Modeling reduced contractility and impaired desmosome assembly due to plakophilin-2 deficiency using isogenic iPS cell-derived cardiomyocytes

Stem Cell Reports. 2022 Feb 8;17(2):337-351. doi: 10.1016/j.stemcr.2021.12.016. Epub 2022 Jan 20.

Abstract

Loss-of-function mutations in PKP2, which encodes plakophilin-2, cause arrhythmogenic cardiomyopathy (AC). Restoration of deficient molecules can serve as upstream therapy, thereby requiring a human model that recapitulates disease pathology and provides distinct readouts in phenotypic analysis for proof of concept for gene replacement therapy. Here, we generated isogenic induced pluripotent stem cell-derived cardiomyocytes (iPSC-CMs) with precisely adjusted expression of plakophilin-2 from a patient with AC carrying a heterozygous frameshift PKP2 mutation. After monolayer differentiation, plakophilin-2 deficiency led to reduced contractility, disrupted intercalated disc structures, and impaired desmosome assembly in iPSC-CMs. Allele-specific fluorescent labeling of endogenous DSG2 encoding desmoglein-2 in the generated isogenic lines enabled real-time desmosome-imaging under an adjusted dose of plakophilin-2. Adeno-associated virus-mediated gene replacement of PKP2 recovered contractility and restored desmosome assembly, which was sequentially captured by desmosome-imaging in plakophilin-2-deficient iPSC-CMs. Our isogenic set of iPSC-CMs recapitulates AC pathology and provides a rapid and convenient cellular platform for therapeutic development.

Keywords: adeno-associated virus; arrhythmogenic cardiomyopathy; desmosome; genome editing; human induced pluripotent stem cell-derived cardiomyocytes; plakophilin-2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arrhythmias, Cardiac / genetics
  • Arrhythmias, Cardiac / pathology*
  • CRISPR-Cas Systems / genetics
  • Cell Differentiation
  • Desmosomes / physiology*
  • Female
  • Gene Editing
  • Genetic Vectors / genetics
  • Genetic Vectors / metabolism
  • Heterozygote
  • Humans
  • Induced Pluripotent Stem Cells / cytology
  • Induced Pluripotent Stem Cells / metabolism
  • Male
  • Models, Biological
  • Myocardial Contraction / physiology*
  • Myocytes, Cardiac / cytology
  • Myocytes, Cardiac / metabolism
  • Pedigree
  • Plakophilins / genetics
  • Plakophilins / metabolism*

Substances

  • Plakophilins