Pharmacological properties and functional role of Kslow current in mouse pancreatic beta-cells: SK channels contribute to Kslow tail current and modulate insulin secretion

J Gen Physiol. 2005 Oct;126(4):353-63. doi: 10.1085/jgp.200509312.

Abstract

The pharmacological properties of slow Ca(2+)-activated K(+) current (K(slow)) were investigated in mouse pancreatic beta-cells and islets to understand how K(slow) contributes to the control of islet bursting, [Ca(2+)](i) oscillations, and insulin secretion. K(slow) was insensitive to apamin or the K(ATP) channel inhibitor tolbutamide, but UCL 1684, a potent and selective nonpeptide SK channel blocker reduced the amplitude of K(slow) tail current in voltage-clamped mouse beta-cells. K(slow) was also selectively and reversibly inhibited by the class III antiarrythmic agent azimilide (AZ). In isolated beta-cells or islets, pharmacologic inhibition of K(slow) by UCL 1684 or AZ depolarized beta-cell silent phase potential, increased action potential firing, raised [Ca(2+)](i), and enhanced glucose-dependent insulin secretion. AZ inhibition of K(slow) also supported mediation by SK, rather than cardiac-like slow delayed rectifier channels since bath application of AZ to HEK 293 cells expressing SK3 cDNA reduced SK current. Further, AZ-sensitive K(slow) current was extant in beta-cells from KCNQ1 or KCNE1 null mice lacking cardiac slow delayed rectifier currents. These results strongly support a functional role for SK channel-mediated K(slow) current in beta-cells, and suggest that drugs that target SK channels may represent a new approach for increasing glucose-dependent insulin secretion. The apamin insensitivity of beta-cell SK current suggests that beta-cells express a unique SK splice variant or a novel heteromultimer consisting of different SK subunits.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Alkanes / pharmacology
  • Animals
  • Calcium / metabolism
  • Calcium Channel Blockers / pharmacology
  • Cell Line
  • Dose-Response Relationship, Drug
  • Glucose / pharmacology
  • Humans
  • Hydantoins
  • Imidazolidines / pharmacology
  • Insulin / metabolism*
  • Insulin-Secreting Cells / drug effects
  • Insulin-Secreting Cells / metabolism*
  • KCNQ1 Potassium Channel / genetics
  • KCNQ1 Potassium Channel / metabolism
  • Membrane Potentials
  • Mice
  • Mice, Knockout
  • Piperazines / pharmacology
  • Potassium / metabolism*
  • Potassium Channels, Voltage-Gated / genetics
  • Potassium Channels, Voltage-Gated / metabolism
  • Quinolinium Compounds / pharmacology
  • Small-Conductance Calcium-Activated Potassium Channels / drug effects
  • Small-Conductance Calcium-Activated Potassium Channels / genetics
  • Small-Conductance Calcium-Activated Potassium Channels / metabolism*
  • Time Factors
  • Transfection

Substances

  • 6,10-diaza-3(1,3),8(1,4)dibenzena-1,5(1,4)diquinolinacyclodecaphane
  • Alkanes
  • Calcium Channel Blockers
  • Hydantoins
  • Imidazolidines
  • Insulin
  • KCNQ1 Potassium Channel
  • Kcne1 protein, mouse
  • Kcnn3 protein, mouse
  • Piperazines
  • Potassium Channels, Voltage-Gated
  • Quinolinium Compounds
  • Small-Conductance Calcium-Activated Potassium Channels
  • azimilide
  • Glucose
  • Potassium
  • Calcium