Electrical dysfunctions in human-induced pluripotent stem cell-derived cardiomyocytes from a patient with an arrhythmogenic right ventricular cardiomyopathy

Europace. 2018 Jun 1;20(FI1):f46-f56. doi: 10.1093/europace/euy042.

Abstract

Aims: Our aim is to investigate the arrhythmogenic mechanism in arrhythmogenic right ventricular cardiomyopathy (ARVC)-patients by using human-induced pluripotent stem cell-derived cardiomyocytes (hiPSC-CMs).

Methods and results: Human-induced pluripotent stem cell-derived cardiomyocytes were generated from human skin fibroblasts of two healthy donors and an ARVC-patient with a desmoglein-2 (DSG2) mutation. Patch clamp, quantitative polymerase chain reaction, and calcium imaging techniques were employed for the study. The amplitude and maximal upstroke velocity (Vmax) of action potential (AP) in ARVC-cells were smaller than that in healthy donor cells, whereas the resting potential and AP duration (APD) was not changed. The reduced Vmax resulted from decreased peak sodium current. The reason for undetected changes in APD may be the counter-action of reduced transient outward, small conductance Ca2+-activated, adenosine triphosphate-sensitive, Na/Ca exchanger (INCX) currents, and enhanced rapidly delayed rectifier currents. Isoprenaline (Iso) reduced INCX and shortened APD in both donor and ARVC-hiPSC-CMs. However, the effects of Iso in ARVC-cells are significantly larger than that in donor cells. In addition, ARVC-hiPSC-CMs showed more frequently than donor cells arrhythmogenic events induced by adrenergic stimulation.

Conclusion: Cardiomyocytes derived from the ARVC patient with a DSG2 mutation displayed multiple ion channel dysfunctions and abnormal cellular electrophysiology as well as enhanced sensitivity to adrenergic stimulation. These may underlie the arrhythmogenesis in ARVC patients.

MeSH terms

  • Action Potentials* / drug effects
  • Adrenergic beta-Agonists / pharmacology
  • Arrhythmogenic Right Ventricular Dysplasia / genetics
  • Arrhythmogenic Right Ventricular Dysplasia / metabolism*
  • Arrhythmogenic Right Ventricular Dysplasia / pathology
  • Arrhythmogenic Right Ventricular Dysplasia / physiopathology
  • Calcium Signaling
  • Case-Control Studies
  • Cells, Cultured
  • Delayed Rectifier Potassium Channels / metabolism
  • Desmoglein 2 / genetics
  • Desmoglein 2 / metabolism
  • Genetic Predisposition to Disease
  • Heart Rate
  • Humans
  • Induced Pluripotent Stem Cells / drug effects
  • Induced Pluripotent Stem Cells / metabolism*
  • Induced Pluripotent Stem Cells / pathology
  • Isoproterenol / pharmacology
  • Kinetics
  • Male
  • Middle Aged
  • Mutation
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / pathology
  • Phenotype
  • Sodium-Calcium Exchanger / metabolism

Substances

  • Adrenergic beta-Agonists
  • DSG2 protein, human
  • Delayed Rectifier Potassium Channels
  • Desmoglein 2
  • Sodium-Calcium Exchanger
  • Isoproterenol