Home LiteratureArticle Details
PMID: 10578013 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Activation of Ca(2+)-dependent K(+) channels contributes to rhythmic firing of action potentials in mouse pancreatic beta cells.

The Journal of general physiology ·Vol. 114 ·No. 6 ·1999-12-00 ·Pages 759-70

Göpel SO, Kanno T, Barg S, Eliasson L, Galvanovskis J, Renström E, Rorsman P

Abstract

We have applied the perforated patch whole-cell technique to beta cells within intact pancreatic islets to identify the current underlying the glucose-induced rhythmic firing of action potentials. Trains of depolarizations (to simulate glucose-induced electrical activity) resulted in the gradual (time constant: 2.3 s) development of a small (<0.8 nS) K(+) conductance. The current was dependent on Ca(2+) influx but unaffected by apamin and charybdotoxin, two blockers of Ca(2+)-activated K(+) channels, and was insensitive to tolbutamide (a blocker of ATP-regulated K(+) channels) but partially (>60%) blocked by high (10-20 mM) concentrations of tetraethylammonium. Upon cessation of electrical stimulation, the current deactivated exponentially with a time constant of 6.5 s. This is similar to the interval between two successive bursts of action potentials. We propose that this Ca(2+)-activated K(+) current plays an important role in the generation of oscillatory electrical activity in the beta cell.

MeSH Terms
ATP-Binding Cassette Transporters Action Potentials/physiology Animals Electrophysiology Hypoglycemic Agents/pharmacology In Vitro Techniques Islets of Langerhans/physiology KATP Channels Large-Conductance Calcium-Activated Potassium Channels Membrane Potentials/physiology Mice Patch-Clamp Techniques Potassium Channel Blockers Potassium Channels/agonists,metabolism,physiology Potassium Channels, Calcium-Activated Potassium Channels, Inwardly Rectifying Tolbutamide/pharmacology
Chemicals
ATP-Binding Cassette Transporters Hypoglycemic Agents KATP Channels Large-Conductance Calcium-Activated Potassium Channels Potassium Channel Blockers Potassium Channels Potassium Channels, Calcium-Activated Potassium Channels, Inwardly Rectifying uK-ATP-1 potassium channel Tolbutamide
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Göpel S O
Department of Physiological Sciences, Division of Molecular and Cellular Physiology, Lund University, SE-223 62 Lund, Sweden.
Kanno T
Barg S
Eliasson L
Galvanovskis J
Renström E
Rorsman P
References (38)
38 references, click to expand
  1. Voltage-gated and resting membrane currents recorded from B-cells in intact mouse pancreatic islets.
    J Physiol. 1999 Dec 15;521 Pt 3:717-28 PMID: 10601501
  2. Glucose-induced cycles of insulin release can be resolved into distinct periods of secretory activity.
    Biochem Biophys Res Commun. 1993 May 14;192(3):1182-8 PMID: 8507191
  3. Mouse pancreatic beta-cells: tetraethylammonium blockage of the potassium permeability increase induced by depolarization.
    J Physiol. 1979 Mar;288:561-74 PMID: 381635
  4. Properties of the Ca-activated K+ channel in pancreatic beta-cells.
    Cell Calcium. 1983 Dec;4(5-6):451-61 PMID: 6323007
  5. Exocytosis elicited by action potentials and voltage-clamp calcium currents in individual mouse pancreatic B-cells.
    J Physiol. 1993 Dec;472:665-88 PMID: 8145165
  6. Endoplasmic reticulum calcium store regulates membrane potential in mouse islet beta-cells.
    J Biol Chem. 1994 May 20;269(20):14359-62 PMID: 8182038
  7. Co-localization of L-type Ca2+ channels and insulin-containing secretory granules and its significance for the initiation of exocytosis in mouse pancreatic B-cells.
    EMBO J. 1995 Jan 3;14(1):50-7 PMID: 7828595
  8. Magnitude and modulation of pancreatic beta-cell gap junction electrical conductance in situ.
    J Membr Biol. 1995 Jul;146(2):163-76 PMID: 7473686
  9. Oscillations in KATP channel activity promote oscillations in cytoplasmic free Ca2+ concentration in the pancreatic beta cell.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):5161-5 PMID: 8643546
  10. Contributions of modeling to understanding stimulus-secretion coupling in pancreatic beta-cells.
    Am J Physiol. 1996 Aug;271(2 Pt 1):E362-72 PMID: 8770032
  11. Crosstalk between the cAMP and inositol trisphosphate-signalling pathways in pancreatic beta-cells.
    Arch Biochem Biophys. 1996 Oct 15;334(2):295-302 PMID: 8900404
  12. Oscillation of gap junction electrical coupling in the mouse pancreatic islets of Langerhans.
    J Physiol. 1997 Feb 1;498 ( Pt 3):753-61 PMID: 9051586
  13. Characterization of a Ca2+-activated K+ current in insulin-secreting murine betaTC-3 cells.
    J Physiol. 1998 Jun 1;509 ( Pt 2):355-70 PMID: 9575286
  14. In situ activation of the type 2 ryanodine receptor in pancreatic beta cells requires cAMP-dependent phosphorylation.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):6145-50 PMID: 9600932
  15. Control of pulsatile 5-HT/insulin secretion from single mouse pancreatic islets by intracellular calcium dynamics.
    J Physiol. 1998 Jul 1;510 ( Pt 1):135-43 PMID: 9625872
  16. Interplay between cytoplasmic Ca2+ and the ATP/ADP ratio: a feedback control mechanism in mouse pancreatic islets.
    Biochem J. 1998 Jul 15;333 ( Pt 2):269-74 PMID: 9657965
  17. Selective activation of Ca2+-activated K+ channels by co-localized Ca2+ channels in hippocampal neurons.
    Nature. 1998 Oct 29;395(6705):900-5 PMID: 9804423
  18. Significance of ionic fluxes and changes in membrane potential for stimulus-secretion coupling in pancreatic B-cells.
    Experientia. 1984 Oct 15;40(10):1043-52 PMID: 6386515
  19. IgE-mediated degranulation of mast cells does not require opening of ion channels.
    Nature. 1986 Jan 9-15;319(6049):150-3 PMID: 2417125
  20. Calcium and delayed potassium currents in mouse pancreatic beta-cells under voltage-clamp conditions.
    J Physiol. 1986 May;374:531-50 PMID: 2427706
  21. Muscarinic activation of ionic currents measured by a new whole-cell recording method.
    J Gen Physiol. 1988 Aug;92(2):145-59 PMID: 2459299
  22. Modulation of the bursting properties of single mouse pancreatic beta-cells by artificial conductances.
    Biophys J. 1999 Mar;76(3):1423-35 PMID: 10049324
  23. Uptake and release of Ca2+ by the endoplasmic reticulum contribute to the oscillations of the cytosolic Ca2+ concentration triggered by Ca2+ influx in the electrically excitable pancreatic B-cell.
    J Biol Chem. 1999 Jul 16;274(29):20197-205 PMID: 10400636
  24. Small-conductance calcium-activated potassium channels.
    Ann N Y Acad Sci. 1999 Apr 30;868:370-8 PMID: 10414306
  25. ATP-sensitive K+ channels may control glucose-induced electrical activity in pancreatic B-cells.
    Biochem Biophys Res Commun. 1988 Oct 31;156(2):769-75 PMID: 3056403
  26. Simultaneous recordings of glucose dependent electrical activity and ATP-regulated K(+)-currents in isolated mouse pancreatic beta-cells.
    FEBS Lett. 1990 Feb 12;261(1):187-90 PMID: 2407553
  27. Effects of external tetraethylammonium ions and quinine on delayed rectifying K+ channels in mouse pancreatic beta-cells.
    J Physiol. 1990 Apr;423:311-25 PMID: 2201760
  28. Block of ATP-regulated and Ca2(+)-activated K+ channels in mouse pancreatic beta-cells by external tetraethylammonium and quinine.
    J Physiol. 1990 Apr;423:327-42 PMID: 2201761
  29. Role of voltage- and Ca2(+)-dependent K+ channels in the control of glucose-induced electrical activity in pancreatic B-cells.
    Pflugers Arch. 1990 Jul;416(5):568-72 PMID: 2235297
  30. Electrophysiology of the pancreatic beta-cell.
    Prog Biophys Mol Biol. 1989;54(2):87-143 PMID: 2484976
  31. Specificity of tetraethylammonium and quinine for three K channels in insulin-secreting cells.
    J Membr Biol. 1991 Mar;120(2):105-14 PMID: 2072381
  32. Low access resistance perforated patch recordings using amphotericin B.
    J Neurosci Methods. 1991 Mar;37(1):15-26 PMID: 2072734
  33. Widespread synchronous [Ca2+]i oscillations due to bursting electrical activity in single pancreatic islets.
    Pflugers Arch. 1991 May;418(4):417-22 PMID: 1876486
  34. Inositol trisphosphate-dependent periodic activation of a Ca(2+)-activated K+ conductance in glucose-stimulated pancreatic beta-cells.
    Nature. 1991 Oct 31;353(6347):849-52 PMID: 1719424
  35. Pancreatic B cells are bursting, but how?
    Trends Neurosci. 1991 Sep;14(9):411-4 PMID: 1720583
  36. Cytoplasmic calcium transients due to single action potentials and voltage-clamp depolarizations in mouse pancreatic B-cells.
    EMBO J. 1992 Aug;11(8):2877-84 PMID: 1639061
  37. Demonstration of a novel apamin-insensitive calcium-activated K+ channel in mouse pancreatic B cells.
    Pflugers Arch. 1993 Feb;422(5):443-8 PMID: 8474849
  38. Electrical activity in pancreatic islet cells.
    Nature. 1968 Jul 27;219(5152):389-90 PMID: 4873864
Article Info
Journal
The Journal of general physiology
Abbr.
J Gen Physiol
ISSN
0022-1295
Published
1999-12-00
Pages
759-70
Language
English
Region
United States
NLM ID
2985110R
PMCID
PMC2230648
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com