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Journal of Experimental Biology, Vol 200, Issue 11 1607-1621, Copyright © 1997 by Company of Biologists
JOURNAL ARTICLES |
H Shiels and A Farrell
The sarcoplasmic reticulum (SR) is central to intracellular Ca2+ regulation during excitation­contraction (E-C) coupling in mammalian cardiac tissue. The importance of the SR to E-C coupling in lower vertebrates is less certain. This uncertainty can be attributed, in part, to the temperature-dependency of the SR Ca2+-release channel and to interspecific differences in the ryanodine-sensitivity of ectotherm cardiac muscle. Furthermore, the relative importance of the SR in contributing intracellular Ca2+ to force development may be influenced by adrenergic stimulation, which increases trans-sarcolemmal (extracellular) Ca2+ influx. The objective of this study was to assess the relative importance of SR (intracellular) and sarcolemmal (SL; extracellular) Ca2+ fluxes during the isometric contraction of isolated ventricular trabeculae from rainbow trout Oncorhynchus mykiss. To approximate in vivo Ca2+ availability to the muscle better, a tonic level (10 nmol l-1) of adrenaline was used in all control experiments, and SL Ca2+ influx was stimulated with high levels (10 µmol l-1) of adrenaline. Ryanodine, a noted blocker of SR Ca2+ release in mammals, was used to assess SR involvement. To examine the role of temperature on the relative Ca2+ contribution from each source, experiments were performed at two temperatures (12 and 22 °C), using ventricular trabeculae from fish acclimated to both 12 and 22 °C. Under all test conditions studied, SL Ca2+ influx was the primary source of activator Ca2+, as assessed by the change in isometric force after ryanodine application. Even so, the SR contribution of activator Ca2+ was significantly greater at a test temperature of 22 °C than at 12 °C. We attribute this observation to the temperature-dependent nature of the SR Ca2+-release channel. At 22 °C and under control conditions, ryanodine reduced peak tension at all pacing frequencies (by approximately 50 % at 0.2 Hz, approximately 25 % at 1.2 Hz and approximately 20 % at 2.0 Hz), regardless of acclimation temperature. Therefore, the SR is a significant, but secondary, contributor of activator Ca2+ for tension development at warm temperatures. The magnitude of SR Ca2+ contribution was inversely related to pacing frequency, but remained significant at physiological pacing frequencies. This was a novel finding. The degree of ryanodine-sensitivity in the present study was greater than that reported previously for the rainbow trout. We attribute this difference to the use of tonic adrenergic stimulation in the present study. In contrast to the experiments at the warmer test temperature, at 12 °C and under control conditions, ryanodine significantly reduced peak tension only at low frequencies (by approximately 25 % at 0.2 Hz), regardless of acclimation temperature. These findings suggest that at cold temperatures, and at physiologically relevant pacing frequencies, the SR may not be important in supplying Ca2+ to the contractile elements of the trout heart. At both test temperatures and regardless of acclimation temperature, stimulation with 10 µmol l-1 adrenaline caused positive inotropy of sufficient magnitude to ameliorate the negative inotropic effect of ryanodine completely, with the exception of high pacing frequencies (>1.2 Hz) at 22 °C, where adrenergic stimulation did not fully compensate for the effects of ryanodine. This exception is discussed in relation to the reduced adrenergic sensitivity of the trout myocardium at warm temperatures. The adrenergically mediated compensation for the loss of the SR Ca2+ supply is a novel finding for fish hearts. Therefore, while our study clearly demonstrates that the relative importance of SR Ca2+ release is subject to temperature and frequency, adrenaline-mediated increases in SL Ca2+ influx decrease the importance of the SR in contributing Ca2+ to E-C coupling in trout ventricular myofilaments.
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