Relaxation in ferret ventricular myocytes: unusual interplay among calcium transport systems

• Published in: The Journal of physiology 1994-04, Vol.476 (2), p.295-308
• Main Authors: Bassani, R A, Bassani, J W, Bers, D M
• Format: Article
• Language: English
• Subjects: Animals; Biological and medical sciences; Biological Transport; Caffeine - pharmacology; Calcium - metabolism; Calcium-Transporting ATPases - metabolism; Carrier Proteins - metabolism; Ferrets; Fluorescence; Fundamental and applied biological sciences. Psychology; Half-Life; Heart; In Vitro Techniques; Male; Mitochondria, Heart - metabolism; Mustela putorius furo; Myocardial Contraction - drug effects; Myocardial Contraction - physiology; Myocardium - cytology; Myocardium - enzymology; Myocardium - metabolism; Sarcoplasmic Reticulum - enzymology; Sarcoplasmic Reticulum - metabolism; Sodium - metabolism; Sodium-Calcium Exchanger; Vertebrates: cardiovascular system
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/jphysiol.1994.sp020131

Transport systems responsible for removing Ca2+ from the myoplasm during relaxation in isolated ferret ventricular myocytes were studied using caffeine-induced contractures. Internal calcium concentration ([Ca2+]i) was measured with the fluorescent calcium indicator indo-1, and the results were compared with our recent detailed characterizations in rabbit and rat myocytes. Relaxation and [Ca2+]i decline during a twitch in ferret myocytes were fast and similar to that in rat myocytes (i.e. half-time, t 1/2 approximately 100-160 ms). During a caffeine-induced contracture (SR Ca2+ accumulation prevented), relaxation was still relatively fast (t 1/2 = 0.57 s) and similar to relaxation in rabbit supported mainly by a strong Na(+)-Ca2+ exchange. When both the SR Ca2+ uptake and Na(+)-Ca2+ exchange are blocked (by caffeine and 0 Na+, 0 Ca2+ solution) relaxation in the ferret myocyte is remarkably fast (approximately 5-fold) compared with rabbit and rat myocytes. The decline of the Cai2+ transient was also fast under these conditions. These values were similar to those in rat under conditions where relaxation is due primarily to Na(+)-Ca2+ exchange. Additional inhibition of either the sarcolemmal Ca(2+)-ATPase or mitochondrial Ca2+ uptake caused only modest slowing of the relaxation of caffeine-induced contracture in 0 Na+, 0 Ca2+ (t 1/2 increased to approximately 3 s). In rabbit myocytes the relaxation t 1/2 is slowed to 20-30 s by these procedures. Even when the systems responsible for slow relaxation in rabbit ventricular myocytes are inhibited (i.e. sarcolemmal Ca(2+)-ATPase and mitochondrial Ca2+ uptake) along with the SR Ca(2+)-ATPase and Na(+)-Ca2+ exchange, relaxation and [Ca2+]i decline in ferret myocytes remain rapid compared with rabbit myocytes. Ca2+ taken up by mitochondria in rabbit myocytes during a caffeine contracture in 0 Na+, 0 Ca2+ solution gradually returns to the SR after caffeine removal, but this component appears to be much smaller in ferret myocytes under the same conditions. We tested for possible residual Ca2+ transport by each of the four systems which suffice to explain Ca2+ removal from the cytoplasm in rabbit (SR Ca(2+)-ATPase, Na(+)-Ca2+ exchange, sarcolemmal Ca(2+)-ATPase and mitochondrial Ca2+ uptake). We conclude that there is an additional calcium transport system at work in ferret myocytes. For this additional system, our results are most compatible with a trans-sarcolemmal Ca2+ transport, but neither a cation exchanger nor a