Membrane potential-dependent inactivation of voltage-gated ion channels in α-cells inhibits glucagon secretion from human islets

Diabetes

Volumn 59, Issue 9, 2010, Pages 2198-2208

  Ramracheya, Reshma ^a   Ward, Caroline ^a   Shigeto, Makoto ^a   Walker, Jonathan N ^a,b   Amisten, Stefan ^a   Zhang, Quan ^a   Johnson, Paul R ^b,c   Rorsman, Patrik ^a,b   Braun, Matthias ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NIHR OXFORD BIOMEDICAL RESEARCH CENTRE   (United Kingdom)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; CALCIUM ION; GLUCAGON; INSULIN; ION CHANNEL; ISRADIPINE; OMEGA AGATOXIN; POTASSIUM CHANNEL; SOMATOSTATIN RECEPTOR 2; TETRODOTOXIN; TOLBUTAMIDE; ZINC CHLORIDE; CALCIUM; CHLORIDE; GLUCOSE; SOMATOSTATIN; ZINC DERIVATIVE;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM CURRENT; CALCIUM TRANSPORT; CONTROLLED STUDY; EXOCYTOSIS; GLUCAGON RELEASE; HUMAN; HUMAN CELL; MEMBRANE CURRENT; MEMBRANE POTENTIAL; PANCREAS ISLET ALPHA CELL; PRIORITY JOURNAL; SODIUM CURRENT; CHANNEL GATING; CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECTS; PANCREAS ISLET; PHYSIOLOGY; SECRETION (PROCESS);

CALCIUM; CELL CULTURE TECHNIQUES; CHLORIDES; GLUCAGON; GLUCAGON-SECRETING CELLS; GLUCOSE; HUMANS; INSULIN; ION CHANNEL GATING; ISLETS OF LANGERHANS; MEMBRANE POTENTIALS; POTASSIUM CHANNELS; SOMATOSTATIN; TETRODOTOXIN; TOLBUTAMIDE; ZINC COMPOUNDS;

EID: 77956364291     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-1505     Document Type: Article

References (34)

1. Cryer PE. Hypoglycaemia: the limiting factor in the glycaemic management of Type I and Type II diabetes. Diabetologia 2002;45:937-948
2. Lefebvre PJ (Ed.). Glucagon and Diabetes. In Handbook of Experimental Pharmacology. Berlin, Springer, 1996, p. 115-131
3. Gromada J, Franklin I, Wollheim CB. Alpha-cells of the endocrine pancreas: 35 years of research but the enigma remains. Endocr Rev 2007;28:84-116 (Pubitemid 46220851)
4. Olofsson CS, Salehi A, Gopel SO, Holm C, Rorsman P. Palmitate stimulation of glucagon secretion in mouse pancreatic alpha-cells results from activation of L-type calcium channels and elevation of cytoplasmic calcium. Diabetes 2004;53:2836-2843 (Pubitemid 39425908)
5. Gromada J, Bokvist K, Ding WG, Barg S, Buschard K, Renstrom E, Rorsman P. Adrenaline stimulates glucagon secretion in pancreatic A-cells by increasing the Ca2+ current and the number of granules close to the L-type Ca2+ channels. J Gen Physiol 1997;110:217-228
6. Miki T, Liss B, Minami K, Shiuchi T, Saraya A, Kashima Y, Horiuchi M, Ashcroft F, Minokoshi Y, Roeper J, Seino S. ATP-sensitive K+ channels in the hypothalamus are essential for the maintenance of glucose homeostasis. Nat Neurosci 2001;4:507-512
7. Macdonald PE, Marinis YZ, Ramracheya R, Salehi A, Ma X, Johnson PR, Cox R, Eliasson L, Rorsman P. A KATP Channel-Dependent Pathway within alpha Cells Regulates Glucagon Release from Both Rodent and Human Islets of Langerhans. PLoS Biol 2007;5:e143
8. Unger RH, Orci L. The role of glucagon in diabetes. Compr Ther 1982;8:53-59
9. Cryer PE. Glucagon and hyperglycemia in diabetes. Clin Sci 2008;114:589-590
10. Cryer PE, Davis SN, Shamoon H. Hypoglycemia in diabetes. Diabetes Care 2003;26:1902-1912
11. Bokvist K, Olsen HL, Hoy M, Gotfredsen CF, Holmes WF, Buschard K, Rorsman P, Gromada J. Characterisation of sulphonylurea and ATP-regulated K+ channels in rat pancreatic A-cells. Pflugers Arch 1999;438:428-436
12. Göpel SO, Kanno T, Barg S, Weng XG, Gromada J, Rorsman P. Regulation of glucagon release in mouse-cells by KATP channels and inactivation of TTX-sensitive Na+ channels. J Physiol 2000;528:509-520
13. Barg S, Galvanovskis J, Göpel SO, Rorsman P, Eliasson L. Tight coupling between electrical activity and exocytosis in mouse glucagon-secreting alpha-cells. Diabetes 2000;49:1500-1510
14. Rorsman P, Salehi SA, Abdulkader F, Braun M, Macdonald PE. K(ATP)-channels and glucose-regulated glucagon secretion. Trends Endocrinol Metab 2008;19:277-284
15. Brissova M, Fowler MJ, Nicholson WE, Chu A, Hirshberg B, Harlan DM, Powers AC. Assessment of human pancreatic islet architecture and composition by laser scanning confocal microscopy. J Histochem Cytochem 2005;53:1087-1097
16. Cabrera O, Berman DM, Kenyon NS, Ricordi C, Berggren PO, Caicedo A. The unique cytoarchitecture of human pancreatic islets has implications for islet cell function. Proc Natl Acad Sci U S A 2006;103:2334-2339
17. Lake SP, Bassett PD, Larkins A, Revell J, Walczak K, Chamberlain J, Rumford GM, London NJ, Veitch PS, Bell PR, et al. Large-scale purification of human islets utilizing discontinuous albumin gradient on IBM 2991 cell separator. Diabetes 1989; 38 (Suppl. 1):143-145
18. Ricordi C, Lacy PE, Finke EH, Olack BJ, Scharp DW. Automated method for isolation of human pancreatic islets. Diabetes 1988;37:413-420
19. Braun M, Ramracheya R, Amisten S, Bengtsson M, Moritoh Y, Zhang Q, Johnson PR, Rorsman P. Somatostatin release, electrical activity, membrane currents and exocytosis in human pancreatic delta cells. Diabetologia 2009;52:1566-1578
20. Braun M, Ramracheya R, Bengtsson M, Zhang Q, Karanauskaite J, Partridge C, Johnson PR, Rorsman P. Voltage-gated ion channels in human pancreatic beta-cells: Electrophysiological characterization and role in insulin secretion. Diabetes 2008;57:1618-1628
21. Göpel SO, Kanno T, Barg S, Eliasson L, Galvanovskis J, Renstrom E, Rorsman P. Activation of Ca(2+)-dependent K(+) channels contributes to rhythmic firing of action potentials in mouse pancreatic beta cells. J Gen Physiol 1999;114:759-770
22. Zhang Q, Bengtsson M, Partridge C, Salehi A, Braun M, Cox R, Eliasson L, Johnson PR, Renstrom E, Schneider T, Berggren PO, Göpel S, Ashcroft FM, Rorsman P. R-type Ca(2+)-channel-evoked CICR regulates glucose-induced somatostatin secretion. Nat Cell Biol 2007;9:453-460
23. Salehi A, Vieira E, Gylfe E. Paradoxical stimulation of glucagon secretion by high glucose concentrations. Diabetes 2006;55:2318-2323
24. Marty A, Neher E. Potassium channels in cultured bovine adrenal chromaffin cells. J Physiol 1985;367:117-141
25. Conley E, Brammar W. VLH Kv4-Shal. In The Ion Channel Facts Book: Voltage-gated Channels. San Diego, CA, Academic Press, 1999, p. 617-646
26. Escoubas P, Diochot S, Celerier ML, Nakajima T, Lazdunski M. Novel tarantula toxins for subtypes of voltage-dependent potassium channels in the Kv2 and Kv4 subfamilies. Mol Pharmacol 2002;62:48-57
27. Zarayskiy VV, Balasubramanian G, Bondarenko VE, Morales MJ. Heteropoda toxin 2 is a gating modifier toxin specific for voltage-gated K+ channels of the Kv4 family. Toxicon 2005;45:431-442
28. Patel SP, Campbell DL. Transient outward potassium current, 'Ito', phenotypes in the mammalian left ventricle: underlying molecular, cellular and biophysical mechanisms. J Physiol 2005;569:7-39
29. Quoix N, Cheng-Xue R, Guiot Y, Herrera PL, Henquin JC, Gilon P. The GluCre-ROSA26EYFP mouse: a new model for easy identification of living pancreatic alpha-cells. FEBS Lett 2007;581:4235-4240
30. Singh V, Brendel MD, Zacharias S, Mergler S, Jahr H, Wiedenmann B, Bretzel RG, Plockinger U, Strowski MZ. Characterization of somatostatin receptor subtype-specific regulation of insulin and glucagon secretion: an in vitro study on isolated human pancreatic islets. J Clin Endocrinol Metab 2007;92:673-680
31. Banarer S, McGregor VP, Cryer PE. Intraislet hyperinsulinemia prevents the glucagon response to hypoglycemia despite an intact autonomic response. Diabetes 2002;51:958-965
32. Ravier MA, Rutter GA. Glucose or insulin, but not zinc ions, inhibit glucagon secretion from mouse pancreatic alpha-cells. Diabetes 2005;54:1789-1797
33. Franklin I, Gromada J, Gjinovci A, Theander S, Wollheim CB. Beta-cell secretory products activate alpha-cell ATP-dependent potassium channels to inhibit glucagon release. Diabetes 2005;54:1808-1815
34. Mathie A, Sutton GL, Clarke CE, Veale EL. Zinc and copper: pharmacological probes and endogenous modulators of neuronal excitability. Pharmacol Ther 2006;111:567-583