Increased Ca2+ transient underlies RyR2-related left ventricular noncompaction

Background: A loss-of-function cardiac ryanodine receptor (RyR2) mutation, I4855M+/–, has recently been linked to a new cardiac disorder termed RyR2 Ca2+ release deficiency syndrome (CRDS) as well as left ventricular noncompaction (LVNC). The mechanism by which RyR2 loss-of-function causes CRDS has...

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Detalles Bibliográficos
Autores: Ni, Mingke, Li, Yanhui, Wei, Jinhong, Song, Zhenpeng, Wang, Hui, Yao, Jinjing, Chen, Yong-Xiang, Belke, Darrell, Estillore, John Paul, Wang, Ruiwu, Vallmitjana Lees, Alexander, Benítez Iglesias, Raúl|||0000-0002-8782-9406, Hove Madsen, Leif, Feng, Wei, Chen, Ju
Tipo de recurso: artículo
Fecha de publicación:2023
País:España
Institución:Universitat Politècnica de Catalunya (UPC)
Repositorio:UPCommons. Portal del coneixement obert de la UPC
Idioma:inglés
OAI Identifier:oai:upcommons.upc.edu:2117/398769
Acceso en línea:https://hdl.handle.net/2117/398769
https://dx.doi.org/10.1161/CIRCRESAHA.123.322504
Access Level:acceso abierto
Palabra clave:Electronics in cardiology
Electrònica en cardiologia
Àrees temàtiques de la UPC::Enginyeria biomèdica::Electrònica biomèdica::Electrònica en cardiologia
Descripción
Sumario:Background: A loss-of-function cardiac ryanodine receptor (RyR2) mutation, I4855M+/–, has recently been linked to a new cardiac disorder termed RyR2 Ca2+ release deficiency syndrome (CRDS) as well as left ventricular noncompaction (LVNC). The mechanism by which RyR2 loss-of-function causes CRDS has been extensively studied, but the mechanism underlying RyR2 loss-of-function-associated LVNC is unknown. Here, we determined the impact of a CRDS-LVNC-associated RyR2-I4855M+/– loss-of-function mutation on cardiac structure and function. Methods: We generated a mouse model expressing the CRDS-LVNC-associated RyR2-I4855M+/– mutation. Histological analysis, echocardiography, ECG recording, and intact heart Ca2+ imaging were performed to characterize the structural and functional consequences of the RyR2-I4855M+/– mutation. Results: As in humans, RyR2-I4855M+/– mice displayed LVNC characterized by cardiac hypertrabeculation and noncompaction. RyR2-I4855M+/– mice were highly susceptible to electrical stimulation–induced ventricular arrhythmias but protected from stress-induced ventricular arrhythmias. Unexpectedly, the RyR2-I4855M+/– mutation increased the peak Ca2+ transient but did not alter the L-type Ca2+ current, suggesting an increase in Ca2+-induced Ca2+ release gain. The RyR2-I4855M+/– mutation abolished sarcoplasmic reticulum store overload–induced Ca2+ release or Ca2+ leak, elevated sarcoplasmic reticulum Ca2+ load, prolonged Ca2+ transient decay, and elevated end-diastolic Ca2+ level upon rapid pacing. Immunoblotting revealed increased level of phosphorylated CaMKII (Ca2+-calmodulin dependent protein kinases II) but unchanged levels of CaMKII, calcineurin, and other Ca2+ handling proteins in the RyR2-I4855M+/– mutant compared with wild type. Conclusions: The RyR2-I4855M+/– mutant mice represent the first RyR2-associated LVNC animal model that recapitulates the CRDS-LVNC overlapping phenotype in humans. The RyR2-I4855M+/– mutation increases the peak Ca2+ transient by increasing the Ca2+-induced Ca2+ release gain and the end-diastolic Ca2+ level by prolonging Ca2+ transient decay. Our data suggest that the increased peak-systolic and end-diastolic Ca2+ levels may underlie RyR2-associated LVNC.