Comparison of sarcoplasmic reticulum calcium content in atrial and ventricular myocytes of three fish species

Abstract

Ryanodine (Ry) sensitivity of cardiac contraction differs between teleost species, between atrium and ventricle, and according to the thermal history of the fish. The hypothesis that variability in Ry sensitivity of contraction is due to species-specific, chamber-specific, and temperature-related differences in the sarcoplasmic reticulum (SR) Ca(2+) content, was tested by comparing steady-state (SS) and maximal (Max) Ca(2+) loads of the SR in three teleost fish, rainbow trout (Oncorhynchus mykiss), burbot (Lota lota), and crucian carp (Carassius carassius), which differ in the extent of SR contribution to excitation-contraction coupling. Fish were acclimated at 4 degrees C (cold-acclimation, CA) or 18 degrees C (warm-acclimation, WA), and SR Ca(2+) content was released by a rapid application of 10 mM caffeine to single cardiac myocytes; its amount was determined from the Na(+)-Ca(2+) exchange current at 18 degrees C. SS Ca(2+) load was larger in atrial (304-915 micromol/l) than ventricular (224-540 micromol/l) myocytes in all fish species (P < 0.05), and the same was true for Max SR Ca(2+) content: 550-1,522 micromol/l and 438-840 micromol/l for atrial and ventricular myocytes, respectively (P < 0.05). Consistent with the hypothesis, acclimation to cold increased Ca(2+) load of the cardiac SR in the burbot heart, but contrary to the hypothesis, temperature acclimation did not affect SR Ca(2+) content in rainbow trout and crucian carp hearts. Furthermore, there was an inverse relation between SR Ca(2+) content and Ry sensitivity of contraction force: the species with the smallest SR Ca(2+) content (burbot) is most sensitive to Ry. Collectively, these findings show that SR Ca(2+) content of fish cardiac myocytes is several times larger than that in mammalian cardiac SR.