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The Journal of Neuroscience, August 15, 2000, 20(16):5940-5948

Two Distinct Ca²⁺-Dependent Signaling Pathways Regulate the Motor Output of Cochlear Outer Hair Cells

Gregory I. Frolenkov¹, Fabio Mammano², Inna A. Belyantseva¹, Donald Coling¹, and Bechara Kachar¹

¹ Section on Structural Cell Biology, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, Maryland 20892-4163, and ² Laboratory of Biophysics and Istituto Nazionale di Fisica della Materia, International School for Advanced Studies, via Beirut 2-4, 34014, Trieste, Italy

The outer hair cells (OHCs) of the cochlea have an electromotility mechanism, based on conformational changes of voltage-sensitive "motor" proteins in the lateral plasma membrane. The translocation of electrical charges across the membrane that accompanies electromotility imparts a voltage dependency to the membrane capacitance. We used capacitance measurements to investigate whether electromotility may be influenced by different manipulations known to affect intracellular Ca²⁺ or Ca²⁺-dependent protein phosphorylation. Application of acetylcholine (ACh) to the synaptic pole of isolated OHCs evoked a Ca²⁺-activated apamin-sensitive outward K⁺ current. It also enhanced electromotility, probably because of a phosphorylation-dependent decrease of the cell's axial stiffness. However, ACh did not change the voltage-dependent capacitance either in conventional whole-cell experiments or under perforated-patch conditions. The effects produced by the Ca²⁺ ionophore ionomycin mimicked those produced by ACh. Hyperpolarizing shifts of the voltage dependence of capacitance and electromotility were induced by okadaic acid, a promoter of protein phosphorylation, whereas trifluoperazine and W-7, antagonists of calmodulin, caused opposite depolarizing shifts. Components of the protein phosphorylation cascadeIP₃ receptors and calmodulin-dependent protein kinase type IVwere immunolocalized to the lateral wall of the OHC. Our results suggest that two different Ca²⁺-dependent pathways may control the OHC motor output. The first pathway modulates cytoskeletal stiffness and can be activated by ACh. The second pathway shifts the voltage sensitivity of the OHC electromotile mechanism and may be activated by the release of Ca²⁺ from intracellular stores located in the proximity of the lateral plasma membrane.

Key words: sensory transduction; electromotility; voltage-dependent capacitance; cochlea; endoplasmic reticulum; patch clamp; organ of Corti

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Copyright © 2000 Society for Neuroscience  0270-6474/00/20165940-09$05.00/0

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