The Ionic Mechanisms of Triggered Atrial Activity under a TBX5-Driven Regulatory Network

Andy Lo1, Jieyun Bai2, Patrick Gladding1, Jichao Zhao3
1University of Auckland, 2Jinan University, 3The University of Auckland


Abstract

Atrial fibrillation (AF) is the most prevalent arrhythmia in clinical practice, yet the pathophysiology by which genetic factors can increase the risk of AF is not well understood. Recently, a multitiered transcriptional network, driven by a T-box transcription factor gene TBX5 and regulated by a paired-like homeodomain transcription factor 2 gene PITX2 was discovered, linking seven previously defined AF risk loci together and plays a critical role in the genesis of AF. This transcriptional network regulates gene expressions associated with ion channels in a complex fashion, and through mice knockout studies, it was found that reducing the expression of TBX5 altered the gene expressions of certain types of ion channels and generated abnormal depolarizations in the form of early afterdepolarizations, delayed afterdepolarizations, or spontaneous triggered action potentials. To systematically investigate the ionic mechanisms by which impaired TBX5 can lead to AF, we developed a new human atrial cellular kinetics model by integrating the calcium dynamics of the Grandi et al. model into the Courtemanche-Ramirez-Nattel model. Our model reproduced all forms of abnormal depolarizations observed in TBX5 knockout atrial myocytes. Furthermore, we discovered that the remodeling of the inward-rectifier potassium channel (IK1) and the L-type calcium channel (ICaL) due to impaired TBX5 causes an elevation in the concentration of calcium ([Ca2+]), which reactivates the sodium-calcium exchanger (INaCa) and ICaL to generate abnormal depolarizations. Inhibition of the latter two currents can suppress these abnormal activities. Our findings provide a deeper insight into the ionic mechanisms underlying impaired TBX5-induced AF, and identifies two potential antiarrhythmic drug targets for AF patients with this predisposition.