Sarcoplasmic reticulum: a key factor in cardiac contractility of sea bass Dicentrarchus labrax and common sole Solea solea during thermal acclimations

Abstract

This study investigated the effects of acclimation temperature upon (i) contractility of ventricular strips (ii) calcium movements in ventricular cardiomyocytes during excitation-contraction coupling (ECC), and (iii) the role of the sarcoplasmic reticulum (SR) in myocardial responses, in two marine teleosts, the sea bass (Dicentrarchus labrax) and the common sole (Solea solea). Because of the different sensitivities of their metabolism to temperature variation, both species were exposed to different thermal ranges. Sea bass were acclimated to 10, 15, 20, and 25 °C, and common sole to 6, 12, 18, and 24 °C, for 1 month. Isometric tension developed by ventricular strips was recorded over a range of physiological stimulation frequencies, whereas the depolarization-induced calcium transients were recorded on isolated ventricular cells through hyperpotassic solution application (at 100 mM). The SR contribution was assessed by ryanodine (RYAN) perfusion on ventricular strips and by caffeine application (at 10 mM) on isolated ventricular cells. Rates of contraction and relaxation of ventricular strip, in both species, increased with increasing acclimation temperature. At a low range of stimulation frequency, ventricular strips of common sole developed a positive force-frequency relationship at high acclimation temperature. In both the species, SR Ca(2+)-cycling was dependent on fish species, acclimation temperature and pacing frequency. The SR contribution was more important to force development at low acclimation temperatures in sea bass but at high acclimation temperatures in common sole. The results also revealed that high acclimation temperature causes an increase in the maximum calcium response amplitude on ventricular cells in both the species. Although sea bass and common sole occupy similar environments and tolerate similar environmental temperatures, this study indicated that sea bass and common sole can acclimatize to new thermal conditions, adjusting their cellular process in a different manner.

Temperature dependence of cardiac sarcoplasmic reticulum and sarcolemma in the ventricle of catfish (Clarias gariepinus)

“…Our study on the fresh water catfish showed that at 20°C, SR contribution is involved at 0.2 and 0.4 Hz pacing frequencies with cardiac force falling by approximately 21% after caffeine treatment and cardiac force increasing by approximately 40% and 18% at 0.2 and 0.4 Hz pacing frequencies after adrenaline treatment. This is in contrast to previous studies which indicated that the SR involvement is limited to low pacing frequency (0.2 Hz) (Shiels and Farrell, 1997;Shiels et al, 1998;Imbert-Auvray et al, 2013). Furthermore, our study showed that the SR-Ca 2+ release contribution is involved at The number of ventricular preparation in each series was 6. d Non significant as compared with control.…”

“…Previous studies have extensively examined and discussed the significance of SR-Ca 2+ release to ventricular force development in marine ectothermic animals at cold and warm temperature (Shiels and Farrell, 1997;Shiels et al, 1998Shiels et al, , 2002Vornanen et al, 2002;Imbert-Auvray et al, 2013). Results of these studies indicate that the role of SR is secondary to that of the sarcolemmal Ca 2+ influx in supplying Ca 2+ for the force development.…”

Reduced n-3 highly unsaturated fatty acids dietary content expected with global change reduces the metabolic capacity of the golden grey mullet

“…For example, the effects of adrenaline were mainly observed in cold-acclimated teleosts (perch: Tirri and Ripatti 1982;Tirri and Lehto 1984;rainbow trout: Graham and Farrell 1989;Keen et al 1994). Moreover, SR-Ca 2+ loading and mobilisation have been shown to depend on species and thermal acclimation (Imbert-Auvray et al 2013).…”

Ocean warming combined with lower omega-3 nutritional availability impairs the cardio-respiratory function of a marine fish

“…From a functional standpoint, this indicates that the cardiac contraction at 12°C depends more on the mobilisation efficiency of intracellular Ca 2+ stored in the SR than on an extracellular Ca 2+ source. This increase in the SR channel contribution to Ca 2+ mobilisation, as usually found in cold-acclimated fish (Imbert-Auvray et al, 2013;Keen et al, 1994;Shiels et al, 2002;Vornanen, 1996Vornanen, , 1998 could be explained by a SR proliferation in heart cells (Bowler and Tirri, 1990;Keen et al, 1994Keen et al, , 2017Shiels and Farrell, 1997;Shiels et al, 2011), a higher ryanodine sensitivity (Vornanen et al, 2005) and/or a partial (or complete) inactivation, due to cold, of the SL channels/exchanger allowing extracellular Ca 2+ influx into the cells (Vornanen, 1998;Vornanen et al, 2002).…”