Ca2+-CaM Dependent Inactivation of RyR2 Underlies Ca2+ Alternans in Intact Heart


Por: Wei, JH, Yao, JJ, Belke, D, Guo, WT, Zhong, XW, Sun, B, Wang, RW, Estillore, JP, Vallmitjana, A, Benitez, R, Hove-Madsen, L, Alvarez-Lacalle, E, Echebarria, B, Chen, SRW

Publicada: 19 feb 2021
Resumen:
Rationale: Ca2+ alternans plays an essential role in cardiac alternans that can lead to ventricular fibrillation, but the mechanism underlying Ca2+ alternans remains undefined. Increasing evidence suggests that Ca2+ alternans results from alternations in the inactivation of cardiac RyR2 (ryanodine receptor 2). However, what inactivates RyR2 and how RyR2 inactivation leads to Ca2+ alternans are unknown. Objective: To determine the role of CaM (calmodulin) on Ca2+ alternans in intact working mouse hearts. Methods and Results: We used an in vivo local gene delivery approach to alter CaM function by directly injecting adenoviruses expressing CaM-wild type, a loss-of-function CaM mutation, CaM (1-4), and a gain-of-function mutation, CaM-M37Q, into the anterior wall of the left ventricle of RyR2 wild type or mutant mouse hearts. We monitored Ca2+ transients in ventricular myocytes near the adenovirus-injection sites in Langendorff-perfused intact working hearts using confocal Ca2+ imaging. We found that CaM-wild type and CaM-M37Q promoted Ca2+ alternans and prolonged Ca2+ transient recovery in intact RyR2 wild type and mutant hearts, whereas CaM (1-4) exerted opposite effects. Altered CaM function also affected the recovery from inactivation of the L-type Ca2+ current but had no significant impact on sarcoplasmic reticulum Ca2+ content. Furthermore, we developed a novel numerical myocyte model of Ca2+ alternans that incorporates Ca2+-CaM-dependent regulation of RyR2 and the L-type Ca2+ channel. Remarkably, the new model recapitulates the impact on Ca2+ alternans of altered CaM and RyR2 functions under 9 different experimental conditions. Our simulations reveal that diastolic cytosolic Ca2+ elevation as a result of rapid pacing triggers Ca2+-CaM dependent inactivation of RyR2. The resultant RyR2 inactivation diminishes sarcoplasmic reticulum Ca2+ release, which, in turn, reduces diastolic cytosolic Ca2+, leading to alternations in diastolic cytosolic Ca2+, RyR2 inactivation, and sarcoplasmic reticulum Ca2+ release (ie, Ca2+ alternans). Conclusions: Our results demonstrate that inactivation of RyR2 by Ca2+-CaM is a major determinant of Ca2+ alternans, making Ca2+-CaM dependent regulation of RyR2 an important therapeutic target for cardiac alternans.

Filiaciones:
Wei, JH:
 Univ Calgary, Libin Cardiovasc Inst, Dept Physiol & Pharmacol, Calgary, AB, Canada

Yao, JJ:
 Univ Calgary, Libin Cardiovasc Inst, Dept Physiol & Pharmacol, Calgary, AB, Canada

Belke, D:
 Univ Calgary, Libin Cardiovasc Inst, Dept Physiol & Pharmacol, Calgary, AB, Canada

Guo, WT:
 Univ Calgary, Libin Cardiovasc Inst, Dept Physiol & Pharmacol, Calgary, AB, Canada

Zhong, XW:
 Univ Calgary, Libin Cardiovasc Inst, Dept Physiol & Pharmacol, Calgary, AB, Canada

Sun, B:
 Univ Calgary, Libin Cardiovasc Inst, Dept Physiol & Pharmacol, Calgary, AB, Canada

Wang, RW:
 Univ Calgary, Libin Cardiovasc Inst, Dept Physiol & Pharmacol, Calgary, AB, Canada

Estillore, JP:
 Univ Calgary, Libin Cardiovasc Inst, Dept Physiol & Pharmacol, Calgary, AB, Canada

Vallmitjana, A:
 Univ Politecn Cataluna, Dept Automat Control, Barcelona, Spain

Benitez, R:
 Univ Politecn Cataluna, Dept Automat Control, Barcelona, Spain

 Inst Recerca St Joan Deu IRSJD, Barcelona, Spain

Hove-Madsen, L:
 Biomed Res Inst Barcelona IIBB CSIC, Barcelona, Spain

 CIBERCV, Barcelona, Spain

 Hosp Santa Creu & Sant Pau, IIB St Pau, Barcelona, Spain

Alvarez-Lacalle, E:
 Univ Politecn Cataluna, Dept Phys, Barcelona, Spain

Echebarria, B:
 Univ Politecn Cataluna, Dept Phys, Barcelona, Spain

Chen, SRW:
 Univ Calgary, Libin Cardiovasc Inst, Dept Physiol & Pharmacol, Calgary, AB, Canada
ISSN: 00097330





CIRCULATION RESEARCH
Editorial
LIPPINCOTT WILLIAMS & WILKINS, TWO COMMERCE SQ, 2001 MARKET ST, PHILADELPHIA, PA 19103 USA, Estados Unidos America
Tipo de documento: Article
Volumen: 128 Número: 4
Páginas: 63-83
WOS Id: 000639313800002
ID de PubMed: 33375811
imagen Green Submitted, Bronze

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