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

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).

Increased reliance on coronary perfusion for cardiorespiratory performance in seawater-acclimated rainbow trout

“…coronary disease; Aizawa and Kawamura, 2021 ). As the AV canal in rainbow trout is composed of compact myocardium ( Icardo and Colvee, 2010 ; Hassinen et al, 2021 ) and is therefore likely to be perfused by coronary blood, coronary ligation might have a similar effect and disrupt the maintenance of membrane potential by impairing O 2 delivery and thus production of ATP necessary for Na + /K + -ATPases in the AV canal. While this needs to be confirmed experimentally, it can be noted that one of the sham-operated fish exhibited clear signs of coronary obstruction following exhaustive exercise (i.e.…”

Cardiac Toxicity of Cadmium Involves Complex Interactions Among Multiple Ion Currents in Rainbow Trout (Oncorhynchus mykiss) Ventricular Myocytes

“…Inhibition of I CaL explains the large decrease in myocardial contractile force of fish, frog, and mammalian hearts in the presence of Cd 2+ (Vornanen 1996; Wang et al 1999; Wasserstrom and Vites 1999; Shemarova et al 2011). The L‐type Ca 2+ channels are also important for the upstroke of pacemaker AP of the sinoatrial tissue and impulse conduction in the atrioventricular node/canal of vertebrate hearts (Toda 1973; Irisawa et al 1993; Hassinen et al 2021). Therefore, Cd 2+ ‐induced depression of heart rate (bradycardia) and atrioventricular block—typical manifestations of cardiac Cd 2+ toxicity—may also be due to the large reduction in I CaL (Toda 1973; Von Westernhagen et al 1975; Hallare et al 2005; Cao et al 2009; Barjhoux et al 2016).…”

“…The mechanism of the shift in voltage dependence of I CaL is less clear. Residual Ca 2+ current in the presence of Cd 2+ could be due to T‐type Ca 2+ current because T‐type Ca 2+ channels are expressed to some extent (25.8% of all Ca 2+ channel transcripts) in rainbow trout ventricular myocytes, and their peak current is at more negative voltages (Hassinen et al 2021). The Ca 2+ current (elicited from the –80 mV holding potential) in rainbow trout cardiac myocytes is completely blocked by 2.5 to 5.0 µM nifedipine, a specific inhibitor of I CaL , suggesting that it is primarily carried by L‐type Ca 2+ channels (Hove‐Madsen et al 1998; Vornanen 1998).…”

Effects of Na+ channel isoforms and cellular environment on temperature tolerance of cardiac Na+ current in zebrafish (Danio rerio) and rainbow trout (Oncorhynchus mykiss)

“…Heterologous expression of SCN4A and SCN5LA genes Due to the whole genome duplications of the teleost lineage, the number of gene paralogues expressed in fish striated muscles is high (Alderman et al, 2012;Glasauer and Neuhauss, 2014). All eight teleost Na + channel genes are expressed in the heart of both zebrafish and rainbow trout (Haverinen et al, 2018;Hassinen et al, 2021). Because striated muscle isoforms, Na V 1.4 and Na V 1.5, make up the great majority (>99%) of all Na + channel transcripts in zebrafish and trout hearts, genes for heterologous expression were selected from these paralogues.…”