Conditional ablation of MCU exacerbated cardiac pathology in a genetic arrhythmic model of CPVT

Background: Catecholaminergic polymorphic ventricular tachycardia (CPVT) is a genetic arrhythmic syndrome caused by mutations in the calcium (Ca2+) release channel ryanodine receptor (RyR2) and its accessory proteins. These mutations make the channel leaky, resulting in Ca2+-dependent arrhythmias. B...

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Main Authors: Arpita Deb, Brian D. Tow, Jie Hao, Branden L. Nguyen, Valeria Gomez, James A. Stewart, Jr, Ashley J. Smuder, Bjorn C. Knollmann, Ying Wang, Bin Liu
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Journal of Molecular and Cellular Cardiology Plus
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Online Access:http://www.sciencedirect.com/science/article/pii/S2772976124000333
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Summary:Background: Catecholaminergic polymorphic ventricular tachycardia (CPVT) is a genetic arrhythmic syndrome caused by mutations in the calcium (Ca2+) release channel ryanodine receptor (RyR2) and its accessory proteins. These mutations make the channel leaky, resulting in Ca2+-dependent arrhythmias. Besides arrhythmias, CPVT hearts typically lack structural cardiac remodeling, a characteristic often observed in other cardiac conditions (heart failure, prediabetes) also marked by RyR2 leak. Recent studies suggest that mitochondria are able to accommodate more Ca2+ influx to inhibit arrhythmias in CPVT. Thus, we hypothesize that CPVT mitochondria can absorb diastolic Ca2+ to protect the heart from cardiac remodeling. Methods and results: The Mitochondrial Ca2+ uniporter (MCU), the main mitochondrial Ca2+ uptake protein, was conditionally knocked out in a CPVT model of calsequestrin 2 (CASQ2) KO. In vivo cardiac function was impaired in the CASQ2−/−-MCUCKO model as assessed by echocardiography. Cardiac dilation and cellular hypertrophy were also observed in the CASQ2−/−-MCUCKO hearts. Live-cell imaging identified altered Ca2+ handling and increased oxidative stress in CASQ2−/−-MCUCKO myocytes. The activation status of Ca2+-dependent remodeling pathways (CaMKII, Calcineurin) was not altered in the CASQ2−/−-MCUCKO model. RNAseq identified changes in the transcriptome of the CASQ2−/−-MCUCKO hearts, distinct from the classic cardiac remodeling program of fetal gene re-expression. Conclusions: We present genetic evidence that mitochondria play a protective role in CPVT. MCU-dependent Ca2+ uptake is crucial for preventing pathological cardiac remodeling in CPVT.
ISSN:2772-9761