A novel computational model of swine ventricular myocyte reveals new insights into disease mechanisms and therapeutic approaches in Timothy Syndrome

Sci Rep. 2024 Nov 30;14(1):29792. doi: 10.1038/s41598-024-80726-2.

Abstract

Timothy syndrome type 1 (TS1), a malignant variant of Long QT Syndrome, is caused by L-type Ca2+ Channel (LTCC) inactivation defects secondary to the p.Gly406Arg mutation in the CACNA1C gene. Leveraging on the experimental in vitro data from our TS1 knock-in swine model and their wild-type (WT) littermates, we first developed a mathematical model of WT large white swine ventricular cardiomyocyte electrophysiology that reproduces a wide range of experimental data, including ionic current properties, action potential (AP) dynamics, and Ca 2 + handling. A sensitivity analysis tested robustness and facilitated comparison with the parent ORd human model. Introducing 22% of TS1-mutated LTCCs, the model faithfully reproduced key disease features, including marked AP prolongation, steeper rate-dependent adaptation of AP duration, Ca 2 + overload, and CaMKII-mediated decreased upstroke velocity. Translational relevance of the TS1 model was investigated by: dissecting the roles of primary and secondary contributors to TS1 phenotype; demonstrating the arrhythmogenic potential of TS1 vs. WT cells; and evaluating the model's capability to identify novel pharmacological targets which could modulate the cellular phenotype. In conclusion, we developed a mathematical large white swine ventricular myocyte model, demonstrating its utility in exploring arrhythmogenic mechanisms and therapeutic interventions in cardiac diseases, such as TS1.

Keywords: CACNA1C; Cardiac Electrophysiology; Long QT Syndrome; Mathematical Modeling; Swine Ventricular Myocyte.

MeSH terms

  • Action Potentials* / drug effects
  • Animals
  • Autistic Disorder* / drug therapy
  • Autistic Disorder* / genetics
  • Autistic Disorder* / metabolism
  • Calcium / metabolism
  • Calcium Channels, L-Type* / genetics
  • Calcium Channels, L-Type* / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / genetics
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism
  • Computer Simulation
  • Disease Models, Animal
  • Heart Ventricles* / drug effects
  • Heart Ventricles* / metabolism
  • Heart Ventricles* / pathology
  • Heart Ventricles* / physiopathology
  • Humans
  • Long QT Syndrome* / drug therapy
  • Long QT Syndrome* / genetics
  • Long QT Syndrome* / metabolism
  • Models, Cardiovascular
  • Mutation
  • Myocytes, Cardiac* / drug effects
  • Myocytes, Cardiac* / metabolism
  • Swine
  • Syndactyly* / genetics
  • Syndactyly* / metabolism

Substances

  • Calcium Channels, L-Type
  • Calcium
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • L-type calcium channel alpha(1C)

Supplementary concepts

  • Timothy syndrome