Summary
The interaction of fragmented sarcoplasmic reticulum (SR) with an artificial planar phospholipid membrane under conditions known to induce fusion of phospholipid vesicles raises the conductance of the planar bilayer by several orders of magnitude. Measurements of steady-state electrical properties of bilayers thus modified by SR show that two types of conductance pathways are present. One is a voltage-independent pathway which may be somewhat anion-selective. The other is a voltagegated ionophore showing selectivity to small monovalent cations. This latter ionophore is fully oriented within the artificial bilayer and is inhibited asymmetrically by divalent cations. It is also inhibited below pH 6. The ionophore displays single-channel conductance fluctuations between two states, “open” and “closed”, with an open-state conductance of 1.4×10−10 mho in 0.1m K+. The physiological function of this ionophore is unknown.
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References
Armstrong, C.M. 1975. Ionic pores, gates, and gating currents.Q. Rev. Biophys. 7: 179
Bamberg, E., Janko, K. 1976. Single channel conductance at lipid bilayer membranes in presence of monazomycin.Biochim. Biophys. Acta 426: 447
Baumann, G., Mueller, P. 1974. A molecular model of membrane excitability.J. Supramol. Struct. 2: 538
Bean, R.C., Chan, W.C., Eichner, H.J. 1969. Discrete conductance fluctuations in lipid bilayer protein membranes.J. Gen. Physiol. 53: 741
Boheim, G. 1974. Statistical analysis of alamethicin channels in black lipid membranes.J. Membrane Biol. 19: 277
Constantin, L.L., Podolsky, R.J. 1967. Depolarization of the internal membrane system in the activation of frog skeletal muscle.J. Gen. Physiol. 50: 1101
DeBoland, A.R., Jilka, R.L., Martonosi, A.N. 1975. Passive Ca2+ permeability of phospholipid vesicles and sarcoplasmic reticulum membranes.J. Biol. Chem. 250: 7501
Düzgünes, N., Ohki, S. 1977. Calcium-induced interaction of phospholipid vesicles and bilayer lipid membranes.Biochim. Biophys. Acta 467: 301
Ebashi, S. 1976. Excitation-contraction coupling.Annu. Rev. Physiol. 38: 293
Ehrenstein, G., Blumenthal, R., Latorre, R., Lecar, H. 1974. Kinetics of the opening and closing of individual excitability-inducing material channels in a lipid bilayer.J. Gen. Physiol. 63: 707
Ehrenstein, G., Lecar, H. 1977. Electrically gated ionic channels in lipid bilayers.Q. Rev. Biophys. 10: 1
Ehrenstein, G., Lecar, H., Nossal, R. 1970. The nature of the negative resistance in bimolecular lipid membranes containing excitability-inducing material.J. Gen. Physiol. 55: 119
Eisenberg, M., Hall, J.E., Mead, C.A. 1973. The nature of the voltage-dependent conductance induced by alamethicin in black lipid membranes.J. Membrane Biol. 14: 143
Eisenman, G., Szabo, G., McLaughlin, S.G.A., Ciani, S.M. 1973. Molecular basis for the action of macrocyclic carriers on passive ionic translocation across lipid bilayer membranes.Bioenergetics 4: 93
Endo, M. 1977. Calcium release from sarcoplasmic reticulum.Physiol. Rev. 57: 71
Frankenhaeuser, B., Hodgkin, A.L. 1957. The action of calcium on the electrical properties of squid axons.J. Physiol. (London) 137: 217
Gordon, L.G.M., Haydon, D.A. 1972. The unit conductance channel of alamethicin.Biochim. Biophys. Acta 255: 1014
Gordon, L.G.M., Haydon, D.A. 1976. Kinetics and stability of alamethicin-conducting channels in lipid bilayers.Biochim. Biophys. Acta 436: 541
Haydon, D.A., Hladky, S.B. 1972. Ion transport across thin lipid membranes: A critical discussion of mechanisms in selected systems.Q. Rev. Biophys. 5: 187
Hladky, S.B., Haydon, D.A. 1970. Discreteness of conductance change in bimolecular lipid membranes in the presence of certain antibiotics.Nature (London) 225: 451
Inesi, G., Malan, N. 1976. Mechanisms of calcium release in sarcoplasmic reticulum.Life Sci. 18: 773
Kagawa, Y., Racker, E. 1971. Partial resolution of the enzymes catalyzing oxidative phosphorylation. XXV. Reconstitution of particles catalyzing32Pi-adenosine triphosphate exchange.J. Biol. Chem. 246: 5477
Kasai, M., Miyamoto, H. 1973. Depolarization-induced calcium release from SR membrane fragments by changing ionic environments.FEBS Lett. 34: 299
Kasai, M., Miyamoto, H. 1976a. Depolarization-induced calcium release from sarcoplasmic reticulum fragments. I. Release of calcium taken up upon using ATP.J. Biochem. 79: 1053
Kasai, M., Miyamoto, H. 1976b. Depolarization-induced calcium release. II. Release of calcium incorporated without ATP.J. Biochem. 79: 1067
Latorre, R., Alvarez, O., Ehrenstein, G., Espinoza, M., Reyes, J. 1975. The nature of the voltage-dependent conductance of the hemocyanin channel.J. Membrane Biol. 25: 163
MacLennan, D.H. 1970. Purification and properties of an adenosine triphosphatase from sarcoplasmic reticulum.J. Biol. Chem. 245: 4508
Meissner, G. 1975. Isolation and characterization of two types of sarcoplasmic reticulum vesicles.Biochim. Biophys. Acta 389: 51
Meissner, G., McKinley, D. 1976. Permeability of sarcoplasmic reticulum membrane. The effect of changed ionic environments on Ca2+ release.J. Membrane Biol. 30: 79
Miller, C., Racker, E., 1976. Ca++-induced fusion of fragmented sarcoplasmic reticulum with artificial planar bilayers.J. Membrane Biol. 30: 283
Montal, M., Mueller, P. 1972. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties.Proc. Nat. Acad. Sci. USA 69: 3561
Mueller, P., Rudin, D.O. 1969. Bimolecular lipid membranes. Techniques of formation, study of electrical properties, and induction of gating phenomena.In: Laboratory Techniques in Membrane Biophysics. H. Passow and R. Stämpfli, editors. pp. 141–156. Springer-Verlag, Berlin
Muller, R.U., Finkelstein, A. 1972. The effect of surface charge on the voltage-dependent conductance induced in thin lipid membranes by monazomycin.J. Gen. Physiol. 60: 285
Neher, E., Sackmann, B. 1976. Single channel currents recorded from membrane of denervated frog muscle fibres.Nature (London) 260: 779
Sergeyeva, N.S., Poglazov, A.F., Vladimirov, Yu.A. 1975. Isledovanie pronitzayemos i ploskoi bisloinoi lipidnoi membrani v prisutstvii vezikul sarkoplazmaticheskovo retikuluma.Biofizika 20: 1029
Shamoo, A.E., MacLennan, D.H. 1974. A Ca++-dependent and-selective ionophore as part of the Ca+++Mg++-dependent adenosinetriphosphatase of sarcoplasmic reticulum.Proc. Nat. Acad. Sci. USA 71: 3522
Shamoo, A.E., MacLennan, D.H. 1975. Separate effects of mercurial compounds on the ionophoric and hydrolytic functions of the (Ca+++Mg++)-ATPase of sarcoplasmic reticulum.J. Membrane Biol. 25: 65
Stephenson, E.W., Podolsky, R.J. 1977. Influence of magnesium on chloride-induced calcium release in skinned muscle fibers.J. Gen. Physiol. 69: 17
Thorens, S., Endo, M. 1975. Ca2+-induced Ca2+ release and “depolarization”-induced Ca2+ release: Their physiological significance.Proc. Jpn. Acad. 51: 473
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Miller, C. Voltage-gated cation conductance channel from fragmented sarcoplasmic reticulum: Steady-state electrical properties. J. Membrain Biol. 40, 1–23 (1978). https://doi.org/10.1007/BF01909736
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DOI: https://doi.org/10.1007/BF01909736