Summary
Previous studies of the electrochemical activity coefficients of intracellular Na+ and K+ have suggested that the free form of these ions may be unevenly distributed within the intracellular fluids. One possible site of such subcellular compartmentalization is the cell nucleus. In order to examine this possibility, the cells ofChironomus salivary glands were studied with conventional liquid ion-exchange microelectrodes sensitive to K+ and Cl−, with a new liquid ion-exchange microelectrode sensitive to Na+, and with open-tipped micropipets. Both the electrochemical activities for Na+, K+ and Cl−, and the electrical potential were the same on both sides of the nuclear membrane. The possibility was considered that a difference in the junction potentials within the nucleoplasm and cytoplasm might have masked a real difference in electrical potential between these two phases. To study that possibility, changes were induced in the junction potentials by altering the composition of the fluid filling the exploring micropipets. The results have suggested that the magnitudes of the junction potentials are the same on both sides of the nuclear envelope. The simplest interpretation of the data is that the chemical activities of Na+, K+ and Cl− are the same within the nucleus and cytoplasm. This suggests that other subcellular structures, possibly the endoplasmic reticulum and mitochondria, are responsible for subcellular compartmentalization.
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Allfrey, V.G., Meudt, R., Hopkins, J.W., Mirsky, A.E. 1961. Sodium-dependent “transport” reactions in the cell nucleus and their role in protein and nucleic acid synthesisProc. Nat. Acad. Sci. USA 47:907
Armstrong, W.McD., Lee, C.O. 1971. Sodium and potassium activities in normal and “sodium-rich” frog skeletal muscle.Science 171:413
Birks, R.I., Davey, D.F. 1969. Osmotic responses demonstrating the extracellular character of the sarcoplasmic reticulum.J. Physiol. (London) 202:171
Brown, A.M., Kunze, D.L. 1974. Ion activities in identifiableAplysia neurons.Adv. Exp. Med. Biol. 50:57
Brown, A.M., Walker, J.L., Sutton, R.B. 1970. Increased Cl− conductance as the proximate cause of hydrogen ion concentration effects inAplysia neurons.J. Gen. Physiol. 56:559
Century, T.J., Fenichel, I.R., Horowitz, S.B. 1970. The concentrations of water, sodium and potassium in the nucleus and cytoplasm of amphibian oocytes.J. Cell Sci. 7:5
Cole, K.S. 1968. Membranes, Ions and Nerve Impulses; a Chapter of Classical Biophysics. U. of California Press, Berkeley, Los Angeles
Dick, D.A.T., McLaughlin, S.G.A. 1969. The activities and concentrations of sodium and potassium in toad oocytes.J. Physiol. (London)205:61
Dörge, A., Gehring, K., Nagel, W., Thurau, K. 1974. Intracellular Na+−K+ concentration of frog skin at different states of Na-transport.In: Microprobe Analysis as Applied to Cells and Tissues. T. Hall, P. Echlin and R. Kaufmann, editors. p. 337. Academic Press, New York
Epstein, M.A. 1957. The fine structural organization of Rous tumour cells.J. Biophys. Biochem. Cytol. 3:851
Frank, H.S. 1963. Single ion activities and ion-solvent interaction in dilute aqueous solutions.J. Phys. Chem. 67:1554
Fry, D.J. 1970. The movement of inorganic ions and water across the nuclear envelope.In: Membranes and Ion Transport. E. Bittar, editor. Vol. 2, p. 259. Wiley-Interscience, London, New York
Garrels, R.M. 1967. Ion-sensitive electrodes and individual ion activity coefficients.In: Glass Electrodes for Hydrogen and other Cations. G. Eisenman, editor. Marcel Dekker, New York
Hinke, J.A.M. 1961. The measurement of sodium and potassium activities in the squid axon by means of cation-selective micro-electrodes.J. Physiol. (London)156:314
Hinke, J.A.M., Caillé, J.P., Gayton, D.C. 1973. Distribution and state of monovalent ions in skeletal muscle based on ion electrode, isotope and diffusion analyses.Ann. N.Y. Acad. Sci. 204:274
Huxley, A.F. 1961. A micromanipulator.J. Physiol. (London) 157:5P
Ingram, F.D., Ingram, M.J., Hogben, C.A.M. 1974. An analysis of the freeze-dried, plastic embedded electron probe specimen preparation.In: Microprobe Analysis as Applied to Cells and Tissues. T. Hall, P. Echlin and R. Kauffman, editors. p. 119. Academic Press, New York
Ito, S., Loewenstein, W.R. 1965. Permeability of a nuclear membrane: Changes during normal development and changes induced by growth hormone.Science 150:909
Janáček, K., Morel, F., Bourguet, J. 1968. Étude experimentale des potentials électriques et des activités ioniques dans les cellules épithéliales de la vessie de grenouille.J. Physiol. (Paris) 80:51
Katzman, R., Lehrer, G., Wilson, C.E. 1969. Sodium and potassium distribution in puffer fish supramedullary nerve cell bodies.J. Gen. Physiol. 54:232
Khuri, R.N., Agulian, S.K., Bogharian, K., Aklanjian, D. 1975. Electrochemical potentials of chloride in proximal renal tubule ofNecturus Maculosus.Comp. Biochem. Physiol. 50A:695
Khuri, R., Hajjar, J.J., Agulian, S., Bogharian, K., Kalloghlian, H., Bizri, H. 1972. Intracellular potassium in cells of the proximal tubule ofNecturus Maculosus.Pfluegers Arch. 338:73
Kostyuk, P.G., Sorokina, Z.A., Kholodova, Yu.D. 1969. Measurement of activity of hydrogen, potassium and sodium ions in striated muscle fibers and nerve cells.In: Glass Microelectrodes. M. Lavallée, O. Schanne and N.C. Hébert, editors. J. Wiley & Sons, New York
Kroeger, H. 1964. Zellphysiologische Mechanismen bei der Regulation von Genaktivitäten in den Riesenchromosomem vonChironomus thummi.Chromosoma 15:36
Lavallée, M., Szabo, G. 1969. The effect of glass surface conductivity phenomena and the tip potential of glass micropipette electrodes.In: Glass Microelectrodes. M. Lavallée, O.F. Schanne, and N.C. Hébert, editors. J. Wiley & Sons, New York
Lee, C.O., Armstrong, W.McD. 1972. Activities of sodium and potassium ions in epithelial cells of small intestine.Science 175:1261
Lehninger, A.L. 1965. The Mitochondrion: Basis of Structure and Function. W. A. Benjamin, New York
Lev, A.A. 1964. Determination of activity coefficients of potassium and sodium in frog muscle fibers.Nature (London) 201:1132
Lev, A.A., Armstrong, W.McD. 1975. Ionic activities in cells.In: Current Topics in Membranes and Transport. F. Bronner and A. Kleinzeller, editors. Vol. 6, pp. 59–123. Academic Press, New York
Lezzi, M., Gilbert, L.I. 1970. Differential effects of K+ and Na+ on specific bands of isolated polytene chromosomes ofChironomus tentans.J. Cell Sci. 6:615
Loewenstein, W.R. 1964. Permeability of the nuclear membrane as determined with electrical methods.In: Protoplasmatologia Handbuch der Protoplasmaforschung. Wien 2, p. 26. Springer-Verlag, Berlin
Loewenstein, W.R., Kanno, Y. 1963. Some electrical properties of a nuclear membrane examined with a microelectrode.J. Gen. Physiol. 46:1123
MacInnes, D.A. 1961. The Principles of Electrochemistry. Dover, New York
Martin, A.R., Wickelgren, W.O., Berànek, R. 1970. Effects of iontophoretically applied drugs on spinal interneurones of the lamprey.J. Physiol. (London)207:653
Naora, H., Naora, H., Izawa, M., Allfrey, V.G., Mirsky, A.E. 1962. Some observations on differences in composition between the nucleus and cytoplasm of the frog oocyte.Proc. Nat. Acad. Sci USA 48:853
Neild, T.O., Thomas, R.C. 1974. Intracellular chloride activity and the effects of acetylcholine in snail neurons.J. Physiol. (London) 242:453
Palay, S.L. 1960. On the appearance of absorbed fat droplets in the nuclear envelope.J. Biophys. Biochem. Cytol. 7:391
Palmer, L.G., Civan, M.M. 1975. Intracellular distribution of free potassium inChironomus salivary glands.Science 188:1321
Palmer, L.G., Civan, M.M. 1976. Distribution of free Cl− across the nuclear membrane of salivary gland cells ofChironomus.Clin. Res. 24:469A
Payne, P.L. 1975. Nucleocytoplasmic movement of fluorescent tracers microinjected into living salivary gland cells.J. Cell Biol. 66:652
Robert, M. 1971. Effect of ion strength and pH on the differential decondensation of nucleotides in isolated salivary gland nuclei and chromosomes ofChironomus thummi.Chromosoma 36:1
Robinson, R.A., Stokes, R.H. 1959.Electrolyte Solutions (2nd ed.). Butterworths, London
Rogus, E., Zierler, K.L. 1973. Sodium and water contents of sarcoplasmic reticulum in rat skeletal muscle: Effects of anisotopic media, ouabain and external sodium.J. Physiol. (London) 233:227
Siebert, G., Langendorf, H. 1970. Ion balance in the cell nucleus.Naturwissenschaften 57:119
Starodubov, S.M., Kurella, G.A. 1972. Concerning the electrical potential difference and the distribution of ions between cytoplasm and cell nucleus.Zhurnal Obshchei Biologii 33 (4):464
Thomas, R.C. 1970. New design for sodium sensitive glass microelectrodes.J. Physiol. (London) 210:82P
Watson, M.L. 1955. The nuclear envelope. Its structure and relation to cytoplasmic membranes.J. Biophys. Biochem. Cytol. 1:257
Wiener, J., Spiro, D., Loewenstein, W.R. 1965. Ultrastructure and permeability of nuclear membranes.J. Cell Biol. 27:107
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Palmer, L.G., Civan, M.M. Distribution of Na+, K+ and Cl− between nucleus and cytoplasm inChironomus salivary gland cells. J. Membrain Biol. 33, 41–61 (1977). https://doi.org/10.1007/BF01869511
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DOI: https://doi.org/10.1007/BF01869511