Exclusive potassium dependence of the membrane potential in cultured mouse oligodendrocytes

Kettenmann, Helmut; Sonnhof, U.; Schachner, Melitta

doi:10.1523/jneurosci.03-03-00500.1983

Cited by 144 publications

(97 citation statements)

References 20 publications

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“…One of the characteristic features of glial cells in several tissues is their membrane selectivity for K ϩ , and a low (in some cases, negligible) permeability to Na ϩ and Cl Ϫ (Bigiani 2001;Kettenmann et al 1983;Newman 1985Newman , 1989Ransom and Sontheimer 1995;Sugihara and Furukawa 1996;Walz and Schule 1982;Walz et al 1984). Results from the ion substitution experiments described here demonstrate that vomeronasal supporting cells have membranes that are permeable not only to K ϩ , but also to Na ϩ and Cl Ϫ .…”

Section: Resting Membrane Permeabilities In Vomeronasal Supporting Cellsmentioning

confidence: 70%

Ion Conductances in Supporting Cells Isolated From the Mouse Vomeronasal Organ

Ghiaroni

Fieni

Tirindelli

et al. 2003

Journal of Neurophysiology

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. Ion conductances in supporting cells isolated from the mouse vomeronasal organ. J Neurophysiol 89: 118 -127, 2003. 10.1152/jn.00545.2002. The vomeronasal organ (VNO) is a chemosensory structure involved in the detection of pheromones in most mammals. The VNO sensory epithelium contains both neurons and supporting cells. Data suggest that vomeronasal neurons represent the pheromonal transduction sites, whereas scarce information is available on the functional properties of supporting cells. To begin to understand their role in VNO physiology, we have characterized with patch-clamp recording techniques the electrophysiological properties of supporting cells isolated from the neuroepithelium of the mouse VNO. Supporting cells were distinguished from neurons by their typical morphology and by the lack of immunoreactivity for G␥8 and OMP, two specific markers for vomeronasal neurons. Unlike glial cells in other tissues, VNO supporting cells exhibited a depolarized resting potential (about Ϫ29 mV). A Goldman-Hodgkin-Katz analysis for resting ion permeabilities revealed indeed an unique ratio of P K :P Na :P Cl ϭ 1:0.23:1.4. Supporting cells also possessed voltage-dependent K ϩ and Na ϩ conductances that differed significantly in their biophysical and pharmacological properties from those expressed by VNO neurons. Thus glial membranes in the VNO can sustain significant fluxes of K ϩ and Na ϩ , as well as Cl Ϫ . This functional property might allow supporting cells to mop-up and redistribute the excess of KCl and NaCl that often occurs in certain pheromone-delivering fluids, like urine, and that could blunt the sensitivity of VNO neurons to pheromones. Therefore vomeronasal supporting cells could affect chemosensory transduction in the VNO by regulating the ionic strength of the pheromone-containing medium.

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Section: Resting Membrane Permeabilities In Vomeronasal Supporting Cellsmentioning

confidence: 70%

Ion Conductances in Supporting Cells Isolated From the Mouse Vomeronasal Organ

Ghiaroni

Fieni

Tirindelli

et al. 2003

Journal of Neurophysiology

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“…The average long and short diameters of the soma were 5.9 and 3 9 ,tm, respectively (twenty-four cells), although these values were possibly over-estimated owing to the fluorescent halo. These structural features of the inexcitable cell generally conform to those of astrocytes (Dennis & Gerschenfeld, 1969;Kelly & van Essen, 1974;Takato & Goldring, 1979;Gutnick, Connors & Ransom, 1981 Dennis & Gerschenfeld, 1969), in vivo (38 mV, Ransom & Goldring, 1973a) and in culture (52 mV, Kettenmann, Sonnhof & Schachner, 1983;51 mV, Walz, Wuttke & Hertz, 1984). [K+o (mM) The input conductance of inexcitable cells during the slow potential was measured by passing hyperpolarizing current pulses of constant intensity (Fig.…”

Section: Morphology Of Inexcitable Cellsmentioning

confidence: 71%

Slow depolarizing potentials recorded from glial cells in the rat superficial dorsal horn.

Takahashi

Tsuruhara

1987

The Journal of Physiology

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SUMMARY1. Intracellular potentials were recorded from inexcitable cells in the superficial dorsal horn of the rat lumbar spinal cord in vitro.2. These cells had a large resting membrane potential (up to -90 mV) but when depolarized were unable to produce action potentials. The resting potential was highly dependent upon extracellular K+ concentrations ([K+]0), with a slope of about 45 mV for a 10-fold change in [K+].3. Electrical stimulation of dorsal roots evoked a slow depolarizing potential lasting for many seconds in the inexcitable cells. The slow potentials were not accompanied by any appreciable change in input conductance, nor were their amplitudes dependent upon the membrane potential.4. The morphology of the inexcitable cells marked by intracellular injection of a fluorescent dye, Lucifer Yellow, was consistent with their being glial cells.5. [K+]. values were measured by K+-sensitive electrodes simultaneously with intracellular glial potentials. Changes in the K+-electrode potential occurred in parallel with slow depolarizing potentials following stimulation of dorsal roots. When the stimulus intensity was altered, changes in the magnitude of the K+-electrode response were correlated with those of the slow potentials.6. Replacement of extracellular Ca2+ by Mg2+ abolished both the slow potentials and K+-electrode responses evoked by afferent stimulation, suggesting that impulses in primary afferent fibres do not directly contribute to the glial slow potentials.7. It is concluded that the slow potentials in glial cells result from a transient increase in [K+]. at the superficial dorsal horn, which is induced by activation of neighbouring internuncial neurones.

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“…Based on this observation, they proposed the "K ϩ spatial buffering hypothesis," which states that astrocytes take up excess extracellular potassium ions, distribute them via the gap junction-coupled cell syncytium, and extrude the ions at sites in which extracellular potassium concentration ([K ϩ ] out ) is low . Subsequently, this phenomenon was confirmed in a variety of nervous tissue preparations (Kettenmann et al, 1983;Coles et al, 1986;Holthoff and Witte, 2000;Amzica et al, 2002). Although several possible mediators of astrocyte K ϩ uptake have been proposed, pharmacological studies suggest that K ir channels predominate in K ϩ buffering (Ballanyi et al, 1987;Karwoski et al, 1989;Oakley et al, 1992).…”

Section: Introductionmentioning

confidence: 75%

Conditional Knock-Out of K_ir4.1 Leads to Glial Membrane Depolarization, Inhibition of Potassium and Glutamate Uptake, and Enhanced Short-Term Synaptic Potentiation

Djukic¹,

Casper²,

Philpot³

et al. 2007

J. Neurosci.

541

654

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During neuronal activity, extracellular potassium concentration ([Kϩ] out ) becomes elevated and, if uncorrected, causes neuronal depolarization, hyperexcitability, and seizures. Clearance of K ϩ from the extracellular space, termed K ϩ spatial buffering, is considered to be an important function of astrocytes. Results from a number of studies suggest that maintenance of [K ϩ ] out by astrocytes is mediated by K ϩ uptake through the inward-rectifying K ir 4.1 channels. To study the role of this channel in astrocyte physiology and neuronal excitability, we generated a conditional knock-out (cKO) of K ir 4.1 directed to astrocytes via the human glial fibrillary acidic protein promoter gfa2. K ir 4.1 cKO mice die prematurely and display severe ataxia and stress-induced seizures. Electrophysiological recordings revealed severe depolarization of both passive astrocytes and complex glia in K ir 4.1 cKO hippocampal slices. Complex cell depolarization appears to be a direct consequence of K ir 4.1 removal, whereas passive astrocyte depolarization seems to arise from an indirect developmental process. Furthermore, we observed a significant loss of complex glia, suggestive of a role for K ir 4.1 in astrocyte development. K ir 4.1 cKO passive astrocytes displayed a marked impairment of both K ϩ and glutamate uptake. Surprisingly, membrane and action potential properties of CA1 pyramidal neurons, as well as basal synaptic transmission in the CA1 stratum radiatum appeared unaffected, whereas spontaneous neuronal activity was reduced in the K ir 4.1 cKO. However, high-frequency stimulation revealed greatly elevated posttetanic potentiation and short-term potentiation in K ir 4.1 cKO hippocampus. Our findings implicate a role for glial K ir 4.1 channel subunit in the modulation of synaptic strength.

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Exclusive potassium dependence of the membrane potential in cultured mouse oligodendrocytes

Cited by 144 publications

References 20 publications

Ion Conductances in Supporting Cells Isolated From the Mouse Vomeronasal Organ

Ion Conductances in Supporting Cells Isolated From the Mouse Vomeronasal Organ

Slow depolarizing potentials recorded from glial cells in the rat superficial dorsal horn.

Conditional Knock-Out of K_ir4.1 Leads to Glial Membrane Depolarization, Inhibition of Potassium and Glutamate Uptake, and Enhanced Short-Term Synaptic Potentiation

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Exclusive potassium dependence of the membrane potential in cultured mouse oligodendrocytes

Cited by 144 publications

References 20 publications

Ion Conductances in Supporting Cells Isolated From the Mouse Vomeronasal Organ

Ion Conductances in Supporting Cells Isolated From the Mouse Vomeronasal Organ

Slow depolarizing potentials recorded from glial cells in the rat superficial dorsal horn.

Conditional Knock-Out of Kir4.1 Leads to Glial Membrane Depolarization, Inhibition of Potassium and Glutamate Uptake, and Enhanced Short-Term Synaptic Potentiation

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Conditional Knock-Out of K_ir4.1 Leads to Glial Membrane Depolarization, Inhibition of Potassium and Glutamate Uptake, and Enhanced Short-Term Synaptic Potentiation