Summary
Calcium efflux was measured in desheathed rabbit vagus nerves loaded with45Ca2+. The effects of extracellular calcium, sodium, phosphate, potassium and lanthanum ions on the calcium efflux were investigated and the distribution of intracellular calcium determined by kinetic analysis of45Ca2+ efflux profiles. The45Ca2+ desaturation curve can be adequately described by three exponential terms. The rate constant of the first component (0.2 min−1) corresponds to an efflux from an extracellular compartment. The two slow components had rate constants of 0.03 and 0.08 min−1 and represent the efflux from two intracellular pools. The amounts of exchangeable calcium in these two pools, after a loading period of 150 min, were 0.170 and 0.102 mmol/kg wet weight, respectively. The total calcium efflux in physiological conditions amounted to about 24 fmol cm−2 sec−1. The magnitude of the two intracellular compartments as well as the total calcium efflux were markedly affected by extracellular phosphate, sodium and lanthanum, whereas the corresponding rate constants remained almost unchanged. Phosphate reversed the effect of sodium withdrawal on the calcium efflux: in the absence of phosphate, sodium withdrawal increased the calcium efflux to 224%, but in the presence of phosphate, sodium withdrawal decreased calcium efflux to 44%. Phosphate also affected the increase in calcium efflux produced by inhibitors of mitochondrial calcium uptake, suggesting that two different mitochondrial pools contribute to the control and regulation of intracellular calcium and of the transmembrane calcium transport.
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Affolter, H., Carafoli, E. 1980. The Ca2+−Na+ antiporter of heart mitochondria operates electroneutrally.Biochem. Biophys. Res. Commun. 95:193–196
Anner, B., Ferrero, J., Jirounek, P., Jones, G.J., Salamin, A., Straub, R.W. 1976. Sodium-dependent influx of orthophosphate in mammalian non-myelinated nerve.J. Physiol. (London) 260:667–686
Baker, P.F., Schlaepfer, W. 1975. Calcium uptake by axoplasm extruded from giant axons ofLoligo.J. Physiol. (London) 249:37P-38P
Baker, P.F., Schlaepfer, W.W. 1978. Uptake and binding of calcium by axoplasm isolated from giant axons ofLoligo andMyxicola.J. Physiol. (London) 276:103–125
Barritt, G.J. 1981. Evidence for two compartments of exchangeable calcium in isolated rat liver mitochondria obtained using a45Ca exchange technique in the presence of magnesium, phosphate, and ATP at 37°C.J. Membrane Biol. 62:53–63
Barritt, G.J., Lamont, S.V. 1982. Kinetic properties of exchangeable calcium in guinea-pig heart mitochondria measured at low concentrations of free calcium and in the presence of Mg2+, ATP4-, and inorganic phosphate.Cell Calcium 3:215–225
Blaustein, M.P. 1977. Effects of internal and external cations and of ATP on sodium-calcium and calcium-calcium exchange in squid axons.Biophys. J. 20:79–111
Blaustein, M.P., Ratzlaff, R.W., Kendrick, N.C., Schweitzer, E.S. 1978b. Calcium buffering in presynaptic nerve terminals. I. Evidence for involvement of a nonmitochondrial ATP-dependent sequestration mechanism.J. Gen. Physiol. 72:15–41
Blaustein, M.P., Ratzlaff, R.W., Schweitzer, E.S. 1978a. Calcium buffering in presynaptic nerve terminals. II. Kinetic properties of the nonmitochondrial Ca sequestration mechanism.J. Gen. Physiol. 72:43–66
Blaustein, M.P., Ratzlaff, R.W., Schweitzer, E.S. 1980. Control of intracellular calcium in presynaptic nerve terminals.Fed. Proc. 39:2790–2795
Borle, A.B. 1972. Kinetic analysis of calcium movements in cell culture. V. Intracellular calcium distribution in kidney cells.J. Membrane Biol. 10:45–66
Brinley, F.J., Jr., Tiffert, T., Scarpa, A. 1978. Mitochondria and other calcium buffers of squid axon studiedin situ.J. Gen. Physiol. 72:101–127
Brinley, F.J., Jr., Tiffert, T., Scarpa, A., Mullins, L.J. 1977. Intracellular calcium buffering capacity in isolated squid axons.J. Gen. Physiol. 70:355–384
Carafoli, E., Crompton, M. 1978. The regulation of intracellular calcium.In: Current Topics in Membranes and Transport. F. Bronner and A. Kleinzeller, editors. pp. 151–199. Academic, New York/San Francisco/London
Crompton, M., Capano, M., Carafoli, E. 1976. The sodium-induced efflux of calcium from heart mitochondria.Eur. J. Biochem. 69:453–462
DiPolo, R., Requena, J., Brinley, F.J., Jr., Mullins, L.J., Scarpa, A., Tiffert, T. 1976. Ionized calcium concentrations in squid axons.J. Gen. Physiol. 67:433–467
Fiskum, G., Lehninger, A.L. 1982. Mitochondrial regulation of intracellular calcium.In: Calcium and Cell Function, C. Wy, editor. Vol. 2, pp. 39–80. Academic, New York
Jirounek, P., Jones, G.J., Pralong, W.F., Straub, R.W. 1983. Continuous measurement of Ca movements in mammalian nerve fibers using45Ca.J. Physiol. (London) 334:117P-118P
Jirounek, P., Nouspikel, T., Pralong, W., Vitus, J., Straub, R.W. 1984a. Effects of phosphate and sodium on calcium influx in mammalian non-myelinated nerve fibers.Experientia 40:647
Jirounek, P., Pralong, W.F., Vitus, J., Straub, R.W. 1986. Continuous measurement of calcium influx in mammalian nonmyelinated nerve fibers: Effects of Nao, Cao, and electrical activity.J. Membrane Biol. 91:157–164
Jirounek, P., Rouiller, M., Jones, G.J., Straub, R.W. 1982. Effects of calcium and lanthanum on phosphate efflux from nonmyelinated nerve fibers.J. Membrane Biol. 65:125–130
Jirounek, P., Vitus, J., Jones, G.J., Pralong, W.F., Straub, R.W. 1984b. Involvement of intracellular calcium in the phosphate efflux from mammalian nonmyelinated nerve fibers.J. Membrane Biol. 79:87–95
McGraw, C.F., Somylo, A.V., Blaustein, M.P. 1980. Probing for calcium at presynaptic nerve terminals.Fed. Proc. 39:2796–2801
Marquardt, D.W. 1963. An algorithm for least-squares estimation of nonlinear parameters.J. Soc. Ind. Appl. Math. 11:431–441
Martonosi, A., Feretos, R. 1964. Sarcoplasmic reticulum. I. The uptake of Ca++ by sarcoplasmic reticulum fragments.J. Biol. Chem. 239:648–658
Nicholls, D., Akerman, K. 1982. Mitochondrial calcium transport.Biochim. Biophys. Acta 683:57–88
Ponce-Hornos, J.E., Langer, G.A. 1982. Effects of inorganic phosphate on ion exchange, energy state, and contraction in mammalian heart.Am. J. Physiol. 242:H79-H88
Ponce-Hornos, J.E., Langer, G.A., Nudd, L.M. 1982. Inorganic phosphate: Its effects on Ca exchange and compartmentalization in cultured heart cells.J. Mol. Cell. Cardiol. 14:41–51
Pralong, W.F., Jirounek, P., Straub, R.W. 1985. Changes in free calcium in mammalian nonmyelinated nerve fibers followed by quin-2.Experientia 41:833
Pralong, W.F., Straub, R.W. 1985. Increase in free Ca in rabbit nerve axons during electrical activity measured by quin 2.J. Physiol. (London) 371:266P
Rasgado-Flores, H., Blaustein, M.P. 1987. ATP-dependent regulation of cytoplasmic free calcium in nerve terminals.Am. J. Physiol. 252:C588-C594
Requena, J., DiPolo, R., Brinley, F.J., Jr., Mullins, L.J. 1977. The control of ionized calcium in squid axons.J. Gen. Physiol. 70:329–353
Ritchie, J.M., Straub, R.W. 1979. Phosphate efflux and oxygen consumption in small non-myelinated nerve fibres at rest and during activity.J. Physiol. (London) 287:315–327
Stout, M.A., Diecke, F.P.J. 1981. Effect of K ions on45Ca fluxes in myelinated nerve.Arch. Int. Pharmacodyn. Ther. 252:17–28
Straub, R.W., Ferrero, J., Jirounek, P., Rouiller, M., Salamin, A. 1977. Sodium-dependent transport of orthophosphate in nerve fibres.In: Phosphate Metabolism. S.G. Massry and E. Ritz, editors. pp. 333–334. Plenum, New York
Studer, R.K., Borle, A.B. 1980. The effects of hydrogen ions on the kinetics of calcium transport by rat kidney mitochondria.Arch. Biochem. Biophys. 203:707–718
Tscharner, P. 1982. Décomposition d'exponentielles. Application à la résonance magnétique nucléaire. Travail de diplôme. Faculté des Sciences, Université de Genève
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Jirounek, P., Vitus, J., Pralong, W.F. et al. Calcium efflux and intracellular exchangeable calcium in mammalian nonmyelinated nerve fibers. J. Membrain Biol. 103, 121–134 (1988). https://doi.org/10.1007/BF01870943
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DOI: https://doi.org/10.1007/BF01870943