Block of K v1.7 potassium currents increases glucose-stimulated insulin secretion

EMBO Molecular Medicine

Volumn 4, Issue 5, 2012, Pages 424-434

  Finol Urdaneta, Rocio K ^a,b   Remedi, Maria S ^c   Raasch, Walter ^d   Becker, Stefan ^e   Clark, Robert B ^a   Strüver, Nina ^a   Pavlov, Evgeny ^a   Nichols, Colin G ^c   French, Robert J ^a   Terlau, Heinrich ^b,d,f  

^a UNIVERSITY OF CALGARY   (Canada)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF LÜBECK   (Germany)

^e MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^f UNIVERSITY OF KIEL   (Germany)

Author keywords

Conkunitzin S1; Electrical signalling; GSIS; Pancreas; Potassium channels

Indexed keywords

CALCIUM; CONKUNITZIN S1; GLUCOSE; INSULIN; TOXIN; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL KV1.7;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CONUS SNAIL; CYTOPLASM; HYPOGLYCEMIA; INSULIN RELEASE; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; REPOLARIZATION;

ANIMALS; BODILY SECRETIONS; GLUCOSE; HUMANS; INSULIN; MALE; MOLLUSK VENOMS; POTASSIUM; RATS; RATS, WISTAR; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS;

EID: 84860524643     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201200218     Document Type: Article

References (42)

1. Amiel SA, Dixon T, Mann R, Jameson K (2008) Hypoglycaemia in Type 2 diabetes. Diab Med 25: 245-254.
2. Anubhuti V Arora S (2008) Leptin and its metabolic interactions: an update. Diabetes Obes Metab 10: 973-993.
3. Ashcroft FM, Rorsman P (1989) Electrophysiology of the pancreatic beta-cell. Prog Biophys Mol Biol 54: 87-143.
4. Bardien-Kruger S, Wulff H, Arieff Z, Brink P, Chandy KG, Corfield V (2002) Characterisation of the human voltage-gated potassium channel gene, KCNA7, a candidate gene for inherited cardiac disorders, and its exclusion as cause of progressive familial heart block I (PFHBI). Eur J Hum Genet 10: 36-43.
5. Bayrhuber M, Vijayan V, Ferber M, Graf R, Korukottu J, Imperial J, Garrett JE, Olivera BM, Terlau H, Zweckstetter M, et al (2005) Conkunitzin-S1 is the first member of a new Kunitz-type neurotoxin family. Structural and functional characterization. J Biol Chem 280: 23766-23770.
6. Bayrhuber M, Graf R, Ferber M, Zweckstetter M, Imperial J, Garrett JE, Olivera BM, Terlau H, Becker S (2006) Production of recombinant Conkunitzin-S1 in Escherichia coli. Protein Expr Purif 47: 640-644.
7. Braun M, Ramracheya R, Bengtsson M, Zhang Q, Karanauskaite J, Partridge C, Johnson PR, Rorsman P (2008) Voltage-gated ion channels in human pancreatic beta-cells: electrophysiological characterization and role in insulin secretion. Diabetes 57: 1618-1628.
8. Bryan J, Crane A, Vila-Carriles WH, Babenko AP, Aguilar-Bryan L (2005) Insulin secretagogues, sulfonylurea receptors and K(ATP) channels. Curr Pharm Des 11: 2699-2716.
9. Chen P, Dendorfer A, Finol-Urdaneta RK, Terlau H, Olivera BM (2010) Biochemical characterization of kappaM-RIIIJ, a Kv1.2 channel blocker: evaluation of cardioprotective effects of kappaM-conotoxins. J Biol Chem 285: 14882-14889.
10. Elayat AA, El-Naggar MM, Tahir M (1995) An immunocytochemical and morphometric study of the rat pancreatic islets. J Anat 186: 629-637.
11. Finol-Urdaneta RK, Struver N, Terlau H (2006) Molecular and functional differences between heart mKv1.7 channel isoforms. J Gen Physiol 128: 133-145.
12. Gillespie JS, Muir TC (1967) A method of stimulating the complete sympathetic outflow from the spinal cord to blood vessels in the pithed rat. Br J Pharmacol Chemother 30: 78-87.
13. Gossett WS, (1958) New tables for testing the significance of observations, In: "Student's" Collected Papers, Pearson ES and Wishart J (eds), Cambridge, University Press: p. 115-120.
14. Hardy A. B, Fox JE, Giglou PR, Wijesekara N, Bhattacharjee A, Sultan S, Gyulkhandanyan AV, Gaisano HY, Macdonald PE, Wheeler MB (2009) Characterization of Erg K+ channels in alpha- and beta-cells of mouse and human islets. J Biol Chem 284: 30441-30452.
15. Herrington J (2007) Gating modifier peptides as probes of pancreatic beta-cell physiology. Toxicon 49: 231-238.
16. Herrington J, Sanchez M, Wunderler D, Yan L, Bugianesi RM, Dick IE, Clark SA, Brochu RM, Priest BT, Kohler MG, et al (2005) Biophysical and pharmacological properties of the voltage-gated potassium current of human pancreatic beta-cells. J Physiol 567: 159-175.
17. Herrington J, Zhou YP, Bugianesi RM, Dulski PM, Feng Y, Warren VA, Smith MM, Kohler MG, Garsky VM, Sanchez M, et al (2006) Blockers of the delayed-rectifier potassium current in pancreatic beta-cells enhance glucose-dependent insulin secretion. Diabetes 55: 1034-1042.
18. Hiriart M, Aguilar-Bryan L (2008) Channel regulation of glucose sensing in the pancreatic beta-cell. Am J Physiol Endocrinol Metab 295: E1298-E1306.
19. Horn R, Marty A (1988) Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92: 145-159.
20. Houamed KM, Sweet IR, Satin LS (2010) BK channels mediate a novel ionic mechanism that regulates glucose-dependent electrical activity and insulin secretion in mouse pancreatic beta-cells. J Physiol 588: 3511-3523.
21. Jacobson DA, Philipson LH (2007) Action potentials and insulin secretion: new insights into the role of Kv channels. Diabetes Obes Metab 9: 89-98.
22. Jacobson DA, Kuznetsov A, Lopez JP, Kash S, Ammala CE, Philipson LH (2007) Kv2.1 ablation alters glucose-induced islet electrical activity, enhancing insulin secretion. Cell Metab 6: 229-235.
23. Jacobson DA, Mendez F, Thompson M, Torres J, Cochet O, Philipson LH (2010) Calcium-activated and voltage-gated potassium channels of the pancreatic islet impart distinct and complementary roles during secretagogue induced electrical responses. J Physiol 588: 3525-3537.
24. Kalman K, Nguyen A, Tseng-Crank J, Dukes ID, Chandy G, Hustad CM, Copeland NG, Jenkins NA, Mohrenweiser H, Brandriff B, et al (1998) Genomic organization, chromosomal localization, tissue distribution, and biophysical characterization of a novel mammalian Shaker-related voltage-gated potassium channel, Kv1.7. J Biol Chem 273: 5851-5857.
25. Kashuba VI, Kvasha SM, Protopopov AI, Gizatullin RZ, Rynditch AV, Wahlestedt C, Wasserman WW, Zabarovsky ER (2001) Initial isolation and analysis of the human Kv1.7 (KCNA7) gene, a member of the voltage-gated potassium channel gene family. Gene 268: 115-122.
26. Katsuta H, Akashi T, Katsuta R, Nagaya M, Kim D, Arinobu Y, Hara M, Bonner-Weir S, Sharma AJ, Akashi K, et al (2010) Single pancreatic beta cells co-express multiple islet hormone genes in mice. Diabetologia 53: 128-138.
27. Kinard TA, de VG, Sherman A, Satin LS (1999) Modulation of the bursting properties of single mouse pancreatic beta-cells by artificial conductances. Biophys J 76: 1423-1435.
28. Liman ER, Tytgat J, Hess P (1992) Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs. Neuron 9: 861-871.
29. Macdonald PE, Ha XF, Wang J, Smukler SR, Sun AM, Gaisano HY, Salapatek AM, Backx PH, Wheeler MB (2001) Members of the Kv1 and Kv2 voltage-dependent K(+) channel families regulate insulin secretion. Mol Endocrinol 15: 1423-1435.
30. Muller H, Schweitzer N, Johren O, Dominiak P, Raasch W (2007) Angiotensin II stimulates the reactivity of the pituitary-adrenal axis in leptin-resistant Zucker rats, thereby influencing the glucose utilization. Am J Physiol Endocrinol Metab 293: E802-E810.
31. Pedersen MG (2010) A biophysical model of electrical activity in human β-cells. Biophys J 99: 3200-3207.
32. Proks P, Reimann F, Green N, Gribble F, Ashcroft F (2002) Sulfonylurea stimulation of insulin secretion. Diabetes 51: S368-S376.
33. Remedi MS, Koster JC, Markova K, Seino S, Miki T, Patton BL, McDaniel ML, Nichols CG (2004) Diet-induced glucose intolerance in mice with decreased beta-cell ATP-sensitive K+ channels. Diabetes 53: 3159-3167.
34. Remedi MS, Rocheleau JV, Tong A, Patton BL, McDaniel ML, Piston DW, Koster JC, Nichols CG (2006) Hyperinsulinism in mice with heterozygous loss of K(ATP) channels. Diabetologia 49: 2368-2378.
35. Rosati B, Marchetti P, Crociani O, Lecchi M, Lupi R, Arcangeli A, Olivotto M, Wanke E (2000) Glucose- and arginine-induced insulin secretion by human pancreatic beta-cells: the role of HERG K(+) channels in firing and release. FASEB J 14: 2601-2610.
36. Smith PA, Bokvist K, Arkhammar P, Berggren PO, Rorsman P (1990) Delayed rectifying and calcium-activated K+ channels and their significance for action potential repolarization in mouse pancreatic beta-cells. J Gen Physiol 95: 1041-1059.
37. Smolen P, Rinzel J, Sherman A (1993) Why pancreatic islets burst but single beta cells do not. The heterogeneity hypothesis. Biophys J 64: 1668-1680.
38. Stahl M, Berger W (1999) Higher incidence of severe hypoglycaemia leading to hospital admission in Type 2 diabetic patients treated with long-acting versus short-acting sulphonylureas. Diab Med 16: 586-590.
39. Terlau H, Olivera BM (2004) Conus venoms: a rich source of novel ion channel-targeted peptides. Physiol Rev 84: 41-68.
40. Wagner TF, Loch S, Lambert S, Straub I, Mannebach S, Mathar I, Dufer M, Lis A, Flockerzi V, Philipp SE, et al (2008) Transient receptor potential M3 channels are ionotropic steroid receptors in pancreatic beta cells. Nat Cell Biol 10: 1421-1430.
41. Yan L, Figueroa DJ, Austin CP, Liu Y, Bugianesi RM, Slaughter RS, Kaczorowski GJ, Kohler MG (2004) Expression of voltage-gated potassium channels in human and rhesus pancreatic islets. Diabetes 53: 597-607.
42. Zhang J, Pfaffendorf M, van Zwieten PA (1993) Positive inotropic action of angiotensin II in the pithed rat. Naunyn Schmiedebergs Arch Pharmacol 347: 658-663.