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The Journal of Neuroscience, April 28, 2004, 24(17):4213-4223; doi:10.1523/JNEUROSCI.0223-04.2004

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Cellular/Molecular
gemini Encodes a Zebrafish L-Type Calcium Channel That Localizes at Sensory Hair Cell Ribbon Synapses

Samuel Sidi,¹ Elisabeth Busch-Nentwich,¹ Rainer Friedrich,² Ulrike Schoenberger,¹ and Teresa Nicolson³

¹Max-Planck-Institut für Entwicklungsbiologie, 72076 Tübingen, Germany, ²Max-Planck-Institut für Medizinische Forschung, 69120 Heidelberg, Germany, and ³Oregon Hearing Research Center and Vollum Institute, Portland, Oregon 97239

L-type Ca²⁺ channels (LTCCs) drive the bulk of voltage-gated Ca²⁺ entry in vertebrate inner ear hair cells (HCs) and are essential for mammalian auditory processing. LTCC currents have been implicated in neurotransmitter release at the HC afferent active zone, the ribbon synapse. It is likely that LTCCs play a direct role in vesicle fusion; however, the subcellular localization of the channels in HCs has not been fully resolved. Via positional cloning, we show that mutations in a zebrafish LTCC encoding gene, cav1.3a, underlie the auditory-vestibular defects of gemini (gem) circler mutants. gem homozygous receptor mutant HCs display normal cell viability, afferent synaptogenesis, and peripheral innervation, yet exhibit strongly reduced extracellular potentials (50% of wild-type potentials). Apical FM1-43 uptake, however, is unaffected in gem mutant HCs, suggesting that mechanotransduction channels are functional. Using a Gem-specific antibody, we show that the bulk of Gem/Ca_v1.3a immunoreactivity in HCs is restricted to basally located focal spots. The number and location of focal spots relative to nerve terminals, and their remarkable ring-shaped structure, which is reminiscent of synaptic dense bodies, are consistent with Gem/Ca_v1.3a channels clustering at HC ribbon synapses.

Key words: gemini; L-type calcium channels; deafness; hair cell; ribbon synapse; microphonics; synaptic transmission

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Received Nov 21, 2003; revised March 12, 2004; accepted March 15, 2004.

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