The Membrane Properties of Cochlear Root Cells are Consistent with Roles in Potassium Recirculation and Spatial Buffering

• Published in: Journal of the Association for Research in Otolaryngology Vol. 11; no. 3; pp. 435 - 448
• Main Authors: Jagger, Daniel J., Nevill, Graham, Forge, Andrew
• Format: Journal Article
• Language: English
• Published: New York Springer-Verlag 01.09.2010; Springer Nature B.V
• Subjects: Animals; Barium - pharmacology; Cochlea - cytology; Cochlea - physiology; Gap Junctions - physiology; Guinea Pigs; Medicine; Medicine & Public Health; Neurobiology; Neurosciences; Otorhinolaryngology; Potassium - metabolism; Potassium Channels, Inwardly Rectifying - physiology; gap junctions; spiral ligament; inward rectifier; Kir4.1; deafness; stria vascularis
• ISSN: 1525-3961; 1438-7573
• DOI: 10.1007/s10162-010-0218-3

Auditory transduction, amplification, and hair cell survival depend on the regulation of extracellular [K + ] in the cochlea. K + is removed from the vicinity of sensory hair cells by epithelial cells, and may be distributed through the epithelial cell syncytium, reminiscent of “spatial buffering” in glia. Hypothetically, K + is then transferred from the epithelial syncytium into the connective tissue syncytium within the cochlear lateral wall, enabling recirculation of K + back into endolymph. This may involve secretion of K + from epithelial root cells, and its re-uptake via transporters into spiral ligament fibrocytes. The molecular basis of this secretion is not known. Using a combination of approaches we demonstrated that the resting conductance in guinea pig root cells was dominated by K + channels, most likely composed of the Kir4.1 subunit. Dye injections revealed extensive intercellular gap junctional coupling, and delineated the root cell processes that penetrated the spiral ligament. Following uncoupling using 1-octanol, individual cells had Ba 2+ -sensitive weakly rectifying currents. In the basal (high-frequency encoding) cochlear region K + loads are predicted to be the highest, and root cells in this region had the largest surface area and the highest current density, consistent with their role in K + secretion. Kir4.1 was localized within root cells by immunofluorescence, and specifically to root cell process membranes by immunogold labeling. These results support a role for root cells in cochlear K + regulation, and suggest that channels composed of Kir4.1 subunits may mediate K + secretion from the epithelial gap junction network.