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First published online August 3, 2006
Journal of Experimental Biology 209, 3091-3100 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02321

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Sarcolemmal ion currents and sarcoplasmic reticulum Ca²⁺ content in ventricular myocytes from the cold stenothermic fish, the burbot (Lota lota)

Holly A. Shiels^1,*, Vesa Paajanen² and Matti Vornanen²

¹ Faculty of Life Sciences, University of Manchester, 2.18c Core Technology Facility, 46 Grafton Street, Manchester, M13 9NT, UK
² Department of Biology, University of Joensuu, PO Box 11, 80101 Joensuu, Finland

^* Author for correspondence (e-mail: holly.shiels{at}manchester.ac.uk)

Accepted 10 May 2006

The burbot (Lota lota) is a cold stenothermic fish species whose heart is adapted to function in the cold. In this study we use whole-cell voltage-clamp techniques to characterize the electrophysiological properties of burbot ventricular myocytes and to test the hypothesis that changes in membrane currents and intracellular Ca²⁺ cycling associated cold-acclimation in other fish species are routine for stenothermic cold-adapted species. Experiments were performed at 4°C, which is the body temperature of burbot for most of the year, and after myocytes were acutely warmed to 11°C, which is in the upper range of temperatures experienced by burbot in nature. Results on K⁺ channels support our hypothesis as the relative density of K-channel conductances in the burbot heart are similar to those found for cold-acclimated cold-active fish species. I_K1 conductance was small (39.2±5.4 pS pF^-1 at 4°C and 71.4±1.7 pS pF^-1 at 11°C) and I_Kr was large (199±27 pS pF^-1 at 4°C and 320.3±8 pS pF^-1 at 11°C) in burbot ventricular myocytes. We found high Na⁺-Ca²⁺ exchange (NCX) activity (35.9±6.3 pS pF^-1 at 4°C and 58.6±8.4 pS pF^-1 at 11°C between -40 and 20 mV), suggesting that it may be the primary pathway for sarcolemmal (SL) Ca²⁺ influx in this species. In contrast, the density (I_Ca, 0.81±0.13 pA pF^-1 at 4°C, and 1.35±0.18 pA pF^-1 at 11°C) and the charge (Q_Ca, 0.24±0.043 pC pF^-1 at 4°C and 0.21±0.034 pC pF^-1 at 11°C) carried by the L-type Ca²⁺ current was small. Our results on sarcolemmal ion currents in burbot ventricular myocytes suggest that cold stenothermy and compensative cold-acclimation involve many of the same subcellular adaptations that culminate in enhanced excitability in the cold.

Key words: action potential, Na⁺-Ca²⁺ exchange, L-type Ca²⁺ channel, K⁺ channel, I_Ca, I_Kr, I_K1, sarcoplasmic reticulum (SR), temperature, fish heart, caffeine, isoprenaline, burbot, Lota lota

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