Altered phenotype of the vestibular organ in GLAST-1 null mice

JARO - Journal of the Association for Research in Otolaryngology

Volumn 13, Issue 3, 2012, Pages 323-333

  Schraven, Sebastian P ^a   Franz, Christoph ^a   Rüttiger, Lukas ^a   Löwenheim, Hubert ^b   Lysakowski, Anna ^c   Stoffel, Wilhelm ^d   Knipper, Marlies ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF ILLINOIS   (United States)

^d UNIVERSITY OF COLOGNE   (Germany)

Author keywords

GLAST 1; KCNQ4; Otoferlin; Supporting cells; Vestibular hair cells; VGLUT

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER 1; POTASSIUM CHANNEL KCNQ4; VESICULAR GLUTAMATE TRANSPORTER 3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCLING BEHAVIOR; HAIR CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NEUROFILAMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; VESTIBULAR FUNCTION; VESTIBULAR SYSTEM;

ANIMALS; EXCITATORY AMINO ACID TRANSPORTER 1; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; SENSORY RECEPTOR CELLS; VESTIBULE, LABYRINTH;

EID: 84865521646     PISSN: 15253961     EISSN: 14387573     Source Type: Journal    
DOI: 10.1007/s10162-011-0311-2     Document Type: Article

References (55)

1. ALTSCHULER RA, SHERIDAN CE, HORN JW, WENTHOLD RJ (1989) Immunocytochemical localization of glutamate immunoreactivity in the guinea pig cochlea. Hear Res 42:167-173
2. BONSACQUET J, BRUGEAUD A, COMPAN V, DESMADRYL G, CHABBERT C (2006) AMPA type glutamate receptormediates neurotransmission at turtle vestibular calyx synapse. J Physiol 576:63-71
3. BRINGMANN A, PANNICKE T, BIEDERMANN B, FRANCKE M, IANDIEV I, GROSCHE J, WIEDEMANN P, ALBRECHT J, REICHENBACH A (2009) Role of retinal glial cells in neurotransmitter uptake and metabolism. Neurochem Int 54:143-160
4. DANBOLT NC (2001) Glutamate uptake. Prog Neurobiol 65:1-105
5. DE LEENHEER EM, HUYGEN PL, COUCKE PJ, ADMIRAAL RJ, VAN CAMP G, CREMERS CW (2002) Longitudinal and cross-sectional phenotype analysis in a new, large Dutch DFNA2/KCNQ4 family. Ann Otol Rhinol Laryngol 111:267-274
6. DESAI SS, ZEH C, LYSAKOWSKI A (2005) Comparative morphology of rodent vestibular periphery. I. Saccular and utricular maculae. J Neurophysiol 93:251-266
7. DULON D, SAFIEDDINE S, JONES SM, PETIT C (2009) Otoferlin is critical for a highly sensitive and linear calcium-dependent exocytosis at vestibular hair cell ribbon synapses. J Neurosci 29:10474-10487
8. FURNESS DN, LAWTON DM (2003) Comparative distribution of glutamate transporters and receptors in relation to afferent innervation density in the mammalian cochlea. J Neurosci 23:11296-11304
9. FURNESS DN, LEHRE KP (1997) Immunocytochemical localization of a high-affinity glutamate-aspartate transporter, GLAST, in the rat and guinea-pig cochlea. Eur J Neurosci 9:1961-1969
10. HAKUBA N, KOGA K, GYO K, USAMI SI, TANAKA K (2000) Exacerbation of noise-induced hearing loss in mice lacking the glutamate transporter GLAST. J Neurosci 20:8750-8753
11. HARADA T, HARADA C, WATANABE M, INOUE Y, SAKAGAWA T, NAKAYAMA N, SASAKI S, OKUYAMA S, WATASE K, WADA K, TANAKA K (1998) Functions of the two glutamate transporters GLAST and GLT-1 in the retina. Proc Natl Acad Sci USA 95:4663-4666
12. HARADA T, HARADA C, NAKAMURA K, QUAH HM, OKUMURA A, NAMEKATA K, SAEKI T, AIHARA M, YOSHIDA H, MITANI A, TANAKA K (2007) The potential role of glutamate transporters in the pathogenesis of normal tension glaucoma. J Clin Invest 117:1763-1770
13. HARADA C, NAMEKATA K, GUO X, YOSHIDA H, MITAMURA Y, MATSUMOTO Y, TANAKA K, ICHIJO H, HARADA T (2010) ASK1 deficiency attenuates neural cell death in GLAST-deficient mice, a model of normal tension glaucoma. Cell Death Differ 17:1751-1759
14. HEIDRYCH P, ZIMMERMANN U, KUHN S, FRANZ C, ENGEL J, DUNCKER SV, HIRT B, PUSCH CM, RUTH P, PFISTER M, MARCOTTI W, BLIN N, KNIPPER M (2009) Otoferlin interacts with myosin VI: implications for maintenance of the basolateral synaptic structure of the inner hair cell. Hum Mol Genet 18:2779-2790
15. HURLEY KM, GABOYARD S, ZHONG M, PRICE SD, WOOLTORTON JR, LYSAKOWSKI A, EATOCK RA (2006) M-like K+currents in type I hair cells and calyx afferent endings of the developing rat utricle. J Neurosci 26:10253-10269
16. KARLSSON RM, TANAKA K, SAKSIDA LM, BUSSEY TJ, HEILIG M, HOLMES A (2009) Assessment of glutamate transporter GLAST (EAAT1)-deficient mice for phenotypes relevant to the negative and executive/cognitive symptoms of schizophrenia. Neuropsychopharmacology 34:1578-1589
17. KHARKOVETS T, HARDELIN JP, SAFIEDDINE S, SCHWEIZER M, EL-AMRAOUI A, PETIT C, JENTSCH TJ (2000) KCNQ4, a K+channel mutated in a form of dominant deafness, is expressed in the inner ear and the central auditory pathway. Proc Natl Acad Sci USA 97:4333-4338
18. KIM E, HYRC KL, SPECK J, LUNDBERG YW, SALLES FT, KACHAR B, GOLDBERG MP, WARCHOL ME, ORNITZ DM (2010) Regulation of cellular calcium in vestibular supporting cells by Otopetrin 1. J Neurophysiol 104:3439-3450
19. KLOCKNER U, STORCK T, CONRADT M, STOFFEL W (1993) Electrogenic L-glutamate uptake in Xenopus laevis oocytes expressing a cloned rat brain L-glutamate/L-aspartate transporter (GLAST-1). J Biol Chem268:14594-14596
20. KLOCKNER U, STORCK T, CONRADT M, STOFFEL W (1994) Functional properties and substrate specificity of the cloned L-glutamate/ L-aspartate transporter GLAST-1 from rat brain expressed in Xenopus oocytes. J Neurosci 14:5759-5765
21. KNIPPER M, ZINN C, MAIER H, PRAETORIUS M, ROHBOCK K, KOPSCHALL I, ZIMMERMANN U (2000) Thyroid hormone deficiency before the onset of hearing causes irreversible damage to peripheral and central auditory systems. J Neurophysiol 83:3101-3112
22. KOEBERLE PD, BAHR M (2008) The upregulation of GLAST-1 is an indirect antiapoptotic mechanism of GDNF and neurturin in the adult CNS. Cell Death Differ 15:471-483
23. KUBISCH C, SCHROEDER BC, FRIEDRICH T, LUTJOHANN B, EL-AMRAOUI A, MARLIN S, PETIT C, JENTSCH TJ (1999) KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness. Cell 96:437-446
24. KUJAWA SG, LIBERMANN MC (2009) Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci 29:14077-14085
25. LEHRE KP, DANBOLT NC (1998) The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J Neurosci 18:8751-8757
26. LYSAKOWSKI A (1999) Development of synaptic innervation in the rodent utricle. Ann N Y Acad Sci 871:422-425
27. LYSAKOWSKI A, GOLDBERG JM (1997) A regional ultrastructural analysis of the cellular and synaptic architecture in the chinchilla cristae ampullares. J Comp Neurol 389:419-443
28. LYSAKOWSKI A, GABOYARD-NIAY S, CALIN-JAGEMAN I, CHATLANI S, PRICE SD, EATOCK RA (2011) Molecular microdomains in a sensory terminal, the vestibular calyx ending. J Neurosci: Off J Soc Neurosci 31:10101-10114
29. MATSUBARA A, TAKUMI Y, NAKAGAWA T, USAMI S, SHINKAWA H, OTTERSEN OP (1999) Immunoelectron microscopy of AMPA receptor subunits reveals three types of putative glutamatergic synapse in the rat vestibular end organs. Brain Res 819:58-64
30. MATSUGAMI TR, TANEMURA K, MIEDA M, NAKATOMI R, YAMADA K, KONDO T, OGAWA M, OBATA K, WATANABE M, HASHIKAWA T, TANAKA K (2006) From the Cover: Indispensability of the glutamate transporters GLAST and GLT1 to brain development. Proc Natl Acad Sci USA 103:12161-12166
31. OLIVER D, KNIPPER M, DERST C, FAKLER B (2003) Resting potential and submembrane calcium concentration of inner hair cells in the isolated mouse cochlea are set by KCNQ-type potassium channels. J Neurosci 23:2141-2149
32. PARK CK, CHA J, PARK SC, LEE PY, KIM JH, KIM HS, KIM SA, KIM IB, CHUN MH (2009) Differential expression of two glutamate transporters, GLAST and GLT-1, in an experimental rat model of glaucoma. Exp Brain Res 197:101-109
33. PEGHINI P, JANZEN J, STOFFELW (1997) Glutamate transporter EAAC-1-deficient mice develop dicarboxylic aminoaciduria and behavioral abnormalities but no neurodegeneration. EMBO J 16:3822-3832
34. ROCHA-SANCHEZ SM, MORRIS KA, KACHAR B, NICHOLS D, FRITZSCH B, BEISEL KW (2007) Developmental expression of Kcnq4 in vestibular neurons and neurosensory epithelia. Brain Res 1139:117-125
35. ROTHSTEIN JD, MARTIN L, LEVEY AI, DYKES-HOBERG M, JIN L, WU D, NASH N, KUNCL RW (1994) Localization of neuronal and glial glutamate transporters. Neuron 13:713-725
36. ROTHSTEIN JD, DYKES-HOBERG M, PARDO CA, BRISTOL LA, JIN L, KUNCL RW, KANAI Y, HEDIGER MA, WANG Y, SCHIELKE JP, WELTY DF (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16:675-686
37. RUTTIGER L, SAUSBIER M, ZIMMERMANN U, WINTER H, BRAIG C, ENGEL J, KNIRSCH M, ARNTZ C, LANGER P, HIRT B, MULLER M, KOPSCHALL I, PFISTER M, MUNKNER S, ROHBOCK K, PFAFF I, RUSCH A, RUTH P, KNIPPER M (2004) Deletion of the Ca2+-activated potassium (BK) alpha-subunit but not the BKbeta1-subunit leads to progressive hearing loss. Proc Natl Acad Sci USA 101:12922-12927
38. SAFIEDDINE S, WENTHOLD RJ (1999) SNARE complex at the ribbon synapses of cochlear hair cells: analysis of synaptic vesicle-and synaptic membrane-associated proteins. Eur J Neurosci 11:803-812
39. SARTHY VP, PIGNATARO L, PANNICKE T, WEICK M, REICHENBACH A, HARADA T, TANAKA K, MARC R (2005) Glutamate transport by retinal Muller cells in glutamate/aspartate transporter-knockout mice. Glia 49:184-196
40. SCHUG N, BRAIG C, ZIMMERMANN U, ENGEL J, WINTER H, RUTH P, BLIN N, PFISTER M, KALBACHER H, KNIPPERM(2006)Differential expression of otoferlin in brain, vestibular system, immature and mature cochlea of the rat. Eur J Neurosci 24:3372-3380
41. SHIMIZU Y, HAKUBA N, HYODO J, TANIGUCHI M, GYO K (2005) Kanamycin ototoxicity in glutamate transporter knockout mice. Neurosci Lett 380:243-246
42. SOUSA AD, ANDRADE LR, SALLES FT, PILLAI AM, BUTTERMORE ED, BHAT MA, KACHAR B (2009) The septate junction protein caspr is required for structural support and retention of KCNQ4 at calyceal synapses of vestibular hair cells. J Neurosci 29:3103-3108
43. STOFFEL W, KORNER R, WACHTMANN D, KELLER BU (2004) Functional analysis of glutamate transporters in excitatory synaptic transmission of GLAST1 and GLAST1/EAAC1 deficient mice. Brain Res Mol Brain Res 128:170-181
44. STORCK T, SCHULTE S, HOFMANN K, STOFFEL W (1992) Structure, expression, and functional analysis of a Na(+)-dependent glutamate/aspartate transporter from rat brain. Proc Natl Acad Sci USA 89:10955-10959
45. TAKAMORI S, RHEE JS, ROSENMUND C, JAHN R (2000) Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407:189-194
46. TAKASAKI C, OKADA R, MITANI A, FUKAYA M, YAMASAKI M, FUJIHARA Y, SHIRAKAWA T, TANAKA K, WATANABE M (2008) Glutamate transporters regulate lesion-induced plasticity in the developing somatosensory cortex. J Neurosci 28:4995-5006
47. TAKUMI Y, MATSUBARA A, DANBOLT NC, LAAKE JH, STORM-MATHISEN J, USAMI S, SHINKAWA H, OTTERSEN OP (1997) Discrete cellular and subcellular localization of glutamine synthetase and the glutamate transporter GLAST in the rat vestibular end organ. Neuroscience 79:1137-1144
48. TSURU N, UEDA Y, DOI T (2002) Amygdaloid kindling in glutamate transporter (GLAST) knockout mice. Epilepsia 43:805-811
49. USAMI S, OTTERSEN OP (1995) Differential cellular distribution of glutamate and glutamine in the rat vestibular endorgans: an immunocytochemical study. Brain Res 676:285-292
50. USAMI S, OSEN KK, ZHANG N, OTTERSEN OP (1992) Distribution of glutamate-like and glutamine-like immunoreactivities in the rat organ of Corti: a light microscopic and semiquantitative electron microscopic analysis with a note on the localization of aspartate. Exp Brain Res 91:1-11
51. WAHLE S, STOFFEL W (1996) Membrane topology of the high-affinity L-glutamate transporter (GLAST-1) of the central nervous system. J Cell Biol 135:1867-1877
52. WATANABE T, MORIMOTO K, HIRAO T, SUWAKI H, WATASE K, TANAKA K (1999) Amygdala-kindled and pentylenetetrazole-induced seizures in glutamate transporter GLAST-deficient mice. Brain Res 845:92-96
53. WATASE K, HASHIMOTO K, KANO M, YAMADA K, WATANABE M, INOUE Y, OKUYAMA S, SAKAGAWA T, OGAWA S, KAWASHIMA N, HORI S, TAKIMOTO M, WADA K, TANAKA K (1998) Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice. Eur J Neurosci 10:976-988
54. WINTER H, BRAIG C, ZIMMERMANN U, GEISLER HS, FRANZER JT, WEBER T, LEY M, ENGEL J, KNIRSCH M, BAUER K, CHRIST S, WALSH EJ, MCGEE J, KOPSCHALL I, ROHBOCK K, KNIPPER M (2006) Thyroid hormone receptors TRalpha1 and TRbeta differentially regulate gene expression of Kcnq4 and prestin during final differentiation of outer hair cells. J Cell Sci 119:2975-2984
55. ZHANG FX, PANG YW, ZHANG MM, ZHANG T, DONG YL, LAI CH, SHUM DK, CHAN YS, LI JL, LI YQ (2010) Expression of vesicular glutamate transporters in peripheral vestibular structures and vestibular nuclear complex of rat. Neuroscience 173:179-189