Isogenic Pairs of hiPSC-CMs with Hypertrophic Cardiomyopathy/LVNC-Associated ACTC1 E99K Mutation Unveil Differential Functional Deficits

Stem Cell Reports. 2018 Nov 13;11(5):1226-1243. doi: 10.1016/j.stemcr.2018.10.006. Epub 2018 Nov 1.

Abstract

Hypertrophic cardiomyopathy (HCM) is a primary disorder of contractility in heart muscle. To gain mechanistic insight and guide pharmacological rescue, this study models HCM using isogenic pairs of human induced pluripotent stem cell-derived cardiomyocytes (hiPSC-CMs) carrying the E99K-ACTC1 cardiac actin mutation. In both 3D engineered heart tissues and 2D monolayers, arrhythmogenesis was evident in all E99K-ACTC1 hiPSC-CMs. Aberrant phenotypes were most common in hiPSC-CMs produced from the heterozygote father. Unexpectedly, pathological phenotypes were less evident in E99K-expressing hiPSC-CMs from the two sons. Mechanistic insight from Ca2+ handling expression studies prompted pharmacological rescue experiments, wherein dual dantroline/ranolazine treatment was most effective. Our data are consistent with E99K mutant protein being a central cause of HCM but the three-way interaction between the primary genetic lesion, background (epi)genetics, and donor patient age may influence the pathogenic phenotype. This illustrates the value of isogenic hiPSC-CMs in genotype-phenotype correlations.

Keywords: arrhythmia; cardiomyopathy; contractile function; hypertrophy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / genetics*
  • Arrhythmias, Cardiac / pathology
  • Arrhythmias, Cardiac / physiopathology
  • CRISPR-Cas Systems / genetics
  • Calcium / metabolism
  • Calcium Signaling
  • Cardiomyopathy, Hypertrophic / pathology*
  • Cardiomyopathy, Hypertrophic / physiopathology
  • Gene Editing
  • Heart Defects, Congenital / pathology
  • Heart Defects, Congenital / physiopathology
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Induced Pluripotent Stem Cells / pathology*
  • Mutation / genetics*
  • Myocardial Contraction
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / pathology*
  • Tissue Engineering

Substances

  • ACTC1 protein, human
  • Actins
  • Calcium

Supplementary concepts

  • Noncompaction of Left Ventricular Myocardium with Congenital Heart Defects