Ionic basis of atrioventricular conduction: ion channel expression and sarcolemmal ion currents of the atrioventricular canal of the rainbow trout (Oncorhynchus mykiss) heart

Minna Hassinen,Irina Dzhumaniiazova,Denis V Abramochkin,Matti Vornanen

doi:10.1007/s00360-021-01344-2

Abstract

Atrioventricular (AV) nodal tissue synchronizes activities of atria and ventricles of the vertebrate heart and is also a potential site of cardiac arrhythmia, e.g., under acute heat stress. Since ion channel composition and ion currents of the fish AV canal have not been previously studied, we measured major cation currents and transcript expression of ion channels in rainbow trout (Oncorhynchus mykiss) AV tissue. Both ion current densities and expression of ion channel transcripts indicate that the fish AV canal has a characteristic electrophysiological phenotype that differs from those of sinoatrial tissue, atrium and ventricle. Two types of cardiomyocytes were distinguished electrophysiologically in trout AV nodal tissue: the one (transitional cell) is functionally intermediate between working atrial/ventricular myocytes and the other (AV nodal cell) has a less negative resting membrane potential than atrial and ventricular myocytes and is a more similar to the sinoatrial nodal cells in ion channel composition. The AV nodal cells are characterized by a small or non-existent inward rectifier potassium current (IK1), low density of fast sodium current (INa) and relatively high expression of T-type calcium channels (CACNA3.1). Pacemaker channel (HCN4 and HCN2) transcripts were expressed in the AV nodal tissue but If current was not found in enzymatically isolated nodal myocytes. The electrophysiological properties of the rainbow trout nodal cells are appropriate for a slow rate of action potential conduction (small INa) and a moderate propensity for pacemaking activity (absence of IK1).

Highlights

The activity of the vertebrate heart is controlled by rhythmic electrical impulses, which originate from the sinoatrial (SA) pacemaker
The annular SA pacemaker at the junction between the sinus venosus and the atrium is the site of origin for electrical excitation (EE) (Yamauchi and Burnstock 1968; Haverinen and Vornanen 2007)
Atrium, AVv atrioventricular valves, V ventricle; com, compact myocardium, tr endocardial trabeculae, *AV myocardium; arrowhead, connective tissue. c, d Photomicrographs of morphological cell types of the rainbow trout AV canal: c spindle-shaped nodal AV cell, d staror spider-shaped nodal AV cell and e transitional AV cell myocardium which is surrounded by a collagen-rich connective tissue from both sides (Fig. 1)

Summary

Introduction

The activity of the vertebrate heart is controlled by rhythmic electrical impulses (action potentials, APs), which originate from the sinoatrial (SA) pacemaker. The heart of teleost fishes consists of six consecutive histologically identifiable parts: Sinus venosus, atrium, atrioventricular (AV) canal, ventricle, conus arteriosus and bulbus arteriosus in the order from caudal to cranial direction (Icardo 2017). The annular SA pacemaker at the junction between the sinus venosus and the atrium is the site of origin for EE (Yamauchi and Burnstock 1968; Haverinen and Vornanen 2007). APs proceed first to the atrium and via the AV canal to the ventricle triggering sequential contractions of these two muscular chambers of the fish heart (McWilliam 1885; Keith and Flack 1907; Nair 1976; Arbel et al 1977; Sedmera et al 2003).

Objectives

Methods

Results

Conclusion