Seasonal acclimatization of the cardiac potassium currents (I_K1 and I_Kr) in an arctic marine teleost, the navaga cod (Eleginus navaga)

Abstract

Several freshwater fishes of north-temperate latitudes exhibit marked seasonal changes in cardiac action potential (AP) waveform as an outcome of temperature-dependent changes in the density of delayed rectifiers (I_Kr, I_Ks) and inward rectifier (I_K1) potassium currents. Thus far, ionic mechanisms of cardiac excitability in arctic marine fishes have not been examined. To this end we examined ventricular AP and the role of two major potassium currents (I_K1, I_Kr) in repolarization of cardiac AP in winter-acclimatized (WA, caught in March) and summer-acclimatized (SA, caught in September) navaga cod (Eleginus navaga) of the White Sea. The duration of ventricular AP of WA navaga at 3 °C (APD50 = 659.5 ± 32.8 ms) was similar to the AP duration of SA navaga at 12 °C (APD50 = 543.9 ± 14.6 ms) (p > 0.05) indicating complete thermal compensation of AP duration. This acclimation effect was associated with strong up-regulation of the cardiac potassium currents in winter. Densities of ventricular I_K1 (at −120 mV) and I_Kr (at +50 mV) of the WA navaga at 3 °C were 2.9 times and 2.8 times, respectively, higher than those of the SA navaga at 12 °C, thus indicating marked thermal overcompensation. Qualitatively similar results were obtained from atrial myocytes. Seasonal changes in I_K1 and I_Kr are more than sufficient to explain the complete thermal compensation of ventricular AP duration. The excellent acclimation capacity of cardiac excitability of the navaga cod is probably needed to maintain high cardiac performance at subzero temperatures in winter and to increase thermal resilience of cardiac function under seasonally variable arctic temperature conditions.