Abstract
Inastrocytes, as [K+]o was increased from 1.2 to 10 mM, [K+]i and [Cl−]i were increased, whereas [Na+]i was decreased. As [K+]o was increased from 10 to 60 mM, intracellular concentration of these three ions showed no significant change. When [K+]o was increased from 60 to 122 mM, an increase in [K+]i and [Cl−]i and a decrease in [Na+]i were observed.Inneurons, as [K+]o was increased from 1.2 to 2.8 mM, [Na+]i and [Cl−]i were decreased, whereas [K+]i was increased. As [K+]o was increased from 2.8 to 30 mM, [K+]i, [Na+]i and [Cl−]i showed no significant change. When [K+]o was increased from 30 to 122 mM, [K+]i and [Cl−]i were increased, whereas [Na+]i was decreased. Inastrocytes, pHi increased when [K+]o was increased. Inneurons, there was a biphasic change in pHi. In lower [K+]o (1.2–2.8 mM) pHi decreased as [K+]o increased, whereas in higher [K+]o (2.8–122 mM) pHi was directly related to [K+]o. In bothastrocytes andneurons, changes in [K+]o did not affect the extracellular water content, whereas the intracellular water content increased as the [K+]o increased. Transmembrane potential (Em) as measured with Tl-204 was inversely related to [K+]o between 1.2 and 90 mM, a ten-fold increase in [K+]o depolarized the astrocytes by about 56 mV and the neurons about 52 mV. The Em values measured with Tl-204 were close to the potassium equilibrium potential (Ek) except those in neurons at lower [K+]o. However, they were not equal to the chloride equilibrium potential (ECl) at [K+]o lower than 30 mM in both astrocytes and neurons. Results of this study demonstrate that alteration of [K+]o produced different changes in [K+]i, [Na+]i, [Cl−]i, and pHi in astrocytes and neurons. The data show that astrocytes can adapt to alterations in [K+]o, in such a way to maintain a more suitable environment for neurons.
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References
Somjen, G. G. 1979. Extracellular potassium in the mammalian central nervous system. Ann. Rev. Physiol. 41:159–177.
Sykova, E. 1983. Extracellular K+ accumulation in the central nervous system. Prog. Biophys. and Mol. Biol. 42:135–190.
Walz, W., and Hertz, L. 1983. Intracellular ion changes of astrocytes in response to extracellular potassium. J. Neurosci. Res. 10:441–424.
Hertz, L. 1965. Possible role of neuroglia: a potassium-mediated neuronal neuroglial-neuronal impulse transmission system. Nature 206:1091–1094.
Hertz, L. 1968. Potassium effects on ion transport in brain slices. J. Neurochem. 15:1–16.
Orkand, R.K., Nicholls, J. G., and Kuffler, S. W. 1966. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29:788–806.
Kuffler, S. W. 1967. Neuroglial cells: physiological properties and a potassium mediated effect of neuronal activity on the glial membrane potential. Proc. R. Soc. B. 168:1–121.
Schousboe, A., and Hertz, L. 1971. Effects of potassium on concentrations of ions and proteins and on pH in brain-cortex slices from new-born and adult rats. Int. J. Neurosci. 1:235–242.
Schlue, W. R., and Wuttke, W. 1983. Potassium activity in leech neuropile glial cells changes with external potassium concentration. Brain Res. 270:368–372.
Ballanyi, K., and Schlue, W. R. 1990. Intracellular chloride activity in glial cells of the leech central nervous system. J. Physiol. 420:325–336.
Walz, W., Wuttke, W., and Hertz, L. 1984. Astrocytes in primary cultures: membrane potential characteristics reveal exclusive potassive conductance and potassium accumulator properties. Brain Res. 292:367–374.
Kettenmann, H., Sonnhof, U., and Schachner, M. 1983. Exclusive potassium dependence of the membrane potential in cultured mouse oligodendrocytes. J. Neurosci. 3:500–505.
Ballanyi, K., Grafe, P., and Bruggencate, G. 1987. Ion activities and potassium uptake mechanisms of glial cells in guinea-pig olfactory cortex slices. J. Physiol. 382:159–174.
Yu, A. C. H., Hertz, E., and Hertz, L. 1984. Alterations in uptake and release rate for GABA, glutamate and glutamine during biochemical maturation of highly purified cultures of cerebral cortical neurons, a GABAergic preparation. J. Neurochem. 42:951–960.
Hertz, L., Juurlink, B. H. J. and Szuchet, S. 1985. Cell culture. Page 603–661,in Lajtha A. (ed.) Handbook of Neurochemistry, Vol. 8. Plenum Publ. Corp., New York.
Booher, J., and Sensenbrenner, M. 1972. Growth and cultivation of dissociated neurons and glial cells from embryonic chick, rat and human brain in flask culture. Neurobiology 2:97–105.
Hertz, L., Juurlink, B. H. J., Fosmark, H., and Schousboe, A. 1982. Methodological appendix: Astrocytes in primary cultures. Page 175–186,in Pfiffer, S. E., (eds.), Neuroscience Approached Through Cell Culture. CRC Press, Boca Raton.
Juurlink, B. H. J., and Hertz, L. 1985. Plasticity of astrocytes in primary cultures; an experimental tool and a reason for methodological caution. Dev. Neurosci. 7:263–277.
Yavin, E., and Yavin, Z. 1974. Attachment and culture of dissociated cells from rat embryo cerebral hemispheres on polylysine coated surface. J. Cell. Biol. 62:540–546.
Chow, S. Y., White, H. S., Yen-Chow, Y. C., and Woodbury, D. M. 1989. Uptakes of iodide and chloride by primary cultures of mouse astrocytes and neurons. Neurochem. Res. 14:963–969.
Lowry, O., Rosebrough, W. J., Farr, A. L., and Randall, R. S. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265–274.
Brisman, T., Collins, V. P., and Kesselberg, M. 1989. Thallium-201 uptake relates to membrane potential and potassium permeability in human glioma cells. Brain Res. 500:30–36.
Waddell, W. J., and Butler, T. C. 1959. Calculation of intracellular pH from the distribution of 5,5′-dimethyl-2,4-oxazolidine (DMO). Application to skeletal muscle of the dog. J. Clin. Invest. 38:720–729.
Chow, S. Y., Yen-Chow, Y. C., and Woodbury, D. M. 1985. Water and electrolyte contents, cell pH and membrane potentials of cultured turtle thyroid cells. J. Endocr. 104:45–52.
Chow, S. Y., Yen-Chow, Y. C., and Woodbury, D. M. 1983. Effects of thyrotropin, acetazolamide, 4-acetamido-4′-isothiocyanostilbene-2-2′-disulfonic acid, perchlorate, ouabain and furosemide on pH and HCO3-concentrations in cells and luminal fluid of turtle thyroid as calculated from the distribution of [14C]dimethyoxazolidine-2,4-dione. J. Pham. Exptl. Thera. 225:17–23.
Hertz, L., and Chaban, G. 1982. Indications for an active role of astrocytes in potassium homeostasis at the cellular level: Potassium uptake and metabolic effects of potassium. Page 157–174,in Pfeiffer S. E., (ed.), Neuroscience Approached Through Cell Culture, Vol. I. CRC Press, Boca Raton, Florida.
Hertz, L. 1978. An intense potassium uptake into astrocytes, its further enhancement by high concentrations of potassium, and its possible involvement in potassium homeostasis at the cellular level. Brain Res. 145:202–208.
Hertz, L. 1979. Inhibition by barbiturates of an intense net uptake of potassium into astrocytes. Neuropharmacology 18:629–632.
Kimelberg, H. K., Bowman, C., Biddlecome, S., and Bourke R. S. 1979. Cation transpaort and membrane potential properties of primary astroglial cultures from neonatal rat brains. Brain Res. 177:533–550.
Gill, T. H., Young, O. M., and Tower, D. B. 1974. The uptake of36Cl− into astrocytes in tissue culture by a potassium-dependent, saturable process. J. Neurochem. 23:1011–1018.
Walz, W., and Hinks, E. C. 1985. Carrier-mediated KCl accumulation accompanied by water movements is involved in the control of physiological K+ levels by astrocytes. Brain Res. 343:44–51.
Russel, J. M. 1983. Cation-coupled chloride influx in squid axon. Role of potassium and stoichiometry of the transport process. J. Gen. Physiol. 81:909–925.
Aickin, C. C., Deisz, R. A., and Lux, H. D. 1984. Mechanisms of chloride transport in crayfish stretch receptor neurons and guinea pig was deferens: implications for inhibition mediated by GABA. Neuroscience Letters 47:239–244.
Kuffler, S. W., Nicholls, J. G., and Orkand, R. 1966. Physiological properties of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29:768–787.
Orkand, R. K. 1977. Glial cells. Page 855–875,in Brookhart J. M. and Mountcastle V. B. (eds.). Handbook of Physiology. Am. Physiol. Soc., Bethesda, MD.
Moonen, G., Franck, G., and Schoffeniels, E. 1980. Glial control of neuronal excitability in mammals. I. Electrophysiological and isotopic evidence in culture. Neurochem. Intl. 2:299–310.
Deitmer, J. W., and Szatkowski, M. 1990. Membrane potential dependence of intracellular pH regulation by identified glial cells in the leech central nervous system. J. Physiol. 421:617–631.
Ransom B. and Corlini W. G. 1986. Electrophysiological properties of astrocytes. Page 1–49,in Fedoroff S. and Vernadakis A, (eds.) Astrocytes. Academic Press Inc., Orlando, FL.
Walz, W. 1989. Role of glial cells in the regulation of the brain ion microenvironment. Progress in Neurobiology 33:309–333.
Walz, W. and Hertz, L. 1983. Comparison between fluxes of potassium and of chloride in astrocytes in primary cultures. Brain Res. 277:321–328.
Grisar, T. M. 1986. Neuron-glial relationships in human and experimental epilepsy: A biochemical point of view. Page 1045–1073,in Delgado-Escueta, A. V., Ward, A. A., Woodbury, D. M. and Porter, R. J. (eds.), Basic Mechanisms of the Epilepsies. Raven Press, New York.
Walz, W., and Hertz, L. 1982. Ouabain-sensitive and ouabainresistant net uptake of potassium into astrocytes and neurons in primary cultures. J. Neurochem. 39:70–77.
Walz, W., and Hertz, L. 1984. Sodium transport in astrocytes. J. Neurosci. Res. 11:231–239.
Tupper, J. T. 1975. Cation flux in the Ehrlich ascites tumor cell. Evidence for Na+-for-Na+ and K+-for-K+ exchange diffusion. Biochim. Biophys. Acta 394:586–596.
Gill, T. H., Young, O. M., and Tower, D. B. 1974. The uptake of36Cl− into astrocytes in tissue culture by a potassium-dependent, saturable process. J Neurochem. 23:1011–1018.
Kimelberg, H. D. 1981. Active accumulation and exchange transport of chloride in astroglial cells in culture. Biochim. Biophys. Acta 646:179–184.
Walz, W., and Schule, W. R. 1982. External ions and membrane potential of leech neuropile glial cells. Brain Res. 239:119–138.
Kennenmann, H. 1987. K+ and Cl− uptake by cultured oligodendrocytes. Can. J. Physiol. Pharmac. 65:1033–1037.
Buhrle, E., and Sonnhof, U. 1983. Intracellular ion activities and equilibrium potentials in motoneurones and glial cells of the frog spinal cord. Pflugers Archiv. 396:144–153.
Gallagher, J. P., Nakamura, J., and Shinnick-Gallagher, P. 1983. The effects of temperature, pH and Cl− pump inhibitors on GABA response recorded from cat dorsal root ganglia. Brain Res. 267:249–259.
Ballanyi, K., and Grafe, P. 1985. An intracellular analysis of aminobutyric-acid-associated ion movements in rat sympathetic neurones. J. Physiol. 365:41–58.
Misgeld, U., Deisz, R. A., Dodt, H. U., and Lux, H. D. 1986. The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 232:1413–1415.
Dichter, M. A. 1980. Physiological identification of GABA as the inhibitory transmitter for mammalian cortical neurons in cell culture. Brain Res. 190:111–121.
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Chow, S.Y., Yen-Chow, Y.C., White, H.S. et al. Effects of potassium on the anion and cation contents of primary cultures of mouse astrocytes and neurons. Neurochem Res 16, 1275–1283 (1991). https://doi.org/10.1007/BF00966658
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DOI: https://doi.org/10.1007/BF00966658