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, MK, Li, YH, Wei, JH, Song, ZP, Wang, H, Yao, JJ, Chen, YX, Belke, D, Estillore, JP, Wang, RW, Vallmitjana, A, Benitez, R, Hove-Madsen, L, Feng, W, Chen, J, Roston, TM, Sanatani, S, Lehman, A, Chen, SRW
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Fundació Sant Joan de Déu
Repositorio:r-FSJD. Repositorio Institucional de Producción Científica de la Fundació Sant Joan de Déu
OAI Identifier:oai:fsjd.fundanetsuite.com:p24136
Acceso en línea:https://fsjd.fundanetsuite.com/Publicaciones/ProdCientif/PublicacionFrw.aspx?id=24136
Access Level:acceso abierto
Palabra clave:cardiomyopathies
sarcoplasmic reticulum
tachycardia
ventricular
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.