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

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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.

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Author notes

  1. Akikazu Fujita

    Present address: Field of Veterinary Pathobiology, Basic Veterinary Science, Department of Veterinary Medicine, Joint Faculty of Veterinary Medicine, Kagoshima University, Korimoto 1-21-24, Kagoshima, 890-0065, Japan

  2. Hiroshi Hibino

    Present address: Department of Molecular Physiology, Niigata University School of Medicine, 1-757 Asahimachi-dori, Chuo-ku, Niigata, Niigata, 951-8510, Japan

Authors and Affiliations

  1. Division of Molecular and Cellular Pharmacology, Department of Pharmacology, Graduate School of Medicine, Osaka University, 2-2 Yamada-oka, Suita, Osaka, 565-0871, Japan

    Akikazu Fujita, Atsushi Inanobe, Hiroshi Hibino & Yoshihisa Kurachi

  2. Center for Molecular Biology and Neuroscience and Department of Anatomy, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway

    Ole Petter Ottersen

  3. Water and Salt Research Center, Department of Biomedicine, Aarhus University, Aarhus, Denmark

    Søren Nielsen

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  1. Akikazu Fujita
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Correspondence to Akikazu Fujita or Yoshihisa Kurachi.

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Fujita, A., Inanobe, A., Hibino, H. et al. Clustering of Kir4.1 at specialized compartments of the lateral membrane in ependymal cells of rat brain. Cell Tissue Res 359, 627–634 (2015). https://doi.org/10.1007/s00441-014-2030-6

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  • DOI: https://doi.org/10.1007/s00441-014-2030-6

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