Glucose-dependent regulation of γ-aminobutyric acid (GABA A) receptor expression in mouse pancreatic islet α-cells

Diabetes

Volumn 56, Issue 2, 2007, Pages 320-327

  Bailey, Sarah J ^a,b   Ravier, Magalie A ^a   Rutter, Guy A ^a,c  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b University of Bath   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; CALCIUM ION; GLUCAGON; GLUCOSE; MESSENGER RNA; POTASSIUM ION; RECEPTOR SUBUNIT;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL LINE; CELL MEMBRANE; CONCENTRATION (PARAMETERS); DEPOLARIZATION; FEMALE; GLUCAGON RELEASE; GLUCOSE BLOOD LEVEL; IMMUNOCYTOCHEMISTRY; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL;

ANIMALS; CALCIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLUCAGON; GLUCAGON-SECRETING CELLS; GLUCOSE; INSULIN; ISLETS OF LANGERHANS; MICE; POTASSIUM; PROTEIN SUBUNITS; PYRIDAZINES; RECEPTORS, GABA-A; RNA, MESSENGER;

EID: 33847012550     PISSN: 00121797     EISSN: 00121797     Source Type: Journal    
DOI: 10.2337/db06-0712     Document Type: Article

References (55)

1. Unger RH, Orci L: Physiology and pathophysiology of glucagon. Physiol Rev 56:778-826, 1976
2. Yoshimoto Y, Fukuyama Y, Horio Y, Inanobe A, Gotoh M, Kurachi Y: Somatostatin induces hyperpolarization in pancreatic islet alpha cells by activating a G protein-gated K+ channel. FEBS Lett 444:265-269, 1999
3. Gopel SO, Kanno T, Barg S, Weng X, Gromada J, Rorsman P: Regulation of glucagon release in mouse α-cells by KATP channels and inactivation of TTX-sensitive Na+ channels. J Physiol 528:509-520, 2000
4. Berts A, Ball A, Gylfe E, Hellman B: Suppression of Ca2+ oscillations in glucagon-producing alpha 2-cells by insulin/glucose and amino acids. Biochim Biophys Acta 1310:212-216, 1996
5. Ravier MA, Rutter GA: Glucose or insulin, but not zinc ions, inhibit glucagon secretion from mouse pancreatic α-cells. Diabetes 54:1789-1797, 2005
6. Taborsky GJ Jr, Ahren B, Havel PJ: Autonomic mediation of glucagon secretion during hypoglycemia: implications for impaired α-cell responses in type 1 diabetes. Diabetes 47:995-1005, 1998
7. Olsen HL, Theander S, Bokvist K, Buschard K, Wollheim CB, Gromada J: Glucose stimulates glucagon release in single rat alpha-cells by mechanisms that mirror the stimulus-secretion coupling in beta-cells. Endocrinology 146:4861-4870, 2005
8. Maruyama H, Hisatomi A, Orci L, Grodsky GM, Unger RH: Insulin within islets is a physiologic glucagon release inhibitor. J Clin Invest 74:2296-2299, 1984
9. Ishihara H, Maechler P, Gjinovci A, Herrera PL, Wollheim CB: Islet beta-cell secretion determines glucagon release from neighbouring alphacells. Nat Cell Biol 5:330-335, 2003
10. Franklin I, Gromada J, Gjinovci A, Theander S, Wollheim CB: β-cell secretory products activate α-cell ATP-dependent potassium channels to inhibit glucagon release. Diabetes 54:1808-1815, 2005
11. Okada Y, Taniguchi H, Schimada C: High concentration of GABA and high glutamate decarboxylase activity in rat pancreatic islets and human insulinoma. Science 194:620-622, 1976
12. Briel G, Gylfe E, Hellman B, Neuhoff V: Microdetermination of free amino acids in pancreatic islets isolated from obese-hyperglycemic mice. Acta Physiol Scand 84:247-253, 1972
13. Gylfe E, Hellman B: Role of glucose as a regulator and precursor of amino acids in the pancreatic beta-cells. Endocrinology 94:1150-1156, 1974
14. Vincent SR, Hokfelt T, Wu JY, Elde RP, Morgan LM, Kimmel JR: Immunohistochemical studies of the GABA system in the pancreas. Neuroendocrinology 36:197-204, 1983
15. Braun M, Wendt A, Birnir B, Broman J, Eliasson L, Galvanovskis J, Gromada J, Mulder H, Rorsman P: Regulated exocytosis of GABA-containing synaptic-like microvesicles in pancreatic beta-cells. J Gen Physiol 123:191-204, 2004
16. Kawai K, Unger RH: Effects of gamma-aminobutyric acid on insulin, glucagon, and somatostatin release from isolated perfused dog pancreas. Endocrinology 113:111-113, 1983
17. Minuk GY, Sarjeant EJ: Insulin and glucagon secretion by the dog pancreas during intravenous and oral administration of gamma aminobutyric acid (GABA). Horm Metab Res 17:313-314, 1985
18. Cavagnini F, Pinto M, Dubini A, Invitti C, Cappelletti G, Polli EE: Effects of gamma aminobutyric acid (GABA) and muscimol on endocrine pancreatic function in man. Metabolism 31:73-77, 1982
19. Passariello N, Giugliano D, Torella R, Sgambato S, Coppola L, Frascolla N: A possible role of gamma-aminobutyric acid in the control of the endocrine pancreas. J Clin Endocrinol Metab 54:1145-1149, 1982
20. Gilon P, Bertrand G, Loubatieres-Mariani MM, Remacle C, Henquin JC: The influence of gamma-aminobutyric acid on hormone release by the mouse and rat endocrine pancreas. Endocrinology 129:2521-2529, 1991
21. Rorsman P, Berggren PO, Bokvist K, Ericson H, Mohler H, Ostenson CG, Smith PA: Glucose-inhibition of glucagon secretion involves activation of GABAA-receptor chloride channels. Nature 341:233-236, 1989
22. Wendt A, Birnir B, Buschard K, Gromada J, Salehi A, Sewing S, Rorsman P, Braun M: Glucose inhibition of glucagon secretion from rat α-cells is mediated by GABA released from neighboring β-cells. Diabetes 53:1038-1045, 2004
23. Xu E, Kumar M, Zhang Y, Ju W, Obata T, Zhang N, Liu S, Wendt A, Deng S, Ebina Y, Wheeler MB, Braun M, Wang Q: Intra-islet insulin suppresses glucagon release via GABA-GABAA receptor system. Cell Metab 3:47-58, 2006
24. Barnard EA, Skolnick P, Olsen RW, Mohler H, Sieghart W, Biggio G, Braestrup C, Bateson AN, Langer SZ: International Union of Pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function. Pharmacol Rev 50:291-313, 1998
25. Chang Y, Wang R, Barot S, Weiss DS: Stoichiometry of a recombinant GABAA receptor. J Neurosci 16:5415-5424, 1996
26. Hevers W, Luddens H: The diversity of GABAA receptors: pharmacological and electrophysiological properties of GABAA channel subtypes. Mol Neurobiol 18:35-86, 1998
27. Laurie DJ, Wisden W, Seeburg PH: The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 12:4151-4172, 1992
28. Smith SS, Gong QH, Hsu FC, Markowitz RS, Ffrench-Mullen, JM, Li, X: GABA(A) receptor alpha4 subunit suppression prevents withdrawal properties of an endogenous steroid. Nature 392:926-930, 1998
29. Redecker C, Wang W, Fritschy JM, Witte OW: Widespread and long-lasting alterations in GABA(A)-receptor subtypes after focal cortical infarcts in rats: mediation by NMDA-dependent processes. J Cereb Blood Flow Metab 22:1463-1475, 2002
30. Wang JB, Kofuji P, Fernando JC, Moss SJ, Huganir RL, Burt DR: The alpha 1, alpha 2, and alpha 3 subunits of GABAA receptors: comparison in seizure-prone and -resistant mice and during development. J Mol Neurosci 3:177-184, 1992
31. Yang W, Reyes AA, Lan NC: Identification of the GABAA receptor subtype mRNA in human pancreatic tissue. FEBS Lett 346:257-262, 1994
32. Borboni P, Porzio O, Fusco A, Sesti G, Lauro R, Marlier LN: Molecular and cellular characterization of the GABAA receptor in the rat pancreas. Mol Cell Endocrinol 103:157-163, 1994
33. von Blankenfeld G, Turner J, Ahnert-Hilger G, John M, Enkvist MO, Stephenson F, Kettenmann H, Wiedenmann B: Expression of functional GABAA receptors in neuroendocrine gastropancreatic cells. Pflugers Arch 430:381-388, 1995
34. Hales TG, Tyndale RF: Few cell lines with GABAA mRNAs have functional receptors. J Neurosci 14:5429-5436, 1994
35. Tyndale RF, Hales TG, Olsen RW, Tobin AJ: Distinctive patterns of GABAA receptor subunit mRNAs in 13 cell lines. J Neurosci 14:5417-5428, 1994
36. Ainscow EK, Rutter GA: Mitochondrial priming modifies Ca2+ oscillations and insulin secretion in pancreatic islets. Biochem J 353:175-180, 2001
37. Gustincich S, Feigenspan A, Sieghart W, Raviola E: Composition of the GABA(A) receptors of retinal dopaminergic neurons. J Neurosci 19:7812-7822, 1999
38. Liu ZF, Burt DR: A synthetic standard for competitive RT-PCR quantitation of 13 GABA receptor type A subunit mRNAs in rats and mice. J Neurosci Methods 85:89-98, 1998
39. Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ, Reed MW: Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem 285:194-204, 2000
40. Bailey SJ, Toth M: Variability in the benzodiazepine response of serotonin 5-HT1A receptor null mice displaying anxiety-like phenotype: evidence for genetic modifiers in the 5-HT-mediated regulation of GABA(A) receptors. J Neurosci 24:6343-6351, 2004
41. Ives JH, Drewery DL, Thompson CL: Neuronal activity and its influence on developmentally regulated GABA(A) receptor expression in cultured mouse cerebellar granule cells. Neuropharmacology 43:715-725, 2002
42. Liu YJ, Vieira E, Gylfe E: A store-operated mechanism determines the activity of the electrically excitable glucagon-secreting pancreatic alphacell. Cell Calcium 35:357-365, 2004
43. Wan Q, Xiong ZG, Man HY, Ackerley CA, Braunton J, Lu WY, Becker LE, MacDonald JF, Wang YT: Recruitment of functional GABA(A) receptors to postsynaptic domains by insulin. Nature 388:686-690, 1997
44. Salehi A, Vieira E, Gylfe E: Paradoxical stimulation of glucagon secretion by high glucose concentrations. Diabetes 55:2318-2323, 2006
45. Brown N, Kerby J, Bonnert TP, Whiting PJ, Wafford KA: Pharmacological characterization of a novel cell line expressing human alpha(4)beta(3)delta GABA(A) receptors. Br J Pharmacol 136:965-974, 2002
46. Akk G, Bracamontes J, Steinbach JH: Activation of GABA(A) receptors containing the alpha4 subunit by GABA and pentobarbital. J Physiol 556:387-399, 2004
47. Wafford KA, Thompson SA, Thomas D, Sikela J, Wilcox AS, Whiting PJ: Functional characterization of human gamma-aminobutyric acidA receptors containing the alpha 4 subunit. Mol Pharmacol 50:670-678, 1996
48. Hosie AM, Dunne EL, Harvey RJ, Smart TG: Zinc-mediated inhibition of GABA(A) receptors: discrete binding sites underlie subtype specificity. Nat Neurosci 6:362-369, 2003
49. Thompson CL, Razzini G, Pollard S, Stephenson FA: Cyclic AM: P-mediated regulation of GABA(A) receptor subunit expression in mature rat cerebellar granule cells: evidence for transcriptional and translational control. J Neurochem 74:920-931, 2000
50. Bulleit RF, Hsieh T: MEK inhibitors block BDNF-dependent and -independent expression of GABA(A) receptor subunit mRNAs in cultured mouse cerebellar granule neurons. Brain Res Dev Brain Res 119:1-10, 2000
51. Klee CB, Ren H, Wang X: Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J Biol Chem 273:13367-13370, 1998
52. Lee B, Butcher GQ, Hoyt KR, Impey S, Obrietan K: Activity-dependent neuroprotection and cAMP response element-binding protein (CREB): kinase coupling, stimulus intensity, and temporal regulation of CREB phosphorylation at serine 133. J Neurosci 25:1137-1148, 2005
53. Stelzer A, Shi H: Impairment of GABAA receptor function by N-methyl-D-aspartate-mediated calcium influx in isolated CA1 pyramidal cells. Neuroscience 62:813-828, 1994
54. Zhang X, Odom DT, Koo SH, Conkright MD, Canettieri G, Best J, Chen H, Jenner R, Herbolsheimer E, Jacobsen E, Kadam S, Ecker JR, Emerson B, Hogenesch JB, Unterman T, Young RA, Montminy M: Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci U S A 102:4459-4464, 2005
55. Kramer D, Fresu L, Ashby DS, Freeman TC, Genazzani AA: Calcineurin controls the expression of numerous genes in cerebellar granule cells. Mol Cell Neurosci 23:325-330, 2003