Screening for acute IKr block is insufficient to detect torsades de pointes liability: role of late sodium current

Circulation. 2014 Jul 15;130(3):224-34. doi: 10.1161/CIRCULATIONAHA.113.007765. Epub 2014 Jun 3.

Abstract

Background: New drugs are routinely screened for IKr blocking properties thought to predict QT prolonging and arrhythmogenic liability. However, recent data suggest that chronic (hours) drug exposure to phosphoinositide 3-kinase inhibitors used in cancer can prolong QT by inhibiting potassium currents and increasing late sodium current (INa-L) in cardiomyocytes. We tested the extent to which IKr blockers with known QT liability generate arrhythmias through this pathway.

Methods and results: Acute exposure to dofetilide, an IKr blocker without other recognized electropharmacologic actions, produced no change in ion currents or action potentials in adult mouse cardiomyocytes, which lack IKr. By contrast, 2 to 48 hours of exposure to the drug generated arrhythmogenic afterdepolarizations and ≥15-fold increases in INa-L. Including phosphatidylinositol 3,4,5-trisphosphate, a downstream effector for the phosphoinositide 3-kinase pathway, in the pipette inhibited these effects. INa-L was also increased, and inhibitable by phosphatidylinositol 3,4,5-trisphosphate, with hours of dofetilide exposure in human-induced pluripotent stem cell-derived cardiomyocytes and in Chinese hamster ovary cells transfected with SCN5A, encoding sodium current. Cardiomyocytes from dofetilide-treated mice similarly demonstrated increased INa-L and afterdepolarizations. Other agents with variable IKr-blocking potencies and arrhythmia liability produced a range of effects on INa-L, from marked increases (E-4031, d-sotalol, thioridazine, and erythromycin) to little or no effect (haloperidol, moxifloxacin, and verapamil).

Conclusions: Some but not all drugs designated as arrhythmogenic IKr blockers can generate arrhythmias by augmenting INa-L through the phosphoinositide 3-kinase pathway. These data identify a potential mechanism for individual susceptibility to proarrhythmia and highlight the need for a new paradigm to screen drugs for QT prolonging and arrhythmogenic liability.

Keywords: KCNH2 potassium channel, human; Nav1.5 voltage-gated sodium channel; phosphatidylinositol 3-kinases; potassium channels.

Publication types

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

MeSH terms

  • 4-Aminopyridine / pharmacology
  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Animals
  • CHO Cells
  • Cells, Cultured
  • Cricetinae
  • Cricetulus
  • Drug Evaluation, Preclinical / methods*
  • Female
  • HEK293 Cells
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Models, Animal
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / physiology
  • NAV1.5 Voltage-Gated Sodium Channel / drug effects*
  • NAV1.5 Voltage-Gated Sodium Channel / genetics
  • NAV1.5 Voltage-Gated Sodium Channel / physiology*
  • Patch-Clamp Techniques
  • Phenethylamines / pharmacology
  • Phosphatidylinositol 3-Kinases / physiology
  • Potassium Channel Blockers / pharmacology*
  • Proto-Oncogene Proteins c-akt / metabolism
  • Risk Factors
  • Signal Transduction / physiology
  • Sulfonamides / pharmacology
  • Torsades de Pointes / epidemiology*
  • Torsades de Pointes / physiopathology
  • Transfection

Substances

  • NAV1.5 Voltage-Gated Sodium Channel
  • Phenethylamines
  • Potassium Channel Blockers
  • Scn5a protein, mouse
  • Sulfonamides
  • 4-Aminopyridine
  • Phosphatidylinositol 3-Kinases
  • Proto-Oncogene Proteins c-akt
  • dofetilide