Advantages of a mouse model for human hearing impairment

Experimental Animals

Volumn 61, Issue 2, 2012, Pages 85-98

  Kikkawa, Yoshiaki ^a   Seki, Yuta ^a   Okumura, Kazuhiro ^b   Ohshiba, Yasuhiro ^a,c   Miyasaka, Yuki ^a,c   Suzuki, Sari ^a,d   Ozaki, Mao ^a,d   Matsuoka, Kunie ^a   Noguchi, Yoshihiro ^e   Yonekawa, Hiromichi ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b CHIBA CANCER CENTER   (Japan)

^c NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^d TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^e TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Hearing impairment; Inner ear hair cell; Model mouse; Stereocilia

Indexed keywords

MYOSIN; MYOSIN VI; PROTEIN TYROSINE PHOSPHATASE RECEPTOR Q; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; USHER SYNDROME 1 PROTEIN; USHER SYNDROME 2 PROTEIN;

CELL ADHESION; CELL FUNCTION; DISEASE MODEL; EXPERIMENTAL MOUSE; FUNCTIONAL MORPHOLOGY; GENETIC ASSOCIATION; HAIR CELL; HEARING IMPAIRMENT; HUMAN; MEMBRANE STRUCTURE; NONHUMAN; REVIEW; STEREOCILIUM;

ANIMALS; DISEASE MODELS, ANIMAL; HAIR CELLS, AUDITORY; HEARING; HEARING LOSS; HUMANS; MICE; MICE, KNOCKOUT; SPECIES SPECIFICITY; STEREOCILIA;

MAMMALIA;

EID: 84861470123     PISSN: 13411357     EISSN: None     Source Type: Journal    
DOI: 10.1538/expanim.61.85     Document Type: Review

References (117)

1. Adato, A., Lefèvre, G., Delprat, B., Michel, V., Michalski, N., Chardenoux, S., Weil, D., El-Amraoui, A., and Petit, C. 2005. Usherin, the defective protein in Usher syndrome type IIA, is likely to be a component of interstereocilia ankle links in the inner ear sensory cells. Hum. Mol. Genet. 14: 3921-3932. [Medline] [CrossRef]
2. Adato, A., Michel, V., Kikkawa, Y., Reiners, J., Alagramam, K.N., Weil, D., Yonekawa, H., Wolfrum, U., El-Amraoui, A., and Petit, C. 2005. Interactions in the network of Usher syndrome type 1 proteins. Hum. Mol. Genet. 14: 347-356. [Medline] [CrossRef]
3. Ahmed, Z.M., Morell, R.J., Riazuddin, S., Gropman, A., Shaukat, S., Ahmad, M.M., Mohiddin, S.A., Fananapazir, L., Caruso, R.C., Husnain, T., Khan, S.N., Riazuddin, S., Griffith, A.J., Friedman, T.B., and Wilcox, E.R. 2003. Mutations of MYO6 are associated with recessive deafness, DFNB37. Am. J. Hum. Genet. 72: 1315-1322. [Medline] [CrossRef]
4. Ahmed, Z.M., Riazuddin, S., Bernstein, S.L., Ahmed, Z., Khan, S., Griffith, A.J., Morell, R.J., Friedman, T.B., Riazuddin, S., and Wilcox, E.R. 2001. Mutations of the protocadherin gene PCDH15 cause Usher syndrome type 1F. Am. J. Hum. Genet. 69: 25-34. [Medline] [CrossRef]
5. Alagramam, K.N., Murcia, C.L., Kwon, H.Y., Pawlowski, K.S., Wright, C.G., and Woychik, R.P. 2001. The mouse Ames waltzer hearing-loss mutant is caused by mutation of Pcdh15, a novel protocadherin gene. Nat. Genet. 27: 99-102. [Medline] [CrossRef]
6. Anagnostopoulos, A.V. 2002. A compendium of mouse knockouts with inner ear defects. Trends Genet. 18: S21-S38. [Medline] [CrossRef]
7. Assad, J.A., Shepherd, G.M., and Corey, D.P. 1991. Tiplink integrity and mechanical transduction in vertebrate hair cells. Neuron 7: 985-994. [Medline] [CrossRef]
8. Avraham, K.B., Hasson, T., Steel, K.P., Kingsley, D.M., Russell, L.B., Mooseker, M.S., Copeland, N.G., and Jenkins, N.A. 1995. The mouse Snell's waltzer deafness gene encodes an unconventional myosin required for structural integrity of inner ear hair cells. Nat. Genet. 11: 369-375. [Medline] [CrossRef]
9. Belyantseva, I.A., Boger, E.T., Naz, S., Frolenkov, G.I., Sellers, J.R., Ahmed, Z.M., Griffith, A.J., and Friedman, T.B. 2005. Myosin-XVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia. Nat. Cell Biol. 7: 148-156. [Medline] [CrossRef]
10. Bitner-Glindzicz, M., Lindley, K.J., Rutland, P., Blaydon, D., Smith, V.V., Milla, P.J., Hussain, K., Furth-Lavi, J., Cosgrove, K.E., Shepherd, R.M., Barnes, P.D., O'Brien, R.E., Farndon, P.A., Sowden, J., Liu, X.Z., Scanlan, M.J., Malcolm, S., Dunne, M.J., Aynsley-Green, A., and 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. [Medline] [CrossRef]
11. Boëda, B., El-Amraoui, A., Bahloul, A., Goodyear, R., Daviet, L., Blanchard, S., Perfettini, I., Fath, K.R., Shorte, S., Reiners, J., Houdusse, A., Legrain, P., Wolfrum, U., Richardson, G., and 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. [Medline] [CrossRef]
12. Bolz, H., von Brederlow, B., Ramírez, A., Bryda, E.C., Kutsche, K., Nothwang, H.G., Seeliger, M., del C-Salcedó Cabrera, M., Vila, M.C., Molina, O.P., Gal, A., and 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. [Medline] [CrossRef]
13. Brown, S.D., Hancock, J.M., and Gates, H. 2006. Understanding mammalian genetic systems: the challenge of phenotyping in the mouse. PLoS Genet. 2: e118. [Medline] [CrossRef]
14. Brown, S.D., Hardisty-Hughes, R.E., and Mburu, P. 2008. Quiet as a mouse: dissecting the molecular and genetic basis of hearing. Nat. Rev. Genet. 9: 277-290. [Medline] [Cross- Ref]
15. Casimiro, M.C., Knollmann, B.C., Ebert, S.N., Vary, J.C. Jr., Greene, A.E., Franz, M.R., Grinberg, A., Huang, S.P., and Pfeifer, K. 2001. Targeted disruption of the Kcnq1 gene produces a mouse model of Jervell and Lange-Nielsen Syndrome. Proc. Natl. Acad. Sci. U.S.A. 98: 2526-2531. [Medline] [CrossRef]
16. Charizopoulou, N., Lelli, A., Schraders, M., Ray, K., Hildebrand, M.S., Ramesh, A., Srisailapathy, C.R., Oostrik, J., Admiraal, R.J., Neely, H.R., Latoche, J.R., Smith, R.J., Northup, J.K., Kremer, H., Holt, J.R., and Noben-Trauth, K. 2011. Gipc3 mutations associated with audiogenic seizures and sensorineural hearing loss in mouse and human. Nat. Commun. 2: 201. [Medline] [CrossRef]
17. Coghill, E.L., Hugill, A., Parkinson, N., Davison, C., Glenister, P., Clements, S., Hunter, J., Cox, R.D., and Brown, S.D. 2002. A gene-driven approach to the identification of ENU mutants in the mouse. Nat. Genet. 30: 255-256. [Medline] [CrossRef]
18. Cohen-Salmon, M., Ott, T., Michel, V., Hardelin, J.P., Perfettini, I., Eybalin, M., Wu, T., Marcus, D.C., Wangemann, P., Willecke, K., and Petit, C. 2002. Targeted ablation of connexin26 in the inner ear epithelial gap junction network causes hearing impairment and cell death. Curr. Biol. 12: 1106-1111. [Medline] [CrossRef]
19. Delprat, B., Michel, V., Goodyear, R., Yamasaki, Y., Michalski, N., El-Amraoui, A., Perfettini, I., Legrain, P., Richardson, G., Hardelin, J.P., and 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. [Medline] [CrossRef]
20. Di Palma, F., Holme, R.H., Bryda, E.C., Belyantseva, I.A., Pellegrino, R., Kachar, B., Steel, K.P., and 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. [Medline] [CrossRef]
21. Drayton, M. and Noben-Trauth, K. 2006. Mapping quantitative trait loci for hearing loss in Black Swiss mice. Hear. Res. 212: 128-139. [Medline] [CrossRef]
22. Ernstson, S. and Smith, C.A. 1986. Stereo-kinociliar bonds in mammalian vestibular organs. Acta Otolaryngol. 101: 395-402. [Medline] [CrossRef]
23. Erway, L.C., Willott, J.F., Archer, J.R., and Harrison, D.E. 1993. Genetics of age-related hearing loss in mice: I. Inbred and F1 hybrid strains. Hear. Res. 65: 125-132. [Medline] [CrossRef]
24. Everett, L.A., Belyantseva, I.A., Noben-Trauth, K., Cantos, R., Chen, A., Thakkar, S.I., Hoogstraten-Miller, S.L., Kachar, B., Wu, D.K., and Green, E.D. 2001. Targeted disruption of mouse Pds provides insight about the inner-ear defects encountered in Pendred syndrome. Hum. Mol. Genet. 10: 153-161. [Medline] [CrossRef]
25. Fortnum, H.M., Summerfield, A.Q., Marshall, D.H., Davis, A.C., and Bamford, J.M. 2001. Prevalence of permanent childhood hearing impairment in the United Kingdom and implications for universal neonatal hearing screening: questionnaire based ascertainment study. BMJ 323: 536-540. [Medline] [CrossRef]
26. Friedman, L.M., Dror, A.A., and Avraham, K.B. 2007. Mouse models to study inner ear development and hereditary hearing loss. Int. J. Dev. Biol. 51: 609-631. [Medline] [CrossRef]
27. Gibson, F., Walsh, J., Mburu, P., Varela, A., Brown, K.A., Antonio, M., Beisel, K.W., Steel, K.P., and Brown, S.D. 1995. A type VII myosin encoded by the mouse deafness gene shaker-1. Nature 374: 62-64. [Medline] [CrossRef]
28. Gillespie, P.G. and Müller, U. 2009. Mechanotransduction by hair cells: models, molecules, and mechanisms. Cell 139: 33-44. [Medline] [CrossRef]
29. Gondo, Y., Fukumura, R., Murata, T., and Makino, S. 2010. ENU-based gene-driven mutagenesis in the mouse: a nextgeneration gene-targeting system. Exp. Anim. 59: 537-548. [Medline] [CrossRef]
30. Goodyear, R.J., Legan, P.K., Wright, M.B., Marcotti, W., Oganesian, A., Coats, S.A., Booth, C.J., Kros, C.J., Seifert, R.A., Bowen-Pope, D.F., and Richardson, G.P. 2003. A receptor-like inositol lipid phosphatase is required for the maturation of developing cochlear hair bundles. J. Neurosci. 23: 9208-9219. [Medline]
31. Goodyear, R.J., Marcotti, W., Kros, C.J., and Richardson, G.P. 2005. Development and properties of stereociliary link types in hair cells of the mouse cochlea. J. Comp. Neurol. 485: 75-85. [Medline] [CrossRef]
32. Goodyear, R.J. and Richardson, G.P. 2003. A novel antigen sensitive to calcium chelation that is associated with the tip links and kinocilial links of sensory hair bundles. J. Neurosci. 23: 4878-4887. [Medline]
33. Gorlin, R.J., Toriello, H.V., and Cohen, M.M. 1995. Hereditary Hearing Loss and Its Syndromes, Oxford University Press, New York, Oxford.
34. Grati, M. and Kachar, B. 2011. Myosin VIIa and sans localization at stereocilia upper tip-link density implicates these Usher syndrome proteins in mechanotransduction. Proc. Natl. Acad. Sci. U.S.A. 108: 11476-11481. [Medline] [CrossRef]
35. Hardisty-Hughes, R.E., Tateossian, H., Morse, S.A., Romero, M.R., Middleton, A., Tymowska-Lalanne, Z., Hunter, A.J., Cheeseman, M., and Brown, S.D. 2006. A mutation in the F-box gene, Fbxo11, causes otitis media in the Jeff mouse. Hum. Mol. Genet. 15: 3273-3279. [Medline] [CrossRef]
36. Hasson, T., Gillespie, P.G., Garcia, J.A., MacDonald, R.B., Zhao, Y., Yee, A.G., Mooseker, M.S., and Corey, D.P. 1997. Unconventional myosins in inner-ear sensory epithelia. J. Cell Biol. 137: 1287-1307. [Medline] [CrossRef]
37. Hasson, T., Heintzelman, M.B., Santos-Sacchi, J., Corey, D.P., and Mooseker, M.S. 1995. Expression in cochlea and retina of myosin VIIa, the gene product defective in Usher syndrome type 1B. Proc. Natl. Acad. Sci. U.S.A. 92: 9815-9819. [Medline] [CrossRef]
38. Hasson, T. and Mooseker, M.S. 1994. Porcine myosin-VI: characterization of a new mammalian unconventional myosin. J. Cell Biol. 127: 425-440. [Medline] [CrossRef]
39. Henry, K.R. and Chole, R.A. 1980. Genotypic differences in behavioral, physiological and anatomical expressions of age-related hearing loss in the laboratory mouse. Audiology 19: 369-383. [Medline] [CrossRef]
40. Hertzano, R., Shalit, E., Rzadzinska, A.K., Dror, A.A., Song, L., Ron, U., Tan, J.T., Shitrit, A.S., Fuchs, H., Hasson, T., Ben-Tal, N., Sweeney, H.L., de Angelis, M.H., Steel, K.P., and Avraham, K.B. 2008. A Myo6 mutation destroys coordination between the myosin heads, revealing new functions of myosin VI in the stereocilia of mammalian inner ear hair cells. PLoS Genet. 4: e1000207. [Medline] [CrossRef]
41. Holley, M.C. 2005. Keynote review: the auditory system, hearing loss and potential targets for drug development. Drug Discov. Today 10: 1269-1282. [Medline] [CrossRef]
42. Hrabé de Angelis, M.H., Flaswinkel, H., Fuchs, H., Rathkolb, B., Soewarto, D., Marschall, S., Heffner, S., Pargent, W., Wuensch, K., Jung, M., Reis, A., Richter, T., Alessandrini, F., Jakob, T., Fuchs, E., Kolb, H., Kremmer, E., Schaeble, K., Rollinski, B., Roscher, A., Peters, C., Meitinger, T., Strom, T., Steckler, T., Holsboer, F., Klopstock, T., Gekeler, F., Schindewolf, C., Jung, T., Avraham, K., Behrendt, H., Ring, J., Zimmer, A., Schughart, K., Pfeffer, K., Wolf, E., and Balling, R. 2000. Genome-wide, large-scale production of mutant mice by ENU mutagenesis. Nat. Genet. 25: 444-447. [Medline] [CrossRef]
43. International Mouse Knockout Consortium, Collins, F.S., Rossant, J., and Wurst, W. 2007. A mouse for all reasons. Cell 128: 9-13. [Medline] [CrossRef]
44. Johnson, K.R., Erway, L.C., Cook, S.A., Willott, J.F., and Zheng, Q.Y. 1997. A major gene affecting age-related hearing loss in C57BL/6J mice. Hear. Res. 114: 83-92. [Medline] [CrossRef]
45. Johnson, K.R., Gagnon, L.H., Longo-Guess, C., and Kane, K.L. 2011. Association of a citrate synthase missense mutation with age-related hearing loss in A/J mice. Neurobiol. Aging (Epub ahead of print). [Medline] [CrossRef]
46. Johnson, K.R., Gagnon, L.H., Webb, L.S., Peters, L.L., Hawes, N.L., Chang, B., and Zheng, Q.Y. 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. [Medline] [CrossRef]
47. Johnson, K.R., Longo-Guess, C., Gagnon, L.H., Yu, H., and Zheng, Q.Y. 2008. A locus on distal chromosome 11 (ahl8) and its interaction with Cdh23ahl underlie the early onset, age-related hearing loss of DBA/2J mice. Genomics 92: 219-225. [Medline] [CrossRef]
48. Johnson, K.R. and Zheng, Q.Y. 2002. Ahl2, a second locus affecting age-related hearing loss in mice. Genomics 80: 461-464. [Medline] [CrossRef]
49. Jones, S.M., Jones, T.A., Johnson, K.R., Yu, H., Erway, L.C., and Zheng, Q.Y. 2006. A comparison of vestibular and auditory phenotypes in inbred mouse strains. Brain Res. 1091: 40-46. [Medline] [CrossRef]
50. Justice, M.J., Noveroske, J.K., Weber, J.S., Zheng, B., and Bradley, A. 1999. Mouse ENU mutagenesis. Hum. Mol. Genet. 8: 1955-1963. [Medline] [CrossRef]
51. Kazmierczak, P., Sakaguchi, H., Tokita, J., Wilson-Kubalek, E.M., Milligan, R.A., Müller, U., and Kachar, B. 2007. Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells. Nature 449: 87-91. [Medline] [CrossRef]
52. Keller, J.M., Neely, H., Latoche, R. Jr., and Noben-Trauth, K. 2011. High-frequency sensorineural hearing loss and its underlying genetics (Hfhl1 and Hfhl2) in NIH Swiss mice. J. Assoc. Res. Otolaryngol. 12: 617-631. [Medline] [Cross- Ref]
53. Kikkawa, Y., Mburu, P., Morse, S., Kominami, R., Townsend, S., and Brown, S.D. 2005. Mutant analysis reveals whirlin as a dynamic organizer in the growing hair cell stereocilium. Hum. Mol. Genet. 14: 391-400. [Medline] [CrossRef]
54. 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., and Yonekawa, H. 2003. Mutations in a new scaffold protein Sans cause deafness in Jackson shaker mice. Hum. Mol. Genet. 12: 453-461. [Medline] [CrossRef]
55. Kudo, T., Kure, S., Ikeda, K., Xia, A.P., Katori, Y., Suzuki, M., Kojima, K., Ichinohe, A., Suzuki, Y., Aoki, Y., Kobayashi, T., and Matsubara, Y. 2003. Transgenic expression of a dominant-negative connexin26 causes degeneration of the organ of Corti and non-syndromic deafness. Hum. Mol. Genet. 12: 995-1004. [Medline] [CrossRef]
56. Lagziel, A., Ahmed, Z.M., Schultz, J.M., Morell, R.J., Belyantseva, I.A., and Friedman, T.B. 2005. Spatiotemporal pattern and isoforms of cadherin 23 in wild type and waltzer mice during inner ear hair cell development. Dev. Biol. 280: 295-306. [Medline] [CrossRef]
57. Latoche, J.R., Neely, H.R., and Noben-Trauth, K. 2011. Polygenic inheritance of sensorineural hearing loss (Snhl2, -3, and -4) and organ of Corti patterning defect in the ALR/ LtJ mouse strain. Hear. Res. 275: 150-159. [Medline] [CrossRef]
58. Lee, M.P., Ravenel, J.D., Hu, R.J., Lustig, L.R., Tomaselli, G., Berger, R.D., Brandenburg, S.A., Litzi, T.J., Bunton, T.E., Limb, C., Francis, H., Gorelikow, M., Gu, H., Washington, K., Argani, P., Goldenring, J.R., Coffey, R.J., and Feinberg, A.P. 2000. Targeted disruption of the Kvlqt1 gene causes deafness and gastric hyperplasia in mice. J. Clin. Invest. 106: 1447-1455. [Medline] [CrossRef]
59. Lefèvre, G., Michel, V., Weil, D., Lepelletier, L., Bizard, E., Wolfrum, U., Hardelin, J.P., and Petit, C. 2008. A core cochlear phenotype in USH1 mouse mutants implicates fibrous links of the hair bundle in its cohesion, orientation and differential growth. Development 135: 1427-1437. [Medline] [CrossRef]
60. Legan, P.K., Lukashkina, V.A., Goodyear, R.J., Kössi, M., Russell, I.J., and Richardson, G.P. 2000. A targeted deletion in alpha-tectorin reveals that the tectorial membrane is required for the gain and timing of cochlear feedback. Neuron 28: 273-285. [Medline] [CrossRef]
61. Legan, P.K., Lukashkina, V.A., Goodyear, R.J., Lukashkin, A.N., Verhoeven, K., Van Camp, G., Russell, I.J., and Richardson, G.P. 2005. A deafness mutation isolates a second role for the tectorial membrane in hearing. Nat. Neurosci. 8: 1035-1042. [Medline] [CrossRef]
62. Lewis, M.A., Quint, E., Glazier, A.M., Fuchs, H., De Angelis, M.H., Langford, C., van Dongen, S., Abreu-Goodger, C., Piipari, M., Redshaw, N., Dalmay, T., Moreno-Pelayo, M.A., Enright, A.J., and Steel, K.P. 2009. An ENU-induced mutation of miR-96 associated with progressive hearing loss in mice. Nat. Genet. 41: 614-618. [Medline] [CrossRef]
63. Liberman, M.C., Gao, J., He, D.Z., Wu, X., Jia, S., and Zuo, J. 2002. Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419: 300-304. [Medline] [CrossRef]
64. Liu, X., Bulgakov, O.V., Darrow, K.N., Pawlyk, B., Adamian, M., Liberman, M.C., and Li, T. 2007. Usherin is required for maintenance of retinal photoreceptors and normal development of cochlear hair cells. Proc. Natl. Acad. Sci. U.S.A. 104: 4413-4418. [Medline] [CrossRef]
65. Manor, U., Disanza, A., Grati, M., Andrade, L., Lin, H., Di Fiore, P.P., Scita, G., and Kachar, B. 2011. Regulation of stereocilia length by myosin XVa and whirlin depends on the actin-regulatory protein Eps8. Curr. Biol. 21: 167-172. [Medline] [CrossRef]
66. Mashimo, T., Erven, A.E., Spiden, S.L., Guénet, J.L., and Steel, K.P. 2006. Two quantitative trait loci affecting progressive hearing loss in 101/H mice. Mamm. Genome 17: 841-850. [Medline] [CrossRef]
67. Masuya, H., Nakai, Y., Motegi, H., Niinaya, N., Kida, Y., Kaneko, Y., Aritake, H., Suzuki, N., Ishii, J., Koorikawa, K., Suzuki, T., Inoue, M., Kobayashi, K., Toki, H., Wada, Y., Kaneda, H., Ishijima, J., Takahashi, K.R., Minowa, O., Noda, T., Wakana, S., Gondo, Y., and Shiroishi, T. 2004. Development and implementation of a database system to manage a large-scale mouse ENU-mutagenesis program. Mamm. Genome 15: 404-411. [Medline] [CrossRef]
68. Mburu, P., Kikkawa, Y., Townsend, S., Romero, R., Yonekawa, H., and Brown, S.D. 2006. Whirlin complexes with p55 at the stereocilia tip during hair cell development. Proc. Natl. Acad. Sci. U.S.A. 103: 10973-10978. [Medline] [CrossRef]
69. Mburu, P., Mustapha, M., Varela, A., Weil, D., El-Amraoui, A., Holme, R.H., Rump, A., Hardisty, R.E., Blanchard, S., Coimbra, R.S., Perfettini, I., Parkinson, N., Mallon, A.M., Glenister, P., Rogers, M.J., Paige, A.J., Moir, L., Clay, J., Rosenthal, A., Liu, X.Z., Blanco, G., Steel, K.P., Petit, C., and Brown, S.D. 2003. Defects in whirlin, a PDZ domain molecule involved in stereocilia elongation, cause deafness in the whirler mouse and families with DFNB31. Nat. Genet. 34: 421-428. [Medline] [CrossRef]
70. Mburu, P., Romero, M.R., Hilton, H., Parker, A., Townsend, S., Kikkawa, Y., and Brown, S.D. 2010. Gelsolin plays a role in the actin polymerization complex of hair cell stereocilia. PLoS ONE 5: e11627. [Medline] [CrossRef]
71. McGee, J., Goodyear, R.J., McMillan, D.R., Stauffer, E.A., Holt, J.R., Locke, K.G., Birch, D.G., Legan, P.K., White, P.C., Walsh, E.J., and Richardson, G.P. 2006. The very large G-protein-coupled receptor VLGR1: a component of the ankle link complex required for the normal development of auditory hair bundles. J. Neurosci. 26: 6543-6553. [Medline] [CrossRef]
72. McGuirt, W.T., Prasad, S.D., Griffith, A.J., Kunst, H.P., Green, G.E., Shpargel, K.B., Runge, C., Huybrechts, C., Mueller, R.F., Lynch, E., King, M.C., Brunner, H.G., Cremers, C.W., Takanosu, M., Li, S.W., Arita, M., Mayne, R., Prockop, D.J., Van Camp, G., and Smith, R.J. 1999. Mutations in COL11A2 cause non-syndromic hearing loss (DFNA13). Nat. Genet. 23: 413-419. [Medline] [CrossRef]
73. Melchionda, S., Ahituv, N., Bisceglia, L., Sobe, T., Glaser, F., Rabionet, R., Arbones, M.L., Notarangelo, A., Di Iorio, E., Carella, M., Zelante, L., Estivill, X., Avraham, K.B., and Gasparini, P. 2001. MYO6, the human homologue of the gene responsible for deafness in Snell's waltzer mice, is mutated in autosomal dominant nonsyndromic hearing loss. Am. J. Hum. Genet. 69: 635-640. [Medline] [CrossRef]
74. Michalski, N., Michel, V., Bahloul, A., Lefèvre, G., Barral, J., Yagi, H., Chardenoux, S., Weil, D., Martin, P., Hardelin, J.P., Sato, M., and Petit, C. 2007. Molecular characterization of the ankle-link complex in cochlear hair cells and its role in the hair bundle functioning. J. Neurosci. 27: 6478-6488. [Medline] [CrossRef]
75. Michel, V., Goodyear, R.J., Weil, D., Marcotti, W., Perfettini, I., Wolfrum, U., Kros, C.J., Richardson, G.P., and 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. [Medline] [CrossRef]
76. Mikaelian, D.O. 1979. Development and degeneration of hearing in the C57/b16 mouse: relation of electrophysiologic responses from the round window and cochlear nucleus to cochlear anatomy and behavioral responses. Laryngoscope 89: 1-15. [Medline]
77. Mochizuki, E., Okumura, K., Ishikawa, M., Yoshimoto, S., Yamaguchi, J., Seki, Y., Wada, K., Yokohama, M., Ushiki, T., Tokano, H., Ishii, R., Shitara, H., Taya, C., Kitamura, K., Yonekawa, H., and Kikkawa, Y. 2010. Phenotypic and expres sion analysis of a novel spontaneous myosin VI null mutant mouse. Exp. Anim. 59: 57-71. [Medline] [CrossRef]
78. Morton, N.E. 1991. Genetic epidemiology of hearing loss Ann. N.Y. Acad. Sci. 630: 16-31. [CrossRef]
79. Nayak, G.D., Ratnayaka, H.S., Goodyear, R.J., and Richardson, G.P. 2007. Development of the hair bundle and mechanotransduction. Int. J. Dev. Biol. 51: 597-608. [Medline] [CrossRef]
80. Nemoto, M., Morita, Y., Mishima, Y., Takahashi, S., Nomura, T., Ushiki, T., Shiroishi, T., Kikkawa, Y., Yonekawa, H., and Kominami, R. 2004. Ahl3, a third locus on mouse chromosome 17 affecting age-related hearing loss. Biochem. Biophys. Res. Commun. 324: 1283-1288. [Medline] [Cross- Ref]
81. Noben-Trauth, K. and Johnson, K.R. 2009. Inheritance patterns of progressive hearing loss in laboratory strains of mice. Brain Res. 1277: 42-51. [Medline] [CrossRef]
82. Noben-Trauth, K., Latoche, J.R., Neely, H.R., and Bennett, B. 2010. Phenotype and genetics of progressive sensorineural hearing loss (Snhl1) in the LXS set of recombinant inbred strains of mice. PLoS ONE 5: e11459. [Medline] [CrossRef]
83. Noben-Trauth, K., Zheng, Q.Y., and Johnson, K.R. 2003. Association of cadherin 23 with polygenic inheritance and genetic modification of sensorineural hearing loss. Nat. Genet. 35: 21-23. [Medline] [CrossRef]
84. Nolan, P.M., Peters, J., Strivens, M., Rogers, D., Hagan, J., Spurr, N., Gray, I.C., Vizor, L., Brooker, D., Whitehill, E., Washbourne, R., Hough, T., Greenaway, S., Hewitt, M., Liu, X., McCormack, S., Pickford, K., Selley, R., Wells, C., Tymowska-Lalanne, Z., Roby, P., Glenister, P., Thornton, C., Thaung, C., Stevenson, J.A., Arkell, R., Mburu, P., Hardisty, R., Kiernan, A., Erven, A., Steel, K.P., Voegeling, S., Guenet, J.L., Nickols, C., Sadri, R., Nasse, M., Isaacs, A., Davies, K., Browne, M., Fisher, E.M., Martin, J., Rastan, S., Brown, S.D., and Hunter, J. 2000. A systematic, genome-wide, phenotype- driven mutagenesis programme for gene function studies in the mouse. Nat. Genet. 25: 440-443. [Medline] [CrossRef]
85. Ohlemiller, K.K. 2006. Contributions of mouse models to understanding of age- and noise-related hearing loss. Brain Res. 1091: 89-102. [Medline] [CrossRef]
86. Okumura, K., Mochizuki, E., Yokohama, M., Yamakawa, H., Shitara, H., Mburu, P., Yonekawa, H., Brown, S.D., and Kikkawa, Y. 2010. Protein 4.1 expression in the developing hair cells of the mouse inner ear. Brain Res. 1307: 53-62. [Medline] [CrossRef]
87. Pan, L., Yan, J., Wu, L., and Zhang, M. 2009. Assembling stable hair cell tip link complex via multidentate interactions between harmonin and cadherin 23. Proc. Natl. Acad. Sci. U.S.A. 106: 5575-5580. [Medline] [CrossRef]
88. Parkinson, N., and Brown, S.D. 2002. Focusing on the genetics of hearing: you ain't heard nothin' yet. Genome Biol. 3: comment2006.1-2006.6. [Medline] [CrossRef]
89. Parkinson, N., Hardisty-Hughes, R.E., Tateossian, H., Tsai, H.T., Brooker, D., Morse, S., Lalane, Z., MacKenzie, F., Fray, M., Glenister, P., Woodward, A.M., Polley, S., Barbaric, I., Dear, N., Hough, T.A., Hunter, A.J., Cheeseman, M.T., and Brown, S.D. 2006. Mutation at the Evi1 locus in Junbo mice causes susceptibility to otitis media. PLoS Genet. 2: e149. [Medline] [CrossRef]
90. Pennacchio, L.A. 2003. Insights from human/mouse genome comparisons. Mamm. Genome 14: 429-436. [Medline] [CrossRef]
91. Petit, C. 2006. From deafness genes to hearing mechanisms: harmony and counterpoint. Trends Mol. Med. 12: 57-64. [Medline] [CrossRef]
92. Pickles, J.O., Comis, S.D., and Osborne, M.P. 1984. Crosslinks between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction. Hear. Res. 15: 103-112. [Medline] [CrossRef]
93. Probst, F.J., Fridell, R.A., Raphael, Y., Saunders, T.L., Wang, A., Liang, Y., Morell, R.J., Touchman, J.W., Lyons, R.H., Noben-Trauth, K., Friedman, T.B., and Camper, S.A. 1998. Correction of deafness in shaker-2 mice by an unconventional myosin in a BAC transgene. Science 280: 1444-1447. [Medline] [CrossRef]
94. Rzadzinska, A.K., Schneider, M.E., Davies, C., Riordan, G.P., and Kachar, B. 2004. An actin molecular treadmill and myosins maintain stereocilia functional architecture and self-renewal. J. Cell Biol. 164: 887-897. [Medline] [Cross- Ref]
95. Sakaguchi, H., Tokita, J., Naoz, M., Bowen-Pope, D., Gov, N.S., and Kachar, B. 2008. Dynamic compartmentalization of protein tyrosine phosphatase receptor Q at the proximal end of stereocilia: implication of myosin VI-based transport. Cell Motil. Cytoskeleton 65: 528-538. [Medline] [CrossRef]
96. Schraders, M., Oostrik, J., Huygen, P.L., Strom, T.M., van Wijk, E., Kunst, H.P., Hoefsloot, L.H., Cremers, C.W., Admiraal, R.J., and Kremer, H. 2010. Mutations in PTPRQ are a cause of autosomal-recessive nonsyndromic hearing impairment DFNB84 and associated with vestibular dysfunction. Am. J. Hum. Genet. 86: 604-610. [Medline] [CrossRef]
97. Schwander, M., Kachar, B., and Müller, U. 2010. Review series: the cell biology of hearing. J. Cell Biol. 190: 9-20. [Medline] [CrossRef]
98. Schwander, M., Sczaniecka, A., Grillet, N., Bailey, J.S., Avenarius, M., Najmabadi, H., Steffy, B.M., Federe, G.C., Lagler, E.A., Banan, R., Hice, R., Grabowski-Boase, L., Keithley, E.M., Ryan, A.F., Housley, G.D., Wiltshire, T., Smith, R.J., Tarantino, L.M., and Müller, U. 2007. A forward genetics screen in mice identifies recessive deafness traits and reveals that pejvakin is essential for outer hair cell function. J. Neurosci. 27: 2163-2175. [Medline] [CrossRef]
99. Schwander, M., Xiong, W., Tokita, J., Lelli, A., Elledge, H.M., Kazmierczak, P., Sczaniecka, A., Kolatkar, A., Wiltshire, T., Kuhn, P., Holt, J.R., Kachar, B., Tarantino, L., and Müller, U. 2009. A mouse model for nonsyndromic deafness (DFNB12) links hearing loss to defects in tip links of mechanosensory hair cells. Proc. Natl. Acad. Sci. U.S.A. 106: 5252-5257. [Medline] [CrossRef]
100. Self, T., Sobe, T., Copeland, N.G., Jenkins, N.A., Avraham, K.B., and Steel, K.P. 1999. Role of myosin VI in the differentiation of cochlear hair cells. Dev. Biol. 214: 331-341. [Medline] [CrossRef]
101. Senften, M., Schwander, M., Kazmierczak, P., Lillo, C., Shin, J.B., Hasson, T., Géléoc, G.S., Gillespie, P.G., Williams, D., Holt, J.R., and Müller, U. 2006. Physical and functional interaction between protocadherin 15 and myosin VIIa in mechanosensory hair cells. J. Neurosci. 26: 2060-2071. [Medline] [CrossRef]
102. Shin, J.B., Longo-Guess, C.M., Gagnon, L.H., Saylor, K.W., Dumont, R.A., Spinelli, K.J., Pagana, J.M., Wilmarth, P.A., David, L.L., Gillespie, P.G., and Johnson, K.R. 2010. The R109H variant of fascin-2, a developmentally regulated actin crosslinker in hair-cell stereocilia, underlies early-onset hearing loss of DBA/2J mice. J. Neurosci. 30: 9683-9694. [Medline] [CrossRef]
103. Siemens, J., Kazmierczak, P., Reynolds, A., Sticker, M., Littlewood-Evans, A., and Müller, U. 2002. The Usher syndrome proteins cadherin 23 and harmonin form a complex by means of PDZ-domain interactions. Proc. Natl. Acad. Sci. U.S.A. 99: 14946-14951. [Medline] [CrossRef]
104. Siemens, J., Lillo, C., Dumont, R.A., Reynolds, A., Williams, D.S., Gillespie, P.G., and Müller, U. 2004. Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature 428: 950-955. [Medline] [CrossRef]
105. 2+ sensitivity of the mechanotransducer require myosin- XVa in inner but not outer cochlear hair cells. J. Neurosci. 29: 4023-4034. [Medline] [CrossRef]
106. Verpy, E., Leibovici, M., Zwaenepoel, I., Liu, X.Z., Gal, A., Salem, N., Mansour, A., Blanchard, S., Kobayashi, I., Keats, B.J., Slim, R., and 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. [Medline] [CrossRef]
107. Wada, T., Wakabayashi, Y., Takahashi, S., Ushiki, T., Kikkawa, Y., Yonekawa, H., and 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. [Medline] [CrossRef]
108. Wakana, S., Suzuki, T., Furuse, T., Kobayashi, K., Miura, I., Kaneda, H., Yamada, I., Motegi, H., Toki, H., Inoue, M., Minowa, O., Noda, T., Waki, K., Tanaka, N., Masuya, H., and Obata, Y. 2009. Introduction to the Japan Mouse Clinic at the RIKEN BioResource Center. Exp. Anim. 58: 443-450. [Medline] [CrossRef]
109. Weil, D., Blanchard, S., Kaplan, J., Guilford, P., Gibson, F., Walsh, J., Mburu, P., Varela, A., Levilliers, J., Weston, M.D., Kelley, P.M., Kimberling, W.J., Wagenaar, M., Levi-Acobas, F., Larget-Piet, D., Munnich, A., Steel, K.P., Brown, S.D., and Christine, P. 1995. Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature 374: 60-61. [Medline] [CrossRef]
110. Weil, D., El-Amraoui, A., Masmoudi, S., Mustapha, M., Kikkawa, Y., Lainé, S., Delmaghani, S., Adato, A., Nadifi, S., Zina, Z.B., Hamel, C., Gal, A., Ayadi, H., Yonekawa, H., and 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. [Medline] [CrossRef]
111. Willott, J.F. 1986. Effects of aging, hearing loss, and anatomical location on thresholds of inferior colliculus neurons in C57BL/6 and CBA mice. J. Neurophysiol. 56: 391-408. [Medline]
112. Yan, D. and Liu, X.Z. 2010. Genetics and pathological mechanisms of Usher syndrome. J. Hum. Genet. 55: 327-335. [Medline] [CrossRef]
113. Yan, J., Pan, L., Chen, X., Wu, L., and Zhang, M. 2010. The structure of the harmonin/sans complex reveals an unexpected interaction mode of the two Usher syndrome proteins. Proc. Natl. Acad. Sci. U.S.A. 107: 4040-4045. [Medline] [CrossRef]
114. Yang, J., Liu, X., Zhao, Y., Adamian, M., Pawlyk, B., Sun, X., McMillan, D.R., Liberman, M.C., and Li, T. 2010. Ablation of whirlin long isoform disrupts the USH2 protein complex and causes vision and hearing loss. PLoS Genet. 6: e1000955. [Medline] [CrossRef]
115. Zhao, Y., Yamoah, E.N., and Gillespie, P.G. 1996. Regeneration of broken tip links and restoration of mechanical transduction in hair cells. Proc. Natl. Acad. Sci. U.S.A. 93: 15469-15474. [Medline] [CrossRef]
116. Zheng, Q.Y., Ding, D., Yu, H., Salvi, R.J., and Johnson, K.R. 2009. A locus on distal chromosome 10 (ahl4) affecting age-related hearing loss in A/J mice. Neurobiol. Aging 30: 1693-1705. [Medline] [CrossRef]
117. Zheng, Q.Y., Johnson, K.R., and Erway, L.C. 1999. Assessment of hearing in 80 inbred strains of mice by ABR threshold analyses. Hear. Res. 130: 94-107. [Medline] [CrossRef]