Deletion of Shank1 has minimal effects on the molecular composition and function of glutamatergic afferent postsynapses in the mouse inner ear

Hearing Research

Volumn 321, Issue , 2015, Pages 52-64

  Braude, Jeremy P ^a   Vijayakumar, Sarath ^b   Baumgarner, Katherine ^a   Laurine, Rebecca ^a   Jones, Timothy A ^b   Jones, Sherri M ^b   Pyott, Sonja J ^a  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

ABR; AMPAR; CNS; CTBP2; DIC; GKAP; IHC; PSD; VsEPs

Indexed keywords

BRAIN PROTEIN; PROTEIN SHANK; UNCLASSIFIED DRUG; GLUTAMIC ACID; NERVE PROTEIN; SHANK1 PROTEIN, MOUSE; SHANK2 PROTEIN, MOUSE; SHANK3 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; BIOCHEMICAL COMPOSITION; COCHLEA; CONTROLLED STUDY; EVOKED AUDITORY RESPONSE; GENE; GENE DELETION; GENE EXPRESSION; GENE IDENTIFICATION; GENOTYPE; GLUTAMATERGIC AFFERENT POSTSYNAPSE; IMMUNOFLUORESCENCE; MORPHOLOGICAL TRAIT; MOUSE; NONHUMAN; POSTSYNAPTIC DENSITY; POSTSYNAPTIC POTENTIAL; REAL TIME POLYMERASE CHAIN REACTION; SHANK1 GENE; SHANK2 GENE; SHANK3 GENE; SYNAPTIC TRANSMISSION; 129 MOUSE; ANIMAL; AUDITORY NERVOUS SYSTEM; C57BL MOUSE; DEFICIENCY; EVOKED BRAIN STEM AUDITORY RESPONSE; GENETICS; HAIR CELL; INNER EAR; INNERVATION; KNOCKOUT MOUSE; METABOLISM; PHENOTYPE; TIME; VESTIBULAR EVOKED MYOGENIC POTENTIAL; VESTIBULE;

ANIMALS; AUDITORY PATHWAYS; COCHLEA; EAR, INNER; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; GENOTYPE; GLUTAMIC ACID; HAIR CELLS, AUDITORY, INNER; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PHENOTYPE; SYNAPTIC TRANSMISSION; TIME FACTORS; VESTIBULAR EVOKED MYOGENIC POTENTIALS; VESTIBULE, LABYRINTH;

EID: 84922356094     PISSN: 03785955     EISSN: 18785891     Source Type: Journal    
DOI: 10.1016/j.heares.2015.01.008     Document Type: Article

References (52)

1. Beurg M., Michalski N., Safieddine S., Bouleau Y., Schneggenburger R., Chapman E.R., Petit C., Dulon D. Control of exocytosis by synaptotagmins and otoferlin in auditory hair cells. J.Neurosci. 2010, 30:13281-13290.
2. Boeckers T.M., Winter C., Smalla K.H., Kreutz M.R., Bockmann J., Seidenbecher C., Garner C.C., Gundelfinger E.D. Proline-rich synapse-associated proteins ProSAP1 and ProSAP2 interact with synaptic proteins of the SAPAP/GKAP family. Biochem. Biophys. Res. Commun. 1999, 264:247-252.
3. Boeckers T.M., Segger-Junius M., Iglauer P., Bockmann J., Gundelfinger E.D., Kreutz M.R., Richter D., Kindler S., Kreienkamp H.J. Differential expression and dendritic transcript localization of Shank family members: identification of a dendritic targeting element in the 3' untranslated region of Shank1 mRNA. Mol. Cell. Neurosci. 2004, 26:182-190.
4. Burkard R., Feldman M., Voigt H.F. Brainstem auditory-evoked response in the rat. Normative studies, with observations concerning the effects of ossicular disruption. Audiology 1990, 29:146-162.
5. Chen Z., Kujawa S.G., Sewell W.F. Auditory sensitivity regulation via rapid changes in expression of surface AMPA receptors. Nat. Neurosci. 2007, 10:1238-1240.
6. Dalet A., Bonsacquet J., Gaboyard-Niay S., Calin-Jageman I., Chidavaenzi R.L., Venteo S., Desmadryl G., Goldberg J.M., Lysakowski A., Chabbert C. Glutamate transporters EAAT4 and EAAT5 are expressed in vestibular hair cells and calyx endings. PLoS One 2012, 7:e46261.
7. Davies C., Tingley D., Kachar B., Wenthold R.J., Petralia R.S. Distribution of members of the PSD-95 family of MAGUK proteins at the synaptic region of inner and outer hair cells of the guinea pig cochlea. Synapse 2001, 40:258-268.
8. Doleviczenyi Z., Halmos G., Repassy G., Vizi E.S., Zelles T., Lendvai B. Cochlear dopamine release is modulated by group II metabotropic glutamate receptors via GABAergic neurotransmission. Neurosci. Lett. 2005, 385:93-98.
9. Eatock R.A., Songer J.E. Vestibular hair cells and afferents: two channels for head motion signals. Annu. Rev. Neurosci. 2011, 34:501-534.
10. El Barbary A. Auditory nerve of the normal and jaundiced rat. I. Spontaneous discharge rate and cochlear nerve histology. Hear Res. 1991, 54:75-90.
11. Glowatzki E., Fuchs P.A. Transmitter release at the hair cell ribbon synapse. Nat. Neurosci. 2002, 5:147-154.
12. Huang L.C., Barclay M., Lee K., Peter S., Housley G.D., Thorne P.R., Montgomery J.M. Synaptic profiles during neurite extension, refinement and retraction in the developing cochlea. Neural Dev. 2012, 7:38.
13. Hung A.Y., Futai K., Sala C., Valtschanoff J.G., Ryu J., Woodworth M.A., Kidd F.L., Sung C.C., Miyakawa T., Bear M.F., Weinberg R.J., Sheng M. Smaller dendritic spines, weaker synaptic transmission, but enhanced spatial learning in mice lacking Shank1. J.Neurosci. 2008, 28:1697-1708.
14. Jones S.M., Erway L.C., Bergstrom R.A., Schimenti J.C., Jones T.A. Vestibular responses to linear acceleration are absent in otoconia-deficient C57BL/6JEi-het mice. Hear Res. 1999, 135:56-60.
15. Jones S.M., Erway L.C., Johnson K.R., Yu H., Jones T.A. Gravity receptor function in mice with graded otoconial deficiencies. Hear Res. 2004, 191:34-40.
16. Jones T.A., Jones S.M. Short latency compound action potentials from mammalian gravity receptor organs. Hear Res. 1999, 136:75-85.
17. Khimich D., Nouvian R., Pujol R., Tom Dieck S., Egner A., Gundelfinger E.D., Moser T. Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 2005, 434:889-894.
18. Kleinlogel S., Oestreicher E., Arnold T., Ehrenberger K., Felix D. Metabotropic glutamate receptors group I are involved in cochlear neurotransmission. Neuroreport 1999, 10:1879-1882.
19. Kuriyama H., Jenkins O., Altschuler R.A. Immunocytochemical localization of AMPA selective glutamate receptor subunits in the rat cochlea. Hear Res. 1994, 80:233-240.
20. Larionov A., Krause A., Miller W. Astandard curve based method for relative real time PCR data processing. BMC Bioinforma. 2005, 6:62.
21. Liberman L.D., Wang H., Liberman M.C. Opposing gradients of ribbon size and AMPA receptor expression underlie sensitivity differences among cochlear-nerve/hair-cell synapses. J.Neurosci. 2011, 31:801-808.
22. Liberman M.C. Single-neuron labeling in the cat auditory nerve. Science 1982, 216:1239-1241.
23. Luo L., Brumm D., Ryan A.F. Distribution of non-NMDA glutamate receptor mRNAs in the developing rat cochlea. J.Comp. Neurol. 1995, 361:372-382.
24. Maison S.F., Pyott S.J., Meredith A.L., Liberman M.C. Olivocochlear suppression of outer hair cells invivo: evidence for combined action of BK and SK2 channels throughout the cochlea. J.Neurophysiol. 2013, 109:1525-1534.
25. Matsubara A., Laake J.H., Davanger S.,miusami S., 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. 1996, 16:4457-4467.
26. McLean W.J., Smith K.A., Glowatzki E., Pyott S.J. Distribution of the Na,K-ATPase alpha subunit in the rat spiral ganglion and organ of corti. J.Assoc. Res. Otolaryngol. 2009, 10:37-49.
27. Meyer A.C., Frank T., Khimich D., Hoch G., Riedel D., Chapochnikov N.M., Yarin Y.M., Harke B., Hell S.W., Egner A., Moser T. Tuning of synapse number, structure and function in the cochlea. Nat. Neurosci. 2009, 12:444-453.
28. Mock B., Jones T.A., Jones S.M. Gravity receptor aging in the CBA/CaJ strain: a comparison to auditory aging. J.Assoc. Res. Otolaryngol. 2011, 12:173-183.
29. Mueller M., von Hunerbein K., Hoidis S., Smolders J.W. Aphysiological place-frequency map of the cochlea in the CBA/J mouse. Hear Res. 2005, 202:63-73.
30. Nouvian R., Beutner D., Parsons T.D., Moser T. Structure and function of the hair cell ribbon synapse. J.Membr. Biol. 2006, 209:153-165.
31. Peca J., Feliciano C., Ting J.T., Wang W., Wells M.F., Venkatraman T.N., Lascola C.D., Fu Z., Feng G. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 2011, 472:437-442.
32. Perry B., Jensen-Smith H.C., Luduena R.F., Hallworth R. Selective expression of beta tubulin isotypes in gerbil vestibular sensory epithelia and neurons. J.Assoc. Res. Otolaryngol. 2003, 4:329-338.
33. Pyott S.J., Glowatzki E., Trimmer J.S., Aldrich R.W. Extrasynaptic localization of inactivating calcium-activated potassium channels in mouse inner hair cells. J.Neurosci. 2004, 24:9469-9474.
34. Roux I., Safieddine S., Nouvian R., Grati M., Simmler M.C., Bahloul A., Perfettini I., Le Gall M., Rostaing P., Hamard G., Triller A., Avan P., Moser T., Petit C. Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 2006, 127:277-289.
35. Ruel J., Wang J., Rebillard G., Eybalin M., Lloyd R., Pujol R., Puel J.L. Physiology, pharmacology and plasticity at the inner hair cell synaptic complex. Hear Res. 2007, 227:19-27.
36. Safieddine S., El-Amraoui A., Petit C. The auditory hair cell ribbon synapse: from assembly to function. Annu. Rev. Neurosci. 2012, 35:509-528.
37. Sager C., Tapken D., Kott S., Hollmann M. Functional modulation of AMPA receptors by transmembrane AMPA receptor regulatory proteins. Neuroscience 2009, 158:45-54.
38. Sala C., Piech V., Wilson N.R., Passafaro M., Liu G., Sheng M. Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 2001, 31:115-130.
39. Schmeisser M.J., et al. Autistic-like behaviours and hyperactivity in mice lacking ProSAP1/Shank2. Nature 2012, 486:256.
40. Schuth O., McLean W.J., Eatock R.A., Pyott S.J. Distribution of Na,K-ATPase alpha subunits in rat vestibular sensory epithelia. J.Assoc. Res. Otolaryngol. 2014, 15:739-754.
41. Seal R.P., Akil O., Yi E., Weber C.M., Grant L., Yoo J., Clause A., Kandler K., Noebels J.L., Glowatzki E., Lustig L.R., Edwards R.H. Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3. Neuron 2008, 57:263-275.
42. Sheng M., Kim E. The Shank family of scaffold proteins. J.Cell. Sci. 2000, 113(Pt 11):1851-1856.
43. Sheng M., Hoogenraad C.C. The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu. Rev. Biochem. 2007, 76:823-847.
44. Silverman J.L., Turner S.M., Barkan C.L., Tolu S.S., Saxena R., Hung A.Y., Sheng M., Crawley J.N. Sociability and motor functions in Shank1 mutant mice. Brain Res. 2011, 1380:120-137.
45. Taberner A.M., Liberman M.C. Response properties of single auditory nerve fibers in the mouse. J.Neurophysiol. 2005, 93:557-569.
46. Truett G.E., Heeger P., Mynatt R.L., Truett A.A., Walker J.A., Warman M.L. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 2000, 29(52):54.
47. Tsuji J., Liberman M.C. Intracellular labeling of auditory nerve fibers in guinea pig: central and peripheral projections. J.Comp. Neurol. 1997, 381:188-202.
48. 2+ channels. J.Neurosci. 2014, 34:10853-10869.
49. Weisz C., Glowatzki E., Fuchs P. The postsynaptic function of type II cochlear afferents. Nature 2009, 461:1126-1129.
50. Wersinger E., McLean W.J., Fuchs P.A., Pyott S.J. BK channels mediate cholinergic inhibition of high frequency cochlear hair cells. PLoS One 2010, 5:e13836.
51. Zheng C.Y., Seabold G.K., Horak M., Petralia R.S. MAGUKs, synaptic development, and synaptic plasticity. Neuroscientist 2011, 17:493-512.
52. Zheng Q.Y., Johnson K.R., Erway L.C. Assessment of hearing in 80 inbred strains of mice by ABR threshold analyses. Hear Res. 1999, 130:94-107.