Antidiabetic sulfonylurea stimulates insulin secretion independently of plasma membrane KATP channels

American Journal of Physiology - Endocrinology and Metabolism

Volumn 293, Issue 1, 2007, Pages

  Geng, Xuehui ^a   Li, Lehong ^a   Bottino, Rita ^a,b   Balamurugan, A N ^a,b,c   Bertera, Suzanne ^a,b   Densmore, Erik ^a   Su, Anjey ^a   Chang, Yigang ^a,b   Trucco, Massimo ^a,b   Drain, Peter ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

cells; Adenosine 5 triphosphate sensitive potassium channels; Endocytosis; Exocytosis; Glibenclamide; Permanent neonatal diabetes

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIDIABETIC AGENT; CALCIUM; GLIBENCLAMIDE; POTASSIUM CHANNEL; SULFONYLUREA;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DEPOLARIZATION; DRUG MECHANISM; INSULIN RELEASE; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CALCIUM; CATION TRANSPORT PROTEINS; CELL MEMBRANE; GLYBURIDE; HYPOGLYCEMIC AGENTS; INSULIN; ISLETS OF LANGERHANS; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED BALB C; POTASSIUM CHLORIDE; SULFONYLUREA COMPOUNDS;

EID: 34547125567     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00016.2007     Document Type: Article

References (50)

1. Aguilar-Bryan L, Nichols CG, Weschler SW, Clement IVJP, Boyd IIIAE, Gonzalez G, Herrera-Sosa H, Nguy K, Bryan J, Nelson DA. Cloning of the β cell high-affinity sulfonylurea receptor: a regulator of insulin secretion. Science 268: 423-426, 1995.
2. Ashcroft FM, Harrison DE, Ashcroft SJ. Glucose induces closure of single potassium channels in isolated rat pancreatic beta-cells. Nature 312: 446-448, 1984.
3. Ashcroft FM. Adenosine 5′-triphosphate-sensitive potassium channels. Annu Rev Neurosci 11: 97-118, 1988.
4. 2+-dependent exocytosis in pancreatic β cells is mediated by a 65-kDa mdr-like P-glycoprotein. Proc Natl Acad Sci USA 96: 5539-5544, 1999.
5. - uptake and acidification. J Cell Sci 114: 2145-2154, 2001.
6. Bertera S, Crawford ML, Alexander AL, Papworth GD, Watkins SC, Robbins PD, Trucco M. Gene transfer of manganese superoxide dismutase extends islets graft function in a model of autoimmune diabetes. Diabetes 52: 387-393, 2003.
7. 3H-glibenclamide in pancreatic islet cells. Diabetologia 29: 259-261, 1986.
8. Codner E, Flanagan S, Ellard S, Garcia H, Hattersley AT. High-dose glibenclamide can replace insulin therapy despite transitory diarrhea in early-onset diabetes caused by a novel R201L Kir6.2 mutation. Diabetes Care 28: 758-759, 2005.
9. Conover WJ. Practical Nonparametric Statistics (2nd ed.). New York: John Wiley & Sons, 1980, p. 344-376.
10. + channels in pancreatic beta-cells. Nature 311: 271-273, 1984.
11. ATP channels by its actions on the sulfonylurea receptor 1 nucleotide-binding folds-1 and -2. J Biol Chem 279: 53259-53265, 2004.
12. Del Nido PJ, Glynn P, Buenaventura PP, Salama G, Koretsky AP. Fluorescence measurement of calcium transients in perfused rabbit heart using rhod 2. Am J Physiol Heart Circ Physiol 274: H728-H741, 1998.
13. Detimary P, Berghe VD, Henquin JC. Concentration dependence and time course of the effects of glucose on adenine and guanine nucleotides in mouse pancreatic islets. J Biol Chem 271: 20559-20565, 1996.
14. Detimary P, Dejonghe S, Ling Z, Pipeleers D, Schuit F, Henquin JC. The changes in adenine nucleotides measured in glucose-stimulated rodent islets occur in beta cells but not in alpha cells and are also observed in human islets. J Biol Chem 273: 33905-33908, 1998.
15. Doliba NM, Qin W, Vatamaniuk MZ, Li C, Zelent D, Najafi H, Buettger CW, Collins HW, Carr RD, Magnuson MA, Matschinsky FM. Restitution of defective glucose-stimulated insulin release of sulfonylurea type 1 receptor knockout mice by acetylcholine. Am J Physiol Endocrinol Metab 286: E834-E843, 2004.
16. ATP channel inhibition by ATP requires distinct functional domains of the cytoplasmic C terminus of the pore-forming subunit. Proc Natl Acad Sci USA 95: 13953-13958, 1998.
17. Eliasson L, Ma X, Renstrom E, Barg S, Berggren PO, Galvanovskis J, Gromada J, Jing X, Lundquist I, Salehi A, Sewing S, Rorsman P. SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J Gen Physiol 121: 181-197, 2003.
18. Eliasson L, Renstrom E, Ammala C, Berggren PO, Bertorello AM, Bokvist K, Chibalin A, Deeney JT, Flatt PR, Gabel J, Gromada J, Larsson O, Lindstrom P, Rhodes CJ, Rorsman P. PKC-dependent stimulation of exocytosis by sulfonylureas in pancreatic β cells. Science 271: 813-815, 1996.
19. Gembal M, Gilon P, Henquin JC. Evidence that glucose can control insulin release independently from its action on ATP-sensitive K channels in mouse beta cells. J Clin Invest 89: 1288-1295, 1992.
20. + channels in mouse β cells. J Clin Invest 91: 871-880, 1993.
21. ATP channels of the endocrine pancreas. Diabetes 52: 767-776, 2003.
22. ir6.2 and permanent neonatal diabetes. N Engl J Med 350: 1838-1849, 2004.
23. Gylfe E, Hellman B, Sehlin J, Taljedal B. Interaction of sulfonylurea with the pancreatic B-cell. Experientia 40: 1126-1134, 1984.
24. ATP channel-independent targets of diazoxide and 5-hydroxydecanoate in the heart. J Physiol 542: 735-741, 2002.
25. Hellman B. Factors affecting the uptake of glibenclamide in microdissected pancreatic islets rich in β cells. Pharmacology 11: 257-267, 1974.
26. Hellman B, Sehlin J, Taljedal IB. Glibenclamide is exceptional among hypoglycaemic sulphonylureas in accumulating progressively in β-cell-rich pancreatic islets. Acta Endocrinol 105: 385-390, 1984.
27. KATP: an inward rectifier subunit plus the sulfonylurea receptor. Science 270: 1166-1170, 1995.
28. Joseph JW, Jensen MV, Ilkayeva O, Palmieri F, Alarcon C, Rhodes CJ, Newgard CB. The mitochondrial citrate/isocitrate carrier plays a regulatory role in glucose-stimulated insulin secretion. J Biol Chem 281:35624-35632, 2006.
29. ATP channels by its actions on nucleotide binding folds 1 and 2 of sulfonylurea receptor 2A. J Biol Chem 279: 47125-47131, 2004.
30. Kawazu S, Sener A, Couturier E, Malaisse WJ. Metabolic, cationic and secretory effects of hypoglycemic sulfonylureas in pancreatic islets. Naunyn Schmiedebergs Arch Pharmacol 312: 277-283, 1980.
31. Li L, Rojas A, Wu J, Jiang C. Disruption of glucose sensing and insulin secretion by ribozyme Kir6.2-gene targeting in insulin-secreting cells. Endocrinology 145: 4408-4414, 2004.
32. ATP channel-deficient mice. Proc Natl Acad Sci USA 95: 10402-10406, 1998.
33. Nenquin M, Szollosi A, Aguilar-Bryan L, Bryan J, Henquin JC. Both triggering and amplifying pathways contribute to fuel-induced insulin secretion in the absence of sulfonylurea receptor-1 in pancreatic β-cells. J Biol Chem 279: 32316-32324, 2004.
34. Ozanne SE, Guest PC, Hutton JC, Hales CN. Intracellular localization and molecular heterogeneity of the sulphonylurea receptor in insulinsecreting cells. Diabetologia 38: 277-282, 1995.
35. ATP channel. J Biol Chem 279: 4234-4240, 2004.
36. Ravier MA, Henquin JC. Time and amplitude regulation of pulsatile insulin secretion by triggering and amplifying pathways in mouse islets. FEBS Lett 530: 215-219, 2002.
37. ATP channels during metabolic inhibition by an indirect mechanism. Cardiovasc Res 61: 570-579, 2004.
38. Ronner P, Naumann CM, Friel E. Effects of glucose and amino acids on free ADP in βHC9 insulin-secreting cells. Diabetes 50: 291-300, 2001.
39. Sagen JV, Raeder H, Hathout E, Shehadeh N, Gudmundsson K, Baevre H, Abuelo D, Phornphutkul C, Molnes J, Bell GI, Gloyn AL, Hattersley AT, Molven A, Sovik O, Njolstad PR. Permanent neonatal diabetes due to mutations in KCNJ11 encoding Kir6.2: patient characteristics and initial response to sulfonylurea therapy. Diabetes 53: 2713-2718, 2004.
40. 2+ influx in rat pancreatic β cell. Diabetes 41: 438-443, 1992.
41. Schafer G, Portenhauser R, Trolp R. Inhibition of mitochondrial metabolism by the diabetogenic thiadiazine diazoxide. I. Action on succinate dehydrogenase and TCA-cycle oxidations. Biochem Pharmacol 20: 1271-1280, 1971.
42. ATP channel-independent regulation of insulin secretion. J Biol Chem 275: 9270-9277, 2000.
43. Shaner NC, Steinbach PA, Tsien RY. A guide to choosing fluorescent proteins. Nat Methods 2: 905-909, 2005.
44. Shiota C, Larsson O, Shelton KD, Shiota M, Efanov AM, Hoy M, Lindner J, Kooptiwut S, Juntti-Berggren L, Gromada J, Berggren PO, Magnuson MA. Sulfonylurea receptor type 1 knock-out mice have intact feeding-stimulated insulin secretion despite marked impairment in their response to glucose. J Biol Chem 277: 37176-37183, 2002.
45. Stiernet P, Guiot Y, Gilon P, Henquin JC. Glucose acutely decreases ph of secretory granules in mouse pancreatic islets: mechanisms and influence on insulin secretion. J Biol Chem 281: 22142-22151, 2006.
46. 2+ indicator GCaMP2. Proc Natl Acad Sci USA 103: 4753-4758, 2006.
47. + channels in mouse pancreatic β cells: against a role in organelle cation homeostasis. Diabetologia 49: 1567-1577, 2006.
48. Watkins S, Geng X, Li L, Papworth G, Robbins PD, Drain P. Imaging secretory vesicles by fluorescent protein insertion in propetide rather than mature secreted peptide. Traffic 3: 461-471, 2002.
49. Zung A, Glaser B, Nimri R, Zadik Z. Glibenclamide treatment in permanent neonatal diabetes mellitus due to an activating mutation in Kir6.2. J Clin Endocrinol Metab 89: 5504-5507, 2004.
50. + currents. Biochem Pharmacol 67: 1437-1444, 2004.