Quantified proarrhythmic potential of selected human embryonic stem cell-derived cardiomyocytes

Stem Cell Res. 2010 May;4(3):189-200. doi: 10.1016/j.scr.2010.02.001. Epub 2010 Feb 17.

Abstract

To improve proarrhythmic predictability of preclinical models, we assessed whether human ventricular-like embryonic stem cell-derived cardiomyocytes (hESC-CMs) can be selected following a standardized protocol. Also, we quantified their arrhythmogenic response and compared this to a contemporary used rabbit Purkinje fiber (PF) model. Multiple transmembrane action potentials (AP) were recorded from 164 hESC-CM clusters (9 different batches), and 12 isolated PFs from New Zealand White rabbits. AP duration (APD), early afterdepolarizations (EADs), triangulation (T), and short-term variability of repolarization (STV) were determined on application of the I(Kr) blocker E-4031 (0.03/0.1/0.3/1 muM). Isoproterenol (0.1 muM) was used to assess adrenergic response. To validate the phenotype, RNA isolated from atrial- and ventricular-like clusters (n=8) was analyzed using low-density Taqman arrays. Based on initial experiments, slow beating rate (<50 bpm) and long APD (>200 ms) were used to select 31 ventricular-like clusters. E-4031 (1 muM) prolonged APD (31/31) and induced EADs only in clusters with APD90>300 ms (11/16). EADs were associated with increased T (1.6+/-0.2 vs 2.0+/-0.3) and STV (2.7+/-1.5 vs 6.9+/-1.9). Rabbit PF reacted in a similar way with regards to EADs (5/12), increased T (1.3+/-0.1 vs 1.9+/-0.4), and STV (1.2+/-0.9 vs 7.1+/-5.6). According to ROC values, hESC-CMs (STV 0.91) could predict EADs at least equivalent to PF (STV 0.69). Isoproterenol shortened APD and completely suppressed EADs. Gene expression analysis revealed that HCN1/2, KCNA5, and GJA5 were higher in atrial/nodal-like cells, whereas KCNJ2 and SCN1B were higher in ventricular-like cells (P<0.05). Selection of hESC-CM clusters with a ventricular-like phenotype can be standardized. The proarrhythmic results are qualitatively and quantitatively comparable between hESC-CMs and rabbit PF. Our results indicate that additional validation of this new safety pharmacology model is warranted.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Cell Line
  • Connexins / metabolism
  • Cyclic Nucleotide-Gated Cation Channels / metabolism
  • Electrocardiography
  • Embryonic Stem Cells / cytology*
  • Gap Junction alpha-5 Protein
  • Humans
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
  • Ion Channels / metabolism
  • Isoproterenol / pharmacology
  • Kv1.5 Potassium Channel / metabolism
  • Models, Biological
  • Myocytes, Cardiac / cytology
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / physiology*
  • Phenotype
  • Potassium Channels / metabolism
  • Potassium Channels, Inwardly Rectifying / metabolism
  • Purkinje Fibers / cytology
  • Purkinje Fibers / physiology
  • RNA, Messenger / metabolism
  • Rabbits
  • Sodium Channels / metabolism

Substances

  • Connexins
  • Cyclic Nucleotide-Gated Cation Channels
  • HCN1 protein, human
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
  • Ion Channels
  • Kir2.1 channel
  • Kv1.5 Potassium Channel
  • Potassium Channels
  • Potassium Channels, Inwardly Rectifying
  • RNA, Messenger
  • Sodium Channels
  • Isoproterenol