Regulated Exocytosis of GABA-containing Synaptic-like Microvesicles in Pancreatic β-cells

Journal of General Physiology

Volumn 123, Issue 3, 2004, Pages 191-204

  Braun, Matthias ^a   Wendt, Anna ^a   Birnir, Bryndis ^a   Broman, Jonas ^a   Eliasson, Lena ^a   Galvanovskis, Juris ^a   Gromada, Jesper ^b   Mulder, Hindrik ^a   Rorsman, Patrik ^a  

^a LUND UNIVERSITY   (Sweden)

^b LILLY DEUTSCHLAND GMBH   (Germany)

Author keywords

GABA; GAD65; Pancreatic islets; Paracrine communication; SLMV

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ADENOVIRUS VECTOR; CHLORIDE CHANNEL; INSULIN; VOLTAGE GATED CALCIUM CHANNEL;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL ULTRASTRUCTURE; CHLORIDE CURRENT; CONTROLLED STUDY; DEPOLARIZATION; ELECTRIC CAPACITANCE; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; EXOCYTOSIS; GABA A RECEPTOR CHLORIDE CHANNEL; INSULIN RELEASE; KINETICS; MATHEMATICAL ANALYSIS; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; NONHUMAN; PANCREAS ISLET BETA CELL; PARACRINE SIGNALING; PROTEIN EXPRESSION; QUANTITATIVE ASSAY; RAT; RECEPTOR DENSITY; SYNAPSE VESICLE; SYNAPTIC LIKE MICROVESICLE;

ANIMALS; CALCIUM SIGNALING; DOSE-RESPONSE RELATIONSHIP, DRUG; EXOCYTOSIS; GAMMA-AMINOBUTYRIC ACID; HUMANS; ISLETS OF LANGERHANS; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; RECEPTORS, GABA-A; SYNAPTIC VESICLES;

EID: 1442358665     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.200308966     Document Type: Article

References (57)

1. Ahnert-Hilger, G., and B. Wiedenmann. 1992. The amphicrine pancreatic cell line, AR42J, secretes GABA and amylase by separate regulated pathways. FEBS Lett. 314:41-44.
2. Albillos, A., G. Dernick, H. Horstmann, W. Almers, G. Alvarez de Toledo, and M. Lindau. 1997. The exocytotic event in chromaffin cells revealed by patch amperometry. Nature. 389:509-512.
3. Amatore, C., Y. Bouret, E.R. Travis, and R.M. Wightman. 2000. Interplay between membrane dynamics, diffusion and swelling pressure governs individual vesicular exocytotic events during release of adrenaline by chromaffin cells. Biochimie. 82:481-496.
4. Ämmälä, C., F.M. Ashcroft, and P. Rorsman. 1993. Calcium-independent potentiation of insulin release by cyclic AMP in single β-cells. Nature. 363:356-358.
5. Antunes, C.M., A.P. Salgado, L.M. Rosario, and R.M. Santos. 2000. Differential patterns of glucose-induced electrical activity and intracellular calcium responses in single mouse and rat pancreatic islets. Diabetes. 49:2028-2038.
6. Bauerfeind, R., A. Regnier-Vigouroux, T. Flatmark, and W.B. Huttner. 1993. Selective storage of acetylcholine, but not catecholamines, in neuroendocrine synaptic-like microvesicles of early endosomal origin. Neuron. 11:105-121.
7. Becker, T.C., R.J. Noel, W.S. Coats, A.M. Gomez-Foix, T. Alam, R.D. Gerard, and C.B. Newgard. 1994. Use of recombinant adenovirus for metabolic engineering of mammalian cells. Methods Cell Biol. 43:161-189.
8. Birnir, B., M.L. Tierney, N.P. Pillai, G.B. Cox, and P.W. Gage. 1995. Rapid desensitization of alpha 1 beta 1 GABA A receptors expressed in Sf9 cells under optimized conditions. J. Membr. Biol. 148:193-202.
9. B receptors contribute to the modulation of glucose-stimulated insulin secretion in pancreatic β-cells. Diabetologia. 45:242-252.
10. Bruns, D., D. Riedel, J. Klingauf, and R. Jahn. 2000. Quantal release of serotonin. Neuron. 28:205-220.
11. Bustamante, J., M.V. Lobo, F.J. Alonso, N.T. Mukala, E. Gine, J.M. Solis, J. Tamarit-Rodriguez, and R. Martin Del Rio. 2001. An osmotic-sensitive taurine pool is localized in rat pancreatic islet cells containing glucagon and somatostatin. Am. J. Physiol. Endocrinol. Metab. 281:E1275-E1285.
12. Dean, P.M. 1973. Ultrastructural morphometry of the pancreatic β-cell. Diabetologia. 9:115-119.
13. Edwards, F.A., A. Konnerth, and B. Sakmann. 1990. Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study. J. Physiol. 430:213-249.
14. Eliasson, L., P. Proks, C. Ämmälä, F.M. Ashcroft, K. Bokvist, E. Renström, P. Rorsman, and P.A. Smith. 1996. Endocytosis of secretory granules in mouse pancreatic β-cells evoked by transient elevation of cytosolic calcium. J. Physiol. 493:755-767.
15. Garry, D.J., N.M. Appel, M.G. Garry, and R.L. Sorenson. 1988. Cellular and subcellular immunolocalization of L-glutamate decarboxylase in rat pancreatic islets. J. Histochem. Cytochem. 36:573-580.
16. Gaskins, H.R., M.E. Baldeon, L. Selassie, and J.L. Beverly. 1995. Glucose modulates gamma-aminobutyric acid release from the pancreatic BTC6 cell line. J. Biol. Chem. 270:30286-30289.
17. Göpel, S., T. Kanno, S. Barg, J. Galvanovskis, and P. Rorsman. 1999. Voltage-gated and resting membrane currents recorded from β-cells in intact mouse pancreatic islets. J. Physiol. 521:717-728.
18. Hayashi, M., H. Yamada, S. Uehara, R. Morimoto, A. Muroyama, S. Yatsushiro, J. Takeda, A. Yamamoto, and Y. Moriyama. 2003. Secretory granule-mediated co-secretion of L-glutamate and glucagon triggers glutamatergic signal transmission in islets of Langerhans. J. Biol. Chem. 278:1966-1974.
19. 2+ channels in rat pancreatic β-cells identified with the reverse hemolytic plaque assay. J. Gen. Physiol. 91:617-639.
20. Hollins, B., and S.R. Ikeda. 1997. Heterologous expression of a P2x-purinoceptor in rat chromaffin cells detects vesicular ATP release. J. Neurophysiol. 78:3069-3076.
21. Inagaki, N., H. Kuromi, T. Gonoi, Y. Okamoto, H. Ishida, Y. Seino, T. Kaneko, T. Iwanaga, and S. Seino. 1995. Expression and role of ionotropic glutamate receptors in pancreatic islet cells. FASEB J. 9:686-691.
22. Ishihara, H., P. Maechler, A. Gjinovci, P.L. Herrera, and C.B. Wollheim. 2003. Islet β-cell secretion determines glucagon release from neighbouring alpha-cells. Nat. Cell Biol. 5:330-335.
23. Jayaraman, V., S. Thiran, and G.P. Hess. 1999. How fast does the g-aminobutyric acid receptor channel open? Kinetic investigations in the microsecond time region using a laser-pulse photolysis technique. Biochemistry. 38:11372-11378.
24. 2-cells by mobilizing calcium incorporated in response to glucose. Cell Calcium. 10:205-211.
25. Karlsson, F.A., C. Berne, E. Bjork, M. Kullin, Z. Li, J.Y. Ma, A. Scholin, and L. Zhao. 2000. β-cell activity and destruction in type 1 diabetes. Ups. J. Med. Sci. 105:85-95.
26. Krentz, A.J., and M. Nattrass. 1997. Acute metabolic complications of diabetes mellitus: diabetic ketoacidosis, hyperosmolar non-ketotic syndrome and lactic acidosis. In Textbook of Diabetes. Vol. 2. J. Pickup and G. Williams, editors. Blackwell Science, Oxford. 39.31-39.23.
27. Michalik, M., and M. Erecinska. 1992. GABA in pancreatic islets: metabolism and function. Biochem. Pharmacol. 44:1-9.
28. Moriyama, Y., M. Hayashi, H. Yamada, S. Yatsushiro, S. Ishio, and A. Yamamoto. 2000. Synaptic-like microvesicles, synaptic vesicle counterparts in endocrine cells, are involved in a novel regulatory mechanism for the synthesis and secretion of hormones. J. Exp. Biol. 203:117-125.
29. Moser, T., and E. Neher. 1997. Estimation of mean exocytic vesicle capacitance in mouse adrenal chromaffin cells. Proc. Natl. Acad. Sci. USA. 94:6735-6740.
30. Nagamatsu, S., T. Watanabe, Y. Nakamichi, C. Yamamura, K. Tsuzuki, and S. Matsushima. 1999. α-Soluble N-ethylmaleimide-sensitive factor attachment protein is expressed in pancreatic β-cells and functions in insulin but not γ-aminobutyric acid secretion. J. Biol. Chem. 274:8053-8060.
31. Neher, E. 1992. Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol. 207:123-131.
32. Nishiki, T., Y. Shoji-Kasai, M. Sekiguchi, S. Iwasaki, K. Kumakura, and M. Takahashi. 1997. Comparison of exocytotic mechanisms between acetylcholine- and catecholamine-containing vesicles in rat pheochromocytoma cells. Biochem. Biophys. Res. Commun. 239:57-62.
33. Olofsson, C.S., S.O. Göpel, S. Barg, J. Galvanovskis, X. Ma, A. Salehi, P. Rorsman, and L. Eliasson. 2002. Fast insulin secretion reflects exocytosis of docked granules in mouse pancreatic β-cells. Pflugers Arch. 444:43-51.
34. Pipeleers, D.G., EC. Schuit, C.F. Van Schravendijk, and M. Van de Winkel. 1985. Interplay of nutrients and hormones in the regulation of glucagon release. Endocrinology. 117:817-823.
35. Plattner, H., A.R. Artajelo, and E. Neher. 1997. Ultrastuctural organization of bovine chromaffin cell cortex-analysis by cryofixation and morphometry of aspects pertinent to exocytosis. J. Cell Biol. 139:1709-1717.
36. Reetz, A., M. Solimena, M. Matteoli, F. Folli, K. Takei, and P. De Camilli. 1991. GABA and pancreatic β-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion. EMBO J. 10:1275-1284.
37. Renström, E., L. Eliasson, K. Bokvist, and P. Rorsman. 1996. Cooling inhibits exocytosis in single mouse pancreatic β-cells by suppression of granule mobilization. J. Physiol. 494:41-52.
38. Robbins, M.S., L.H. Grouse, R.L. Sorenson, and R.P. Elde. 1981. Effect of muscimol on glucose-stimulated somatostatin and insulin release from the isolated, perfused rat pancreas. Diabetes. 30:168-171.
39. A-receptor chloride channels. Nature. 341:233-236.
40. Rorsman, P., L. Eliasson, E. Renström, J. Gromada, S. Barg, and S. Göpel. 2000. The cell physiology of biphasic insulin secretion. News Physiol. Sci. 15:72-77.
41. Schmidli, R.S., P.G. Colman, E. Bonifacio, G.F. Bottazzo, and L.C. Harrison. 1994. High level of concordance between assays for glutamic acid decarboxylase antibodies. The first international glutamic acid decarboxylase antibody workshop. Diabetes. 43:1005-1009.
42. Shah, P., A. Vella, A. Basu, R. Basu, W.F. Schwenk, and R.A. Rizza. 2000. Lack of suppression of glucagon contributes to postprandial hyperglycemia in subjects with type 2 diabetes mellitus. J. Clin. Endocrinol. Metab. 85:4053-4059.
43. Shi, Y., J. Kanaani, V. Menard-Rose, Y.H. Ma, P.Y. Chang, D. Hanahan, A. Tobin, G. Grodsky, and S. Baekkeskov. 2000. Increased expression of GAD65 and GABA in pancreatic β-cells impairs first-phase insulin secretion. Am. J. Physiol. Endocrinol. Metab. 279:E684-E694.
44. Smismans, A., F. Schuit, and D. Pipeleers. 1997. Nutrient regulation of g-aminobutyric acid release from islet β-cells. Diabetologia. 40:1411-1415.
45. Sorenson, R.L., D.G. Garry, and T.C. Brelje. 1991. Structural and functional considerations of GABA in islets of Langerhans. β-cells and nerves. Diabetes. 40:1365-1374.
46. 2+ affinities. EMBO J. 21:270-280.
47. Takahashi, N., T. Kadowaki, Y. Yazaki, Y. Miyashita, and H. Kasai. 1997. Multiple exocytotic pathways in pancreatic β-cells. J. Cell Biol. 138:55-64.
48. Taniguchi, H., Y. Okada, C. Shimada, and S. Baba. 1977. GABA in pancreatic islets. Arch. Histol. Jpn. 40:87-97.
49. Thomas-Reetz, A., J.W. Hell, M.J. During, C. Walch-Solimena, R. Jahn, and P. De Camilli. 1993. A g-aminobutyric acid transporter driven by a proton pump is present in synaptic-like microvesicles of pancreatic β-cells. Proc. Natl. Acad. Sci. USA. 90:5317-5321.
50. Thomas-Reetz, A.C., and P. De Camilli. 1994. A role for synaptic vesicles in non-neuronal cells: clues from pancreatic β-cells and from chromaffin cells. FASEB J. 8:209-216.
51. Tillakaratne, N.J., L. Medina-Kauwe, and K.M. Gibson. 1995. g-aminobutyric acid (GABA) metabolism in mammalian neural and nonneural tissues. Comp. Biochem. Physiol. A. Physiol. 112:247-263.
52. Travis, E.R., and R.M. Wightman. 1998. Spatio-temporal resolution of exocytosis from individual cells. Annu. Rev. Biophys. Biomol. Struct. 27:77-103.
53. A receptors in neuroendocrine gastropancreatic cells. Pflugers Arch. 430:381-388.
54. Whim, M.D., and G.W. Moss. 2001. A novel technique that measures peptide secretion on a millisecond timescale reveals rapid changes in release. Neuron. 30:37-50.
55. Winnock, F., Z. Ling, R. De Proft, S. Dejonghe, F. Schuit, F. Gorus, and D. Pipeleers. 2002. Correlation between GABA release from rat islet β-cells and their metabolic state. Am. J. Physiol. Endocrinol. Metab. 282:E937-E942.
56. A receptor subtype mRNA in human pancreatic tissue. FEBS Lett. 346:257-262.
57. Yoon, J.W., C.S. Yoon, H.W. Lim, Q.Q. Huang, Y. Kang, K.H. Pyun, K. Hirasawa, R.S. Sherwin, and H.S. Jun. 1999. Control of autoimmune diabetes in NOD mice by GAD expression or suppression in β-cells. Science. 284:1183-1187.