Clustering of Kir4.1 at specialized compartments of the lateral membrane in ependymal cells of rat brain

Cell Tissue Res. 2015 Feb;359(2):627-634. doi: 10.1007/s00441-014-2030-6. Epub 2014 Nov 8.

Abstract

Brain ependymal cells, which form an epithelial layer covering the cerebral ventricles, have been shown to play a role in the regulation of cerebrospinal and interstitial fluids. The machinery underlying this, however, remains largely unknown. Here, we report the specific localization of an inwardly rectifying K(+) channel, Kir4.1, on the ependymal cell membrane suggesting involvement of the channel in this function. Immunohistochemical study with confocal microscopy identified Kir4.1 labeling on the lateral but not apical membrane of ependymal cells. Ultrastructural analysis revealed that Kir4.1-immunogold particles were specifically localized and clustered on adjacent membranes at puncta adherens type junctions, whereas an aquaporin water channel, AQP4, that was also detected on the lateral membrane only occurred at components other than adherens junctions. Therefore, in ependymal cells, Kir4.1 and AQP4 are partitioned into distinct membrane compartments that might respectively transport either K(+) or water. Kir4.1 was also expressed in a specialized form of ependymal cell, namely the tanycyte, being abundant in tanycyte processes wrapping neuropils and blood vessels. These specific localizations suggest that Kir4.1 mediates intercellular K(+) exchange between ependymal cells and also K(+)-buffering transport via tanycytes that can interconnect neurons and vessels/ventricles. We propose that ependymal cells and tanycytes differentially operate Kir4.1 and AQP4 actively to control the property of fluids at local areas in the brain.

MeSH terms

  • Animals
  • Aquaporin 4 / metabolism
  • Cell Compartmentation*
  • Cell Membrane / metabolism*
  • Cell Membrane / ultrastructure
  • Ependyma / cytology*
  • Ependyma / metabolism
  • Ependyma / ultrastructure
  • Ependymoglial Cells / cytology
  • Ependymoglial Cells / metabolism
  • Male
  • Potassium Channels, Inwardly Rectifying / metabolism*
  • Protein Transport
  • Rats, Wistar
  • Subcellular Fractions / metabolism

Substances

  • Aquaporin 4
  • Kcnj10 (channel)
  • Potassium Channels, Inwardly Rectifying