The residue I257 at S4-S5 linker in KCNQ1 determines KCNQ1/KCNE1 channel sensitivity to 1-alkanols

Acta Pharmacol Sin. 2016 Jan;37(1):124-33. doi: 10.1038/aps.2015.133.

Abstract

Aim: KCNQ1 and KCNE1 form a complex in human ventricular cardiomyocytes, which are important in maintaining a normal heart rhythm. In the present study we investigated the effects of a homologous series of 1-alkanols on KCNQ1/KCNE1 channels expressed in Xenopus oocytes.

Methods: ECG recording was made in rats injected with ethanol-containing solution (0.3 mL, ip). Human KCNQ1 channel and its auxiliary subunit KCNE1 were heterologously coexpressed in Xenopus oocytes, which were superfused with ND96 solution; 1-alkanols (ethanol, 1-butanol and 1-hexanol) were delivered through a gravity-driven perfusion device. The slow-delayed rectifier potassium currents IKs (KCNQ1/KCNE1 currents) were recorded using a two-electrode voltage clamp method. Site-directed mutations (I257A) were made in KCNQ1.

Results: In ECG recordings, a low concentration of ethanol (3%, v/v) slightly increased the heart rate of rats, whereas the higher concentrations of ethanol (10%, 50%, v/v) markedly reduced it. In oocytes coexpressing KCNQ1/KCNE1 channels, ethanol, 1-butanol and 1-hexanol dose-dependently inhibited IKs currents with IC50 values of 80, 11 and 2.7 mmol/L, respectively. Furthermore, the 1-alkanols blocked the KCNQ1 channel in both open and closed states, and a four-state model could adequately explain the effects of 1-alkanols on the closed-state channel block. Moreover, the mutation of I257A at the intracellular loop between S4 and S5 in KCNQ1 greatly decreased the sensitivity to 1-alkanols; and the IC50 values of ethanol, 1-butanol and 1-hexanol were increased to 634, 414 and 7.4 mmol/L, respectively. The mutation also caused the ablation of closed-state channel block.

Conclusion: These findings provide new insight into the intricate mechanisms of the blocking effects of ethanol on the KCNQ1 channel.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 1-Butanol / pharmacology*
  • Animals
  • Electrocardiography
  • Ethanol / pharmacology*
  • Female
  • Heart Rate / drug effects
  • Hexanols / pharmacology*
  • Ion Channel Gating
  • KCNQ1 Potassium Channel / antagonists & inhibitors
  • KCNQ1 Potassium Channel / genetics
  • KCNQ1 Potassium Channel / metabolism*
  • Male
  • Models, Biological
  • Mutation
  • Oocytes / metabolism
  • Potassium Channels, Voltage-Gated / antagonists & inhibitors
  • Potassium Channels, Voltage-Gated / genetics
  • Potassium Channels, Voltage-Gated / metabolism*
  • Rats, Wistar
  • Structure-Activity Relationship
  • Xenopus laevis

Substances

  • Hexanols
  • KCNE1 protein, human
  • KCNQ1 Potassium Channel
  • KCNQ1 protein, human
  • Potassium Channels, Voltage-Gated
  • Ethanol
  • 1-hexanol
  • 1-Butanol