Abstract
Radial glial (Müller) cells were isolated from rabbit retinae by papaine and mechanical dissociation. Regional membrane properties of these cells were studied by using the patch-clamp technique. In the course of our experiments, we found three distinct types of large K+ conducting channels. The vitread process membrane was dominated by high conductance inwardly rectifying (HCR) channels which carried, in the open state, inward currents along a conductance of about 105 pS (symmetrical solutions with 140 mM K+) but almost no outward currents. In the membrane of the soma and the proximal distal process, we found low conductance inwardly rectifying (LCR) channels which had an open state-conductance of about 60 pS and showed rather weak rectification. The endfoot membrane, on the other hand, was found to contain non-rectifying very high conductance (VHC) channels with an open state-conductance of about 360 pS (same solutions). These results suggest that mammalian Müller cells express regional membrane specializations which are optimized to carry spatial buffering currents of excess K+ ions.
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References
Attwell D, Brew H, Gray P, Mobbs P (1986) Single potassium channels in Müller cells of the salamander retina. J Physiol 371:35P
Brew H, Gray PTA, Mobbs P, Attwell D (1986) Endfeet of retinal glial cells have higher densities of ion channels that mediate K+ buffering. Nature 324:466–468
Conner JD, Detwiler PB, Sarthy PV (1985) Ionic and electrophysiological properties of retinal Müller (glial) cells of the turtle. J Physiol 362:79–92
Corey DP, Barres BA, Chun LLY (1985) An inwardly rectifying potassium channel in oligodendroglia. Soc Neurosci Abst 11:148
Dick E, Miller RF, Bloomfield S (1985) Extracellular K+ activity changes related to electroretinogram components. II. Rabbit (E-type) retinas. J Gen Physiol 85:911–931
Fukushima Y (1982) Blocking kinetics of the anomalous potassium rectifier of tunicate egg studied by single channel recording. J Physiol 331:311–331
Gardner-Medwin AR (1984) A foot in the vitreous fluid. Nature 309:113
Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85–100
Hanke S, Reichenbach A (1987) Quantitative-morphometric aspects of Bergmann glial (Golgi epithelial) cell development in rats. A Golgi study. Anat Embryol 177:183–188
Karwoski CJ, Newman EA, Shimazaki H, Proenza LM (1985) Light-evoked increases in extracellular K+ in the plexiform layers of amphibian retina. J Gen Physiol 86:189–213
Landis DMD, Reese TS (1981) Membrane structure of mammalian astrocytes: a review of freeze-fracture studies in adult, developing, reactive and cultured astrocytes. J Exp Biol 95:35–48
Newman EA (1984) Regional specialization of retinal glial cell membrane. Nature 309:155–157
Newman EA (1985a) Membrane physiology of retinal glial (Müller) cells. J Neurosci 5:2225–2239
Newman EA (1985b) Voltage-dependent calcium and potassium channels in retinal glial cells. Nature 317:809–811
Newman EA (1986) Potassium conductance hot-spots in mammalian Müller (glial) cells. Soc Neurosci Abst 12: (part 1) 633
Newman EA (1987) Distribution of potassium conductance in mammalian Müller (glial) cells. A comparative study. J Neurosci 7:2423–2432
Newman EA, Odette LL (1984) Model of electroretinogram b-wave generation: a test of the K+ hypothesis. J Neurophysiol 51:164–182
Newman EA, Frambach DA, Odette LL (1984) Control of extracellular potassium levels by retinal glial cell K+ siphoning. Science 225:1174–1175
Nilius B, Benndorf K, Markwardt F (1986) Modified gating behaviour of aconitine treated single sodium channels from adult cardiac myocytes. Pflügers Arch 407:691–693
Pappone PA, Cahalan (1986) Ion permeation in cell membranes. In: Andreoli TE, Hoffman JF, Fanestil DD, Schultz SG (eds) Physiology of membrane disorders. Plenum Press, New York, pp 249–272
Puro DG, Roberge F, Chan C-C (1986) Two types of ionic channels in glial cells derived from the adult rat retina. Soc Neurosci Abst 12: (Part 1) 633
Rall W (1977) Core conductance theory and cable properties of neurons. In: Brookhart JM, Mountcastle VB (eds) Handbook of Physiology, vol 1, Section 1, Part 1. Am Physiol Soc, Bethesda, pp 39–97
Raviola G (1977) The structural basis of the blood-ocular barriers. Exp Eye Res 25 (Suppl):27–63
Reale E, Luciano L, Spitznas M (1974) Introduction to freeze-fracture method in retinal research. Graefes Arch Clin Exp Ophthalmol 192:73–87
Reichenbach A, Birkenmeyer G (1984) Preparation of isolated Müller cells of the mammalian (rabbit) retina. Z Mikrosk Anat Forsch 98:789–792
Reichenbach A, Eberhardt W (1986) Intracellular recordings from isolated rabbit retinal Müller (glial) cells. Pflügers Arch 407:348–353
Sakman B, Trube G (1984) Conductance properties of single inwardly rectifying potassium channels in ventricular cells from guinea pig heart. J Physiol 347:641–657
Wolburg H, Berg K (1987) Freeze-fracture studies on Müller cells in the retina. I. Heterogeneity of Müller cell endfeet in the rabbit retina. Neurosci Lett 82:273–277
Zahradník I, Zahradníková A, Zachar J (1986) Two types of potassium channels in human glioma cells revealed by the patch clamp technique. In: Tuček S, Štípek S, Štástný F, Křivánek J (eds) Molecular basis of neuronal function. Eur Soc Neurochem, Prague, p 280
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Nilius, B., Reichenbach, A. Efficient K+ buffering by mammalian retinal glial cells is due to cooperation of specialized ion channels. Pflugers Arch. 411, 654–660 (1988). https://doi.org/10.1007/BF00580862
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DOI: https://doi.org/10.1007/BF00580862