The unique ion permeability profile of cochlear fibrocytes and its contribution to establishing their positive resting membrane potential

Takamasa Yoshida, Fumiaki Nin, Shingo Murakami, Genki Ogata, Satoru Uetsuka, Samuel Choi, Takashi Nakagawa, Hidenori Inohara, Shizuo Komune, Yoshihisa Kurachi, Hiroshi Hibino

Research output: Contribution to journalArticle

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Abstract

Eukaryotic cells exhibit negative resting membrane potential (RMP) owing to the high K+ permeability of the plasma membrane and the asymmetric [K+] between the extracellular and intracellular compartments. However, cochlear fibrocytes, which comprise the basolateral surface of a multilayer epithelial-like tissue, exhibit a RMP of +5 to +12 mV in vivo. This positive RMP is critical for the formation of an endocochlear potential (EP) of +80 mV in a K+-rich extracellular fluid, endolymph. The epithelial-like tissue bathes fibrocytes in a regular extracellular fluid, perilymph, and apically faces the endolymph. The EP, which is essential for hearing, represents the potential difference across the tissue. Using in vivo electrophysiological approaches, we describe a potential mechanism underlying the unusual RMP of guinea pig fibrocytes. The RMP was +9.0 ± 3.7 mV when fibrocytes were exposed to an artificial control perilymph (n = 28 cochleae). Perilymphatic perfusion of a solution containing low [Na+] (1 mM) markedly hyperpolarized the RMP to −31.1 ± 11.2 mV (n = 10; p < 0.0001 versus the control, Tukey–Kramer test after one-way ANOVA). Accordingly, the EP decreased. Little change in RMP was observed when the cells were treated with a high [K+] of 30 mM (+10.4 ± 2.3 mV; n = 7; p = 0.942 versus the control). During the infusion of a low [Cl] solution (2.4 mM), the RMP moderately hyperpolarized to −0.9 ± 3.4 mV (n = 5; p < 0.01 versus the control), although the membranes, if governed by Cl permeability, should be depolarized. These observations imply that the fibrocyte membranes are more permeable to Na+ than K+ and Cl, and this unique profile and [Na+] gradient across the membranes contribute to the positive RMP.

Original languageEnglish
Pages (from-to)1609-1619
Number of pages11
JournalPflugers Archiv European Journal of Physiology
Volume468
Issue number9
DOIs
Publication statusPublished - Sep 1 2016

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Cochlea
Membrane Potentials
Permeability
Ions
Membranes
Endolymph
Perilymph
Extracellular Fluid
Tissue
Epithelium
Eukaryotic Cells
Hearing
Fluids
Analysis of Variance
Guinea Pigs
Audition
Cell membranes
Perfusion
Analysis of variance (ANOVA)
Cell Membrane

All Science Journal Classification (ASJC) codes

  • Physiology
  • Clinical Biochemistry
  • Physiology (medical)

Cite this

The unique ion permeability profile of cochlear fibrocytes and its contribution to establishing their positive resting membrane potential. / Yoshida, Takamasa; Nin, Fumiaki; Murakami, Shingo; Ogata, Genki; Uetsuka, Satoru; Choi, Samuel; Nakagawa, Takashi; Inohara, Hidenori; Komune, Shizuo; Kurachi, Yoshihisa; Hibino, Hiroshi.

In: Pflugers Archiv European Journal of Physiology, Vol. 468, No. 9, 01.09.2016, p. 1609-1619.

Research output: Contribution to journalArticle

Yoshida, Takamasa ; Nin, Fumiaki ; Murakami, Shingo ; Ogata, Genki ; Uetsuka, Satoru ; Choi, Samuel ; Nakagawa, Takashi ; Inohara, Hidenori ; Komune, Shizuo ; Kurachi, Yoshihisa ; Hibino, Hiroshi. / The unique ion permeability profile of cochlear fibrocytes and its contribution to establishing their positive resting membrane potential. In: Pflugers Archiv European Journal of Physiology. 2016 ; Vol. 468, No. 9. pp. 1609-1619.
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AU - Choi, Samuel

AU - Nakagawa, Takashi

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