Abstract
We demonstrate for the first time in this study that triadic vesicles derived from skeletal muscle display a voltage dependence of depolarization-induced calcium release similar to that found in intact muscle. We confirm previous studies by Dunn (1989) which demonstrated that changes in extravesicular potassium induced membrane potential changes in isolated transverse tubules with the voltage sensitive dye DiSC(3)-5. Depolarization-induced calcium release was studied in isolated triadic vesicles through similar changes in extravesicular [K] while clamping extravesicular Ca++ to submicromolar concentrations. The amplitude of fast phase of calcium release, identified as depolarizationinduced calcium release, varied with the percentage of transverse tubules in the preparation (determined through 3 H-PN200-110 specific activity) and different levels of depolarization. Threshold activation of calcium release was obtained with a 40.5 mV potential change; maximal calcium release was obtained with a 75 to 81 mV potential change. Boltzmann fits to the normalized depolarization induced calcium release plotted against the membrane potential change yielded a voltage dependence (k = 4.5 mV per e-fold change) very similar to that found in intact muscle (k = 3–4 mV per e-fold change; Baylor, Chandler & Marshall 1978, 1983; Miledi et al., 1981). Substitution of methanesulfonate for propionate as the impermeant ion or addition of valinomycin in the depolarizing solutions had little effect on the voltage dependence of calcium release.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Baylor, S.M., Chandler, W.K., Marshall, M.W. 1978. Arsenazo III signals in singly dissected frog twitch fibers. J. Physiol. 287:23–24P
Baylor, S.M., Chandler, W.K., Marshall, M.W. 1983. Sarcoplasmic reticulum calcium release in frog skeletal muscle fibres estimated from arsenazo III calcium transients. J. Physiol. 344:625–666
Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein dye binding. Analytical Biochemistry 72:248–254
Cabrini, G., Verkman, A.S. 1986. Potential-sensitive response mechanism of DiS-C3-(5) in biological membranes. J. Membrane Biol. 92:171–182
Corbett, A.M., Bian, J., Wade, J.B., Schneider, M.F. 1992. Depolarization-induced calcium release from isolated triads measured with impermeant fura-2. J. Membrane Biol. 128:165–179
Delbono, O., Stefani, E. 1993. Calcium transients in single mammalian skeletal muscle fibers. J. Physiol. 463:689–707
Donaldson, S.K.B. 1985. Peeled mammalian skeletal muscle fibers: Possible stimulation of Ca2+ release via transverse tubulesarcoplasmic reticulum mechanism. J. Gen. Physiol 86:501–525
Dunn, S.M.J. 1989. Voltage-dependent calcium channels in skeletal muscle transverse tubules: measurements of calcium efflux in membrane vesicles. J. Biol. Chem. 264:11053–11060
Grynkiewicz, G., Poenie, M., Tsien, R.Y. 1985. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:3440–3450
Hidalgo, C., Parra, C., Riquelme, G., Jaimovich, E. 1986. Transverse tubules from frog skeletal muscle. Purification and properties of vesicles sealed with the inside-out orientation. Biochem. Biophys. Acta 855:79–88
Ikemoto, N., Antoniu, B. 1993. Depolarization-induced calcium release from SR in vitro: Its dependence on the magnitude of t-tubule depolarization. Biophys. J. 64:A9 (Abstract)
Ikemoto, N., Antoniu, B., Kang, J. 1992. Characterization of “depolarization”-induced calcium release from sarcoplasmic reticulum in vitro with the use of membrane potential probe. Biochem. Biophys. Res Comm. 184:538–543
Ikemoto, N., Antoniu, B., Kim, D.H. 1984. Rapid calcium release from isolated sarcoplasmic reticulum is triggered via the attached transverse tubular system. J. Biol. Chem. 259:13151–13158
Ikemoto, N., Bozena, A., Meszaros, L.G. 1985. Rapid flow chemical quench studies of calcium release from isolated sarcoplasmic reticulum. J. Biol. Chem. 260:14096–14100
Imagawa, T., Smith, J., Coronado, R., Campbell, K. 1987. Purified ryanodine receptor from skeletal muscle sarcoplasmic reticulum is the Ca2+-permeable pore of the calcium release channel. J. Biol. Chem. 262:16636–16643
Klein, M.G., Simon, B.J., Schneider, M.F. 1992. Effects of procaine and caffeine on calcium release from the sarcoplasmic reticulum in frog skeletal muscle. J. Physiol. 453:341–366
Lamb, G.D., Stephenson, D.G. 1990. Control of calcium release in skinned muscle fibres of the toad. J. Physiol. 423:519–542
Meissner, G. 1984. Adenine nucleotide stimulation of Ca2+-induced Ca2+ release in sarcoplasmic reticulum. J. Biol. Chem. 259:2365–2374
Meissner, G. 1986. Kinetics of rapid Ca2+ release by sarcoplasmic reticulum. Effects of Ca2+, Mg2+, and adenine nucleotides. Biochemistry 25:244–250
Melzer, W., Schneider, M.F., Simon, B.J. Szücs, G. 1986. Intramembrane charge movement and calcium release in frog skeletal muscle. J. Physiol. 373:481–511
Miledi, R., Nakajima, S., Parker, I., Takahashi, T. 1981. Effects of membrane polarization on sarcoplasmic calcium release in skeletal muscle. Proc. R. Soc. London, B: Biological Sciences. 213:1–13
Miledi, R., Parker, I., Schaow, G. 1977. Measurements of calcium transients in frog muscle by the use of arsenazo III. Proc. R. Soc. London. B: Biological Sciences. 198:201–210
Ohkusa, T., Carlos, A.D., Kang, J.-J., Smilowitz, H., Ikemoto, N. 1991. Effects of dihydropyridines on calcium release from the isolated membrane complex consisting of the transverse tubule and sarcoplasmic reticulum. Biochem. Biophys. Res. Commun. 175:271–276
Ohkusa, T., Smilowitz, H.M., Ikemoto, N. 1990. Effects of the dihydropyridine (DHP) receptor-specific agents on depolarizationinduced Ca2+ release from SR in vitro. Biophys. J. 57:498a (Abstr.)
Palade, P. 1987. Drug-induced Ca release from isolated sarcoplasmic reticulum. I. Use of pyrophosphate to study caffeine-induced Ca2+ release. J. Biol. Chem. 262:6142–6148
Ríos, E., Brum, G. 1987. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 325:717–720
Schneider, M.F., Chandler, W.K. 1973. Voltage dependent charge movement in skeletal muscle: a possible step in excitation contraction coupling. Nature 242:244–246
Sims, P.J., Waggoner, A.S., Wang, C.H., Hoffman, J.F. 1974. Studies on the mechanism by which cyanine dyes measure membrane potential in red blood cells and phosphatidylcholine vesicles. Biochemistry 13:3315–3330
Stephenson, E.W. 1985. Excitation of skinned muscle fibers by imposed ion gradients. I. Stimulation of 45Ca efflux at constant [K][C1] product. J. Gen. Physiol. 86:813–832
Stephenson, E.W. 1989. Excitation of skinned muscle fibers by imposed ion gradients. IV. Effects of stretch and perchlorate ion. J. Gen. Physiol. 93:173–192
Szücs, G., Simon, B.S., Schneider, M.F. (1984). Voltage dependence of calcium release and intramembrane charge movement in frog skeletal muscle. J. Gen. Physiol. 84:35a (Abstr.)
Volpe, P., Stephenson, E.W. 1986. Ca2+ dependence of transverse tubule-mediated calcium release in skinned skeletal muscle fibers. J. Gen. Physiol. 87:271–288
Author information
Authors and Affiliations
Additional information
We thank Dr. Judith Heiny for her helpful discussions about voltagesensitive fluorescent dyes. This work was supported by the American Heart Association (Ohio Affiliate) grant MV-90 and the State of Ohio Research Challenge Grant.
Rights and permissions
About this article
Cite this article
Kramer, J.W., Corbett, A.M. The voltage dependence of depolarization-induced calcium release in isolated skeletal muscle triads. J. Membarin Biol. 144, 217–230 (1995). https://doi.org/10.1007/BF00236835
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00236835