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Impairment of SLC17A8 encoding vesicular glutamate transporter-3, VGLUT3, underlies nonsyndromic deafness DFNA25 and inner hair cell dysfunction in null mice
Journal article   Open access   Peer reviewed

Impairment of SLC17A8 encoding vesicular glutamate transporter-3, VGLUT3, underlies nonsyndromic deafness DFNA25 and inner hair cell dysfunction in null mice

Jérôme Ruel, Sarah Emery, Régis Nouvian, Tiphaine Bersot, Bénédicte Amilhon, Jana Van Rybroek, Guy Rebillard, Marc Lenoir, Michel Eybalin, Benjamin Delprat, …
American journal of human genetics, Vol.83(2), pp.278-292
08/2008
DOI: 10.1016/j.ajhg.2008.07.008
PMCID: PMC2495073
PMID: 18674745
url
https://doi.org/10.1016/j.ajhg.2008.07.008View
Published (Version of record) Open Access

Abstract

Autosomal-dominant sensorineural hearing loss is genetically heterogeneous, with a phenotype closely resembling presbycusis, the most common sensory defect associated with aging in humans. We have identified SLC17A8, which encodes the vesicular glutamate transporter-3 (VGLUT3), as the gene responsible for DFNA25, an autosomal-dominant form of progressive, high-frequency nonsyndromic deafness. In two unrelated families, a heterozygous missense mutation, c.632C-->T (p.A211V), was found to segregate with DFNA25 deafness and was not present in 267 controls. Linkage-disequilibrium analysis suggested that the families have a distant common ancestor. The A211 residue is conserved in VGLUT3 across species and in all human VGLUT subtypes (VGLUT1-3), suggesting an important functional role. In the cochlea, VGLUT3 accumulates glutamate in the synaptic vesicles of the sensory inner hair cells (IHCs) before releasing it onto receptors of auditory-nerve terminals. Null mice with a targeted deletion of Slc17a8 exon 2 lacked auditory-nerve responses to acoustic stimuli, although auditory brainstem responses could be elicited by electrical stimuli, and robust otoacoustic emissions were recorded. Ca(2+)-triggered synaptic-vesicle turnover was normal in IHCs of Slc17a8 null mice when probed by membrane capacitance measurements at 2 weeks of age. Later, the number of afferent synapses, spiral ganglion neurons, and lateral efferent endings below sensory IHCs declined. Ribbon synapses remaining by 3 months of age had a normal ultrastructural appearance. We conclude that deafness in Slc17a8-deficient mice is due to a specific defect of vesicular glutamate uptake and release and that VGLUT3 is essential for auditory coding at the IHC synapse.
Deafness Life Sciences Mutation Hair Cells, Auditory Humans Neurons and Cognition Chromosome Mapping Amino Acid Transport Systems, Acidic Mice, Knockout Linkage Disequilibrium Animals Models, Genetic Polymorphism, Single Nucleotide Vesicular Glutamate Transport Proteins Mice Genome Disease Models, Animal

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