Studying arrhythmogenic right ventricular dysplasia with patient-specific iPSCs

Nature. 2013 Feb 7;494(7435):105-10. doi: 10.1038/nature11799. Epub 2013 Jan 27.

Abstract

Cellular reprogramming of somatic cells to patient-specific induced pluripotent stem cells (iPSCs) enables in vitro modelling of human genetic disorders for pathogenic investigations and therapeutic screens. However, using iPSC-derived cardiomyocytes (iPSC-CMs) to model an adult-onset heart disease remains challenging owing to the uncertainty regarding the ability of relatively immature iPSC-CMs to fully recapitulate adult disease phenotypes. Arrhythmogenic right ventricular dysplasia/cardiomyopathy (ARVD/C) is an inherited heart disease characterized by pathological fatty infiltration and cardiomyocyte loss predominantly in the right ventricle, which is associated with life-threatening ventricular arrhythmias. Over 50% of affected individuals have desmosome gene mutations, most commonly in PKP2, encoding plakophilin-2 (ref. 9). The median age at presentation of ARVD/C is 26 years. We used previously published methods to generate iPSC lines from fibroblasts of two patients with ARVD/C and PKP2 mutations. Mutant PKP2 iPSC-CMs demonstrate abnormal plakoglobin nuclear translocation and decreased β-catenin activity in cardiogenic conditions; yet, these abnormal features are insufficient to reproduce the pathological phenotypes of ARVD/C in standard cardiogenic conditions. Here we show that induction of adult-like metabolic energetics from an embryonic/glycolytic state and abnormal peroxisome proliferator-activated receptor gamma (PPAR-γ) activation underlie the pathogenesis of ARVD/C. By co-activating normal PPAR-alpha-dependent metabolism and abnormal PPAR-γ pathway in beating embryoid bodies (EBs) with defined media, we established an efficient ARVD/C in vitro model within 2 months. This model manifests exaggerated lipogenesis and apoptosis in mutant PKP2 iPSC-CMs. iPSC-CMs with a homozygous PKP2 mutation also had calcium-handling deficits. Our study is the first to demonstrate that induction of adult-like metabolism has a critical role in establishing an adult-onset disease model using patient-specific iPSCs. Using this model, we revealed crucial pathogenic insights that metabolic derangement in adult-like metabolic milieu underlies ARVD/C pathologies, enabling us to propose novel disease-modifying therapeutic strategies.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Age of Onset
  • Apoptosis / genetics
  • Arrhythmogenic Right Ventricular Dysplasia / genetics
  • Arrhythmogenic Right Ventricular Dysplasia / metabolism*
  • Arrhythmogenic Right Ventricular Dysplasia / pathology*
  • Arrhythmogenic Right Ventricular Dysplasia / physiopathology
  • Cellular Reprogramming
  • Culture Media / pharmacology
  • Embryoid Bodies / drug effects
  • Embryoid Bodies / physiology
  • Energy Metabolism / genetics
  • Fatty Acids / metabolism
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Glucose / metabolism
  • Glycolysis
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Induced Pluripotent Stem Cells / pathology*
  • Lipogenesis / genetics
  • Models, Biological*
  • Myocardial Contraction / drug effects
  • Myocytes, Cardiac / pathology
  • PPAR alpha / metabolism
  • PPAR gamma / metabolism
  • Phenotype
  • Plakophilins / genetics
  • Time Factors
  • beta Catenin / metabolism

Substances

  • Culture Media
  • Fatty Acids
  • PKP2 protein, human
  • PPAR alpha
  • PPAR gamma
  • Plakophilins
  • beta Catenin
  • Glucose