Bioenergetic and metabolic aberrations in induced pluripotent stem cell-derived cardiomyocytes generated from a patient with Wolff-Parkinson-White syndrome caused a PRKAG2 mutation

由一名患有沃尔夫-帕金森-怀特综合征的患者诱导多能干细胞分化而来的心肌细胞的生物能量和代谢异常导致了PRKAG2基因突变。

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Abstract

INTRODUCTION: The PRKAG2 gene encodes the AMPK (AMP-activated protein kinase) γ2 subunit, regulating cellular energy homeostasis. PRKAG2 mutations such as R302Q are associated with familial Wolff-Parkinson-White syndrome and hypertrophic cardiomyopathy, leading to metabolic dysregulation and cardiac dysfunction. Accordingly, we hypothesized that PRKAG2 (R 3 0 2 Q) mutation is associated with cardiac bioenergetic/metabolic deficits, causing cardiac dysfunction. METHODS: Using WPW patient' iPSC-derived cardiomyocytes (iPSC-CMs) and a murine model carrying a PRKAG2 mutation, we investigated the mutations-associated functional abnormalities. RESULTS: We found in mutant iPSC-CMs compared to health iPSC-CMs, reduced glycolytic function and increased maximal mitochondrial respiration associated with elevated mitochondrial content, alongside increased glycogen accumulation, lipid storage and alterations in pathways related to redox regulation. Mutated murine hearts exhibited glycogen accumulation, altered glucose and lipid metabolism, elevated triacylglycerol levels and enhanced fatty acid oxidation pathways. Lipidomic and metabolomic analyses in both models revealed disrupted pathways linked to glucose and lipid metabolism. RNA-seq identified gene expression changes associated with redox regulation, mitochondrial function and hypertrophic signaling, aligned with the observed cellular and tissue-level dysfunction. Metformin treatment reduced mitochondrial content and respiration in mutant iPSC-CMs and significantly attenuated the arrhythmias. DISCUSSION: These findings increase our understanding of PRKAG2-associated cardiomyopathy, and propose metformin as a novel modality for managing the metabolic and electrophysiological aberrations of this genetic disorder.

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