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

Abstract

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 ) and calcium (I) currents in heat tolerance of cardiac excitability was examined in a eurythermic fish, the roach (Rutilus rutilus). Densities of cardiac I and I 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 °C, respectively. A robust L-type Ca current (I ), but no T-type Ca current, was present in roach atrial and ventricular myocytes. Peak density of I 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 did not change between seasons in either cell type. In contrast to I, marked differences appeared in I between WiR and SuR. I 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 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 was lower in WiR with a breakpoint temperature of 20.3 ± 1.2 °C than in SuR (23.8 ± 0.7 °C) (p< 0.05). The response of I to seasonal acclimatization conforms to the TDEE hypothesis. The lower heat tolerance of I 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 may be involved.

Feeling the heat: source–sink mismatch as a mechanism underlying the failure of thermal tolerance

“…However, the density of the atrial I K1 is small and therefore the R in of atrial myocytes is about an order of magnitude higher than in ventricular myocytes (Vornanen et al, 2002;Haverinen and Vornanen, 2009;Abramochkin and Vornanen, 2015;Badr et al, 2017a). In contrast, the density of atrial I Na is similar to or higher than that of ventricular myocytes (Haverinen and Vornanen, 2006;Badr et al, 2017b). The favorable I Na :I K1 ratio (large safety factor) makes the atrial myocytes easily excitable and protects them against heat-dependent deterioration of excitability.…”

“…However, at critically high temperatures, the safety factor reduces and may be totally lost owing to opposing effects of high temperature on I Na and I K1 (Box 2). Initially, moderate increases in temperature increase the density of both I Na and I K1 , and the excitation of ventricular myocytes is ensured (Vornanen et al, 2014;Badr et al, 2017b;Badr et al, 2018). However, the charge transfer (see Glossary) by I Na starts to decline immediately when temperature rises, because the fast inactivation of the channels allows less time for Na + influx (Fig.…”

“…spontaneously active. The AP upstroke of nodal cells is based on the L-type Ca 2+ current (I CaL ), which is resistant to high temperatures in fish (Vornanen et al, 2014;Badr et al, 2017b). Thus, nodal cells do not experience the antagonism between I Na and I K1 , at least not to the same extent as ventricular myocytes.…”

“…In brief, temperature dependencies of the inward Na + current (I Na ) and the outward K + current (I K1 )two antagonistic ion currents critical for the initiation of cardiac action potentials (APs) (Varghese, 2016) are widely different. I Na is depressed at relatively low temperatures, whereas I K1 is heat resistant and increases almost linearly with rising temperature (Vornanen et al, 2014;Badr et al, 2017b). The temperature-induced mismatch between I Na and I K1 is considered to result in temperature-dependent depression of electrical excitability (EE) (Vornanen, 2016).…”

Electrical excitability of roach (Rutilus rutilus) ventricular myocytes: effects of extracellular K+, temperature, and pacing frequency

“…and brown trout cardiac myocytes (4,46). It is depressed at temperatures where the densities of the outward K + currents, I K1 and I Kr , are still increasing.…”