SLC4A3-related short QT syndrome assessed in human induced pluripotent stem cell-derived cardiomyocytes: mechanisms of ventricular arrhythmia and sudden cardiac death

Eur Heart J. 2026 Mar 5:ehag068. doi: 10.1093/eurheartj/ehag068. Online ahead of print.

Abstract

Background and aims: Short QT syndrome (SQTS) is an inherited channelopathy that can cause sudden cardiac death. Recent research has implicated mutations in the SLC4A3 gene as a cause of SQTS, but the mechanisms of shortened action potential duration (APD) and arrhythmia vulnerability have not been described. This study aims to evaluate the underlying pathophysiology causing a shortened APD and ventricular arrhythmia vulnerability in SLC4A3-associated SQTS through mechanistic studies of novel SLC4A3 mutations responsible for familial SQTS.

Methods: This study evaluated the function and pathophysiology of two novel SLC4A3 variants (p.Arg370Cys and p.Lys531Thr) responsible for SQTS in their respective families. Human induced pluripotent stem cell-derived cardiomyocytes (hiPSC-CMs) from each index SQTS patient were developed, as well as an isogenic cell line with variant correction (using CRISPR/Cas9) and HEK 293T cells transfected with SLC4A3 expression constructs expressing either wild type (WT) SLC4A3 or the variants. SLC4A3-SQTS variants were physiologically characterized by patch-clamp analysis, Ca2+ imaging, single cell contraction, intracellular pH measurement, protein structure analyses, immunostaining, and optical mapping studies in a human organoid model.

Results: SQTS-hiPSC-CMs showed significantly shorter APD and a higher rate of arrhythmia-like events, as recorded by spontaneous action potentials, calcium transient imaging, and rhythmicity of visualized single cell contractions. SQTS-hiPSC-CMs exhibited decreased L-type calcium channel current (ICa-L), and significantly increased Na/Ca exchange current (INCX). Frequent delayed afterdepolarization (DAD) events were recorded from mutant cells but not WT or isogenic cell lines. The intracellular pH value was significantly higher (alkaline) in SQTS-hiPSC-CMs and in transfected heterologous cells expressing mutant SLC4A3, as compared to WT-SLC4A3. Experimental-induced alkalinization of WT-hiPSC-CMs by NH4Cl resulted in shortened APD, enhanced INCX, and reduced ICa-L, similar to observations in cells expressing mutant SLC4A3 proteins. Quinidine and sotalol were found to prolong APD and decrease the occurrence of arrhythmia-like events (DADs) in SQTS-hiPSC-CMs.

Conclusions: In human cell models, SLC4A3 mutations responsible for SQTS result in loss-of-function leading to intracellular alkalinization, decreased ICa-L, and shortened APD, accounting for the clinical phenotype of short QT. Arrhythmic events in SLC4A3-associated SQTS are provoked by enhanced INCX evoking DADs.

Keywords: SLC4A3; Arrhythmias; Gene; Human induced pluripotent stem cell-derived cardiomyocytes; Short QT syndrome; Sudden cardiac death.