Calcium signaling consequences of RyR2 mutations associated with CPVT1 introduced via CRISPR/Cas9 gene editing in human-induced pluripotent stem cell-derived cardiomyocytes: Comparison of RyR2-R420Q, F2483I, and Q4201R

利用 CRISPR/Cas9 基因编辑技术在人诱导多能干细胞来源的心肌细胞中引入与儿茶酚胺敏感性室性心动过速1型 (CPVT1) 相关的 RyR2 突变,并比较 RyR2-R420Q、F2483I 和 Q4201R 突变对钙信号传导的影响。

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Abstract

BACKGROUND: Human-induced pluripotent stem cell-derived cardiomyocytes (hiPSC-CMs) created from patients with catecholaminergic polymorphic ventricular tachycardia 1 (CPVT1) have been used to study CPVT1 arrhythmia. OBJECTIVE: The purpose of this study was to evaluate the Ca(2+) signaling aberrancies and pharmacological sensitivities of 3 CRISPR/Cas9-introduced CPVT1 mutations located in different molecular domains of ryanodine receptor 2 (RyR2). METHODS: CRISPR/Cas9-engineered hiPSC-CMs carrying RyR2 mutations-R420Q, Q4201R, and F2483I-were voltage clamped, and their electrophysiology, pharmacology, and Ca(2+) signaling phenotypes measured using total internal reflection fluorescence microscopy. RESULTS: R420Q and Q4201R mutant hiPSC-CMs exhibit irregular, long-lasting, spatially wandering Ca(2+) sparks and aberrant Ca(2+) releases similar to F2483I unlike the wild-type myocytes. Large sarcoplasmic reticulum (SR) Ca(2+) leaks and smaller SR Ca(2+) contents were detected in cells expressing Q4201R and F2483I, but not R420Q. Fractional Ca(2+) release and calcium-induced calcium release gain were higher in Q4201R than in R420Q and F2483I hiPSC-CMs. JTV519 was equally effective in suppressing Ca(2+) sparks, waves, and SR Ca(2+) leaks in hiPSC-CMs derived from all 3 mutant lines. Flecainide and dantrolene similarly suppressed SR Ca(2+) leaks, but were less effective in decreasing spark frequency and durations. CONCLUSION: CRISPR/Cas9 gene editing of hiPSCs provides a novel approach in studying CPVT1-associated RyR2 mutations and suggests that Ca(2+)-signaling aberrancies and drug sensitivities may vary depending on the mutation site.

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