pancreatic islet revascularization. Diabetes 60:2571-2577
31. 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
32. 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
33. Kwan EP, Xie L, Sheu L et al (2006) Munc13-1 deficiency reduces insulin secretion and causes abnormal glucose tolerance.Diabetes 55:1421-1429 (Pubitemid 44195382)
34. Vikman J, Svensson H, Huang YC et al (2009) Truncation of SNAP-25 reduces the stimulatory action of cAMP on rapid exocytosis in insulin-secreting cells. Am J Physiol 297:E452-E461
35. 2+ channel null mice. EMBO J 22:3844-3854
36. Gaisano HY, Ghai M, Malkus PN et al (1996) Distinct cellular locations of the syntaxin family of proteins in rat pancreatic acinar cells. Mol Biol Cell 7:2019-2027 (Pubitemid 26415007)
37. Behrendorff N, Dolai S, Hong WJ, Gaisano HY, Thorn P (2011) Vesicle-associated membrane protein 8 (VAMP8) is a SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor) selectively required for sequential granule-to-granule fusion. J Biol Chem 286:29627-29634
38. Jacobsson G, Bean AJ, Scheller RH et al (1994) Identification of synaptic proteins and their isoform messenger-RNAs in compartments of pancreatic endocrine-cells. Proc Natl Acad Sci U S A 91:12487-12491
39. Ohara-Imaizumi M, Fujiwara T, Nakamichi Y et al (2007) Imaging analysis reveals mechanistic differences between first- and secondphase insulin exocytosis. J Cell Biol 177:695-705 (Pubitemid 46799840)
40. Lammert E, Gu GQ, McLaughlin M et al (2003) Role of VEGF-A in vascularization of pancreatic islets. Curr Biol 13:1070-1074 (Pubitemid 36726045)
41. Sudhof TC (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455:903-911
42. Bottos A, Destro E, Rissone A et al (2009) The synaptic proteins neurexins and neuroligins are widely expressed in the vascular system and contribute to its functions. Proc Natl Acad Sci U S A 106:20782-20787
43. + channels in pancreatic beta-cells through a phosphatidylinositol 3-kinase-dependent pathway. Diabetes 50:2192-2198
44. Wang MH, Li JX, Lim GE, Johnson JD (2013) Is dynamic autocrine insulin signaling possible? A mathematical model predicts picomolar concentrations of extracellular monomeric insulin within human pancreatic islets. PLoS One 8(6):e64860
45. Cabrera O, Berman DM, Kenyon NS, Ricordi C, Berggrern PO, Caicedo A (2006) The unique cytoarchitecture of human pancreatic islets has implications for islet cell function. Proc Natl Acad Sci U S A 103:2334-2339 (Pubitemid 43271670)
46. Wendt A, Birnir B, Buschard K et al (2004) Glucose inhibition of glucagon secretion from rat alpha-cells is mediated by GABA released from neighboring beta-cells. Diabetes 53:1038-1045 (Pubitemid 38436616)
47. Franklin I, Gromada J, Gjinovci A, Theander S, Wollheim CB (2005) Beta-cell secretory products activate alpha-cell ATP-dependent potassium channels to inhibit glucagon release. Diabetes 54:1808-1815 (Pubitemid 40770771)
48. Ravier MA, Rutter GA (2005) Glucose or insulin, but not zinc ions, inhibit glucagon secretion from mouse pancreatic alpha-cells. Diabetes 54:1789-1797 (Pubitemid 40770769)
49. Talchai C, Xuan S, Lin HV, Sussel L, Accili D (2012) Pancreatic beta cell dedifferentiation as amechanism of diabetic beta cell failure. Cell 150:1223-1234
50. Li X, Zhang L, Meshinchi S et al (2006) Islet microvasculature in islet hyperplasia and failure in a model of type 2 diabetes. Diabetes 55:2965-2973 (Pubitemid 44929429)