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

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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 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 °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 °C than in SuR (23.8 ± 0.7 °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.

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Abbreviations

AP:

Action potential

CD:

Critical depolarization

f H :

Heart rate

HP:

Holding potential

I Ca :

Calcium current

I CaL :

L-type calcium current

I CaT :

T-type calcium current

I K1 :

Inward rectifier K+ current

I Na :

Sodium current

OCLTT:

Oxygen- and capacity-limited thermal tolerance hypothesis

SuR:

Summer-acclimatized roach

T BP :

Breakpoint temperature

TDEE:

Temperature-dependent deterioration of electrical excitability hypothesis

TP:

Threshold potential

V 0.5 :

Voltage for half-maximal of activation or inactivation of I CaL

WiR:

Winter-acclimatized roach

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Acknowledgements

AB was supported by a personal grant from the Ministry of Higher Education (Cultural affairs and missions sector) of Egypt and Finnish Cultural foundation. A research Grant from the Academy of Finland (#14955) to MV covered the material costs of the study. We thank Kari Ratilainen for catching the fish and Anita Kervinen for assistance in taking care of the fishes and preparing the solutions.

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Authors and Affiliations

  1. Department of Environmental and Biological Sciences, University of Eastern Finland, P.O. Box 111, 80101, Joensuu, Finland

    Ahmed Badr, Hanna Korajoki & Matti Vornanen

  2. Department of Zoology, Faculty of Science, Sohag University, P.O. Box 82524, Sohag, Egypt

    Ahmed Badr, El-Sabry Abu-Amra & Mohamed F. El-Sayed

Authors
  1. Ahmed Badr
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  2. Hanna Korajoki
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  3. El-Sabry Abu-Amra
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  4. Mohamed F. El-Sayed
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  5. Matti Vornanen
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Corresponding author

Correspondence to Ahmed Badr.

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All experiments were authorized by the national animal experimental board in Finland (permission ESAVI/2832/04.10.07/2015).

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The authors declare that they have no conflict of interest.

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Communicated by G. Heldmaier.

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Badr, A., Korajoki, H., Abu-Amra, ES. et al. Effects of seasonal acclimatization on thermal tolerance of inward currents in roach (Rutilus rutilus) cardiac myocytes. J Comp Physiol B 188, 255–269 (2018). https://doi.org/10.1007/s00360-017-1126-1

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  • DOI: https://doi.org/10.1007/s00360-017-1126-1

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