Stereoselective block of the hERG potassium channel by the Class Ia antiarrhythmic drug disopyramide

Cell Mol Life Sci. 2024 Nov 28;81(1):466. doi: 10.1007/s00018-024-05498-4.

Abstract

Potassium channels encoded by human Ether-à-go-go-Related Gene (hERG) are inhibited by diverse cardiac and non-cardiac drugs. Disopyramide is a chiral Class Ia antiarrhythmic that inhibits hERG at clinical concentrations. This study evaluated effects of disopyramide enantiomers on hERG current (IhERG) from hERG expressing HEK 293 cells at 37 °C. S(+) and R(-) disopyramide inhibited wild-type (WT) IhERG with IC50 values of 3.9 µM and 12.9 µM respectively. The attenuated-inactivation mutant N588K had little effect on the action of S(+) disopyramide but the IC50 for the R(-) enantiomer was ~ 15-fold that for S(+) disopyramide. The enhanced inactivation mutant N588E only slightly increased the potency of R(-) disopyramide. S6 mutation Y652A reduced S(+) disopyramide potency more than that of R(-) disopyramide (respective IC50 values ~ 49-fold and 11-fold their WT controls). The F656A mutation also exerted a stronger effect on S(+) than R(-) disopyramide, albeit with less IC50 elevation. A WT-Y652A tandem dimer exhibited a sensitivity to the enantiomers that was intermediate between that of WT and Y652A, suggesting Y652 groups on adjacent subunits contribute to the binding. Moving the Y (normally at site 652) one residue in the N- terminal (up) direction in N588K hERG markedly increased the blocking potency of R(-) disopyramide. Molecular dynamics simulations using a hERG pore model produced different binding modes for S(+) and R(-) disopyramide consistent with the experimental observations. In conclusion, S(+) disopyramide interacts more strongly with S6 aromatic binding residues on hERG than does R(-) disopyramide, whilst optimal binding of the latter is more reliant on intact inactivation.

Keywords: Disopyramide; Enantiomer; HERG; Long QT; QT interval; Stereoselectivity.

MeSH terms

  • Anti-Arrhythmia Agents* / chemistry
  • Anti-Arrhythmia Agents* / pharmacology
  • Disopyramide* / chemistry
  • Disopyramide* / metabolism
  • Disopyramide* / pharmacology
  • ERG1 Potassium Channel / antagonists & inhibitors
  • ERG1 Potassium Channel / genetics
  • ERG1 Potassium Channel / metabolism
  • Ether-A-Go-Go Potassium Channels / antagonists & inhibitors
  • Ether-A-Go-Go Potassium Channels / genetics
  • Ether-A-Go-Go Potassium Channels / metabolism
  • HEK293 Cells
  • Humans
  • Mutation
  • Potassium Channel Blockers / chemistry
  • Potassium Channel Blockers / metabolism
  • Potassium Channel Blockers / pharmacology
  • Stereoisomerism

Substances

  • Disopyramide
  • Anti-Arrhythmia Agents
  • Ether-A-Go-Go Potassium Channels
  • Potassium Channel Blockers
  • ERG1 Potassium Channel