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Auditory and vestibular hair cell stereocilia: relationship between functionality and inner ear disease

Published online by Cambridge University Press:  21 July 2011

R R Ciuman
R R Ciuman*
Affiliation:
Department of Otorhinolaryngology, Head and Neck Surgery, Marienhospital Gelsenkirchen, Germany
*
Address for correspondence: Dr Raphael R Ciuman, Uranusbogen 15, 45478 Mülheim, Germany E-mail: [email protected]
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Abstract

The stereocilia of the inner ear are unique cellular structures which correlate anatomically with distinct cochlear functions, including mechanoelectrical transduction, cochlear amplification, adaptation, frequency selectivity and tuning. Their function is impaired by inner ear stressors, by various types of hereditary deafness, syndromic hearing loss and inner ear disease (e.g. Ménière's disease). The anatomical and physiological characteristics of stereocilia are discussed in relation to inner ear malfunctions.

Keywords

CiliaBiochemistryCochleaPhysiologyPathologyUsher SyndromeHearing Loss
Type
Review Article
Information
The Journal of Laryngology & Otology , Volume 125 , Issue 10 , October 2011 , pp. 991 - 1003
Copyright
Copyright © JLO (1984) Limited 2011

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References

1http://www.neuroreille.com/promenade/english/corti/hcells/vue_sfce/v_sfce.htm; [Accessed 2 June 2011]Google Scholar
2Wright, A. Dimensions of the cochlear stereocilia in man and the guinea pig. Hear Res 1984;13:89–98CrossRefGoogle ScholarPubMed
3Rzadzinska, AK, Schneider, ME, Davies, C, Riordan, GP, Kachar, B. An actin molecular treadmill and myosins maintain stereocilia functional architecture and self-renewal. J Cell Biol 2004;164:887–97CrossRefGoogle ScholarPubMed
4Schneider, ME, Beyantseva, IA, Azevedo, RB, Kachar, B. Rapid renewal of auditory hair bundles. Nature 2002;418:837–8CrossRefGoogle ScholarPubMed
5Pack, AK, Slepecky, NB. Cytoskeletal and calcium-binding proteins in the mammalian organ of Corti: cell type-specific proteins displaying longitudinal and radial gradients. Hear Res 1995;91:119–35CrossRefGoogle ScholarPubMed
6DeRosier, DJ, Tilney, LG. The structure of the cuticular plate, an in vivo actin gel. J Cell Biol 1989;109:2853–67CrossRefGoogle Scholar
7Slepecky, N, Chamberlain, SC. Immunoelectron microscopic and immunofluorescent localization of cytoskeletal and muscle-like contractile proteins in inner ear sensory hair cells. Hear Res 1985;20:245–60CrossRefGoogle ScholarPubMed
8Hu, BH, Henderson, D. Changes in F-actin labelling in the outer hair cell and the Deiters cell in the chinchilla cochlea following noise exposure. Hear Res 1997;110:209–18CrossRefGoogle ScholarPubMed
9Lapeyre, P, Guilhaume, A, Cazals, Y. Differences in hair bundles associated with type I and type II hair cells of the guinea pig saccule. Acta Otolaryngol 1992;112:635–42CrossRefGoogle ScholarPubMed
10Morita, I, Komatsuzaki, A, Tatsuoka, H. The morphological differences of stereocilia and cuticular plates between type I and type II hair cells of human vestibular sensory epithelia. ORL J Otorhinolaryngol Relat Spec 1997;59:193–7CrossRefGoogle ScholarPubMed
11Rowe, MH, Peterson, EH. Quantitative analysis of stereociliary arrays on vestibular hair cells. Hear Res 2004;190:10–24CrossRefGoogle ScholarPubMed
12Bagger-Sjoback, D, Takumida, M. Geometrical array of the vestibular sensory hair bundle. Acta Otolaryngol 1988;106:393–403CrossRefGoogle ScholarPubMed
13Ernston, S, Smith, CA. Stereo-kinociliar bonds in mammalian vestibular organs. Acta Otolaryngol 1986;101:395–402CrossRefGoogle Scholar
14Ross, D, Komorowski, TE, Rogers, CM, Pote, KG, Donovan, KM. Macular suprastructure, stereociliary bonding and kinociliary/stereociliary coupling in rat utricular macula. Acta Otolaryngol 1987;104:56–65CrossRefGoogle ScholarPubMed
15Takumida, M. Functional morphology of the crista ampullaris: with special interests in sensory hairs and cupula: a review. Biol Sci Space 2001;15:356–8CrossRefGoogle ScholarPubMed
16Raphael, Y, Athey, BD, Wang, Y, Lee, MK, Altschuler, RA. F-actin, tubulin and spectrin in the organ of Corti: comparative distribution in different cell types and mammalian species. Hear Res 1994;76:173–87CrossRefGoogle ScholarPubMed
17Steyger, PS, Furness, DN, Hackney, CM, Richardson, GP. Tubulin and microtubules in cochlear hair cells: comparative immunocytochemistry and ultrastructure. Hear Res 1989;42:1–16CrossRefGoogle ScholarPubMed
18Sobkowicz, HM, Slapnick, SM, August, BK. The kinocilium of auditory hair cells and evidence for its morphogenetic role during the regeneration of stereocilia and cuticular plates. J Neurocytol 1995;24:633–53CrossRefGoogle ScholarPubMed
19Flock, A, Flock, B, Murray, E. Studies on the sensory hairs of receptor cells in the inner ear. Acta Otolaryngol 1977;83:85–91CrossRefGoogle ScholarPubMed
20Vater, M, Lenoir, M, Pujol, R. Development of the organ of Corti in horseshoe bats: scanning and transmission electron microscopy. J Comp Neurol 1997;377:520–343.0.CO;2-4>CrossRefGoogle ScholarPubMed
21Raphael, Y, Lenoir, R, Wroblewski, R, Pujol, R. The sensory epithelium and its innervation in the mole rat cochlea. J Comp Neurol 1991;314:367–82CrossRefGoogle ScholarPubMed
22Wright, A. Scanning electron microscopy of the human cochlea – the organ of Corti. Arch Otorhinolaryngol 1981;230:11–19CrossRefGoogle ScholarPubMed
23Lim, DJ. Cochlear anatomy related to cochlear micromechanics. A review. J Acoust Soc Am 1980;67:1686–95CrossRefGoogle ScholarPubMed
24Gu, ZP, Goodwen, J. Observation on Corti's organ of entire cochlea in the guinea pig by scanning electron microscopy. Chin Med J 1989;102:251–6Google ScholarPubMed
25Santi, PA, Anderson, CB. A newly identified surface coat on cochlear hair cells. Hear Res 1987;27:47–65CrossRefGoogle ScholarPubMed
26Valk, WL, Oei, ML, Segenhout, JM, Dijk, F, Stokroos, I, Albers, FW. The glycocalyx and stereociliary interconnections of the vestibular sensory epithelia of the guinea pig. A freeze-fracture, low-voltage cryo-SEM, SEM and TEM study. ORL J Otorhinolaryngol Relat Spec 2002;64:242–6CrossRefGoogle ScholarPubMed
27Takumida, M, Wersall, J, Bagger-Sjoback, D. Stereociliary glycocalyx and interconnections in the guinea pig vestibular organs. Acta Otolaryngol 1988;106:130–9CrossRefGoogle ScholarPubMed
28Takumida, M, Wersäll, J, Bagger-Sjöbäck, D, Harada, Y. Observation of the glycocalyx of the organ of Corti: an investigation by electron microscopy in the normal and gentamicin treated guinea pig. J Laryngol Otol 1989;103:133–6CrossRefGoogle ScholarPubMed
29Takumida, M, Harada, Y, Wersäll, J, Bagger-Sjöbäck, D. The glycocalyx of inner ear sensory and supporting cells. Acta Otolaryngol Suppl 1988;458:84–9CrossRefGoogle ScholarPubMed
30Prieto, JJ, Merchan, JA. Regional specialization of the cell coat in the hair cells of the organ of Corti. Hear Res 1987;31:223–7CrossRefGoogle ScholarPubMed
31Prieto, JJ, Merchan, JA. Tannic acid staining of the cell coat of the organ of Corti. Hear Res 1986;24:237–41CrossRefGoogle ScholarPubMed
32Gil-Loyzaga, P, Bueno, AM, Broto, JP, Pérez, AM. Effects of perinatal hypothyroidism in the carbohydrate composition of cochlear tectorial membrane. Hear Res 1990;45:151–5CrossRefGoogle ScholarPubMed
33Nayak, GN, Ratnayaka, HSK, Goodyear, RJ, Richardson, GP. Development of the hair bundle and mechanotransduction. Int J Dev Biol 2007;51:597–608CrossRefGoogle ScholarPubMed
34Goodyear, R, Richardson, G. Distribution of the 275 kD hair cell antigen and cell surface specialisations on auditory and vestibular hair bundles in the chicken inner ear. J Comp Neurol 1992;325:243–56CrossRefGoogle ScholarPubMed
35Goodyear, RJ, Richardson, GP. A novel antigen sensitive to calcium chelation that is associated with the tip links and kinocilial links of sensory hair bundles. J Neurosci 2003;23:4878–87CrossRefGoogle ScholarPubMed
36Goodyear, RJ, Legan, PK, Wright, MB, Marcotti, W, Oganesian, A, Coats, SA. A receptor-like inositol lipid phosphatase is required for the maturation of developing cochlear hair bundles. J Neurosci 2003;23:9208–19CrossRefGoogle ScholarPubMed
37Goodyear, RJ, Marcotti, W, Kros, CJ, Richardson, GP. Development and properties of stereociliary link types in hair cells of the mouse cochlea. J Comp Neurol 2005;485:75–85CrossRefGoogle ScholarPubMed
38Osborne, MP, Comis, SD. High resolution scanning electron microscopy of stereocilia in the cochlea of normal, postmortem, and drug-treated guinea pigs. J Electron Microsc Tech 1990;15:245–60CrossRefGoogle ScholarPubMed
39Ahmed, ZM, Goodyear, R, Riazuddin, S, Lagziel, A, Legan, PK, Behra, M et al. The tip-link, a protein associated with the transduction complex of sensory hair cells, is protocadherin-15. J Neurosci 2006;26:7022–34CrossRefGoogle ScholarPubMed
40Siemens, J, Lillo, C, Dumont, RA, Reynolds, A, Williams, DS, Gillespie, PG et al. Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature 2004;428:950–5CrossRefGoogle ScholarPubMed
41Watson, GM, Mire, P. A comparison of hair bundle mechanoreceptors in sea anemones and vertebrate systems. Curr Top Dev Biol 1999;43:51–84CrossRefGoogle ScholarPubMed
42Osborne, MP, Comis, SD. Action of elastase, collagenase and other enzymes upon linkages between stereocilia in the guinea-pig cochlea. Acta Otolaryngol 1990;110:37–45CrossRefGoogle ScholarPubMed
43Katori, Y, Hackney, CM, Furness, DN. Immunoreactivity of sensory hair bundles of the guinea-pig cochlea to antibodies against elastin and keratan sulphate. Cell Tissue Res 1996;284:473–9CrossRefGoogle ScholarPubMed
44Pickles, JO, Comis, SD, Osborne, MP. The effect of chronic application of kanamycin on stereocilia and their tip links in hair cells of the guinea pig cochlea. Hear Res 1987;28:237–44CrossRefGoogle Scholar
45Tsuprun, V, Schachern, PA, Cureoglu, S, Paparella, M. Structure of the stereocilia side links and morphology of auditory hair bundle in relation to noise in the chinchilla. J Neurocytol 2003;32:1117–28CrossRefGoogle ScholarPubMed
46Pickles, JO, Osborne, MP, Comis, SD. Vulnerability of tip links between stereocilia to acoustic trauma in the guinea pig. Hear Res 1987;25:173–83CrossRefGoogle ScholarPubMed
47Tsuprun, V, Santi, P. Structure of outer hair cell stereocilia side and attachment links in the chinchilla cochlea. J Histochem Cytochem 2002;50:493–502CrossRefGoogle ScholarPubMed
48Mermall, V, Post, PL, Mooseker, MS. Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 1998;279:527–33CrossRefGoogle ScholarPubMed
49Gillespie, PG, Cyr, JL. Myosin-1c, the hair cell's adaptation motor. Ann Rev Physiol 2004;66:521–45CrossRefGoogle ScholarPubMed
50Cyr, JL, Dumont, RA, Gillespie, PG. Myosin-1c interacts with hair-cell receptors through its calmodulin-binding IQ domains. J Neurosci 2002;22:2487–95CrossRefGoogle ScholarPubMed
51Gillespie, PG. Myosin I and adaptation of mechanical transduction by the inner ear. Philos Trans R Soc Lond B Biol Sci 2004;359:1945–51Google ScholarPubMed
52Metcalf, AB. Immunolocalization of myosin I beta in the hair cell's hair bundle. Cell Motil Cytoskeleton 1998;39:159–653.0.CO;2-1>CrossRefGoogle Scholar
53Self, T, Sobe, T, Copeland, NG, Jenkins, NA, Avraham, KB, Steel, KP. Role of myosin VI in the differentiation of cochlear hair cells. Dev Biol 1999;214:331–41CrossRefGoogle ScholarPubMed
54Brown, SD, Hardisty-Hughes, RE, Mburu, P. Quiet as a mouse: dissecting the molecular and genetic basis of hearing. Nat Rev Genet 2008;9:277–90CrossRefGoogle ScholarPubMed
55Kussel-Andermann, P, El-Amraoui, A, Safieddine, S, Nouaille, S, Perfettini, I, Lecuit, M et al. Vezatin, a novel transmembrane protein, bridges myosin VIIa to the cadherin-catenins complex. Embo J 2000;19:6020–9CrossRefGoogle Scholar
56Kros, CJ, Marcotti, W, Van, Netten, Self, TJ, Libby, RT, Brown, SD et al. Reduced climbing and increased slipping adaptation in cochlear hair cells of mice with Myo 7a mutations. Nat Neurosci 2002;5:3–4CrossRefGoogle Scholar
57Redowicz, JA. Myosins and pathology: genetics and biology. Acta Biochim Pol 2002;49:789–804CrossRefGoogle ScholarPubMed
58Salles, FT, Merritt, RC Jr, Manor, U, Dougherty, GW, Sousa, AD, Moore, JE et al. Myosin IIIa boosts elongation of stereocilia by transporting espin 1 to the plus ends of actin filaments. Nat Cell Biol 2009;11:443–50CrossRefGoogle Scholar
59Anderson, DW, Probst, FJ, Belyantseva, IA, Fridell, RA, Beyer, L, Martin, DM et al. The motor and tail regions of myosin XV are critical for normal structure and function of auditory and vestibular hair cells. Hum Mol Genet 2000;9:1729–38CrossRefGoogle ScholarPubMed
60Lin, HW, Schneider, ME, Kachar, B. When size matters: the dynamic regulation of stereocilia lengths. Curr Opin Cell Biol 2005;17:55–61CrossRefGoogle ScholarPubMed
61Belyantseva, IA, Boger, ET, Friedman, TB. Myosin XVa localizes to the tips of inner ear sensory cell stereocilia and is essential for staircase formation of the hair bundle. Proc Natl Acad Sci U S A 2003;100:13958–63CrossRefGoogle Scholar
62Belyantseva, IA, Boger, ET, Naz, S, Frolenkov, GI, Sellers, JR, Ahmed, ZM et al. Myosin-XVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia. Nat Cell Biol 2005;7:148–56CrossRefGoogle Scholar
63Siemens, J, Kazmierczak, P, Reynolds, A, Sticker, M, Littlewood-Evans, A, Muller, U. The Usher syndrome proteins cadherin 23 and harmonin form a complex by means of PDZ-domain interactions. Proc Natl Acad Sci U S A 2002;99:14946–51CrossRefGoogle Scholar
64Boeda, B, El-Amraoui, A, Bahloul, A, Goodyear, R, Daviet, L, Blanchard, S et al. Myosin VIIa, harmonin and cadherin 23, three Usher I gene products that cooperate to shape the sensory hair cell bundle. EMBO J 2002;21:6689–99CrossRefGoogle Scholar
65Weil, D, El-Amraoui, A, Masmoudi, S, Mustapha, M, Kikkawa, Y, Laine, S et al. Usher syndrome type IG (USHIG) is caused by mutations in the gene encoding SANS, a protein that associates with the USHIC protein harmonin. Hum Mol Genet 2003;12:463–71CrossRefGoogle Scholar
66Kikkawa, Y, Mburu, P, Morse, S, Kominami, R, Townsend, S, Brown, SD. Mutant analysis reveals whirlin as a dynamic organizer in the growing hair cell stereocilium. Hum Mol Genet 2005;14:391–400CrossRefGoogle ScholarPubMed
67Belyantseva, IA, Labay, Y, Boger, ET, Griffith, AJ, Friedman, TB. Stereocilia: the long and the short of it. Trends Mol Med 2003;9:458–61CrossRefGoogle Scholar
68Delprat, B, Michel, V, Goodyear, R, Yamasaki, Y, Michalski, N, El-Amraoui, A et al. Myosin XVa and whirlin, two deafness gene products required for hair bundle growth, are located at the stereocilia and interact directly. Hum Mol Genet 2005;14:401–10CrossRefGoogle ScholarPubMed
69Kitajiri, S, Fukumoto, K, Hata, M, Sasaki, H, Katsuno, T, Nakagawa, T et al. Radixin deficiency causes deafness associated with progressive degeneration of cochlear stereocilia. J Cell Biol 2004;166:559–70CrossRefGoogle ScholarPubMed
70Riazuddin, S, Khan, SN, Ahmed, ZM, Ghosh, M, Caution, K, Nazli, S et al. Mutations in TRIOBP, which encodes a putative cytoskeletal-organizing protein, are associated with nonsyndromic recessive deafness. Am J Hum Genet 2006;78:137–43CrossRefGoogle ScholarPubMed
71Shahin, H, Walsh, T, Sobe, T, AbuSaed, J, AbuRayan, A, Lynch, ED et al. Mutations in a novel isoform of TRIOBP that encodes a filamentous-actin binding protein are responsible for DFNB28 recessive nonsyndromic hearing loss. Am J Hum Genet 2006;78:144–52CrossRefGoogle Scholar
72Kitajiri, S, Sakamato, T, Belyantseva, IA, Goodyear, RJ, Stepanyan, R, Fujiwara, I et al. Actin-bundling protein TRIOBP forms resilient rootlets of hair cell stereocilia essential for hearing. Cell 2010;141:786–98CrossRefGoogle ScholarPubMed
73Hudspeth, AJ. How the ear's works work. Nature 1989;341:397–404CrossRefGoogle ScholarPubMed
74Beurg, M, Fettiplace, R, Nam, JH, Ricci, AJ. Localization of inner hair cell mechanotransducer channels using high speed calcium imaging. Nat Neurosci 2009;12:553–8CrossRefGoogle ScholarPubMed
75Lumpkin, EA, Hudspeth, AJ. Detection of Ca2+ entry through mechanosensitive channels localizes the site of mechanoelectrical transduction in hair cells. Proc Natl Acad Sci U S A 1995;92:10297–301CrossRefGoogle ScholarPubMed
76Geleoc, GS, Lennan, GW, Richardson, GP, Kros, CJ. A quantitative comparison of mechanoelectrical transduction in vestibular and auditory hair cells of neonatal mice. Proc Biol Sci 1997;261:611–21CrossRefGoogle Scholar
77Howard, J, Roberts, WM, Hudspeth, AJ. Mechanoelectrical transduction by hair cells. Annu Rev Biophys Chem 1988;17:99–124CrossRefGoogle ScholarPubMed
78Martin, P, Mehta, AD, Hudspeth, AJ. Negative hair-bundle stiffness betrays a mechanism for mechanical amplification by the hair cell. Proc Natl Acad Sci U S A 2000;97:12026–31CrossRefGoogle ScholarPubMed
79Ricci, AJ, Crawford, AC, Fettiplace, R. Mechanisms of active hair bundle motion in auditory hair cells. J Neurosci 2002;22:44–52CrossRefGoogle ScholarPubMed
80Kachar, B, Parakkal, M, Kurc, M, Zhao, Y, Gillepsie, PG. High-resolution structure of hair-cell tip links. Proc Natl Acad Sci U S A 2000;97:13336–41CrossRefGoogle ScholarPubMed
81Sotomayor, M, Corey, DP, Schulten, K. In search of the hair-cell gating spring elastic properties of ankyrin and cadherin repeats. Structure 2005;13:669–82CrossRefGoogle ScholarPubMed
82Fettiplace, R, Ricci, AJ, Hackney, CM. Clues to the cochlear amplifier from the turtle ear. Trends Neurosci 2001;24:169–75CrossRefGoogle Scholar
83Sotomayor, M, Weihofen, WA, Gaudet, R, Corey, DP. Structural determinants of cadherin-23 function in hearing and deafness. Neuron 2010;66:85–100CrossRefGoogle ScholarPubMed
84Brownell, WE, Bader, CR, Bertrand, D, deRibaupierre, Y. Evoked mechanical responses of isolated outer hair cells. Science 1985;227:641–54CrossRefGoogle Scholar
85Bekesy, G. Experiments in Hearing. New York: McGraw Hill, 1960Google Scholar
86Shatz, LF. The effect of hair bundle shape on hair bundle hydrodynamics of inner hair cells at low and high frequencies. Hear Res 2000;141:39–50CrossRefGoogle ScholarPubMed
87Ehret, G. Stiffness gradient along the basilar membrane as a basis for spatial frequency analysis within the cochlea. J Acoust Soc Am 1978;64:1723–6CrossRefGoogle ScholarPubMed
88Flock, A, Strelioff, D. Graded and nonlinear mechanical properties of sensory hairs in the mammalian hearing organ. Nature 1984;10:597–9CrossRefGoogle Scholar
89Robles, L, Ruggero, MA. Mechanics of the mammalian cochlea. Phys Rev 2001;81:1305–52Google ScholarPubMed
90Ruggero, MA, Rich, NC, Recio, A, Narayan, SS, Robles, L. Basilar-membrane responses to tones at the base of the chinchilla cochlea. J Acoust Soc Am 1997;101:2151–63CrossRefGoogle ScholarPubMed
91Cooper, NP, Rhode, WS. Mechanical responses to two-tone distortion products in the apical and basal turns of the mammalian cochlea. J Neurophysiol 1997;78:261–70CrossRefGoogle ScholarPubMed
92Johnstone, BM, Patuzzi, R, Yates, G. Basilar membrane measurements and the travelling wave. Hear Res 1986;22:147–54CrossRefGoogle ScholarPubMed
93Camalet, S, Duke, T, Julicher, F, Prost, J. Auditory sensitivity provided by self-tuned critical oscillations of hair cells. Proc Natl Acad Sci U S A 2000;97:3183–8CrossRefGoogle ScholarPubMed
94Ricci, AJ, Fettiplace, R. Calcium permeation of the turtle hair cell mechanotransducer channel and its relation to the composition of endolymph. J Physiol 1998;506:159–73CrossRefGoogle Scholar
95Vilfan, A, Duke, T. Two adaptation processes in auditory hair cells together can provide an active amplifier. Biophys J 2003;85:191–203CrossRefGoogle ScholarPubMed
96Chan, DK, Hudspeth, AJ. Ca2+ current-driven nonlinear amplification by the mammalian cochlea in vitro. Nat Neurosci 2005;8:149–55CrossRefGoogle ScholarPubMed
97Kennedy, HJ, Crawford, AC, Fettiplace, R. Force generation by mammalian hair bundles supports a role in cochlear amplification. Nature 2005;433:880–3CrossRefGoogle ScholarPubMed
98Fettiplace, R, Ricci, AJ. Adaptation in auditory hair cells. Curr Opin Neurobiol 2003;13:446–51CrossRefGoogle ScholarPubMed
99Martin, P, Hudspeth, AJ. Compressive nonlinearity in the hair bundle's active response to mechanical stimulation. Proc Natl Acad Sci U S A 2001;98:14386–91CrossRefGoogle ScholarPubMed
100Howard, J, Hudspeth, AJ. Compliance of the hair bundle associated with gating of mechanoelectrical transduction by the bullfrog's saccular hair cell. Proc Natl Acad Sci U S A 1987;84:3064–8CrossRefGoogle Scholar
101Eatock, RA. Adaptation in hair cells. Annu Rev Neurosci 2000;23:285–314CrossRefGoogle ScholarPubMed
102Wu, YC, Ricci, AJ, Fettiplace, R. Two components of transducer adaptation in auditory hair cells. J Neurophysiol 1999;82:2171–81CrossRefGoogle ScholarPubMed
103Assad, JA, Corey, DP. An active motor model for adaptation by vertebrate hair cells. J Neurosci 1992;12:3291–309CrossRefGoogle ScholarPubMed
104Gillespie, PG, Corey, DP. Myosin and adaptation by hair cells. Neuron 1997;19:955–8CrossRefGoogle ScholarPubMed
105Assad, JA, Hacohen, N, Corey, DP. Voltage dependence of adaptation and active bundle movement in bullfrog saccular hair cells. Proc Natl Acad Sci U S A 1989;86:2918–22CrossRefGoogle ScholarPubMed
106Eatock, RA, Corey, DP, Hudspeth, AJ. Adaptation of mechanoelectrical transduction in hair cells of the bullfrog's sacculus. J Neurosci 1987;7:2821–36CrossRefGoogle ScholarPubMed
107Kros, CJ, Lennan, GWT, Richardson, GP. Transducer currents and bundle movements in outer hair cells of neonatal mice. In: Flock, AO, Ulfendahl, M, eds. Active Hearing. Oxford: Elsevier, 1995;113–25Google Scholar
108Holt, JR, Gillespie, SK, Provance, DW, Shah, K, Shokat, KM, Corey, DP et al. A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell 2002;108:371–81CrossRefGoogle ScholarPubMed
109Holt, JR, Corey, DP, Eatock, RA. Mechanoelectrical transduction and adaptation in hair cells of the mouse utricle, a low-frequency vestibular organ. J Neurosci 1997;17:8739–48CrossRefGoogle ScholarPubMed
110Crawford, AC, Evans, MG, Fettiplace, R. Activation and adaptation of transducer currents in turtle hair cells. J Physiol 1989;419:405–34CrossRefGoogle ScholarPubMed
111Ricci, AJ, Wu, YC, Fettiplace, R. The endogenous calcium buffer and the time course of transducer adaptation in auditory hair cells. J Neurosci 1998;18:8261–77CrossRefGoogle ScholarPubMed
112Lumpkin, EA, Hudspeth, AJ. Regulation of free Ca2+ concentration in hair-cell stereocilia. J Neurosci 1998;18:6300–18CrossRefGoogle ScholarPubMed
113Slepecky, NB, Ulfendahl, M. Evidence for calcium-binding and calcium-dependent regulatory proteins in sensory cells of the organ of Corti. Hear Res 1993;70:73–84CrossRefGoogle ScholarPubMed
114Jurado, LA, Chockalingam, PS, Jarrett, HW. Apocalmodulin. Physiol Rev 1999;79:661–82CrossRefGoogle ScholarPubMed
115Caride, AJ, Filoteo, AG, Penheiter, AR, Paszty, K, Enyedi, A, Penniston, JT. Delayed activation of the plasma membrane calcium pump by a sudden increase in Ca2+: fast pumps reside in fast cells. Cell Calcium 2001;30:49–57CrossRefGoogle ScholarPubMed
116Wood, JD, Muchinsky, SJ, Filoteo, AG, Penniston, JT, Tempel, BL. Low endolymph calcium concentrations in deafwaddler2J mice suggest that PMCA2 contributes to endolymph calcium maintenance. Assoc Res Otolaryngol 2004;5:99–110Google ScholarPubMed
117Lopez, I, Ishiyama, G, Ishiyama, A, Jen, JC, Liu, F, Balow, RW. Differential subcellular immunolocalization of voltage-gated calcium channel alpha1 subunits in the chinchilla cristae ampullaris. Neuroscience 1999;92:773–82CrossRefGoogle ScholarPubMed
118Davis, RR, Kozel, P, Erway, LC. Genetic influences in individual susceptibility to noise: a review. Noise Health 2003;5:19–28Google ScholarPubMed
119Takumida, M, Fredelius, L, Bagger-Sjoback, D, Harada, Y, Wersall, J. Effect of acoustic overstimulation on the glycocalyx and the ciliary interconnections in the organ of Corti: high resolution scanning electron microscopic investigation. J Laryngol Otol 1989;103:1125–9CrossRefGoogle ScholarPubMed
120Clark, JA, Pickles, JO. The effects of moderate and low levels of acoustic overstimulation on stereocilia and their tip links in the guinea pig. Hear Res 1996;99:119–28CrossRefGoogle ScholarPubMed
121Nordmann, AS, Bohne, BA, Harding, GW. Histopathological differences between temporary and permanent threshold shift. Hear Res 2000;139:13–30CrossRefGoogle ScholarPubMed
122Gao, WY, Ding, DL, Zheng, XY, Ruan, FM, Liu, YJ. A comparison of changes in the stereocilia between temporary and permanent hearing losses in acoustic trauma. Hear Res 1992;62:27–41CrossRefGoogle ScholarPubMed
123Slepecky, N, Hamernik, R, Henderson, D, Coling, D. Correlation of audiometric data changes in cochlear hair cell stereocilia resulting from impulse noise trauma. Acta Otolaryngol 1982;93:329–40CrossRefGoogle ScholarPubMed
124Patuzzi, R. Non-linear aspects of outer hair cell transduction and the temporary threshold shifts after acoustic trauma. Audiol Neurootol 2002;7:17–20CrossRefGoogle ScholarPubMed
125Canlon, B. The effect of acoustic trauma on the tectorial membrane, stereocilia, and hearing sensitivity: possible mechanisms underlying damage, recovery, and protection. Scand Audiol Suppl 1988;27:1–45Google ScholarPubMed
126Saunders, JC, Canlon, B, Flock, A. Growth of threshold shift in hair-cell stereocilia following overstimulation. Hear Res 1986;23:245–55CrossRefGoogle ScholarPubMed
127Wang, JC, Raybould, NP, Luo, L, Ryan, AF, Cannell, MB, Thorne, PR et al. Noise induces up-regulation of P2X2 receptor subunit of ATP-gated ion channels in the rat cochlea. Neuroreport 2003;14:817–23CrossRefGoogle ScholarPubMed
128Housley, GD, Kanjhan, R, Raybould, NP, Greenwood, D, Salih, SG, Järlebark, L et al. Expression of the P2X2 receptor subunit of the ATP-gated ion channel in the cochlea: implications for sound transduction and auditory neurotransmission. J Neurosci 1999;19:8377–8388CrossRefGoogle ScholarPubMed
129Takumida, M, Urquiza, R, Bagger-Sjoback, D, Wersall, J. Effect of gentamicin on the carbohydrates of the vestibular end organs: an investigation by the use of FITC-lectins. J Laryngol Otol 1989;103:357–62CrossRefGoogle ScholarPubMed
130Takumida, M, Bagger-Sjoback, D, Wersall, J, Harada, Y. The effect of gentamicin on the glycocalyx and the ciliary interconnections in vestibular sensory cells: a high resolution scanning electron microscopic investigation. Hear Res 1989;37:163–70CrossRefGoogle Scholar
131Richardson, GP, Forge, A, Kros, CJ, Fleming, J, Brown, SD, Steel, KP. Myosin VIIa is required for aminoglycoside accumulation in cochlear hair cells. J Neurosci 1997;17:9506–19CrossRefGoogle ScholarPubMed
132Rydmarker, S, Horner, KC. Atrophy of outer hair cell stereocilia and hearing loss in hydropic cochleae. Hear Res 1991;53:113–22CrossRefGoogle ScholarPubMed
133Ruding, PR, Veldman, JE, Berendsen, W, Huizing, EH. Scanning electron microscopy of hair cells, stereocilia and cross-linkage in experimentally induced endolymphatic hydrops. Eur Arch Otorhinolaryngol 1991;248:313–18CrossRefGoogle ScholarPubMed
134Van Benthem, PP, De Groot, JC, Albers, FW, Veldman, JE, Huizing, EH. Structure and composition of stereocilia cross-links in normal and hydropic cochleas of the guinea pig. Eur Arch Otorhinolaryngol 1993;250:73–7CrossRefGoogle ScholarPubMed
135Van Benthem, PP, Albers, FW, De Groot, , Veldman, JE, Huizing, EH. Glycocalyx heterogeneity in normal and hydropic cochleas of the guinea pig. Acta Otolaryngol 1992;112:976–84CrossRefGoogle ScholarPubMed
136Schwaber, MK. Medical evaluation of tinnitus. Otolaryngol Clin North Am 2003;36:287–92CrossRefGoogle ScholarPubMed
137Zhou, Y, Zhai, S, Yang, W. The protective effects of ciliary neurotrophic factor on inner ear damage induced by intensive impulse noise [in Chinese]. Zhonghua Er Bi Yan Hou Ke Za Zhi 1999;34:150–3Google ScholarPubMed
138Kang, S, He, C, Shi, X. Protective effect of ciliary neurotrophic factor against the ototoxicity of gentamicin in guinea pigs [in Chinese]. Zhuongua Ying Yong Sheng Li Xue Za Zhi 1997;13:124–7Google ScholarPubMed
139Zine, A, De Ribaupierre, F. Tissue-specific levels and cellular distribution of epidermal growth factor receptors within control and neomycin-damaged neonatal rat organ of Corti. J Neurobiol 1999;38:313–223.0.CO;2-O>CrossRefGoogle ScholarPubMed
140Kimberling, WJ, Moller, C. Clinical and molecular genetics of Usher syndrome. J Am Acad Audiol 1995;6:63–72Google ScholarPubMed
141Bougham, JA, Vernon, M, Shaver, KA. Usher syndrome: definition and estimate of prevalence from two high risk populations. J Chron Dis 1983;36:595–603Google Scholar
142Vernon, M. Usher syndrome-deafness and progressive blindness. Clinical cases, prevention, theory and literature survey. J Chron Dis 1969;22:133–51CrossRefGoogle ScholarPubMed
143Otterstede, CR, Spandau, U, Blankenagel, A, Kimberling, WJ, Reisser, C. A new clinical classification for Usher's syndrome based on a new subtype of Usher's syndrome type 1. Laryngoscope 2001;111:84–6CrossRefGoogle Scholar
144Auffarth, GU, Tetz, MR, Krastel, H, Blanckenagel, A, Volcker, HE. Complicated cataracts in various forms of retinitis pigmentosa. Type and incidence [in German]. Ophthalmologe 1997;94:642–6CrossRefGoogle ScholarPubMed
145Loundon, N, Marlin, S, Busquet, D, Denoyelle, F, Roger, G, Renaud, F et al. Usher syndrome and cochlear implantation. Otol Neurotol 2003;24:216–21CrossRefGoogle ScholarPubMed
146Smith, RJH, Berlin, CI, Hejtmack, JF, Keats, BJ, Kimberling, WJ, Lewis, RA et al. Clinical diagnosis of the Usher syndromes. Usher syndrome consortium. Am J Med Genet 1994;50:32–8CrossRefGoogle ScholarPubMed
147Moller, CG, Kimberling, WJ, Davenport, SL, Priluck, I, White, V, Biscone-Halterman, K et al. Usher syndrome: an otoneurologic study. Laryngoscope 1989;99:73–9CrossRefGoogle ScholarPubMed
148Adato, A, Michel, V, Kikkawa, Y, Reiners, J, Alagramam, KN, Weil, D et al. Interactions in the network of Usher syndrome type 1 proteins. Hum Mol Genet 2005;14:347–56CrossRefGoogle Scholar
149Keats, BJ, Corey, DP. The usher syndromes. Am J Med Genet 1999;89:158–663.0.CO;2-#>CrossRefGoogle ScholarPubMed
150Bolz, H, Bolz, SS, Schade, G, Kothe, C, Mohrmann, G, Hess, M et al. Impaired calmodulin binding of myosin-7A causes autosomal dominant hearing loss (DFNA11). Hum Mutat 2004;24:274–5CrossRefGoogle ScholarPubMed
151Wilson, SM, Householder, DB, Coppola, V, Tessarollo, L, Fritzsch, B, Lee, EC et al. Mutations in Cdh23 cause nonsyndromic hearing loss in waltzer mice. Genomics 2001;74:228–33CrossRefGoogle ScholarPubMed
152Bolz, H, Von Brederlow, B, Ramirez, A, Bryda, EC, Kutsche, K, Nothwang, HG et al. Mutation of VDH23, encoding a new member of the cadherin gene family, causes Usher syndrome type 1D. Nat Genetics 2001;27:108–12CrossRefGoogle ScholarPubMed
153Ahmed, ZM, Riazuddin, S, Ahmad, J, Bernstein, SL, Guo, Y, Sabar, MF et al. PCDH15 is expressed in the neurosensory epithelium of the eye and ear mutant alleles are responsible for both USH1F and DFNB23. Hum Mol Genet 2003;12:3215–23CrossRefGoogle ScholarPubMed
154Liang, Y, Wang, A, Belyantseva, IA, Anderson, DW, Probst, FJ, Barber, TD et al. Characterization of the human and mouse unconventional myosin XV genes responsible for hereditary deafness DFNB3 and shaker 2. Genomics 1999;61:243–58CrossRefGoogle ScholarPubMed
155Zhu, M, Yang, T, Wei, S, DeWan, AT, Morell, RJ, Elfenbein, JL et al. Mutations in the gamma-actin gene (ACTG1) are associated with dominant progressive deafness (DFNA20/26). Am J Hum Genet 2003;73:1082–91CrossRefGoogle ScholarPubMed
156Jovine, L, Park, J, Wassarman, PM. Sequence similarity between stereocilin and otoancorin points to a unified mechanism for mechanotransduction in the mammalian inner ear. BMC Cell Biol 2002;3:28. doi: 10.1186/1471-2121-3-28CrossRefGoogle ScholarPubMed
157Verpy, E, Masmoudi, S, Zwaenepoel, I, Leibovici, M, Hutchin, TP, Del Castillo, I et al. Mutations in a new gene encoding a protein of the hair bundle cause non-syndromic deafness at the DFNB16 locus. Nat Genet 2001;29:345–9CrossRefGoogle Scholar
158Zwaenepoel, I, Mustapha, M, Leibovici, M, Verpy, E, Goodyear, R, Liu, XZ et al. Otoancorin, an inner ear protein restricted to the interface between the apical surface of sensory epithelia and their overlying acellular gels, is defective in autosomal recessive deafness DFNB22. Proc Natl Acad Sci U S A 2002;99:6240–5CrossRefGoogle Scholar
159Bearer, EL, Chen, AF, Chen, AH, Li, Z, Mark, HF, Smith, RJ et al. 2E4/kaptin (KPTN) – a candidate gene for the hearing loss locus, DFNA4. Ann Hum Genet 2000;64:189–96CrossRefGoogle ScholarPubMed
160Bearer, EL, Abraham, MT. 2E4 (kaptin): a novel actin-associated protein from human blood platelets found in lamellipodia and the tips of the stereocilia of the inner ear. Eur J Cell Biol 1999;78:117–26CrossRefGoogle ScholarPubMed
161Loomis, PA, Zheng, L, Sekerkova, G, Changyaleket, B, Mugnaini, E, Bartles, JR. Espin cross-links cause the elongation of microvillus-type parallel actin bundles in vivo. J Cell Biol 2003;163:1045–55CrossRefGoogle ScholarPubMed
162Donaudy, F, Zheng, L, Ficarcella, R, Ballana, E, Carella, M, Melchionda, S et al. Espin gene (ESPN) mutations associated with autosomal dominant hearing loss cause defects in microvillar elongation or organization. J Med Genet 2006;43:157–61CrossRefGoogle ScholarPubMed
163Naz, S, Griffith, AJ, Riazuddin, S, Hampton, LL, Battey, JF Jr, Khan, SN et al. Mutations of ESPN cause autosomal recessive deafness and vestibular dysfunction. J Med Genet 2004;41:591–5CrossRefGoogle ScholarPubMed