Phosphorylation of the IKs channel complex inhibits drug block: novel mechanism underlying variable antiarrhythmic drug actions

Circulation. 2003 Jul 15;108(2):132-4. doi: 10.1161/01.CIR.0000082708.86266.B8. Epub 2003 Jun 30.

Abstract

Background: IKs, an important repolarizing current in heart, is an antiarrhythmic drug target and is markedly increased by activation of protein kinase A (PKA; eg, by beta-adrenergic stimulation). Because beta-adrenergic stimulation is a frequent trigger of arrhythmias, we hypothesized that PKA stimulation inhibits drug block.

Methods and results: CHO cells were transfected with KCNQ1 cDNA (encoding the pore-forming subunit) with or without the ancillary subunit KCNE1. IC50 for quinidine block of basal IKs was 5.8+/-1.2 micromol/L, versus 19.9+/-3.2 micromol/L (P<0.01) for PKA-stimulated current. A similar >3-fold shift was apparent in the absence of KCNE1 and with the IKs-specific blocker chromanol 293B. The first current recorded after channels were held at rest and exposed to the drug was reduced approximately 40%, and further depolarizations increased the block with a time constant (tau) of 181+/-27 seconds. By contrast, PKA-stimulated channels displayed a <5% first-pulse block and much slower block development (tau=405+/-85 seconds). Alanine substitution at 3 potential PKA target sites (S27, S468, and T470) generated an IKs that did not increase with PKA stimulation; this mutant retained wild-type drug sensitivity that was unaffected by PKA.

Conclusions: Activation of this key intracellular signaling pathway blunts drug block. The onset of block and the data with the PKA-resistant mutant support the concept that phosphorylation of the KCNQ1 subunit directly modulates drug access to a binding site on the channel. These data identify a novel mechanism for modulation of drug-channel interactions that may be especially important during beta-adrenergic stimulation.

Publication types

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

MeSH terms

  • Adrenergic alpha-Antagonists / pharmacology
  • Amino Acid Substitution
  • Animals
  • Anti-Arrhythmia Agents / pharmacology*
  • Arrhythmias, Cardiac / drug therapy*
  • CHO Cells
  • Cricetinae
  • Cyclic AMP-Dependent Protein Kinases / drug effects
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Dose-Response Relationship, Drug
  • Drug Interactions
  • Female
  • KCNQ Potassium Channels
  • KCNQ1 Potassium Channel
  • Macromolecular Substances
  • Ovary / cytology
  • Ovary / metabolism
  • Phosphorylation / drug effects
  • Potassium Channels / drug effects*
  • Potassium Channels / genetics
  • Potassium Channels / metabolism*
  • Potassium Channels, Voltage-Gated*
  • Quinidine / pharmacology
  • Structure-Activity Relationship
  • Transfection

Substances

  • Adrenergic alpha-Antagonists
  • Anti-Arrhythmia Agents
  • KCNQ Potassium Channels
  • KCNQ1 Potassium Channel
  • Macromolecular Substances
  • Potassium Channels
  • Potassium Channels, Voltage-Gated
  • Cyclic AMP-Dependent Protein Kinases
  • Quinidine