Using lidocaine and benzocaine to link sodium channel molecular conformations to state-dependent antiarrhythmic drug affinity

Circ Res. 2009 Aug 28;105(5):492-9. doi: 10.1161/CIRCRESAHA.109.198572. Epub 2009 Aug 6.

Abstract

Rationale: Lidocaine and other antiarrhythmic drugs bind in the inner pore of voltage-gated Na channels and affect gating use-dependently. A phenylalanine in domain IV, S6 (Phe1759 in Na(V)1.5), modeled to face the inner pore just below the selectivity filter, is critical in use-dependent drug block.

Objective: Measurement of gating currents and concentration-dependent availability curves to determine the role of Phe1759 in coupling of drug binding to the gating changes.

Methods and results: The measurements showed that replacement of Phe1759 with a nonaromatic residue permits clear separation of action of lidocaine and benzocaine into 2 components that can be related to channel conformations. One component represents the drug acting as a voltage-independent, low-affinity blocker of closed channels (designated as lipophilic block), and the second represents high-affinity, voltage-dependent block of open/inactivated channels linked to stabilization of the S4s in domains III and IV (designated as voltage-sensor inhibition) by Phe1759. A homology model for how lidocaine and benzocaine bind in the closed and open/inactivated channel conformation is proposed.

Conclusions: These 2 components, lipophilic block and voltage-sensor inhibition, can explain the differences in estimates between tonic and open-state/inactivated-state affinities, and they identify how differences in affinity for the 2 binding conformations can control use-dependence, the hallmark of successful antiarrhythmic drugs.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Anti-Arrhythmia Agents / chemistry
  • Anti-Arrhythmia Agents / metabolism
  • Anti-Arrhythmia Agents / pharmacology*
  • Benzocaine / chemistry
  • Benzocaine / metabolism
  • Benzocaine / pharmacology*
  • Binding Sites
  • Cell Line
  • Dose-Response Relationship, Drug
  • Humans
  • Ion Channel Gating / drug effects*
  • Lidocaine / chemistry
  • Lidocaine / metabolism
  • Lidocaine / pharmacology*
  • Membrane Potentials
  • Models, Molecular
  • Molecular Structure
  • Muscle Proteins / chemistry
  • Muscle Proteins / drug effects*
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism
  • NAV1.5 Voltage-Gated Sodium Channel
  • Phenylalanine
  • Protein Conformation
  • Protein Structure, Tertiary
  • Sodium Channels / chemistry
  • Sodium Channels / drug effects*
  • Sodium Channels / genetics
  • Sodium Channels / metabolism
  • Transfection

Substances

  • Anti-Arrhythmia Agents
  • Muscle Proteins
  • NAV1.5 Voltage-Gated Sodium Channel
  • SCN5A protein, human
  • Sodium Channels
  • Phenylalanine
  • Lidocaine
  • Benzocaine