Atrial-like cardiomyocytes from human pluripotent stem cells are a robust preclinical model for assessing atrial-selective pharmacology

EMBO Mol Med. 2015 Apr;7(4):394-410. doi: 10.15252/emmm.201404757.

Abstract

Drugs targeting atrial-specific ion channels, Kv1.5 or Kir3.1/3.4, are being developed as new therapeutic strategies for atrial fibrillation. However, current preclinical studies carried out in non-cardiac cell lines or animal models may not accurately represent the physiology of a human cardiomyocyte (CM). In the current study, we tested whether human embryonic stem cell (hESC)-derived atrial CMs could predict atrial selectivity of pharmacological compounds. By modulating retinoic acid signaling during hESC differentiation, we generated atrial-like (hESC-atrial) and ventricular-like (hESC-ventricular) CMs. We found the expression of atrial-specific ion channel genes, KCNA5 (encoding Kv1.5) and KCNJ3 (encoding Kir 3.1), in hESC-atrial CMs and further demonstrated that these ion channel genes are regulated by COUP-TF transcription factors. Moreover, in response to multiple ion channel blocker, vernakalant, and Kv1.5 blocker, XEN-D0101, hESC-atrial but not hESC-ventricular CMs showed action potential (AP) prolongation due to a reduction in early repolarization. In hESC-atrial CMs, XEN-R0703, a novel Kir3.1/3.4 blocker restored the AP shortening caused by CCh. Neither CCh nor XEN-R0703 had an effect on hESC-ventricular CMs. In summary, we demonstrate that hESC-atrial CMs are a robust model for pre-clinical testing to assess atrial selectivity of novel antiarrhythmic drugs.

Keywords: COUP‐TF; arrhythmias; atrial cardiomyocytes; atrial fibrillation; ion channels.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Atrial Fibrillation* / drug therapy
  • Atrial Fibrillation* / metabolism
  • Atrial Fibrillation* / pathology
  • Drug Delivery Systems / methods*
  • Drug Evaluation, Preclinical / methods
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / antagonists & inhibitors
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / biosynthesis
  • Gene Expression
  • Heart Atria / metabolism
  • Heart Atria / pathology
  • Humans
  • Kv1.5 Potassium Channel / antagonists & inhibitors
  • Kv1.5 Potassium Channel / biosynthesis
  • Models, Biological*
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / pathology
  • Pluripotent Stem Cells / metabolism*
  • Pluripotent Stem Cells / pathology
  • Potassium Channel Blockers / pharmacology*

Substances

  • G Protein-Coupled Inwardly-Rectifying Potassium Channels
  • KCNA5 protein, human
  • KCNJ3 protein, human
  • Kv1.5 Potassium Channel
  • Potassium Channel Blockers