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The unique ion permeability profile of cochlear fibrocytes and its contribution to establishing their positive resting membrane potential.
Pflugers Arch. 2016 09; 468(9):1609-19.PA

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.

Authors+Show Affiliations

Department of Molecular Physiology, Niigata University School of Medicine, 1-757 Asahimachi-dori, Chuo-ku, Niigata, Niigata, 951-8510, Japan. Center for Transdisciplinary Research, Niigata University, Niigata, Niigata, 950-2181, Japan. Department of Otorhinolaryngology, Graduate School of Medical Sciences, Kyushu University, Fukuoka, 812-8582, Japan.Department of Molecular Physiology, Niigata University School of Medicine, 1-757 Asahimachi-dori, Chuo-ku, Niigata, Niigata, 951-8510, Japan. Center for Transdisciplinary Research, Niigata University, Niigata, Niigata, 950-2181, Japan.Division of Molecular and Cellular Pharmacology, Department of Pharmacology, Osaka University, Suita, Osaka, 565-0871, Japan. The Center for Advanced Medical Engineering and Informatics, Osaka University, Suita, Osaka, 565-0871, Japan.Department of Molecular Physiology, Niigata University School of Medicine, 1-757 Asahimachi-dori, Chuo-ku, Niigata, Niigata, 951-8510, Japan. Center for Transdisciplinary Research, Niigata University, Niigata, Niigata, 950-2181, Japan.Department of Molecular Physiology, Niigata University School of Medicine, 1-757 Asahimachi-dori, Chuo-ku, Niigata, Niigata, 951-8510, Japan. Center for Transdisciplinary Research, Niigata University, Niigata, Niigata, 950-2181, Japan. Department of Otorhinolaryngology-Head and Neck Surgery, Graduate School of Medicine, Osaka University, Suita, Osaka, 565-0871, Japan.Department of Electrical and Electronics Engineering, Niigata University, Niigata, 950-2181, Niigata, Japan. AMED-CREST, AMED, Niigata, Japan.Department of Otorhinolaryngology, Graduate School of Medical Sciences, Kyushu University, Fukuoka, 812-8582, Japan.Department of Otorhinolaryngology-Head and Neck Surgery, Graduate School of Medicine, Osaka University, Suita, Osaka, 565-0871, Japan.Department of Otorhinolaryngology, Graduate School of Medical Sciences, Kyushu University, Fukuoka, 812-8582, Japan. Division of Otolaryngology-Head and Neck Surgery, Yuaikai Oda Hospital, Saga, 849-1392, Japan.Division of Molecular and Cellular Pharmacology, Department of Pharmacology, Osaka University, Suita, Osaka, 565-0871, Japan. The Center for Advanced Medical Engineering and Informatics, Osaka University, Suita, Osaka, 565-0871, Japan.Department of Molecular Physiology, Niigata University School of Medicine, 1-757 Asahimachi-dori, Chuo-ku, Niigata, Niigata, 951-8510, Japan. hibinoh@med.niigata-u.ac.jp. Center for Transdisciplinary Research, Niigata University, Niigata, Niigata, 950-2181, Japan. hibinoh@med.niigata-u.ac.jp. AMED-CREST, AMED, Niigata, Japan. hibinoh@med.niigata-u.ac.jp.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

27344659

Citation

Yoshida, Takamasa, et al. "The Unique Ion Permeability Profile of Cochlear Fibrocytes and Its Contribution to Establishing Their Positive Resting Membrane Potential." Pflugers Archiv : European Journal of Physiology, vol. 468, no. 9, 2016, pp. 1609-19.
Yoshida T, Nin F, Murakami S, et al. The unique ion permeability profile of cochlear fibrocytes and its contribution to establishing their positive resting membrane potential. Pflugers Arch. 2016;468(9):1609-19.
Yoshida, T., Nin, F., Murakami, S., Ogata, G., Uetsuka, S., Choi, S., Nakagawa, T., Inohara, H., Komune, S., Kurachi, Y., & Hibino, H. (2016). The unique ion permeability profile of cochlear fibrocytes and its contribution to establishing their positive resting membrane potential. Pflugers Archiv : European Journal of Physiology, 468(9), 1609-19. https://doi.org/10.1007/s00424-016-1853-2
Yoshida T, et al. The Unique Ion Permeability Profile of Cochlear Fibrocytes and Its Contribution to Establishing Their Positive Resting Membrane Potential. Pflugers Arch. 2016;468(9):1609-19. PubMed PMID: 27344659.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - The unique ion permeability profile of cochlear fibrocytes and its contribution to establishing their positive resting membrane potential. AU - Yoshida,Takamasa, AU - Nin,Fumiaki, AU - Murakami,Shingo, AU - Ogata,Genki, AU - Uetsuka,Satoru, AU - Choi,Samuel, AU - Nakagawa,Takashi, AU - Inohara,Hidenori, AU - Komune,Shizuo, AU - Kurachi,Yoshihisa, AU - Hibino,Hiroshi, Y1 - 2016/06/25/ PY - 2016/02/29/received PY - 2016/06/14/accepted PY - 2016/05/30/revised PY - 2016/6/27/entrez PY - 2016/6/28/pubmed PY - 2017/7/1/medline KW - Endocochlear potential KW - Inner ear KW - Na+ permeability KW - Resting membrane potential KW - Spiral ligament SP - 1609 EP - 19 JF - Pflugers Archiv : European journal of physiology JO - Pflugers Arch. VL - 468 IS - 9 N2 - 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. SN - 1432-2013 UR - https://www.unboundmedicine.com/medline/citation/27344659/The_unique_ion_permeability_profile_of_cochlear_fibrocytes_and_its_contribution_to_establishing_their_positive_resting_membrane_potential_ L2 - https://dx.doi.org/10.1007/s00424-016-1853-2 DB - PRIME DP - Unbound Medicine ER -