Language

English

Publication Date

5-5-2025

Journal

The Journal of Physiology

DOI

10.1113/JP288499

PMID

40320903

PMCID

PMC12787628

PubMedCentral® Posted Date

1-10-2026

PubMedCentral® Full Text Version

Author MSS

Abstract

Catecholaminergic polymorphic ventricular tachycardia (CPVT) is an inherited stress-induced arrhythmogenic disease often caused by point variants in the cardiac ryanodine receptor (RyR2) that enhance diastolic sarcoplasmic reticulum (SR) Ca2+ leak. These RyR2 variants cluster in three hot-spots (N-terminal, central and C-terminal domains). We previously demonstrated a pathologic diastolic RyR2 conformation in heart failure, oxidative stress and CaMKII phosphorylation exhibiting a trilogy of effects: (1) reduced calmodulin (CaM)-RyR2 affinity, (2) enhanced unzipping peptide (DPc10) binding and (3) elevated diastolic SR Ca2+ leak that are dantrolene-sensitive. Here we test whether this pathological trilogy occurs in CPVT knock-in (KI) mice bearing N-terminal (R176Q/+), central (R2474S/+) and C-terminal variants (R4496C/+). Isolated saponin-permeabilized ventricular myocytes from all three KI mice exhibited unaltered baseline CaM and DPc10 binding to RyR2 versus wild-type (WT) myocytes. However cAMP-induced protein kinase A (PKA)-dependent RyR2 phosphorylation revealed the pathological trilogy, but only in R176Q and R2474S KI myocytes. That contrasts with WT and R4496C KI myocytes where cAMP enhanced SR Ca2+ leak without altering either CaM- or DPc10-RyR2 affinity. We conclude that CPVT-linked RyR2 variants at baseline may not exhibit the pathological diastolic trilogy above, but that trilogy is induced by PKA activation only in N-terminal and central domain CPVT variants. Thus the mechanism of arrhythmogenic RyR2 leak in pore domain variants (e.g. R4496C) may not involve the same pathological conformational changes as in N-terminal and central domain variants. This may inform which specific CPVT-linked RyR2 variants may benefit from therapeutic strategies that target this pathological trilogy conformation.

Keywords

calmodulin, catecholaminergic polymorphic ventricular tachycardia, dantrolene, fluorescence resonance energy transfer, ryanodine receptor

Published Open-Access

yes

nihms-2116360-f0011.jpg (269 kB)
Graphical Abstract

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