Skip to main content
Log in

Efficient K+ buffering by mammalian retinal glial cells is due to cooperation of specialized ion channels

  • Excitable Tissues and Central Nervous Physiology
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Attwell D, Brew H, Gray P, Mobbs P (1986) Single potassium channels in Müller cells of the salamander retina. J Physiol 371:35P

    Google Scholar 

  • 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

    Google Scholar 

  • Conner JD, Detwiler PB, Sarthy PV (1985) Ionic and electrophysiological properties of retinal Müller (glial) cells of the turtle. J Physiol 362:79–92

    Google Scholar 

  • Corey DP, Barres BA, Chun LLY (1985) An inwardly rectifying potassium channel in oligodendroglia. Soc Neurosci Abst 11:148

    Google Scholar 

  • 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

    Google Scholar 

  • Fukushima Y (1982) Blocking kinetics of the anomalous potassium rectifier of tunicate egg studied by single channel recording. J Physiol 331:311–331

    Google Scholar 

  • Gardner-Medwin AR (1984) A foot in the vitreous fluid. Nature 309:113

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Newman EA (1984) Regional specialization of retinal glial cell membrane. Nature 309:155–157

    Google Scholar 

  • Newman EA (1985a) Membrane physiology of retinal glial (Müller) cells. J Neurosci 5:2225–2239

    Google Scholar 

  • Newman EA (1985b) Voltage-dependent calcium and potassium channels in retinal glial cells. Nature 317:809–811

    Google Scholar 

  • Newman EA (1986) Potassium conductance hot-spots in mammalian Müller (glial) cells. Soc Neurosci Abst 12: (part 1) 633

    Google Scholar 

  • Newman EA (1987) Distribution of potassium conductance in mammalian Müller (glial) cells. A comparative study. J Neurosci 7:2423–2432

    Google Scholar 

  • Newman EA, Odette LL (1984) Model of electroretinogram b-wave generation: a test of the K+ hypothesis. J Neurophysiol 51:164–182

    Google Scholar 

  • Newman EA, Frambach DA, Odette LL (1984) Control of extracellular potassium levels by retinal glial cell K+ siphoning. Science 225:1174–1175

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Raviola G (1977) The structural basis of the blood-ocular barriers. Exp Eye Res 25 (Suppl):27–63

    Google Scholar 

  • Reale E, Luciano L, Spitznas M (1974) Introduction to freeze-fracture method in retinal research. Graefes Arch Clin Exp Ophthalmol 192:73–87

    Google Scholar 

  • Reichenbach A, Birkenmeyer G (1984) Preparation of isolated Müller cells of the mammalian (rabbit) retina. Z Mikrosk Anat Forsch 98:789–792

    Google Scholar 

  • Reichenbach A, Eberhardt W (1986) Intracellular recordings from isolated rabbit retinal Müller (glial) cells. Pflügers Arch 407:348–353

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00580862

Key words

Navigation