In situ electrophysiological examination of pancreatic α cells in the streptozotocin-induced diabetes model, revealing the cellular basis of glucagon hypersecretion

Diabetes

Volumn 62, Issue 2, 2013, Pages 519-530

  Huang, Ya Chi ^a   Rupnik, Marjan S ^a,b   Karimian, Negar ^a   Herrera, Pedro L ^c   Gilon, Patrick ^d   Feng, Zhong Ping ^e   Gaisano, Herbert Y ^a,e  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF MARIBOR   (Slovenia)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCAGON; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; ELECTRIC CAPACITANCE; ELECTROPHYSIOLOGY; EXOCYTOSIS; GLUCOSE INTOLERANCE; HYPERGLUCAGONEMIA; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN SECRETION; STREPTOZOCIN DIABETES;

ACTION POTENTIALS; ANIMALS; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; ELECTROPHYSIOLOGICAL PHENOMENA; EXOCYTOSIS; GLUCAGON; GLUCAGON-SECRETING CELLS; GLUCOSE INTOLERANCE; HYPERGLYCEMIA; MICE; POTASSIUM CHANNELS, VOLTAGE-GATED; SECRETORY VESICLES; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84873049748     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-0786     Document Type: Article

References (39)

1. Dunning BE, Gerich JE. The role of alpha-cell dysregulation in fasting and postprandial hyperglycemia in type 2 diabetes and therapeutic implications. Endocr Rev 2007;28:253-283
2. Quesada I, Tudurí E, Ripoll C, Nadal A. Physiology of the pancreatic alpha-cell and glucagon secretion: role in glucose homeostasis and diabetes. J Endocrinol 2008;199:5-19
3. Cryer PE. Hypoglycaemia: the limiting factor in the glycaemic management of Type I and Type II diabetes. Diabetologia 2002;45:937-948
4. Butler PC, Rizza RA. Contribution to postprandial hyperglycemia and effect on initial splanchnic glucose clearance of hepatic glucose cycling in glucose-intolerant or NIDDM patients. Diabetes 1991;40:73-81
5. Gerich JE. Lilly lecture 1988. Glucose counterregulation and its impact on diabetes mellitus. Diabetes 1988;37:1608-1617
6. Huang YC, Rupnik M, Gaisano HY. Unperturbed islet a-cell function examined in mouse pancreas tissue slices. J Physiol 2011;589:395-408
7. Ramracheya R, Ward C, Shigeto M, et al. Membrane potential-dependent inactivation of voltage-gated ion channels in alpha-cells inhibits glucagon secretion from human islets. Diabetes 2010;59:2198-2208
8. Like AA, Rossini AA. Streptozotocin-induced pancreatic insulitis: new model of diabetes mellitus. Science 1976;193:415-417
9. O'Brien BA, Harmon BV, Cameron DP, Allan DJ. Beta-cell apoptosis is responsible for the development of IDDM in the multiple low-dose streptozotocin model. J Pathol 1996;178:176-181
10. 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
11. Anderson MS, Bluestone JA. The NOD mouse: a model of immune dys-regulation. Annu Rev Immunol 2005;23:447-485
12. Wang Q, Brubaker PL. Glucagon-like peptide-1 treatment delays the onset of diabetes in 8 week-old db/db mice. Diabetologia 2002;45:1263-1273
13. Kwan EP, Gaisano HY. Glucagon-like peptide 1 regulates sequential and compound exocytosis in pancreatic islet beta-cells. Diabetes 2005;54:2734-2743
14. Andersson SA, Pedersen MG, Vikman J, Eliasson L. Glucose-dependent docking and SNARE protein-mediated exocytosis in mouse pancreatic alpha-cell. Pflugers Arch 2011;462:443-454
15. Gustavsson N, Wei SH, Hoang DN, et al. Synaptotagmin-7 is a principal Ca2+ sensor for Ca2+-induced glucagon exocytosis in pancreas. J Physiol 2009;587:1169-1178
16. Quoix N, Cheng-Xue R, Mattart L, et al. Glucose and pharmacological modulators of ATP-sensitive K+ channels control [Ca2+]c by different mechanisms in isolated mouse alpha-cells. Diabetes 2009;58:412-421
17. Spigelman AF, Dai X, MacDonald PE. Voltage-dependent K(+) channels are positive regulators of alpha cell action potential generation and glucagon secretion in mice and humans. Diabetologia 2010;53:1917-1926
18. Leung YM, Ahmed I, Sheu L, Tsushima RG, Diamant NE, Gaisano HY. Two populations of pancreatic islet alpha-cells displaying distinct Ca2+ channel properties. Biochem Biophys Res Commun 2006;345:340-344
19. Leung YM, Ahmed I, Sheu L, et al. Electrophysiological characterization of pancreatic islet cells in the mouse insulin promoter-green fluorescent protein mouse. Endocrinology 2005;146:4766-4775
20. Thorel F, Népote V, Avril I, et al. Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature 2010;464:1149-1154
21. 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
22. Hille B, Hille B. Ion Channels of Excitable Membranes. Sunderland, MA, Sinauer, 2001
23. Braun M, Ramracheya R, Bengtsson M, et al. Voltage-gated ion channels in human pancreatic beta-cells: electrophysiological characterization and role in insulin secretion. Diabetes 2008;57:1618-1628
24. Houamed KM, Sweet IR, Satin LS. BK channels mediate a novel ionic mechanism that regulates glucose-dependent electrical activity and insulin secretion in mouse pancreatic b-cells. J Physiol 2010;588:3511-3523
25. 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
26. Atkinson MA, Bluestone JA, Eisenbarth GS, et al. How does type 1 diabetes develop?: the notion of homicide or b-cell suicide revisited. Diabetes 2011; 60:1370-1379
27. Wendt A, Birnir B, Buschard K, et al. Glucose inhibition of glucagon secretion from rat alpha-cells is mediated by GABA released from neighboring beta-cells. Diabetes 2004;53:1038-1045
28. Xu E, Kumar M, Zhang Y, et al. Intra-islet insulin suppresses glucagon release via GABA-GABAA receptor system. Cell Metab 2006;3:47-58
29. Zhou H, Tran PO, Yang S, et al. Regulation of alpha-cell function by the beta-cell during hypoglycemia in Wistar rats: the "switch-off" hypothesis. Diabetes 2004;53:1482-1487
30. Zhou H, Zhang T, Harmon JS, Bryan J, Robertson RP. Zinc, not insulin, regulates the rat alpha-cell response to hypoglycemia in vivo. Diabetes 2007;56:1107-1112
31. Ibeakanma C, Vanner S. TNFalpha is a key mediator of the pronociceptive effects of mucosal supernatant from human ulcerative colitis on colonic DRG neurons. Gut 2010;59:612-621
32. Beyak MJ, Ramji N, Krol KM, Kawaja MD, Vanner SJ. Two TTX-resistant Na+ currents in mouse colonic dorsal root ganglia neurons and their role in colitis-induced hyperexcitability. Am J Physiol Gastrointest Liver Physiol 2004;287:G845-G855
33. Beyak MJ, Vanner S. Inflammation-induced hyperexcitability of nociceptive gastrointestinal DRG neurones: the role of voltage-gated ion channels. Neurogastroenterol Motil 2005;17:175-186
34. King DE, Macleod RJ, Vanner SJ. Trinitrobenzenesulphonic acid colitis alters Na 1.8 channel expression in mouse dorsal root ganglia neurons. Neurogastroenterol Motil 2009;21:880-e64
35. Stewart T, Beyak MJ, Vanner S. Ileitis modulates potassium and sodium currents in guinea pig dorsal root ganglia sensory neurons. J Physiol 2003; 552:797-807
36. Walker JN, Johnson PR, Shigeto M, Hughes SJ, Clark A, Rorsman P. Glucose-responsive beta cells in islets isolated from a patient with long-standing type 1 diabetes mellitus. Diabetologia 2011;54:200-202
37. Heimberg H, De Vos A, Pipeleers D, Thorens B, Schuit F. Differences in glucose transporter gene expression between rat pancreatic alpha-and beta-cells are correlated to differences in glucose transport but not in glucose utilization. J Biol Chem 1995;270:8971-8975
38. Sato Y, Ito T, Udaka N, et al. Immunohistochemical localization of facilitated-diffusion glucose transporters in rat pancreatic islets. Tissue Cell 1996;28: 637-643
39. Zhou H, Zhang T, Oseid E, Harmon J, Tonooka N, Robertson RP. Reversal of defective glucagon responses to hypoglycemia in insulin-dependent autoimmune diabetic BB rats. Endocrinology 2007;148:2863-2869