Role of KATP channels in glucose-regulated glucagon secretion and impaired counterregulation in type 2 diabetes

Cell Metabolism

Volumn 18, Issue 6, 2013, Pages 871-882

  Zhang, Quan ^a   Ramracheya, Reshma ^a   Lahmann, Carolina ^b   Tarasov, Andrei ^a   Bengtsson, Martin ^a   Braha, Orit ^a   Braun, Matthias ^a   Brereton, Melissa ^b   Collins, Stephan ^a   Galvanovskis, Juris ^b   Gonzalez, Alejandro ^a   Groschner, Lukas N ^a   Rorsman, Nils J G ^a   Salehi, Albert ^a   Travers, Mary E ^a   Walker, Jonathan N ^a   Gloyn, Anna L ^a,c   Gribble, Fiona ^d   Johnson, Paul R V ^a,c   Reimann, Frank ^d   Ashcroft, Frances M ^b   Rorsman, Patrik ^a,c   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c NIHR OXFORD BIOMEDICAL RESEARCH CENTRE   (United Kingdom)

^d ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CALCIUM ION; GLUCOSE; INSULIN; TOLBUTAMIDE; VOLTAGE GATED CHLORIDE CHANNEL; CALCIUM; CALCIUM CHANNEL; GLUCAGON; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; ELECTRIC ACTIVITY; ENZYME INHIBITION; GENE MUTATION; GLUCAGON RELEASE; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERGLYCEMIA; HYPOGLYCEMIA; INSULIN RELEASE; METABOLIC ACTIVATION; METABOLIC INHIBITION; METABOLIC REGULATION; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; ORGAN DONOR; PRIORITY JOURNAL; SUPPRESSOR CELL; WHOLE CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; DONOR; DRUG EFFECTS; EXOCYTOSIS; GENETICS; IN VITRO STUDY; MEMBRANE POTENTIAL; METABOLISM; MUTATION; PANCREAS ISLET ALPHA CELL; PATCH CLAMP TECHNIQUE; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS);

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CALCIUM CHANNELS; DIABETES MELLITUS, TYPE 2; EXOCYTOSIS; GLUCAGON; GLUCAGON-SECRETING CELLS; GLUCOSE; HUMANS; IN VITRO TECHNIQUES; KATP CHANNELS; MEMBRANE POTENTIALS; MICE; MUTATION; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS, INWARDLY RECTIFYING; TISSUE DONORS; TOLBUTAMIDE;

MLCS; MLOWN;

EID: 84889670998     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2013.10.014     Document Type: Article

References (47)

1. S. Barg, J. Galvanovskis, S.O. Göpel, P. Rorsman, and L. Eliasson Tight coupling between electrical activity and exocytosis in mouse glucagon-secreting alpha-cells Diabetes 49 2000 1500 1510
2. J. Berg, Y.P. Hung, and G. Yellen A genetically encoded fluorescent reporter of ATP:ADP ratio Nat. Methods 6 2009 161 166
3. K. Bokvist, H.L. Olsen, M. Hoy, C.F. Gotfredsen, W.F. Holmes, K. Buschard, P. Rorsman, and J. Gromada Characterisation of sulphonylurea and ATP-regulated K+ channels in rat pancreatic A-cells Pflugers Arch. 438 1999 428 436
4. R. Cheng-Xue, A. Gómez-Ruiz, N. Antoine, L.A. Noël, H.Y. Chae, M.A. Ravier, F. Chimienti, F.C. Schuit, and P. Gilon Tolbutamide controls glucagon release from mouse islets differently than glucose: involvement of K(ATP) channels from both α-cells and δ-cells Diabetes 62 2013 1612 1622
5. R.H. Clark, J.S. McTaggart, R. Webster, R. Mannikko, M. Iberl, X.L. Sim, P. Rorsman, M. Glitsch, D. Beeson, and F.M. Ashcroft Muscle dysfunction caused by a KATP channel mutation in neonatal diabetes is neuronal in origin Science 329 2010 458 461
6. P.E. Cryer Hypoglycaemia: the limiting factor in the glycaemic management of Type I and Type II diabetes Diabetologia 45 2002 937 948
7. J. de Heer, C. Rasmussen, D.H. Coy, and J.J. Holst Glucagon-like peptide-1, but not glucose-dependent insulinotropic peptide, inhibits glucagon secretion via somatostatin (receptor subtype 2) in the perfused rat pancreas Diabetologia 51 2008 2263 2270
8. Y.Z. De Marinis, A. Salehi, C.E. Ward, Q. Zhang, F. Abdulkader, M. Bengtsson, O. Braha, M. Braun, R. Ramracheya, and S. Amisten GLP-1 inhibits and adrenaline stimulates glucagon release by differential modulation of N- and L-type Ca2+ channel-dependent exocytosis Cell Metab. 11 2010 543 553
9. P. Detimary, S. Dejonghe, Z. Ling, D. Pipeleers, F. Schuit, and J.C. Henquin 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 1998 33905 33908
10. N.M. Doliba, W. Qin, H. Najafi, C. Liu, C.W. Buettger, J. Sotiris, H.W. Collins, C. Li, C.A. Stanley, and D.F. Wilson Glucokinase activation repairs defective bioenergetics of islets of Langerhans isolated from type 2 diabetics Am. J. Physiol. Endocrinol. Metab. 302 2012 E87 E102
11. B.E. Dunning, J.E. Foley, and B. Ahrén Alpha cell function in health and disease: influence of glucagon-like peptide-1 Diabetologia 48 2005 1700 1713
12. H.Y. Gaisano, P.E. Macdonald, and M. Vranic Glucagon secretion and signaling in the development of diabetes Front. Physiol. 3 2012 349
13. A.L. Gloyn, M.N. Weedon, K.R. Owen, M.J. Turner, B.A. Knight, G. Hitman, M. Walker, J.C. Levy, M. Sampson, and S. Halford Large-scale association studies of variants in genes encoding the pancreatic beta-cell KATP channel subunits Kir6.2 (KCNJ11) and SUR1 (ABCC8) confirm that the KCNJ11 E23K variant is associated with type 2 diabetes Diabetes 52 2003 568 572
14. A.L. Gloyn, E.R. Pearson, J.F. Antcliff, P. Proks, G.J. Bruining, A.S. Slingerland, N. Howard, S. Srinivasan, J.M. Silva, and J. Molnes Activating mutations in the gene encoding the ATP-sensitive potassium-channel subunit Kir6.2 and permanent neonatal diabetes N. Engl. J. Med. 350 2004 1838 1849
15. S.O. Göpel, T. Kanno, S. Barg, and P. Rorsman Patch-clamp characterisation of somatostatin-secreting -cells in intact mouse pancreatic islets J. Physiol. 528 2000 497 507
16. S.O. Göpel, T. Kanno, S. Barg, X.G. Weng, J. Gromada, and P. Rorsman Regulation of glucagon release in mouse -cells by KATP channels and inactivation of TTX-sensitive Na+ channels J. Physiol. 528 2000 509 520
17. S. Göpel, Q. Zhang, L. Eliasson, X.S. Ma, J. Galvanovskis, T. Kanno, A. Salehi, and 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
18. J. Gromada, X. Ma, M. Høy, K. Bokvist, A. Salehi, P.O. Berggren, and P. Rorsman ATP-sensitive K+ channel-dependent regulation of glucagon release and electrical activity by glucose in wild-type and SUR1-/- mouse alpha-cells Diabetes 53 Suppl 3 2004 S181 S189
19. J. Gromada, I. Franklin, and C.B. Wollheim Alpha-cells of the endocrine pancreas: 35 years of research but the enigma remains Endocr. Rev. 28 2007 84 116
20. H. Ishihara, P. Maechler, A. Gjinovci, P.L. Herrera, and C.B. Wollheim Islet beta-cell secretion determines glucagon release from neighbouring alpha-cells Nat. Cell Biol. 5 2003 330 335
21. B. Kailey, M. van de Bunt, P. Johnson, P.E. MacDonald, A.L. Gloyn, P. Rorsman, and M. Braun Subtype 2 is the functionally dominant somatostatin receptor in human pancreatic β- and α-cells Am. J. Physiol. Endocrinol. Metab. 2013
22. D. Kawamori, A.J. Kurpad, J. Hu, C.W. Liew, J.L. Shih, E.L. Ford, P.L. Herrera, K.S. Polonsky, O.P. McGuinness, and R.N. Kulkarni Insulin signaling in alpha cells modulates glucagon secretion in vivo Cell Metab. 9 2009 350 361
23. S.J. Le Marchand, and D.W. Piston Glucose suppression of glucagon secretion: metabolic and calcium responses from alpha-cells in intact mouse pancreatic islets J. Biol. Chem. 285 2010 14389 14398
24. Y.M. Leung, I. Ahmed, L. Sheu, R.G. Tsushima, N.E. Diamant, M. Hara, and H.Y. Gaisano Electrophysiological characterization of pancreatic islet cells in the mouse insulin promoter-green fluorescent protein mouse Endocrinology 146 2005 4766 4775
25. C. Li, C. Liu, I. Nissim, J. Chen, P. Chen, N. Doliba, T. Zhang, I. Nissim, Y. Daikhin, and D. Stokes Regulation of glucagon secretion in normal and diabetic human islets by γ-hydroxybutyrate and glycine J. Biol. Chem. 288 2013 3938 3951
26. P.E. MacDonald, Y.Z. De Marinis, R. Ramracheya, A. Salehi, X. Ma, P.R. Johnson, R. Cox, L. Eliasson, and P. Rorsman A K ATP channel-dependent pathway within alpha cells regulates glucagon release from both rodent and human islets of Langerhans PLoS Biol. 5 2007 e143
27. A. Muñoz, M. Hu, K. Hussain, J. Bryan, L. Aguilar-Bryan, and A.S. Rajan Regulation of glucagon secretion at low glucose concentrations: evidence for adenosine triphosphate-sensitive potassium channel involvement Endocrinology 146 2005 5514 5521
28. H.L. Olsen, S. Theander, K. Bokvist, K. Buschard, C.B. Wollheim, and J. Gromada Glucose stimulates glucagon release in single rat alpha-cells by mechanisms that mirror the stimulus-secretion coupling in beta-cells Endocrinology 146 2005 4861 4870
29. N. Quoix, R. Cheng-Xue, L. Mattart, Z. Zeinoun, Y. Guiot, M.C. Beauvois, J.C. Henquin, and P. Gilon Glucose and pharmacological modulators of ATP-sensitive K+ channels control [Ca2+]c by different mechanisms in isolated mouse alpha-cells Diabetes 58 2009 412 421
30. R. Ramracheya, C. Ward, M. Shigeto, J.N. Walker, S. Amisten, Q. Zhang, P.R. Johnson, P. Rorsman, and M. Braun Membrane potential-dependent inactivation of voltage-gated ion channels in alpha-cells inhibits glucagon secretion from human islets Diabetes 59 2010 2198 2208
31. M.A. Ravier, and G.A. Rutter Glucose or insulin, but not zinc ions, inhibit glucagon secretion from mouse pancreatic alpha-cells Diabetes 54 2005 1789 1797
32. M.S. Remedi, and C.G. Nichols Hyperinsulinism and diabetes: genetic dissection of beta cell metabolism-excitation coupling in mice Cell Metab. 10 2009 442 453
33. D. Rudman, D.E. Mattson, A.G. Feller, R. Cotter, and R.C. Johnson Fasting plasma amino acids in elderly men Am. J. Clin. Nutr. 49 1989 559 566
34. C. Schwanstecher, U. Meyer, and M. Schwanstecher K(IR)6.2 polymorphism predisposes to type 2 diabetes by inducing overactivity of pancreatic beta-cell ATP-sensitive K(+) channels Diabetes 51 2002 875 879
35. S. Seino, T. Shibasaki, and K. Minami Dynamics of insulin secretion and the clinical implications for obesity and diabetes J. Clin. Invest. 121 2011 2118 2125
36. S.M. Sherck, M. Shiota, J. Saccomando, S. Cardin, E.J. Allen, J.R. Hastings, D.W. Neal, P.E. Williams, and A.D. Cherrington Pancreatic response to mild non-insulin-induced hypoglycemia does not involve extrinsic neural input Diabetes 50 2001 2487 2496
37. C. Shiota, J.V. Rocheleau, M. Shiota, D.W. Piston, and M.A. Magnuson Impaired glucagon secretory responses in mice lacking the type 1 sulfonylurea receptor Am. J. Physiol. Endocrinol. Metab. 289 2005 E570 E577
38. A.I. Tarasov, F. Semplici, M.A. Ravier, E.A. Bellomo, T.J. Pullen, P. Gilon, I. Sekler, R. Rizzuto, and G.A. Rutter The mitochondrial Ca2+ uniporter MCU is essential for glucose-induced ATP increases in pancreatic beta-cells PloS One 7 2012 e39722
39. F. Thorel, N. Damond, S. Chera, A. Wiederkehr, B. Thorens, P. Meda, C.B. Wollheim, and P.L. Herrera Normal glucagon signaling and β-cell function after near-total α-cell ablation in adult mice Diabetes 60 2011 2872 2882
40. O. Tschritter, M. Stumvoll, F. Machicao, M. Holzwarth, M. Weisser, E. Maerker, A. Teigeler, H. Häring, and A. Fritsche The prevalent Glu23Lys polymorphism in the potassium inward rectifier 6.2 (KIR6.2) gene is associated with impaired glucagon suppression in response to hyperglycemia Diabetes 51 2002 2854 2860
41. R.H. Unger, and A.D. Cherrington Glucagonocentric restructuring of diabetes: a pathophysiologic and therapeutic makeover J. Clin. Invest. 122 2012 4 12
42. R.H. Unger, and L. Orci Paracrinology of islets and the paracrinopathy of diabetes Proc. Natl. Acad. Sci. USA 107 2010 16009 16012
43. E. Vieira, A. Salehi, and E. Gylfe Glucose inhibits glucagon secretion by a direct effect on mouse pancreatic alpha cells Diabetologia 50 2007 370 379
44. J.N. Walker, R. Ramracheya, Q. Zhang, P.R. Johnson, M. Braun, and P. Rorsman Regulation of glucagon secretion by glucose: paracrine, intrinsic or both? Diabetes Obes. Metab. 13 Suppl 1 2011 95 105
45. J.T. Yue, E. Burdett, D.H. Coy, A. Giacca, S. Efendic, and M. Vranic Somatostatin receptor type 2 antagonism improves glucagon and corticosterone counterregulatory responses to hypoglycemia in streptozotocin-induced diabetic rats Diabetes 61 2012 197 207
46. Q. Zhang, M. Bengtsson, C. Partridge, A. Salehi, M. Braun, R. Cox, L. Eliasson, P.R. Johnson, E. Renström, and T. Schneider R-type Ca(2+)-channel-evoked CICR regulates glucose-induced somatostatin secretion Nat. Cell Biol. 9 2007 453 460
47. Q. Zhang, J. Galvanovskis, F. Abdulkader, C.J. Partridge, S.O. Gopel, L. Eliasson, and P. Rorsman Cell coupling in mouse pancreatic beta-cells measured in intact islets of Langerhans Philos. Transact. A Math. Phys. Eng. Sci. 366 2008 3503 3523