Intra-islet insulin suppresses glucagon release via GABA-GABAA receptor system

Cell Metabolism

Volumn 3, Issue 1, 2006, Pages 47-58

  Xu, Elaine ^a,b   Kumar, Mohan ^a,b   Zhang, Yi ^a,b   Ju, William ^a,b   Obata, Toshiyuki ^c   Zhang, Nina ^b   Liu, Shiying ^b   Wendt, Anna ^d   Deng, Shaoping ^e   Ebina, Yousuke ^c   Wheeler, Michael B ^a   Braun, Matthias ^d,f   Wang, Qinghua ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

^d LUND UNIVERSITY   (Sweden)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cellbio; Humdisease; Signaling

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; GLUCAGON; GLUCOSE; INSULIN; PROTEIN KINASE B;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL SECRETION; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME LINKED IMMUNOSORBENT ASSAY; GLUCAGON RELEASE; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IN VIVO STUDY; INHIBITION KINETICS; INSULIN RELEASE; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET ALPHA CELL; PATHOPHYSIOLOGY; POLARIZATION; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; FEMALE; GLUCAGON; GLUCAGON-SECRETING CELLS; GUINEA PIGS; HUMANS; INSULIN; INSULIN RESISTANCE; ISLETS OF LANGERHANS; MALE; MODELS, BIOLOGICAL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A;

ANIMALIA;

EID: 33645051453     PISSN: 15504131     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cmet.2005.11.015     Document Type: Article

References (60)

1. S. Banarer V.P. McGregor P.E. Cryer Intraislet hyperinsulinemia prevents the glucagon response to hypoglycemia despite an intact autonomic response Diabetes 51 2002 958-965
2. S. Barg J. Galvanovskis S.O. Gopel P. Rorsman L. Eliasson Tight coupling between electrical activity and exocytosis in mouse glucagon-secreting alpha-cells Diabetes 49 2000 1500-1510
3. R.N. Bergman D.T. Finegood S.E. Kahn The evolution of beta-cell dysfunction and insulin resistance in type 2 diabetes Eur. J. Clin. Invest. 32 Suppl. 3 2002 35-45
4. K. Bokvist H.L. Olsen M. Hoy C.F. Gotfredsen W.F. Holmes K. Buschard P. Rorsman J. Gromada Characterisation of sulphonylurea and ATP-regulated K+ channels in rat pancreatic A-cells Pflugers Arch. 438 1999 428-436
5. S. Bonner-Weir L. Orci New perspectives on the microvasculature of the islets of Langerhans in the rat Diabetes 31 1982 883-889
6. N.J. Brandon P. Delmas J.T. Kittler B.J. McDonald W. Sieghart D.A. Brown T.G. Smart S.J. Moss GABAA receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway J. Biol. Chem. 275 2000 38856-38862
7. N.J. Brandon J.N. Jovanovic T.G. Smart S.J. Moss Receptor for activated C kinase-1 facilitates protein kinase C-dependent phosphorylation and functional modulation of GABA(A) receptors with the activation of G-protein-coupled receptors J. Neurosci. 22 2002 6353-6361
8. M. Braun A. Wendt B. Birnir J. Broman L. Eliasson J. Galvanovskis J. Gromada H. Mulder P. Rorsman Regulated exocytosis of GABA-containing synaptic-like microvesicles in pancreatic beta-cells J. Gen. Physiol. 123 2004 191-204
9. K. Cejvan D.H. Coy S. Efendic Intra-islet somatostatin regulates glucagon release via type 2 somatostatin receptors in rats Diabetes 52 2003 1176-1181
10. C.B. Chan R.M. MacPhail K. Mitton Evidence for defective glucose sensing by islets of fa/fa obese Zucker rats Can. J. Physiol. Pharmacol. 71 1993 34-39
11. M. Chebib G.A. Johnston The 'ABC' of GABA receptors: A brief review Clin. Exp. Pharmacol. Physiol. 26 1999 937-940
12. S.D. Chessler W.T. Simonson I.R. Sweet L.P. Hammerle Expression of the vesicular inhibitory amino acid transporter in pancreatic islet cells: distribution of the transporter within rat islets Diabetes 51 2002 1763-1771
13. H. Cinar E.M. Barnes Jr. Clathrin-independent endocytosis of GABA(A) receptors in HEK 293 cells Biochemistry 40 2001 14030-14036
14. C.N. Connolly J.T. Kittler P. Thomas J.M. Uren N.J. Brandon T.G. Smart S.J. Moss Cell surface stability of gamma-aminobutyric acid type A receptors. Dependence on protein kinase C activity and subunit composition J. Biol. Chem. 274 1999 36565-36572
15. P.E. Cryer Banting Lecture. Hypoglycemia: The limiting factor in the management of IDDM Diabetes 43 1994 1378-1389
16. D.J. Drucker R. Campos R. Reynolds K. Stobie P.L. Brubaker The rat glucagon gene is regulated by a protein kinase A-dependent pathway in pancreatic islet cells Endocrinology 128 1991 394-400
17. W. El Kholy P.E. Macdonald J.H. Lin J. Wang J.M. Fox P.E. Light Q. Wang R.G. Tsushima M.B. Wheeler The phosphatidylinositol 3-kinase inhibitor LY294002 potently blocks K(V) currents via a direct mechanism FASEB J. 17 2003 720-722
18. E. Ferrannini Insulin resistance versus insulin deficiency in non-insulin-dependent diabetes mellitus: Problems and prospects Endocr. Rev. 19 1998 477-490
19. I. Franklin J. Gromada A. Gjinovci S. Theander C.B. Wollheim Beta-cell secretory products activate alpha-cell ATP-dependent potassium channels to inhibit glucagon release Diabetes 54 2005 1808-1815
20. R. Gammelsaeter M. Froyland C. Aragon N.C. Danbolt D. Fortin J. Storm-Mathisen S. Davanger V. Gundersen Glycine, GABA and their transporters in pancreatic islets of Langerhans: Evidence for a paracrine transmitter interplay J. Cell Sci. 117 2004 3749-3758
21. J.C. Gerber GABA in peripheral tissue: Presence and action in pancreatic function. Hare T.A. Brain Res. Bull. 5 Suppl. 2 1980 341-346
22. P. Gilon G. Bertrand M.M. Loubatieres-Mariani C. Remacle J.C. Henquin The influence of gamma-aminobutyric acid on hormone release by the mouse and rat endocrine pancreas Endocrinology 129 1991 2521-2529
23. S. Göpel Q. Zhang L. Eliasson X.S. Ma J. Galvanovskis T. Kanno A. Salehi P. Rorsman Capacitance measurements of exocytosis in mouse pancreatic alpha-, beta- and delta-cells within intact islets of Langerhans J. Physiol. 556 2004 711-726
24. C.J. Greenbaum P.J. Havel G.J. Taborsky Jr. L.J. Klaff Intra-islet insulin permits glucose to directly suppress pancreatic A cell function J. Clin. Invest. 88 1991 767-773
25. T.G. Hales R.F. Tyndale Few cell lines with GABAA mRNAs have functional receptors J. Neurosci. 14 1994 5429-5436
26. T. Hamaguchi H. Fukushima M. Uehara S. Wada T. Shirotani H. Kishikawa K. Ichinose K. Yamaguchi M. Shichiri Abnormal glucagon response to arginine and its normalization in obese hyperinsulinaemic patients with glucose intolerance: Importance of insulin action on pancreatic alpha cells Diabetologia 34 1991 801-806
27. M. Hayashi H. Yamada S. Uehara R. Morimoto A. Muroyama S. Yatsushiro J. Takeda A. Yamamoto Y. Moriyama Secretory granule-mediated co-secretion of L-glutamate and glucagon triggers glutamatergic signal transmission in islets of Langerhans J. Biol. Chem. 278 2003 1966-1974
28. K.M. Hope P.O. Tran H. Zhou E. Oseid E. Leroy R.P. Robertson Regulation of alpha-cell function by the beta-cell in isolated human and rat islets deprived of glucose: The "switch-off" hypothesis Diabetes 53 2004 1488-1495
29. C. Huang R. Somwar N. Patel W. Niu D. Torok A. Klip Sustained exposure of L6 myotubes to high glucose and insulin decreases insulin-stimulated GLUT4 translocation but upregulates GLUT4 activity Diabetes 51 2002 2090-2098
30. H. Ishihara P. Maechler A. Gjinovci P.L. Herrera C.B. Wollheim Islet beta-cell secretion determines glucagon release from neighbouring alpha-cells Nat. Cell Biol. 5 2003 330-335
31. K. Kaneko T. Shirotani E. Araki K. Matsumoto T. Taguchi H. Motoshima K. Yoshizato H. Kishikawa M. Shichiri Insulin inhibits glucagon secretion by the activation of PI3-kinase in In-R1-G9 cells Diabetes Res. Clin. Pract. 44 1999 83-92
32. T. Katome T. Obata R. Matsushima N. Masuyama L.C. Cantley Y. Gotoh K. Kishi H. Shiota Y. Ebina Use of RNA interference-mediated gene silencing and adenoviral overexpression to elucidate the roles of AKT/protein kinase B isoforms in insulin actions J. Biol. Chem. 278 2003 28312-28323
33. J.K. Kim J.J. Fillmore M.J. Sunshine B. Albrecht T. Higashimori D.W. Kim Z.X. Liu T.J. Soos G.W. Cline W.R. O'Brien et. al. PKC-theta knockout mice are protected from fat-induced insulin resistance J. Clin. Invest. 114 2004 823-827
34. K. Kisanuki H. Kishikawa E. Araki T. Shirotani M. Uehara S. Isami S. Ura H. Jinnouchi N. Miyamura M. Shichiri Expression of insulin receptor on clonal pancreatic alpha cells and its possible role for insulin-stimulated negative regulation of glucagon secretion Diabetologia 38 1995 422-429
35. J.T. Kittler S.J. Moss Modulation of GABAA receptor activity by phosphorylation and receptor trafficking: Implications for the efficacy of synaptic inhibition Curr. Opin. Neurobiol. 13 2003 341-347
36. B.J. Krishek X. Xie C. Blackstone R.L. Huganir S.J. Moss T.G. Smart Regulation of GABAA receptor function by protein kinase C phosphorylation Neuron 12 1994 1081-1095
37. T.K. Lam H. Yoshii C.A. Haber E. Bogdanovic L. Lam I.G. Fantus A. Giacca Free fatty acid-induced hepatic insulin resistance: A potential role for protein kinase C-delta Am. J. Physiol. Endocrinol. Metab. 283 2002 E682-E691
38. B. Lu D. Ennis R. Lai E. Bogdanovic R. Nikolov L. Salamon C. Fantus H. Le Tien I.G. Fantus Enhanced sensitivity of insulin-resistant adipocytes to vanadate is associated with oxidative stress and decreased reduction of vanadate (+5) to vanadyl (+4) J. Biol. Chem. 276 2001 35589-35598
39. B. Luscher C.A. Keller Regulation of GABAA receptor trafficking, channel activity, and functional plasticity of inhibitory synapses Pharmacol. Ther. 102 2004 195-221
40. H. Maruyama A. Hisatomi L. Orci G.M. Grodsky R.H. Unger Insulin within islets is a physiologic glucagon release inhibitor J. Clin. Invest. 74 1984 2296-2299
41. B.J. McDonald S.J. Moss Conserved phosphorylation of the intracellular domains of GABA(A) receptor beta2 and beta3 subunits by cAMP-dependent protein kinase, cGMP-dependent protein kinase protein kinase C and Ca2+/ calmodulin type II-dependent protein kinase Neuropharmacology 36 1997 1377-1385
42. I. Mody R.A. Pearce Diversity of inhibitory neurotransmission through GABA(A) receptors Trends Neurosci. 27 2004 569-575
43. H.K. Muller M. Kellerer B. Ermel A. Muhlhofer B. Obermaier-Kusser B. Vogt H.U. Haring Prevention by protein kinase C inhibitors of glucose-induced insulin-receptor tyrosine kinase resistance in rat fat cells Diabetes 40 1991 1440-1448
44. W.A. Muller G.R. Faloona R.H. Unger The effect of experimental insulin deficiency on glucagon secretion J. Clin. Invest. 50 1971 1992-1999
45. K. Nakajima K. Yamauchi S. Shigematsu S. Ikeo M. Komatsu T. Aizawa K. Hashizume Selective attenuation of metabolic branch of insulin receptor down-signaling by high glucose in a hepatoma cell line, HepG2 cells J. Biol. Chem. 275 2000 20880-20886
46. D.G. Pipeleers F.C. Schuit C.F. Van Schravendijk W.M. Van Interplay of nutrients and hormones in the regulation of glucagon release Endocrinology 117 1985 817-823
47. M.A. Ravier G.A. Rutter Glucose or insulin, but not zinc ions, inhibit glucagon secretion from mouse pancreatic {alpha}-cells Diabetes 54 2005 1789-1797
48. A. Reetz M. Solimena M. Matteoli F. Folli K. Takei P. De Camilli GABA and pancreatic beta-cells: Colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion EMBO J. 10 1991 1275-1284
49. P. Ronner F.M. Matschinsky T.L. Hang A.J. Epstein C. Buettger Sulfonylurea-binding sites and ATP-sensitive K+ channels in alpha-TC glucagonoma and beta-TC insulinoma cells Diabetes 42 1993 1760-1772
50. P. Rorsman P.O. Berggren K. Bokvist H. Ericson H. Mohler C.G. Ostenson P.A. Smith Glucose-inhibition of glucagon secretion involves activation of GABAA-receptor chloride channels Nature 341 1989 233-236
51. A. Smismans F. Schuit D. Pipeleers Nutrient regulation of gamma-aminobutyric acid release from islet beta cells Diabetologia 40 1997 1411-1415
52. R.L. Sorenson D.G. Garry T.C. Brelje Structural and functional considerations of GABA in islets of Langerhans. Beta-cells and nerves Diabetes 40 1991 1365-1374
53. A. Starke T. Imamura R.H. Unger Relationship of glucagon suppression by insulin and somatostatin to the ambient glucose concentration J. Clin. Invest. 79 1987 20-24
54. H. Taniguchi Y. Okada H. Seguchi C. Shimada M. Seki A. Tsutou S. Baba High concentration of gamma-aminobutyric acid in pancreatic beta cells Diabetes 28 1979 629-633
55. Q. Wang Z. Khayat K. Kishi Y. Ebina A. Klip GLUT4 translocation by insulin in intact muscle cells: Detection by a fast and quantitative assay FEBS Lett. 427 1998 193-197
56. Q. Wang L. Liu L. Pei W. Ju G. Ahmadian J. Lu Y. Wang F. Liu Y.T. Wang Control of synaptic strength, a novel function of Akt Neuron 38 2003 915-928
57. A. Wendt B. Birnir K. Buschard J. Gromada A. Salehi S. Sewing P. Rorsman M. Braun Glucose inhibition of glucagon secretion from rat alpha-cells is mediated by GABA released from neighboring beta-cells Diabetes 53 2004 1038-1045
58. F. Winnock Z. Ling R. De Proft S. Dejonghe F. Schuit F. Gorus D. Pipeleers Correlation between GABA release from rat islet beta-cells and their metabolic state Am. J. Physiol. Endocrinol. Metab. 282 2002 E937-E942
59. H. Yamada M. Otsuka M. Hayashi S. Nakatsuka K. Hamaguchi A. Yamamoto Y. Moriyama Ca2+-dependent exocytosis of L-glutamate by alphaTC6, clonal mouse pancreatic alpha-cells Diabetes 50 2001 1012-1020
60. H. Zhou P.O. Tran S. Yang T. Zhang E. Leroy E. Oseid R.P. Robertson Regulation of alpha-cell function by the beta-cell during hypoglycemia in Wistar rats: The "switch-off" hypothesis Diabetes 53 2004 1482-1487