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The Journal of Neuroscience, August 15, 1999, 19(16):6918-6929

ATP-Induced Ca²⁺ Release in Cochlear Outer Hair Cells: Localization of an Inositol Triphosphate-Gated Ca²⁺ Store to the Base of the Sensory Hair Bundle

Fabio Mammano¹, Gregory I. Frolenkov², Laura Lagostena¹, Inna A. Belyantseva², Mauricio Kurc², Valerie Dodane², Alberto Colavita³, and Bechara Kachar²

¹ Biophysics Sector and Istituto Nazionale di Fisica della Materia Unit, International School for Advanced Studies, 34014 Trieste, Italy, ² Section on Structural Cell Biology, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, Maryland 20892-4163, and ³ Microprocessor Laboratory, Abdus Salam Centre for Theoretical Physics and Istituto Nazionale di Fisica Nucleare, 34014 Trieste, Italy

We used a high-performance fluorescence imaging system to visualize rapid changes in intracellular free Ca²⁺ concentration ([Ca²⁺]_i) evoked by focal applications of extracellular ATP to the hair bundle of outer hair cells (OHCs): the sensory-motor receptors of the cochlea. Simultaneous recordings of the whole-cell current and Calcium Green-1 fluorescence showed a two-component increase in [Ca²⁺]_i. After an initial entry of Ca²⁺ through the apical membrane, a second and larger, inositol triphosphate (InsP₃)-gated, [Ca²⁺]_i surge occurred at the base of the hair bundle. Electron microscopy of this intracellular Ca²⁺ release site showed that it coincides with the localization of a unique system of endoplasmic reticulum (ER) membranes and mitochondria known as Hensen's body. Using confocal immunofluorescence microscopy, we showed that InsP₃ receptors share this location. Consistent with a Ca²⁺-mobilizing second messenger system linked to ATP-P2 receptors, we also determined that an isoform of G-proteins is present in the stereocilia. Voltage-driven cell shape changes and nonlinear capacitance were monitored before and after ATP application, showing that the ATP-evoked [Ca²⁺]_i rise did not interfere with the OHC electromotility mechanism. This second messenger signaling mechanism bypasses the Ca²⁺-clearance power of the stereocilia and transiently elevates [Ca²⁺]_i at the base of the hair bundle, where it can potentially modulate the action of unconventional myosin isozymes involved in maintaining the hair bundle integrity and potentially influence mechanotransduction.

Key words: sensory transduction; cochlea; purinergic receptors; InsP₃; endoplasmic reticulum; mitochondria; G-proteins; electromotility; patch-clamp; calcium imaging; organ of Corti; Hensen's body

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Copyright © 1999 Society for Neuroscience  0270-6474/99/19166918-12$05.00/0

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