Molecular mechanisms of arrhythmogenesis in a loss of function KCND3-mutation linked to clinical diagnosis of long-QT-syndrome and aborted SCD

https://doi.org/10.1007/s00392-025-02625-4

Ann-Kathrin Rahm (Heidelberg)1, M. E. Müller (Heidelberg)1, E. Kayvanpour (Heidelberg)1, F. Sedaghat-Hamedani (Heidelberg)1, J. Haas (Heidelberg)1, K. Streckfuß-Bömeke (Würzburg)2, X. Zhou (Mannheim)3, I. Akin (Mannheim)3, J. Heijman (Maastricht)4, X. Wan (Columbus)5, I. Deschenes (Columbus)5, M. P. Penazola Amnion (Karlsruhe)6, W. Wenzel (Karlsruhe)6, N. Ullrich (Bern)7, C. Afting (Heidelberg)8, J. Wittbrodt (Heidelberg)8, D. Gramlich (Stuttgart)9, P. Schweizer (Heidelberg)1, P. Lugenbiel (Heidelberg)1, N. Frey (Heidelberg)1, B. Meder (Heidelberg)1, D. Thomas (Heidelberg)1

1Universitätsklinikum Heidelberg Klinik für Innere Med. III, Kardiologie, Angiologie u. Pneumologie Heidelberg, Deutschland; 2Universitätsklinikum Würzburg Institut für Pharmakologie und Toxikologie Würzburg, Deutschland; 3Universitätsklinikum Mannheim GmbH I. Medizinische Klinik Mannheim, Deutschland; 4Maastricht University Cardiovascular Research Institute Maastricht, Niederlande; 5The Ohio State University, Frick Center for Heart Failure and Arrhythmias, Davis Heart and Lung Research Institute Department of Physiology and Cell Biology Columbus, USA; 6Karlsruher Institut für Technologie (KIT) Institut für Biomedizinische Technik Karlsruhe, Deutschland; 7Universität Bern Institut für Physiologie Bern, Schweiz; 8Heidelberg University Centre for Organismal Studies (COS) Heidelberg, Deutschland; 9Robert-Bosch-Krankenhaus Kardiologie und Angiologie Stuttgart, Deutschland

 

Background
Sixteen genes encoding for cardiac ion channels and associated proteins have been linked to long-QT-syndrome (LQTS) in humans. So far, no pathogenic variant in the KCND3 gene coding for Kv4.3, the main component of the transient-outward potassium current (Ito), has been described in LQTS. 

Purpose
This study presents a novel KCND3 variant in a patient with aborted sudden cardiac death with LQTS as the most likely clinical diagnosis and aimed to identify the underlying genetic and biophysical basis for arrhythmogenesis.

Methods
The index-patient and index-family were examined by electrocardiography, echocardiography and cardiac magnetic resonance imaging. Whole-genome sequencing identified a novel  KCND3-C1469G variant, which was generated by in-vitro mutagenesis and heterologously expressed in Xenopus laevis oocytes and CHO cells for studies using dual-electrode voltage clamp, patch-clamp, western blot and immunofluorescence staining. Current measurements in human induced pluripotent stem cell-derived cardiomyocytes (hiPSC-CM) of the index-patient were compared to a genotype-negative family member. 

Results
QTc prolongation and T wave alterans led to the clinical diagnosis of LQTS in the index-patient. Brugada syndrome and cardiac structural abnormalities were ruled out. The KCND3-C1469G (rs1256867747) variant resulted in a serine-to-cysteine substitution at position 490 in the Kv4.3 C-terminus. Heterologous expression of Kv4.3-S490C revealed reduced Ito amplitude and a change in Kv4.3 channel inactivation kinetics. A comparison of protein expression levels between wildtype and mutant samples isolated from injected Xenopus laevis oocytes showed no significant difference. We propose the formation of a new disulfide bond as potential biophysical mechanism, as in-vitro mutagenesis of serine-457 partially restored current amplitudes. Reduced Ito amplitudes, identified as a specific electrophysiological alteration underlying LQTS, were confirmed in hiPSC-CM derived from the index-patient compared to a genotype-negative family member.

Conclusion
The novel KCND3-C1469G (rs1256867747) variant leads to reduced Ito amplitude and is linked to LQTS and aborted sudden cardiac death. Further studies are needed to identify the arrhythmogenic mechanism in more detail.

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