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The Journal of Neuroscience, August 24, 2005, 25(34):7867-7875; doi:10.1523/JNEUROSCI.1196-05.2005

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Cellular/Molecular
The Concentrations of Calcium Buffering Proteins in Mammalian Cochlear Hair Cells

Carole M. Hackney,^1,2 Shanthini Mahendrasingam,¹ Andrew Penn,¹ and Robert Fettiplace³

¹MacKay Institute of Communication and Neuroscience, School of Life Sciences, Keele University, Keele, Staffordshire ST5 5BG, United Kingdom, and Departments of ²Anatomy and ³Physiology, University of Wisconsin Medical School, Madison, Wisconsin 53706

Calcium buffers are important for shaping and localizing cytoplasmic Ca²⁺ transients in neurons. We measured the concentrations of the four main calcium-buffering proteins (calbindin-D28k, calretinin, parvalbumin-, and parvalbumin-) in rat cochlear hair cells in which Ca²⁺ signaling is a central element of fast transduction and synaptic transmission. The proteins were quantified by calibrating immunogold tissue counts against gels containing known amounts of each protein, and the method was verified by application to Purkinje cells in which independent estimates exist for some of the protein concentrations. The results showed that, in animals with fully developed hearing, inner hair cells had of the proteinaceous calcium buffer of outer hair cells in which the cell body contained parvalbumin- (oncomodulin) and calbindin-D28k at levels equivalent to 5 mM calcium-binding sites. Both proteins were partially excluded from the hair bundles, which may permit fast unbuffered Ca²⁺ regulation of the mechanotransducer channels. The sum of the calcium buffer concentrations decreased in inner hair cells and increased in outer hair cells as the cells developed their adult properties during cochlear maturation. The results suggest that Ca²⁺ has distinct roles in the two types of hair cell, reflecting their different functions in auditory transduction. Ca²⁺ is used in inner hair cells primarily for fast phase-locked synaptic transmission, whereas Ca²⁺ may be involved in regulating the motor capability underlying cochlear amplification of the outer hair cell. The high concentration of calcium buffer in outer hair cells, similar only to skeletal muscle, may protect against deleterious consequences of Ca²⁺ loading after acoustic overstimulation.

Key words: cochlea; calcium; calbindin-D28k; calretinin; hair cells; immunocytochemistry; oncomodulin; parvalbumin-; postembedding labeling

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Received March 28, 2005; revised July 18, 2005; accepted July 19, 2005.

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