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Co-localisation of Kir4.1 and AQP4 in rat and human cochleae reveals a gap in water channel expression at the transduction sites of endocochlear K+ recycling routes

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Abstract

Sensory transduction in the cochlea depends on perilymphatic-endolymphatic potassium (K+) recycling. It has been suggested that the epithelial supporting cells (SCs) of the cochlear duct may form the intracellular K+ recycling pathway. Thus, they must be endowed with molecular mechanisms that facilitate K+ uptake and release, along with concomitant osmotically driven water movements. As yet, no molecules have been described that would allow for volume-equilibrated transepithelial K+ fluxes across the SCs. This study describes the subcellular co-localisation of the Kir4.1 K+ channel (Kir4.1) and the aquaporin-4 water channel (AQP4) in SCs, on the basis of immunohistochemical double-labelling experiments in rat and human cochleae. The results of this study reveal the expression of Kir4.1 in the basal or basolateral membranes of the SCs in the sensory domain of the organ of Corti that are adjacent to hair cells and in the non-sensory domains of the inner and outer sulci that abut large extracellular fluid spaces. The SCs of the inner sulcus (interdental cells, inner sulcus cells) and the outer sulcus (Hensen’s cells, outer sulcus cells) display the co-localisation of Kir4.1 and AQP4 expression. However, the SCs in the sensory domain of the organ of Corti reveal a gap in the expression of AQP4. The outer pillar cell is devoid of both Kir4.1 and AQP4. The subcellular co-localisation of Kir4.1 and AQP4 in the SCs of the cochlea described in this study resembles that of the astroglia of the central nervous system and the glial Mueller cells in the retina.

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Abbreviations

AQP4:

aquaporin-4

Kir4.1:

inwardly rectifying potassium channel Kir4.1

EP:

endocochlear potential

HBSS:

Hanks’ balanced saline solution

HEPES:

4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid

PTA:

pure tone audiometry

IDC:

interdental cell

ISC-sl:

inner sulcus cell near the spiral limbus

ISC-oc:

inner sulcus cell near the organ of Corti

IHC:

inner hair cell

IPhC:

inner phalangeal cell

IPC:

inner pillar cell

OPC:

outer pillar cell

OHC:

outer hair cell

DC:

outer phalangeal cell (Deiters’ cell)

HC:

Hensen’s cell

CC:

Claudius cell

OSC:

outer sulcus cell

SV:

stria vascularis

SCs:

supporting cells

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Acknowledgments

We are grateful to Prof. Hans-Joachim Wagner and Prof. Hans-Peter Zenner for their continued support. We thank Dr. Karina Gültig, Andrea Müller and Xenia Härtel for excellent technical assistance.

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Authors and Affiliations

  1. Hearing Research Centre Department of Otorhinolaryngology-Head & Neck Surgery, University of Tübingen Medical Center, Elfriede-Aulhorn-Straße 5, 72076, Tübingen, Germany

    Andreas Eckhard, Heinz Arnold, Marcus Müller, Hubert Löwenheim & Bernhard Hirt

  2. Department of Anatomy, University of Tübingen, Tübingen, Germany

    Corinna Gleiser, Andreas Mack & Bernhard Hirt

  3. Department of Surgical Sciences, Section of Otolaryngology, Uppsala University Hospital, Uppsala, Sweden

    Helge Rask-Andersen & Wei Liu

Authors
  1. Andreas Eckhard
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  2. Corinna Gleiser
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  3. Helge Rask-Andersen
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  4. Heinz Arnold
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  5. Wei Liu
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  6. Andreas Mack
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  7. Marcus Müller
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  8. Hubert Löwenheim
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  9. Bernhard Hirt
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Corresponding author

Correspondence to Hubert Löwenheim.

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This study was supported by the “fortüne” program (Project number: 1477-0-0) of the University of Tübingen Medical School.

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Eckhard, A., Gleiser, C., Rask-Andersen, H. et al. Co-localisation of Kir4.1 and AQP4 in rat and human cochleae reveals a gap in water channel expression at the transduction sites of endocochlear K+ recycling routes. Cell Tissue Res 350, 27–43 (2012). https://doi.org/10.1007/s00441-012-1456-y

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