Integrative Analysis of PRKAG2 Cardiomyopathy iPS and Microtissue Models Identifies AMPK as a Regulator of Metabolism, Survival, and Fibrosis

Cell Rep. 2016 Dec 20;17(12):3292-3304. doi: 10.1016/j.celrep.2016.11.066.

Abstract

AMP-activated protein kinase (AMPK) is a metabolic enzyme that can be activated by nutrient stress or genetic mutations. Missense mutations in the regulatory subunit, PRKAG2, activate AMPK and cause left ventricular hypertrophy, glycogen accumulation, and ventricular pre-excitation. Using human iPS cell models combined with three-dimensional cardiac microtissues, we show that activating PRKAG2 mutations increase microtissue twitch force by enhancing myocyte survival. Integrating RNA sequencing with metabolomics, PRKAG2 mutations that activate AMPK remodeled global metabolism by regulating RNA transcripts to favor glycogen storage and oxidative metabolism instead of glycolysis. As in patients with PRKAG2 cardiomyopathy, iPS cell and mouse models are protected from cardiac fibrosis, and we define a crosstalk between AMPK and post-transcriptional regulation of TGFβ isoform signaling that has implications in fibrotic forms of cardiomyopathy. Our results establish critical connections among metabolic sensing, myocyte survival, and TGFβ signaling.

Keywords: AMP-activated protein kinase; AMPK; PRKAG2; TGF-beta; Wolff-Parkinson-White syndrome; fibrosis; glycogen storage disease; hypertrophic cardiomyopathy.

Publication types

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

MeSH terms

  • AMP-Activated Protein Kinases / genetics*
  • AMP-Activated Protein Kinases / metabolism
  • Animals
  • Cardiomyopathies / genetics*
  • Cardiomyopathies / metabolism
  • Cardiomyopathies / pathology
  • Cell Survival / genetics
  • Glycogen / metabolism
  • Humans
  • Hypertrophy, Left Ventricular / genetics*
  • Hypertrophy, Left Ventricular / metabolism
  • Hypertrophy, Left Ventricular / pathology
  • Induced Pluripotent Stem Cells / transplantation
  • Metabolome / genetics
  • Mice
  • Muscle Cells / metabolism
  • Muscle Cells / pathology
  • Mutation, Missense
  • Sequence Analysis, RNA
  • Signal Transduction
  • Tissue Engineering / methods
  • Transforming Growth Factor beta1 / genetics*
  • Transforming Growth Factor beta1 / metabolism

Substances

  • Transforming Growth Factor beta1
  • Glycogen
  • PRKAG2 protein, human
  • AMP-Activated Protein Kinases