Acute heat tolerance of cardiac excitation in the brown trout (Salmo trutta fario).
The upper thermal tolerance and mechanisms of heat-induced cardiac failure in the brown trout (Salmo trutta fario) was examined. The point above which ion channel function and sinoatrial contractility in vitro, and electrocardiogram (ECG) in vivo, started to fail (break point temperature, BPT) was determined by acute temperature increases. In general, electrical excitation of the heart was most sensitive to heat in the intact animal (electrocardiogram, ECG) and least sensitive in isolated cardiac myocytes (ion currents). BPTs of Ca(2+) and K(+) currents of cardiac myocytes were much higher (>28°C) than BPT of in vivo heart rate (23.5 ± 0.6°C) (P<0.05). A striking exception among sarcolemmal ion conductances was the Na(+) current (INa), which was the most heat-sensitive molecular function, with a BPT of 20.9 ± 0.5°C. The low heat tolerance of INa was reflected as a low BPT for the rate of action potential upstroke in vitro (21.7 ± 1.2°C) and the velocity of impulse transmission in vivo (21.9 ± 2.2°C). These findings from different levels of biological organization strongly suggest that heat-dependent deterioration of Na(+) channel function disturbs normal spread of electrical excitation over the heart, leading to progressive variability of cardiac rhythmicity (missed beats, bursts of fast beating), reduction of heart rate and finally cessation of the normal heartbeat. Among the cardiac ion currents INa is 'the weakest link' and possibly a limiting factor for upper thermal tolerance of electrical excitation in the brown trout heart. Heat sensitivity of INa may result from functional requirements for very high flux rates and fast gating kinetics of the Na(+) channels, i.e. a trade-off between high catalytic activity and thermal stability.
University of Eastern Finland, Department of Biology, PO Box 111, 80101 Joensuu, Finland.
Matti
M
Vornanen
Jaakko
J
Haverinen
Stuart
S
Egginton
D000064:Acclimatization; D000200:Action Potentials; D000818:Animals; D002118:Calcium / Q000378:metabolism; D006321:Heart / Q000502:physiology*; D006358:Hot Temperature; D011188:Potassium / Q000378:metabolism; D012964:Sodium / Q000378:metabolism; D014337:Trout / Q000502:physiology*
D012964:Sodium; D011188:Potassium; D002118:Calcium
Action potential; Electrocardiogram; Fish heart; High temperature tolerance; Ion current