Summary
Tissue composition, membrane potentials and cellular activity of potassium, sodium and chloride have been measured in innervated and denervated rat skeletal muscles incubatedin vitro. After denervation for 3 days, tissue water, sodium and chloride were increased but cellular potassium content and measured activity were little affected, despite a decrease of 16 mV in resting membrane potential which would have necessitated a decrease in cellular potassium activity of almost 50% were potassium distributed at electrochemical equilibrium. These findings, therefore, preclude a decreased electrochemical potential gradient for potassium as the cause of the membrane depolarization characteristic of denervated muscle fibers. Analysis of the data excludes an important contribution of rheogenic sodium transport to the resting potential of innervated muscles. These results strongly support the hypothesis that the decreased membrane potential in denervated fibers reflects a relative increase in the membrane permeability to sodium.
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Albuquerque, E.X., McIsaac, R.J. 1970. Fast and slow mammalian muscles after denervation.Exp. Neurol. 26:183–202
Albuquerque, E.X., Schuh, F.T., Kauffmann, F.C. 1971. Early membrane depolarisation of the fast mammalian muscle after denervation.Pfluegers Arch. 328:36–50
Albuquerque, E.X., Thesleff, S. 1968. A comparative study of membrane properties of innervated and chronically denervated fast and slow skeletal muscles of the rat.Acta Physiol. Scand. 73:471–481
Bray, J.J., Hawken, M.J., Hubbard, J.I., Pockett, S., Wilson, L. 1976. The membrane potential of rat diaphragm muscle fibres and the effect of denervation.J. Physiol. (London) 225:651–667
Bray, J.J., Hubbard, J.I., Mills, R.G. 1979. The trophic influence of tetrodotoxin-inactive nerves on normal and reinnervated rat skeletal muscles.J. Physiol. (London) 297:479–491
Brown, K.T., Flaming, D.G. 1977. New microelectrode techniques for intracellular work in small cells.Neuroscience 2:813–827
Burg, M.B., Orloff, J. 1964. Active cation transport by kidney tubules at 0°C.Am. J. Physiol. 207:983–988
Camerino, D., Bryant, S.H. 1976. Effects of denervation and colchicine treatment on the chloride conductance of rat skeletal muscle fibres.J. Neurobiol. 7:221–228
Charlton, M.P., Silverman, H., Atwood, H.L. 1981. Intracellular potassium activity in muscles of normal and dystrophic muscle: Anin vivo electrometric study.Exp. Neurol. 71:203–219
Clausen, T., Sellin, L.C., Thesleff, S. 1981. Quantitative changes in ouabain binding after denervation and during reinnervation of mouse skeletal muscle.Acta Physiol. Scand. 111:373–375
Cotlove, E., Trantham, H.V., Bowman, R.L. 1958. An instrument and method for automatic, rapid, accurate and sensitive titration of chloride in biological samples.J. Lab. Clin. Med. 51:461–468
Creese, R., El-Shafie, A.L., Vebova, G. 1968. Sodium movements in denervated muscle and the effects of antimycin A.J. Physiol. (London) 197:279–294
Delong, J., Civan, M.M. 1980. Intracellular chemical activity of potassium in toad urinary bladder.Curr. Topics Membr. Transp. 13:93–105
Dulhunty, A. 1978. The dependence of membrane potential on extracellular chloride concentration in mammalian skeletal muscle fibres.J. Physiol. (London) 276:67–82
Fenn, W.O. 1937. Loss of potassium in voluntary contraction.Am. J. Physiol. 120:675–680
Festoff, B.W., Oliver, K.L., Reddy, N.B. 1977.In vitro studies of skeletal muscle membranes: Effects of denervation on the macromolecular components of cation transport in red and white skeletal muscle.J. Membrane Biol. 32:345–360
Glynn, I.M., Karlish, S.J.D. 1975. The sodium pump.Annu. Rev. Physiol. 37:13–55
Goldmann, D.E. 1943. Potential, impedance and rectification in membranes.J. Gen. Physiol. 27:37–60
Hodgkin, A.L., Katz, B. 1949. The effect of sodium ions on the electrical activity of the giant axon of the squid.J. Physiol. (London) 108:37–77
Jacquez, J.A., Schultz, S.G. 1974. A general relation between membrane potential, ion activities, and pump fluxes for symmetric cells in a steady state.Math. Biosci. 20:19–25
Jakobsson, E. 1980. Interactions of cell volume, membrane potential, and membrane transport parameters.Am. J. Physiol. 238:C196-C206
Jørgensen, P.L. 1980. Sodium and potassium ion pump activity in kidney tubules.Physiol. Rev. 60:864–917
Kernan, R.P., MacDermott, M. 1976. Intracellular potassium concentrations and extracellular spaces in rat skeletal muscles immersed in normal, hypotonic and high-K modified Krebs fluid, determined by potassium-selective microelectrodes.J. Physiol. (London) 263:158P-160P
Leader, J.P. 1982. An improved technique for the construction of a recessed-tip solid-state chloride electrode for intracellular use.Proc. Univ. Otago Med. Sch. 60:34–36
Locke, S., Solomon, H.C. 1967. Relation of resting potential of gastrocnemius and soleus muscles to innervation, activity and the Na−K pump.J. Exp. Zool. 166:377–386
Lullmann, H. 1958. Uber die Knostanz des Membranpotentials bei spontanen Anderungen der Ionesgradienten am normalen und denervierten Rattenzwerchfell.Pfluegers Arch. 267:188–199
McArdle, J.J., Albuquerque, E.X. 1975. Effects of ouabain on denervated and dystrophic muscles of the mouse.Exp. Neurol. 47:353–356
McCaig, D., Leader, J.P. 1984. Intracellular chloride activity in theextensor digitorum longus (EDL) muscle of the rat.J. Membrane Biol. 81:9–17
McIver, D.J.L., Macknight, A.D.C. 1974. Extracellular space in some isolated tissues.J. Physiol. (London) 239:31–49
Moore, E.W., Dietschy, J.M. 1964. Na and K activity coefficients in bile and bile salts determined by glass electrodes.Am. J. Physiol 206:1111–1117
Mullins, L.J., Noda, K. 1963. The influence of sodium-free solutions on the membrane potential of frog muscle fibres.J. Gen. Physiol. 47:117–132
O'Doherty, J., Garcia-Diaz, J.F., Armstrong, W.McD. 1979. Sodium-selective liquid ion-exchange microelectrodes for intracellular measurement.Science 203:1349–1351
Pappone, P.A. 1980. Voltage-clamp experiments in normal and denervated mammalian skeletal muscle fibres.J. Physiol. (London) 306:377–410
Robbins, N. 1977. Cation movements in normal and short-term denervated rat fast twitch muscle.J. Physiol. (London) 271:605–624
Robinson, J.R. 1965. Oxygen consumption and electrolyte composition of kidney slices between 20 and 0°C.J. Physiol. (London) 177:112–121
Sellin, L.C., McArdle, J.J. 1977. Effect of ouabain on reinnervating mammalian skeletal muscle.Eur. J. Pharmacol. 41:337–340
Severin, S.E., Boldyrev, A.A., Tkachuk, V.A. 1974. Some properties of Na+, K+-stimulated ATPase from normal and denervated muscles of rabbit with special reference to its sensitivity to acetylcholine.Comp. Gen. Pharmacol. 5:181–185
Shabunova, I., Vyskocil, F. 1982. Postdenervation changes of intracellular potassium and sodium measured by ion-selective microelectrodes in rat soleus and extensor digitorum longus muscle fibres.Pfluegers Arch. 394:161–164
Wallick, E.T., Lane, E.K., Schwartz, A. 1979. Biochemical mechanism of the sodium pump.Annu. Rev. Physiol. 41:397–411
Ware, F., Bennett, A.L., McIntyre, A.R. 1954. Membrane resting potential of denervated mammalian skeletal muscle measuredin vivo.Am. J. Physiol. 177:115–118
Wareham, A.C. 1978. Effect of denervation and ouabain on the response of the resting membrane potential of rat skeletal muscle to potassium.Pfluegers Arch. 373:225–228
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Leader, J.P., Bray, J.J., Macknight, A.D.C. et al. Cellular ions in intact and denervated muscles of the rat. J. Membrain Biol. 81, 19–27 (1984). https://doi.org/10.1007/BF01868806
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DOI: https://doi.org/10.1007/BF01868806