Effects of seasonal acclimatization on thermal tolerance of inward currents in roach (Rutilus rutilus) cardiac myocytes

To test the hypothesis of temperature-dependent deterioration of electrical excitability (TDEE) (Vornanen, J Exp Biol 219:1941-1952, 2016), the role of sodium (I (Na)) and calcium (I (Ca)) currents in heat tolerance of cardiac excitability was examined in a eurythermic fish, the roach (Rutilus rutilus). Densities of cardiac I (Ca) and I (Na) and their acute heat tolerance were measured in winter-acclimatized (WiR) and summer-acclimatized (SuR) fish maintained in the laboratory at 4 +/- 1 and 18 +/- 1 A degrees C, respectively. A robust L-type Ca2+ current (I (CaL)), but no T-type Ca2+ current, was present in roach atrial and ventricular myocytes. Peak density of I (CaL) was smaller in atrial (- 1.97 +/- 0.14 and - 1.75 +/- 0.19 pA/pF for WiR and SuR, respectively) than ventricular myocytes (- 4.00 +/- 0.59 and - 2.88 +/- 0.47 pA/pF for WiR and SuR, respectively) (p < 0.05), but current density and heat tolerance of I (CaL) did not change between seasons in either cell type. In contrast to I (Ca), marked differences appeared in I (Na) between WiR and SuR. I (Na) density was 38% higher in WiR than SuR atrial myocytes (- 80.03 +/- 5.92 vs. - 49.77 +/- 4.72 pA/pF; p < 0.05) and 48% higher in WiR than SuR ventricular myocytes (- 39.25 +/- 3.06 vs. - 20.03 +/- 1.79 pA/pF; p < 0.05). The winter increase in I (Na) density was associated with 55% (1.70 +/- 0.27 vs. 0.77 +/- 0.12) and 54% (1.08 +/- 0.19 vs. 0.50 +/- 0.10) up-regulation of the total Na+ channel (scn4 + scn5 + scn8) transcripts in atrium and ventricle, respectively (p < 0.05). Heat tolerance of atrial I (Na) was lower in WiR with a breakpoint temperature of 20.3 +/- 1.2 A degrees C than in SuR (23.8 +/- 0.7 A degrees C) (p < 0.05). The response of I (Na) to seasonal acclimatization conforms to the TDEE hypothesis. The lower heat tolerance of I (Na) in WiR is consistent with the lower heat tolerance of in vivo heart rate in WiR in comparison to SuR, but the match is not quantitatively perfect, suggesting that other factors in addition to I (Na) may be involved.