Auditory transduction in the mouse

Pflugers Archiv European Journal of Physiology

Volumn 454, Issue 5, 2007, Pages 793-804

  Grant, Lisa ^a   Fuchs, Paul A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Hair cell mechanotransduction; Mouse mutants and transgenic models; Sensory hair cells

Indexed keywords

AUDITORY STIMULATION; CEREBROSPINAL FLUID; CHEMICAL STRUCTURE; COCHLEA; ENDOLYMPH; HAIR CELL; HEARING; HEARING ACUITY; MAMMAL; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PERILYMPH; PRIORITY JOURNAL; REVIEW; SEMICIRCULAR CANAL; SENSITIVITY ANALYSIS; TRANSGENIC MOUSE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; DISEASE MODELS, ANIMAL; HAIR CELLS; HEARING; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC;

EID: 34250858976     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-007-0253-z     Document Type: Review

References (94)

1. Adato A, Michel V, Kikkawa Y, Reiners J, Alagramam KN, Weil D, Yonekawa H, Wolfrum U, El-Amraoui A, Petit C (2005) Interactions in the network of Usher syndrome type 1 proteins. Hum Mol Genet 14:347-356
2. Ahmed ZM, Goodyear R, Riazuddin S, Lagziel A, Legan PK, Behra M, Burgess SM, Lilley KS, Wilcox ER, Riazuddin S, Griffith AJ, Frolenkov GI, Belyantseva IA, Richardson GP, Friedman TB (2006) The tip-link antigen, a protein associated with the transduction complex of sensory hair cells, is protocadherin-15. J Neurosci 26:7022-7034
3. Ahmed ZM, Riazuddin S, Bernstein SL, Ahmed Z, Khan S, Griffith AJ, Morell RJ, Friedman TB, Riazuddin S, Wilcox ER (2001) Mutations of the protocadherin gene PCDH15 cause Usher syndrome type 1F. Am J Hum Genet 69:25-34
4. Alagramam KN, Murcia CL, Kwon HY, Pawlowski KS, Wright CG, Woychik RP (2001) The mouse Ames waltzer hearing-loss mutant is caused by mutation of Pcdh15, a novel protocadherin gene. Nat Genet 27:99-102
5. Alagramam KN, Yuan H, Kuehn MH, Murcia CL, Wayne S, Srisailpathy CR, Lowry RB, Knaus R, Van Laer L, Bernier FP, Schwartz S, Lee C, Morton CC, Mullins RF, Ramesh A, Van Camp G, Hageman GS, Woychik RP, Smith RJ (2001) Mutations in the novel protocadherin PCDH15 cause Usher syndrome type 1F. Hum Mol Genet 10:1709-1718
6. Assad JA, Hacohen N, Corey DP (1989) Voltage dependence of adaptation and active bundle movement in bullfrog saccular hair cells. Proc Natl Acad Sci USA 86:2918-2922
7. Assad JA, Shepherd GM, Corey DP (1991) Tip-link integrity and mechanical transduction in vertebrate hair cells. Neuron 7:985-994
8. Belyantseva IA, Boger ET, Naz S, Frolenkov GI, Sellers JR, Ahmed ZM, Griffith AJ, Friedman TB (2005) Myosin-XVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia. Nat Cell Biol 7:148-156
9. Belyantseva IA, Labay V, Boger ET, Griffith AJ, Friedman TB (2003) Stereocilia: the long and the short of it. Trends Mol Med 9:458-461
10. Bermingham NA, Hassan BA, Price SD, Vollrath MA, Ben-Arie N, Eatock RA, Bellen HJ, Lysakowski A, Zoghbi HY (1999) Math1: an essential gene for the generation of inner ear hair cells. Science 284:1837-1841
11. Bitner-Glindzicz M, Lindley KJ, Rutland P, Blaydon D, Smith VV, Milla PJ, Hussain K, Furth-Lavi J, Cosgrove KE, Shepherd RM, Barnes PD, O'Brien RE, Farndon PA, Sowden J, Liu XZ, Scanlan MJ, Malcolm S, Dunne MJ, Aynsley-Green A, Glaser B (2000) A recessive contiguous gene deletion causing infantile hyperinsulinism, enteropathy and deafness identifies the Usher type 1C gene. Nat Genet 26:56-60
12. Boeda B, El-Amraoui A, Bahloul A, Goodyear R, Daviet L, Blanchard S, Perfettini I, Fath KR, Shorte S, Reiners J, Houdusse A, Legrain P, Wolfrum U, Richardson G, Petit C (2002) Myosin VIIa, harmonin and cadherin 23, three Usher I gene products that cooperate to shape the sensory hair cell bundle. EMBO J 21:6689-6699
13. Bolz H, von Brederlow B, Ramirez A, Bryda EC, Kutsche K, Nothwang HG, Seeliger M, del CSCM, Vila MC, Molina OP, Gal A, Kubisch C (2001) Mutation of CDH23, encoding a new member of the cadherin gene family, causes Usher syndrome type 1D. Nat Genet 27:108-112
14. Bork JM, Peters LM, Riazuddin S, Bernstein SL, Ahmed ZM, Ness SL, Polomeno R, Ramesh A, Schloss M, Srisailpathy CR, Wayne S, Bellman S, Desmukh D, Ahmed Z, Khan SN, Kaloustian VM, Li XC, Lalwani A, Riazuddin S, Bitner-Glindzicz M, Nance WE, Liu XZ, Wistow G, Smith RJ, Griffith AJ, Wilcox ER, Friedman TB, Morell RJ (2001) Usher syndrome 1D and nonsyndromic autosomal recessive deafness DFNB12 are caused by allelic mutations of the novel cadherin-like gene CDH23. Am J Hum Genet 68:26-37
15. Chow LM, Tian Y, Weber T, Corbett M, Zuo J, Baker SJ (2006) Inducible Cre recombinase activity in mouse cerebellar granule cell precursors and inner ear hair cells. Dev Dyn 235:2991-2998
16. Corey DP (2006) What is the hair cell transduction channel? J Physiol 576:23-28
17. Corey DP, Garcia-Anoveros J, Holt JR, Kwan KY, Lin SY, Vollrath MA, Amalfitano A, Cheung EL, Derfler BH, Duggan A, Geleoc GS, Gray PA, Hoffman MP, Rehm HL, Tamasauskas D, Zhang DS (2004) TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432:723-730
18. Corey D, Hudspeth A (1980) Mechanical stimulation and micromanipulation with piezoelectric bimorph elements. J Neurosci Methods 3:183-202
19. Corey DP, Hudspeth AJ (1983) Kinetics of the receptor current in bullfrog saccular hair cells. J Neurosci 3:962-976
20. Crawford AC, Evans MG, Fettiplace R (1989) Activation and adaptation of transducer currents in turtle hair cells. J Physiol 419:405-434
21. Crawford AC, Evans MG, Fettiplace R (1991) The actions of calcium on the mechano-electrical transducer current of turtle hair cells. J Physiol 434:369-398
22. Crawford AC, Fettiplace R (1985) The mechanical properties of ciliary bundles of turtle cochlear hair cells. J Physiol 364:359-379
23. Delprat B, Michel V, Goodyear R, Yamasaki Y, Michalski N, El-Amraoui A, Perfettini I, Legrain P, Richardson G, Hardelin JP, Petit C (2005) Myosin XVa and whirlin, two deafness gene products required for hair bundle growth, are located at the stereocilia tips and interact directly. Hum Mol Genet 14:401-410
24. Di Palma F, Belyantseva IA, Kim HJ, Vogt TF, Kachar B, Noben-Trauth K (2002) Mutations in Mcoln3 associated with deafness and pigmentation defects in varitint-waddler (Va) mice. Proc Natl Acad Sci USA 99:14994-14999
25. Di Palma F, Holme RH, Bryda EC, Belyantseva IA, Pellegrino R, Kachar B, Steel KP, Noben-Trauth K (2001) Mutations in Cdh23, encoding a new type of cadherin, cause stereocilia disorganization in waltzer, the mouse model for Usher syndrome type 1D. Nat Genet 27:103-107
26. Eatock RA, Corey DP, Hudspeth AJ (1987) Adaptation of mechanoelectrical transduction in hair cells of the bullfrog's sacculus. J Neurosci 7:2821-2836
27. Feil R, Brocard J, Mascrez B, LeMeur M, Metzger D, Chambon P (1996) Ligand-activated site-specific recombination in mice. Proc Natl Acad Sci USA 93:10887-10890
28. Friedman TB, Liang Y, Weber JL, Hinnant JT, Barber TD, Winata S, Arhya IN, Asher JH Jr (1995) A gene for congenital, recessive deafness DFNB3 maps to the pericentromeric region of chromosome 17. Nat Genet 9:86-91
29. Gao J, Wu X, Zuo J (2004) Targeting hearing genes in mice. Brain Res Mol Brain Res 132:192-207
30. Gibson F, Walsh J, Mburu P, Varela A, Brown KA, Antonio M, Beisel KW, Steel KP, Brown SD (1995) A type VII myosin encoded by the mouse deafness gene shaker-1. Nature 374:62-64
31. Gillespie PG, Wagner MC, Hudspeth AJ (1993) Identification of a 120 kd hair-bundle myosin located near stereociliary tips. Neuron 11:581-594
32. Goodyear R, Richardson G (1999) The ankle-link antigen: an epitope sensitive to calcium chelation associated with the hair-cell surface and the calycal processes of photoreceptors. J Neurosci 19:3761-3772
33. Hasson T, Gillespie PG, Garcia JA, MacDonald RB, Zhao Y, Yee AG, Mooseker MS, Corey DP (1997) Unconventional myosins in inner-ear sensory epithelia. J Cell Biol 137:1287-1307
34. Holt JR, Corey DP, Eatock RA (1997) Mechanoelectrical transduction and adaptation in hair cells of the mouse utricle, a low-frequency vestibular organ. J Neurosci 17:8739-8748
35. Holt JR, Gillespie SK, Provance DW, Shah K, Shokat KM, Corey DP, Mercer JA, Gillespie PG (2002) A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell 108:371-381
36. Howard J, Hudspeth AJ (1987) Mechanical relaxation of the hair bundle mediates adaptation in mechanoelectrical transduction by the bullfrog's saccular hair cell. Proc Natl Acad Sci USA 84:3064-3068
37. Howard J, Hudspeth AJ (1988) Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cell. Neuron 1:189-199
38. Hudspeth AJ, Corey DP (1977) Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. Proc Natl Acad Sci USA 74:2407-2411
39. Hung AY, Sheng M (2002) PDZ domains: structural modules for protein complex assembly. J Biol Chem 277:5699-5702
40. Johnson KR, Gagnon LH, Webb LS, Peters LL, Hawes NL, Chang B, Zheng QY (2003) Mouse models of USH1C and DFNB18: phenotypic and molecular analyses of two new spontaneous mutations of the Ush1c gene. Hum Mol Genet 12:3075-3086
41. Kachar B, Parakkal M, Kurc M, Zhao Y, Gillespie PG (2000) High-resolution structure of hair-cell tip links. Proc Natl Acad Sci USA 97:13336-13341
42. Kennedy HJ, Evans MG, Crawford AC, Fettiplace R (2003) Fast adaptation of mechanoelectrical transducer channels in mammalian cochlear hair cells. Nat Neurosci 6:832-836
43. Kikkawa Y, Shitara H, Wakana S, Kohara Y, Takada T, Okamoto M, Taya C, Kamiya K, Yoshikawa Y, Tokano H, Kitamura K, Shimizu K, Wakabayashi Y, Shiroishi T, Kominami R, Yonekawa H (2003) Mutations in a new scaffold protein Sans cause deafness in Jackson shaker mice. Hum Mol Genet 12:453-461
44. Kros CJ, Marcotti W, van Netten SM, Self TJ, Libby RT, Brown SD, Richardson GP, Steel KP (2002) Reduced climbing and increased slipping adaptation in cochlear hair cells of mice with Myo7a mutations. Nat Neurosci 5:41-47
45. Kros CJ, Rusch A, Richardson GP (1992) Mechano-electrical transducer currents in hair cells of the cultured neonatal mouse cochlea. Proc Biol Sci 249:185-193
46. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277-289
47. Lee G, Abdi K, Jiang Y, Michaely P, Bennett V, Marszalek PE (2006) Nanospring behaviour of ankyrin repeats. Nature 440:246-249
48. Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S (2000) Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103:525-535
49. Liu XZ, Walsh J, Mburu P, Kendrick-Jones J, Cope MJ, Steel KP, Brown SD (1997) Mutations in the myosin VIIA gene cause non-syndromic recessive deafness. Nat Genet 16:188-190
50. Lord EM, Gates WH (1929) Shaker, a new mutation of the house mouse (Mus musculus). Am Nat 63:435-442
51. Martin P, Bozovic D, Choe Y, Hudspeth AJ (2003) Spontaneous oscillation by hair bundles of the bullfrog's sacculus. J Neurosci 23:4533-4548
52. Mburu P, Kikkawa Y, Townsend S, Romero R, Yonekawa H, Brown SD (2006) Whirlin complexes with p55 at the stereocilia tip during hair cell development. Proc Natl Acad Sci USA 103:10973-10978
53. Mburu P, Liu XZ, Walsh J, Saw D Jr, Cope MJ, Gibson F, Kendrick-Jones J, Steel KP, Brown SD (1997) Mutation analysis of the mouse myosin VIIA deafness gene. Genes Funct 1:191-203
54. Mhatre AN, Li Y, Atkin G, Maghnouj A, Lalwani AK (2006) Expression of Myh9 in the mammalian cochlea: localization within the stereocilia. J Neurosci Res 84:809-818
55. Michel V, Goodyear RJ, Weil D, Marcotti W, Perfettini I, Wolfrum U, Kros CJ, Richardson GP, Petit C (2005) Cadherin 23 is a component of the transient lateral links in the developing hair bundles of cochlear sensory cells. Dev Biol 280:281-294
56. Moore DR (2006) Auditory processing disorder (APD)-potential contribution of mouse research. Brain Res 1091:200-206
57. Nagata K, Duggan A, Kumar G, Garcia-Anoveros J (2005) Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J Neurosci 25:4052-4061
58. Noben-Trauth K, Zheng QY, Johnson KR (2003) Association of cadherin 23 with polygenic inheritance and genetic modification of sensorineural hearing loss. Nat Genet 35:21-23
59. Ohlemiller KK (2006) Contributions of mouse models to understanding of age- and noise-related hearing loss. Brain Res 1091:89-102
60. Osborne MP, Comis SD (1990) Action of elastase, collagenase and other enzymes upon linkages between stereocilia in the guinea-pig cochlea. Acta Otolaryngol 110:37-45
61. Phillips KR, Tong S, Goodyear R, Richardson GP, Cyr JL (2006) Stereociliary myosin-1c receptors are sensitive to calcium chelation and absent from cadherin 23 mutant mice. J Neurosci 26:10777-10788
62. Pickles JO, Comis SD, Osborne MP (1984) Cross-links between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction. Hear Res 15:103-112
63. Reiners J, Marker T, Jurgens K, Reidel B, Wolfrum U (2005) Photoreceptor expression of the Usher syndrome type 1 protein protocadherin 15 (USH1F) and its interaction with the scaffold protein harmonin (USH1C). Mol Vis 11:347-355
64. Ricci AJ, Crawford AC, Fettiplace R (2000) Active hair bundle motion linked to fast transducer adaptation in auditory hair cells. J Neurosci 20:7131-7142
65. Rusch A, Hummler E (1999) Mechano-electrical transduction in mice lacking the alpha-subunit of the epithelial sodium channel. Hear Res 131:170-176
66. Senften M, Schwander M, Kazmierczak P, Lillo C, Shin JB, Hasson T, Geleoc GS, Gillespie PG, Williams D, Holt JR, Muller U (2006) Physical and functional interaction between protocadherin 15 and myosin VIIa in mechanosensory hair cells. J Neurosci 26:2060-2071
67. Sheng M, Sala C (2001) PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 24:1-29
68. Shotwell SL, Jacobs R, Hudspeth AJ (1981) Directional sensitivity of individual vertebrate hair cells to controlled deflection of their hair bundles. Ann N Y Acad Sci 374:1-10
69. Siemens J, Kazmierczak P, Reynolds A, Sticker M, Littlewood-Evans A, Muller U (2002) The Usher syndrome proteins cadherin 23 and harmonin form a complex by means of PDZ-domain interactions. Proc Natl Acad Sci USA 99:14946-14951
70. Siemens J, Lillo C, Dumont RA, Reynolds A, Williams DS, Gillespie PG, Muller U (2004) Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature 428:950-955
71. Sollner C, Rauch GJ, Siemens J, Geisler R, Schuster SC, Muller U, Nicolson T (2004) Mutations in cadherin 23 affect tip links in zebrafish sensory hair cells. Nature 428:955-959
72. Sotomayor M, Corey DP, Schulten K (2005) In search of the hair-cell gating spring elastic properties of ankyrin and cadherin repeats. Structure 13:669-682
73. Stauffer EA, Scarborough JD, Hirono M, Miller ED, Shah K, Mercer JA, Holt JR, Gillespie PG (2005) Fast adaptation in vestibular hair cells requires myosin-1c activity. Neuron 47:541-553
74. Stepanyan R, Belyantseva IA, Griffith AJ, Friedman TB, Frolenkov GI (2006) Auditory mechanotransduction in the absence of functional myosin-XVa. J Physiol 576:801-808
75. Strelioff D, Flock A (1984) Stiffness of sensory-cell hair bundles in the isolated guinea pig cochlea. Hear Res 15:19-28
76. Tabuchi K, Suzuki M, Mizuno A, Hara A (2005) Hearing impairment in TRPV4 knockout mice. Neurosci Lett 382:304-308
77. Tian Y, James S, Zuo J, Fritzsch B, Beisel KW (2006) Conditional and inducible gene recombineering in the mouse inner ear. Brain Res 1091:243-254
78. Utomo AR, Nikitin AY, Lee WH (1999) Temporal, spatial, and cell type-specific control of Cre-mediated DNA recombination in transgenic mice. Nat Biotechnol 17:1091-1096
79. Vernon M (1969) Usher's syndrome-deafness and progressive blindness. Clinical cases, prevention, theory and literature survey. J Chronic Dis 22:133-151
80. Verpy E, Leibovici M, Zwaenepoel I, Liu XZ, Gal A, Salem N, Mansour A, Blanchard S, Kobayashi I, Keats BJ, Slim R, Petit C (2000) A defect in harmonin, a PDZ domain-containing protein expressed in the inner ear sensory hair cells, underlies Usher syndrome type 1C. Nat Genet 26:51-55
81. Wada T, Wakabayashi Y, Takahashi S, Ushiki T, Kikkawa Y, Yonekawa H, Kominami R (2001) A point mutation in a cadherin gene, Cdh23, causes deafness in a novel mutant, Waltzer mouse niigata. Biochem Biophys Res Commun 283:113-117
82. Walker RG, Hudspeth AJ (1996) Calmodulin controls adaptation of mechanoelectrical transduction by hair cells of the bullfrog's sacculus. Proc Natl Acad Sci USA 93:2203-2207
83. Weil D, Blanchard S, Kaplan J, Guilford P, Gibson F, Walsh J, Mburu P, Varela A, Levilliers J, Weston MD et al (1995) Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature 374:60-61
84. Weil D, El-Amraoui A, Masmoudi S, Mustapha M, Kikkawa Y, Laine S, Delmaghani S, Adato A, Nadifi S, Zina ZB, Hamel C, Gal A, Ayadi H, Yonekawa H, Petit C (2003) Usher syndrome type I G (USH1G) is caused by mutations in the gene encoding SANS, a protein that associates with the USH1C protein, harmonin. Hum Mol Genet 12:463-471
85. Weil D, Kussel P, Blanchard S, Levy G, Levi-Acobas F, Drira M, Ayadi H, Petit C (1997) The autosomal recessive isolated deafness, DFNB2, and the Usher 1B syndrome are allelic defects of the myosin-VIIA gene. Nat Genet 16:191-193
86. Wilson SM, Householder DB, Coppola V, Tessarollo L, Fritzsch B, Lee EC, Goss D, Carlson GA, Copeland NG, Jenkins NA (2001) Mutations in Cdh23 cause nonsyndromic hearing loss in waltzer mice. Genomics 74:228-233
87. Woods C, Montcouquiol M, Kelley MW (2004) Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat Neurosci 7:1310-1318
88. Woolfson DN (2005) The design of coiled-coil structures and assemblies. Adv Protein Chem 70:79-112
89. Yajnik V, Paulding C, Sordella R, McClatchey AI, Saito M, Wahrer DC, Reynolds P, Bell DW, Lake R, van den Heuvel S, Settleman J, Haber DA (2003) DOCK4, a GTPase activator, is disrupted during tumorigenesis. Cell 112:673-684
90. Yan D, Li F, Hall ML, Sage C, Hu WH, Giallourakis C, Upadhyay G, Ouyang XM, Du LL, Bethea JR, Chen ZY, Yajnik V, Liu XZ (2006) An isoform of GTPase regulator DOCK4 localizes to the stereocilia in the inner ear and binds to harmonin (USH1C). J Mol Biol 357:755-764
91. Yap AS, Brieher WM, Gumbiner BM (1997) Molecular and functional analysis of cadherin-based adherens junctions. Annu Rev Cell Dev Biol 13:119-146
92. Yoneda M (1960) Force exerted by a single cilium of mytilus edulis. J Exp Biol 37:461-468
93. Zarrinpar A, Bhattacharyya RP, Lim WA (2003) The structure and function of proline recognition domains. Sci STKE 2003:RE8
94. Zhao Y, Yamoah EN, Gillespie PG (1996) Regeneration of broken tip links and restoration of mechanical transduction in hair cells. Proc Natl Acad Sci USA 93:15469-15474