Impairment of SLC17A8 Encoding Vesicular Glutamate Transporter-3, VGLUT3, Underlies Nonsyndromic Deafness DFNA25 and Inner Hair Cell Dysfunction in Null Mice

American Journal of Human Genetics

Volumn 83, Issue 2, 2008, Pages 278-292

  Ruel, Jérôme ^a,b   Emery, Sarah ^c   Nouvian, Régis ^d   Bersot, Tiphaine ^a,b   Amilhon, Bénédicte ^e   Van Rybroek, Jana M ^f   Rebillard, Guy ^a,b   Lenoir, Marc ^a,b   Eybalin, Michel ^a,b   Delprat, Benjamin ^a,b   Sivakumaran, Theru A ^c   Giros, Bruno ^e   El Mestikawy, Salah ^e   Moser, Tobias ^d,g   Smith, Richard J H ^f   Lesperance, Marci M ^c   Puel, Jean Luc ^a,b  

^a HÔPITAL SAINT ELOI   (France)

^b UNIV MONTPELLIER   (France)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d Center for Molecular Physiology of the Brain   (Germany)

^e INSERM   (France)

^f UNIVERSITY OF IOWA   (United States)

^g BERNSTEIN CENTER FOR COMPUTATIONAL NEUROSCIENCE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; GLUTAMIC ACID; PROTEIN SUBUNIT; VESICULAR GLUTAMATE TRANSPORTER 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; COCHLEA; COCHLEAR NERVE; CONTROLLED STUDY; ELECTROSTIMULATION; EVOKED BRAIN STEM AUDITORY RESPONSE; EXON; FAMILY; GENE DELETION; GENE LINKAGE DISEQUILIBRIUM; GENETIC IDENTIFICATION; HAIR CELL; HEARING IMPAIRMENT; HETEROZYGOSITY; HUMAN; MISSENSE MUTATION; MOUSE; NERVE ENDING; NONHUMAN; NUCLEOTIDE SEQUENCE; OTOACOUSTIC EMISSION; PRIORITY JOURNAL; SYNAPSE; SYNAPSE VESICLE;

AMINO ACID TRANSPORT SYSTEMS, ACIDIC; ANIMALS; CHROMOSOME MAPPING; DEAFNESS; DISEASE MODELS, ANIMAL; GENOME; HAIR CELLS, AUDITORY; HUMANS; LINKAGE DISEQUILIBRIUM; MICE; MICE, KNOCKOUT; MODELS, GENETIC; MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

MUS;

EID: 48349111572     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ajhg.2008.07.008     Document Type: Article

References (53)

1. Pleis J.R., and Lethbridge-Cejku M. Summary health statistics for U.S. adults: National Health Interview Survey, 2005. Vital Health Stat. 10 (2006) 1-153
2. Gates G.A., Couropmitree N.N., and Myers R.H. Genetic associations in age-related hearing thresholds. Arch. Otolaryngol. Head Neck Surg. 125 (1999) 654-659
3. Cruickshanks K.J., Wiley T.L., Tweed T.S., Klein B.E., Klein R., Mares-Perlman J.A., and Nondahl D.M. Prevalence of hearing loss in older adults in Beaver Dam, Wisconsin. The Epidemiology of Hearing Loss Study. Am. J. Epidemiol. 148 (1998) 879-886
4. Brown S.D., Hardisty-Hughes R.E., and Mburu P. Quiet as a mouse: Dissecting the molecular and genetic basis of hearing. Nat. Rev. Genet. 9 (2008) 277-290
5. Greene C.C., McMillan P.M., Barker S.E., Kurnool P., Lomax M.I., Burmeister M., and Lesperance M.M. DFNA25, a novel locus for dominant nonsyndromic hereditary hearing impairment, maps to 12q21-24. Am. J. Hum. Genet. 68 (2001) 254-260
6. Fuchs P.A., Glowatzki E., and Moser T. The afferent synapse of cochlear hair cells. Curr. Opin. Neurobiol. 13 (2003) 452-458
7. Nouvian R., Beutner D., Parsons T.D., and Moser T. Structure and function of the hair cell ribbon synapse. J. Membr. Biol. 209 (2006) 153-165
8. Khimich D., Nouvian R., Pujol R., Tom Dieck S., Egner A., Gundelfinger E.D., and Moser T. Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434 (2005) 889-894
9. Roux I., Safieddine S., Nouvian R., Grati M., Simmler M.C., Bahloul A., Perfettini I., Le Gall M., Rostaing P., Hamard G., et al. Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 127 (2006) 277-289
10. Varga R., Kelley P.M., Keats B.J., Starr A., Leal S.M., Cohn E., and Kimberling W.J. Non-syndromic recessive auditory neuropathy is the result of mutations in the otoferlin (OTOF) gene. J. Med. Genet. 40 (2003) 45-50
11. Yasunaga S., Grati M., Cohen-Salmon M., El-Amraoui A., Mustapha M., Salem N., El-Zir E., Loiselet J., and Petit C. A mutation in OTOF, encoding otoferlin, a FER-1-like protein, causes DFNB9, a nonsyndromic form of deafness. Nat. Genet. 21 (1999) 363-369
12. Seal R.P., Akil O., Yi E., Weber C.M., Grant L., Yoo J., Clause A., Kandler K., Noebels J.L., Glowatzki E., et al. Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3. Neuron 57 (2008) 263-275
13. Gras C., Amilhon B., Lepicard E.M., Poirel O., Vinatier J., Herbin M., Dumas S., Tzavara E.T., Wade M.R., Nomikos G.G., et al. The vesicular glutamate transporter VGLUT3 synergizes striatal acetylcholine tone. Nat. Neurosci. 11 (2008) 292-300
14. Thirlwall A.S., Brown D.J., McMillan P.M., Barker S.E., and Lesperance M.M. Phenotypic characterization of hereditary hearing impairment linked to DFNA25. Arch. Otolaryngol. Head Neck Surg. 129 (2003) 830-835
15. Brown Jr. J., Fingert J.H., Taylor C.M., Lake M., Sheffield V.C., and Stone E.M. Clinical and genetic analysis of a family affected with dominant optic atrophy (OPA1). Arch. Ophthalmol. 115 (1997) 95-99
16. Moser T., and Beutner D. Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc. Natl. Acad. Sci. USA 97 (2000) 883-888
17. Nouvian R. Temperature enhances exocytosis efficiency at the mouse inner hair cell ribbon synapse. J. Physiol. 584 (2007) 535-542
18. Lindau M., and Neher E. Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflugers Arch. 411 (1988) 137-146
19. Schmitz F., Konigstorfer A., and Sudhof T.C. RIBEYE, a component of synaptic ribbons: A protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28 (2000) 857-872
20. Knirsch M., Brandt N., Braig C., Kuhn S., Hirt B., Munkner S., Knipper M., and Engel J. Persistence of Ca(v)1.3 Ca2+ channels in mature outer hair cells supports outer hair cell afferent signaling. J. Neurosci. 27 (2007) 6442-6451
21. Schug N., Braig C., Zimmermann U., Engel J., Winter H., Ruth P., Blin N., Pfister M., Kalbacher H., and Knipper M. Differential expression of otoferlin in brain, vestibular system, immature and mature cochlea of the rat. Eur. J. Neurosci. 24 (2006) 3372-3380
22. Wenthold R.J., Yokotani N., Doi K., and Wada K. Immunochemical characterization of the non-NMDA glutamate receptor using subunit-specific antibodies. Evidence for a hetero-oligomeric structure in rat brain. J. Biol. Chem. 267 (1992) 501-507
23. Niedzielski A.S., and Wenthold R.J. Expression of AMPA, kainate, and NMDA receptor subunits in cochlear and vestibular ganglia. J. Neurosci. 15 (1995) 2338-2353
24. Matsubara A., Laake J.H., Davanger S., Usami S., and Ottersen O.P. Organization of AMPA receptor subunits at a glutamate synapse: A quantitative immunogold analysis of hair cell synapses in the rat organ of Corti. J. Neurosci. 16 (1996) 4457-4467
25. Vissavajjhala P., Janssen W.G., Hu Y., Gazzaley A.H., Moran T., Hof P.R., and Morrison J.H. Synaptic distribution of the AMPA-GluR2 subunit and its colocalization with calcium-binding proteins in rat cerebral cortex: An immunohistochemical study using a GluR2-specific monoclonal antibody. Exp. Neurol. 142 (1996) 296-312
26. Eybalin M., Caicedo A., Renard N., Ruel J., and Puel J.L. Transient Ca2+-permeable AMPA receptors in postnatal rat primary auditory neurons. Eur. J. Neurosci. 20 (2004) 2981-2989
27. Trigueiros-Cunha N., Renard N., Humbert G., Tavares M.A., and Eybalin M. Catecholamine-independent transient expression of tyrosine hydroxylase in primary auditory neurons is coincident with the onset of hearing in the rat cochlea. Eur. J. Neurosci. 18 (2003) 2653-2662
28. Borgdorff A.J., and Choquet D. Regulation of AMPA receptor lateral movements. Nature 417 (2002) 649-653
29. Eybalin M., Renard N., Aure F., and Safieddine S. Cysteine-string protein in inner hair cells of the organ of Corti: Synaptic expression and upregulation at the onset of hearing. Eur. J. Neurosci. 15 (2002) 1409-1420
30. Nemzou N.R.M., Bulankina A.V., Khimich D., Giese A., and Moser T. Synaptic organization in cochlear inner hair cells deficient for the CaV1.3 (alpha1D) subunit of L-type Ca2+ channels. Neuroscience 141 (2006) 1849-1860
31. Almqvist J., Huang Y., Laaksonen A., Wang D.N., and Hovmoller S. Docking and homology modeling explain inhibition of the human vesicular glutamate transporters. Protein Sci. 16 (2007) 1819-1829
32. Reimer R.J., and Edwards R.H. Organic anion transport is the primary function of the SLC17/type I phosphate transporter family. Pflugers Arch. 447 (2004) 629-635
33. Cruickshanks K.J., Klein R., Klein B.E., Wiley T.L., Nondahl D.M., and Tweed T.S. Cigarette smoking and hearing loss: The epidemiology of hearing loss study. JAMA 279 (1998) 1715-1719
34. Gabriel S.B., Schaffner S.F., Nguyen H., Moore J.M., Roy J., Blumenstiel B., Higgins J., DeFelice M., Lochner A., Faggart M., et al. The structure of haplotype blocks in the human genome. Science 296 (2002) 2225-2229
35. Kim T.B., Isaacson B., Sivakumaran T.A., Starr A., Keats B.J., and Lesperance M.M. A gene responsible for autosomal dominant auditory neuropathy (AUNA1) maps to 13q14-21. J. Med. Genet. 41 (2004) 872-876
36. Starr A., Isaacson B., Michalewski H.J., Zeng F.G., Kong Y.Y., Beale P., Paulson G.W., Keats B.J., and Lesperance M.M. A dominantly inherited progressive deafness affecting distal auditory nerve and hair cells. J. Assoc. Res. Otolaryngol. 5 (2004) 411-426
37. Rodriguez-Ballesteros M., del Castillo F.J., Martin Y., Moreno-Pelayo M.A., Morera C., Prieto F., Marco J., Morant A., Gallo-Teran J., Morales-Angulo C., et al. Auditory neuropathy in patients carrying mutations in the otoferlin gene (OTOF). Hum. Mutat. 22 (2003) 451-456
38. Puel J.L. Chemical synaptic transmission in the cochlea. Prog. Neurobiol. 47 (1995) 449-476
39. Fremeau Jr. R.T., Burman J., Qureshi T., Tran C.H., Proctor J., Johnson J., Zhang H., Sulzer D., Copenhagen D.R., Storm-Mathisen J., et al. The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc. Natl. Acad. Sci. USA 99 (2002) 14488-14493
40. Herzog E., Gilchrist J., Gras C., Muzerelle A., Ravassard P., Giros B., Gaspar P., and El Mestikawy S. Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123 (2004) 983-1002
41. Gras C., Herzog E., Bellenchi G.C., Bernard V., Ravassard P., Pohl M., Gasnier B., Giros B., and El Mestikawy S. A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J. Neurosci. 22 (2002) 5442-5451
42. Schafer M.K., Varoqui H., Defamie N., Weihe E., and Erickson J.D. Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. J. Biol. Chem. 277 (2002) 50734-50748
43. Wojcik S.M., Rhee J.S., Herzog E., Sigler A., Jahn R., Takamori S., Brose N., and Rosenmund C. An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc. Natl. Acad. Sci. USA 101 (2004) 7158-7163
44. Brandt A., Striessnig J., and Moser T. CaV1.3 channels are essential for development and presynaptic activity of cochlear inner hair cells. J. Neurosci. 23 (2003) 10832-10840
45. Henry K.R., and Chole R.A. Genotypic differences in behavioral, physiological and anatomical expressions of age-related hearing loss in the laboratory mouse. Audiology 19 (1980) 369-383
46. Obholzer N., Wolfson S., Trapani J.G., Mo W., Nechiporuk A., Busch-Nentwich E., Seiler C., Sidi S., Sollner C., Duncan R.N., et al. Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells. J. Neurosci. 28 (2008) 2110-2118
47. Rajan I., and Cline H.T. Glutamate receptor activity is required for normal development of tectal cell dendrites in vivo. J. Neurosci. 18 (1998) 7836-7846
48. Oestreicher E., Knipper M., Arnold A., Zenner H.P., and Felix D. Neurotrophin 3 potentiates glutamatergic responses of IHC afferents in the cochlea in vivo. Eur. J. Neurosci. 12 (2000) 1584-1590
49. Blaesse P., Ehrhardt S., Friauf E., and Nothwang H.G. Developmental pattern of three vesicular glutamate transporters in the rat superior olivary complex. Cell Tissue Res. 320 (2005) 33-50
50. Boulland J.L., Qureshi T., Seal R.P., Rafiki A., Gundersen V., Bergersen L.H., Fremeau Jr. R.T., Edwards R.H., Storm-Mathisen J., and Chaudhry F.A. Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J. Comp. Neurol. 480 (2004) 264-280
51. Gillespie D.C., Kim G., and Kandler K. Inhibitory synapses in the developing auditory system are glutamatergic. Nat. Neurosci. 8 (2005) 332-338
52. Roehm P.C., and Hansen M.R. Strategies to preserve or regenerate spiral ganglion neurons. Curr. Opin. Otolaryngol. Head Neck Surg. 13 (2005) 294-300
53. Botstein D., and Risch N. Discovering genotypes underlying human phenotypes: Past successes for mendelian disease, future approaches for complex disease. Nat. Genet. 33 Suppl (2003) 228-237