Electrical excitability of the heart in a Chondrostei fish, the Siberian sturgeon (Acipenser baerii)

Abstract

Sturgeon (family Acipenseridae) are regarded as living fossils due to their ancient origin and exceptionally slow evolution. To extend our knowledge of fish cardiac excitability to a Chondrostei fish, we examined electrophysiological phenotype of the Siberian sturgeon (Acipenser baerii) heart with recordings of epicardial ECG, intracellular action potentials (APs), and sarcolemmal ion currents. Epicardial ECG of A. baerii had the typical waveform of the vertebrate ECG with Q-T interval (average duration of ventricular AP) of 650±30 ms and an intrinsic heart rate of 45.5±5 beats min(-1) at 20°C. Similar to other fish species, atrial AP was shorter in duration (402±33 ms) than ventricular AP (585±40) (P<0.05) at 20°C. Densities of atrial and ventricular Na+ currents were similar (-47.6±4.5 and -53.2±5.1 pA/pF, respectively) and close to the typical values of teleost hearts. Two major K+ currents, the inward rectifier K+ current (IK1), and the delayed rectifier K+ current (IKr) were found under basal conditions in sturgeon cardiomyocytes. The atrial IKr (3.3±0.2 pA/pF) was about twice as large as the ventricular IKr (1.3±0.4 pA/pF) (P<0.05) conforming to the typical pattern of teleost cardiac IKr. Divergent from other fishes, the ventricular IK1 was remarkably small (-2.5±0.07 pA/pF) and not different from that of the atrial myocytes (-1.9±0.06 pA/pF) (P>0.05). Two ligand-gated K+ currents were also found: ACh-activated inward rectifier (IKACh) was present only in atrial cells, while ATP-sensitive K+ current (IKATP) was activated by a mitochondrial blocker, CCCP, in both atrial and ventricular cells. The most striking difference to other fishes appeared in Ca2+ currents (ICa). In atrial myocytes, ICa was predominated by nickel-sensitive and nifedipine-resistant T-type ICa, while ventricular myocytes had mainly nifedipine-sensitive and nickel-resistant L-type ICa. ICaT/ICaL ratio of the sturgeon atrial myocytes (2.42) is the highest value ever measured for a vertebrate species. In ventricular myocytes, ICaT/ICaL ratio was 0.09. With the exception of the large atrial ICaT and small ventricular IK1, electrical excitability of A. baerii heart is similar to that of teleost hearts.

The mammalian skeletal muscle DHPR has larger Ca2+ conductance and is phylogenetically ancient to the early ray-finned fish sterlet (Acipenser ruthenus)

“…We used gar-α 1C as a cardiac reference sequence because sterlet α 1C sequence is not available so far. However, sterlet cardiac Ca 2+ currents have been characterized as fast activating and inactivating [38] similar to mammalian cardiac L-type currents [10,36]. Altogether, it appears that the identified amino acid exchanges in the IS3 and IS3-IS4 linker region of st-α 1S are responsible for its α 1C -type accelerated current activation kinetics.…”

Warmer, faster, stronger: Ca2+ cycling in avian myocardium

“…2D), which should inactivate any potential I CaT and allowed us to record I CaL only. Indeed, the component activated by square pulses from V h =−90 mV and inactivated at V h =−50 mV has been referred to as I CaT (Haworth et al, 2014). The corresponding current-voltage relationship for I Ca in atrial and ventricular myocytes (Fig.…”

Expression of calcium channel transcripts in the zebrafish heart: dominance of T-type channels

“…In contrast, a large cardiac I CaT has previously been documented for a few endothermic and ectothermic vertebrates. A relatively large I CaT exists in ventricular myocytes of finch (5.9 pA pF −1 ; 56% of I CaL ; Bogdanov et al, 1995) and shark (S. acanthias; −9.8 pA pF −1 ; 92.4% of I CaL ; Maylie and Morad, 1995), and atrial myocytes of the Siberian sturgeon (A. baerii; 3.52 pA pF −1 ; 242% of I CaL ) (Haworth et al, 2014). The peak density of I CaT in zebrafish ventricular myocytes is 2-6 times higher than the reported I CaT density in atrial and nodal tissues of other vertebrate species (for references, see Maylie and Morad, 1995).…”

“…I CaL has been recorded in atrial and ventricular myocytes of several fish species including the zebrafish (Danio rerio) (Maylie and Morad, 1995;Vornanen, 1997Vornanen, , 1998Hove-Madsen and Tort, 1998;Vornanen et al, 2002;Shiels et al, 2006;Brette et al, 2008;Zhang et al, 2011;Galli et al, 2011;Haworth et al, 2014;Haverinen et al, 2014). I CaT has been shown to be present in atrial and ventricular myocytes of the dogfish (Squalus acanthias) and zebrafish hearts, and in atrial myocytes of the Siberian sturgeon (Acipenser baerii) heart (Maylie and Morad, 1995;Warren et al, 2001;Nemtsas et al, 2010;Haworth et al, 2014). In contrast to the rich data on the mammalian cardiac Ca 2+ channels, very little is known about Ca 2+ channels of the fish heart, even though sarcolemmal Ca 2+ channels play a central role in cardiac E-C coupling of fish (Vornanen et al, 2002;Zhang et al, 2011).…”