The genetics of hair cell development and regeneration

Annual Review of Neuroscience

Volumn 36, Issue , 2013, Pages 361-381

  Groves, Andrew K ^a   Zhang, Kaidi D ^b   Fekete, Donna M ^b,c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b PURDUE UNIVERSITY   (United States)

^c Purdue University   (United States)

Author keywords

Atoh1; Cell cycle; Cochlea; MiRNA; Notch

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BONE MORPHOGENETIC PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1B; DNA; FIBROBLAST GROWTH FACTOR; MICRORNA; NEUROGENIC DIFFERENTIATION FACTOR; NEUROGENIN 1; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR ATOH1; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; AUTOREGULATION; CELL ADHESION; CELL CYCLE; CELL DIFFERENTIATION; CELL DIVISION; CELL MATURATION; CELL METABOLISM; CELL REGENERATION; CHROMOSOME STRUCTURE; COCHLEA DUCT; CORTI ORGAN; GENE EXPRESSION REGULATION; HAIR CELL; HEARING IMPAIRMENT; HOMOZYGOTE; HUMAN; INTRACELLULAR SIGNALING; MESENCHYME; NONHUMAN; POINT MUTATION; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVIEW; VERTEBRATE; WNT SIGNALING PATHWAY;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; HAIR CELLS, AUDITORY; HUMANS; MECHANORECEPTORS; REGENERATION;

EID: 84880262810     PISSN: 0147006X     EISSN: 15454126     Source Type: Book Series    
DOI: 10.1146/annurev-neuro-062012-170309     Document Type: Review

References (147)

1. Ahmed M, Wong EY, Sun J, Xu J, Wang F, Xu PX. 2012. Eya1-Six1 interaction is sufficient to induce hair cell fate in the cochlea by activating Atoh1 expression in cooperation with Sox2. Dev. Cell 22:377-900
2. Akazawa C, Ishibashi M, Shimizu C, Nakanishi S, Kageyama R. 1995. A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J. Biol. Chem. 270:8730-388
3. Alsina B, Giraldez F, Pujades C. 2009. Patterning and cell fate in ear development. Int. J. Dev. Biol. 53:1503-133
4. Avallone B, Fascio U, Balsamo G, Marmo F. 2008. Gentamicin ototoxicity in the saccule of the lizard Podarcis Sicula induces hair cell recovery and regeneration. Hear. Res. 235:15-222
5. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. 2008. The impact of microRNAs on protein output. Nature 455:64-711
6. Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136:215-333
7. Bejarano F, Smibert P, Lai EC. 2010. miR-9a prevents apoptosis during wing development by repressing Drosophila LIM-only. Dev. Biol. 338:63-733
8. Bermingham NA, Hassan BA, Price SD, Vollrath MA, Ben-Arie N, et al. 1999. Math1: an essential gene for the generation of inner ear hair cells. Science 284:1837-411
9. Bok J, Chang W, Wu DK. 2007. Patterning and morphogenesis of the vertebrate inner ear. Int. J. Dev. Biol. 51:521-333
10. Briggs KJ, Eberhart CG, Watkins DN. 2008. Just say no to ATOH: howHIC1 methylation might predispose medulloblastoma to lineage addiction. Cancer Res. 68:8654-566
11. Brooker R, Hozumi K, Lewis J. 2006. Notch ligands with contrasting functions: Jagged1 and Delta1 in the mouse inner ear. Development 133:1277-866
12. Burns JC, Christophel JJ, Collado MS, Magnus C, Carfrae M, Corwin JT. 2008. Reinforcement of cell junctions correlates with the absence of hair cell regeneration in mammals and its occurrence in birds. J. Comp. Neurol. 511:396-4144
13. Burns JC, Cox BC, Thiede BR, Zuo J, Corwin JT. 2012a. In vivo proliferative regeneration of balance hair cells in newborn mice. J. Neurosci. 32:6570-777
14. Burns JC, On D, Baker W, Collado MS, Corwin JT. 2012b. Over half the hair cells in the mouse utricle first appear after birth, with significant numbers originating from early postnatal mitotic production in peripheral and striolar growth zones. J. Assoc. Res. Otolaryngol. 13:609-277
15. Cafaro J, Lee GS, Stone JS. 2007. Atoh1 expression defines activated progenitors and differentiating hair cells during avian hair cell regeneration. Dev. Dyn. 236:156-700
16. Chen P, Johnson JE, Zoghbi HY, Segil N. 2002. The role ofMath1 in inner ear development: uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 129:2495-5055
17. Chen P, Segil N. 1999. p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126:1581-900
18. Collado MS, Thiede BR, Baker W, Askew C, Igbani LM, Corwin JT. 2011. The postnatal accumulation of junctional E-cadherin is inversely correlated with the capacity for supporting cells to convert directly into sensory hair cells in mammalian balance organs. J. Neurosci. 31:11855-666
19. Corwin JT, Cotanche DA. 1988. Regeneration of sensory hair cells after acoustic trauma. Science 240:1772-744
20. D'Angelo A, Bluteau O, Garcia-Gonzalez MA, Gresh L, Doyen A, et al. 2010. Hepatocyte nuclear factor 1alpha and beta control terminal differentiation and cell fate commitment in the gut epithelium. Development 137:1573-822
21. Daudet N, Gibson R, Shang J, Bernard A, Lewis J, Stone J. 2009. Notch regulation of progenitor cell behavior in quiescent and regenerating auditory epithelium of mature birds. Dev. Biol. 326:86-1000
22. Diensthuber M, Oshima K, Heller S. 2009. Stem/progenitor cells derived from the cochlear sensory epithelium give rise to spheres with distinct morphologies and features. J. Assoc. Res. Otolaryngol. 10:173-900
23. Doetzlhofer A, Basch ML, Ohyama T, Gessler M, Groves AK, Segil N. 2009. Hey2 regulation by FGF provides a Notch-independent mechanism for maintaining pillar cell fate in the organ of Corti. Dev. Cell 16:58-699
24. Driver EC, Pryor SP, Hill P, Turner J, Ruther U, et al. 2008. Hedgehog signaling regulates sensory cell formation and auditory function in mice and humans. J. Neurosci. 28:7350-588
25. Ebert PJ, Timmer JR, Nakada Y, Helms AW, Parab PB, et al. 2003. Zic1 represses Math1 expression via interactions with the Math1 enhancer and modulation of Math1 autoregulation. Development 130:1949-599
26. Esquela-Kerscher A, Slack FJ. 2006. Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer 6:259-699
27. Filipowicz W, Bhattacharyya SN, Sonenberg N. 2008. Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat. Rev. Genet. 9:102-144
28. Forge A, Li L, Corwin JT, Nevill G. 1993. Ultrastructural evidence for hair cell regeneration in themammalian inner ear. Science 259:1616-199
29. Forge A, Li L, Nevill G. 1998. Hair cell recovery in the vestibular sensory epithelia of mature guinea pigs. J. Comp. Neurol. 397:69-888
30. Friedman LM, Dror AA, Mor E, Tenne T, Toren G, et al. 2009. MicroRNAs are essential for development and function of inner ear hair cells in vertebrates. Proc. Natl. Acad. Sci. USA 106:7915-200
31. Gleich O, Fischer FP, K? oppl C, Manley GA. 2004. Hearing organ evolution and specialization: Archosaurs. In Evolution of the Vertebrate Auditory System, ed. GA Manley, AN Popper, RR Fay, pp. 224-55. New York: Springer-Verlagg
32. Goodyear R, Richardson G. 1997. Pattern formation in the basilar papilla: evidence for cell rearrangement. J. Neurosci. 17:6289-3011
33. Groves AK. 2010. The challenge of hair cell regeneration. Exp. Biol. Med. 235:434-466
34. Groves AK, Fekete DM. 2012. Shaping sound in space: the regulation of inner ear patterning. Development 139:245-577
35. Guo H, Ingolia NT, Weissman JS, Bartel DP. 2010. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466:835-400
36. Guttilla IK, White BA. 2009. Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J. Biol. Chem. 284:23204-166
37. Hayashi T, Ray CA, Bermingham-McDonogh O. 2008. Fgf20 is required for sensory epithelial specification in the developing cochlea. J. Neurosci. 28:5991-999
38. Hei R, Chen J, Qiao L, Li X, Mao X, et al. 2011. Dynamic changes in microRNA expression during differentiation of rat cochlear progenitor cells in vitro. Int. J. Pediatr. Otorhinolaryngol. 75:1010-144
39. Helms AW, Abney AL, Ben-Arie N, Zoghbi HY, Johnson JE. 2000. Autoregulation and multiple enhancers control Math1 expression in the developing nervous system. Development 127:1185-966
40. Henson BJ, Zhu W, Hardaway K, Wetzel JL, Stefan M, et al. 2012. Transcriptional and post-transcriptional regulation of SPAST, the gene most frequently mutated in hereditary spastic paraplegia. PLoS One 7:e365055
41. Hobert O. 2007. miRNAs play a tune. Cell 131:22-244
42. Hobert O. 2008. Gene regulation by transcription factors and microRNAs. Science 319:1785-866
43. Holley M, Rhodes C, Kneebone A, Herde MK, Fleming M, Steel KP. 2010. Emx2 and early hair cell development in the mouse inner ear. Dev. Biol. 340:547-566
44. Hori R, Nakagawa T, Sakamoto T, Matsuoka Y, Takebayashi S, Ito J. 2007. Pharmacological inhibition of Notch signaling in the mature guinea pig cochlea. NeuroReport 18:1911-144
45. Huh SH, Jones J, Warchol ME, Ornitz DM. 2012. Differentiation of the lateral compartment of the cochlea requires a temporally restricted FGF20 signal. PLoS Biol. 10:e10012311
46. Hwang CH, Guo D, Harris MA, Howard O, Mishina Y, et al. 2010. Role of bone morphogenetic proteins on cochlear hair cell formation: analyses of Noggin and Bmp2 mutant mice. Dev. Dyn. 239:505-133
47. Izumikawa M, Minoda R, Kawamoto K, Abrashkin KA, Swiderski DL, et al. 2005. Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat. Med. 11:271-766
48. Jahan I, Pan N, Kersigo J, Calisto LE, Morris KA, et al. 2012. Expression of Neurog1 instead of Atoh1 can partially rescue organ of Corti cell survival. PLoS One 7:e308533
49. Jahan I, Pan N, Kersigo J, Fritzsch B. 2010. Neurod1 suppresses hair cell differentiation in ear ganglia and regulates hair cell subtype development in the cochlea. PLoS One 5:e116611
50. Jalvy-Delvaille S, Maurel M, Majo V, Pierre N, Chabas S, et al. 2012. Molecular basis of differential target regulation by miR-96 and miR-182: the Glypican-3 as a model. Nucleic Acids Res. 40:1356-655
51. Jensen KP, Covault J. 2010. Human miR-1271 is a miR-96 paralog with distinct non-conserved brain expression pattern. Nucleic Acids Res. 39:701-111
52. Jensen KP, Covault J, Conner TS, Tennen H, Kranzler HR, Furneaux HM. 2009. A common polymorphism in serotonin receptor 1B mRNA moderates regulation by miR-96 and associates with aggressive human behaviors. Mol. Psychiatry 14:381-899
53. Jones C, Chen P. 2007. Planar cell polarity signaling in vertebrates. BioEssays 29:120-322
54. Kamaid A, Neves J, Giraldez F. 2010. Id gene regulation and function in the prosensory domains of the chicken inner ear: a link between Bmp signaling and Atoh1. J. Neurosci. 30:11426-344
55. Kanzaki S, Beyer LA, Swiderski DL, Izumikawa M, Stover T, et al. 2006. p27(Kip1) deficiency causes organ of Corti pathology and hearing loss. Hear. Res. 214:28-366
56. Katayama A, Corwin JT. 1989. Cell production in the chicken cochlea. J. Comp. Neurol. 281:129-355
57. Kawamoto K, Ishimoto S, Minoda R, Brough DE, Raphael Y. 2003. Math1 gene transfer generates new cochlear hair cells in mature guinea pigs in vivo. J. Neurosci. 23:4395-4000
58. Kawamoto K, Izumikawa M, Beyer LA, Atkin GM, Raphael Y. 2009. Spontaneous hair cell regeneration in the mouse utricle following gentamicin ototoxicity. Hear. Res. 247:17-266
59. Kelley MW. 2006. Regulation of cell fate in the sensory epithelia of the inner ear. Nat. Rev. Neurosci. 7:837-499
60. Kelley MW, Talreja DR, Corwin JT. 1995. Replacement of hair cells after laser microbeam irradiation in cultured organs of corti from embryonic and neonatal mice. J. Neurosci. 15:3013-266
61. Kelly MC, Chang Q, Pan A, Lin X, Chen P. 2012. Atoh1 directs the formation of sensorymosaics and induces cell proliferation in the postnatal mammalian cochlea in vivo. J. Neurosci. 32:6699-7100
62. Kiernan AE, Pelling AL, Leung KK, Tang AS, Bell DM, et al. 2005. Sox2 is required for sensory organ development in the mammalian inner ear. Nature 434:1031-355
63. Kiernan AE, Xu J, Gridley T. 2006. The Notch ligand JAG1 is required for sensory progenitor development in the mammalian inner ear. PLoS Genet. 2:e44
64. Kirkegaard M, Nyengaard Jr. 2005. Stereological study of postnatal development in the mouse utricular macula. J. Comp. Neurol. 492:132-444
65. Klisch TJ, Xi Y, Flora A, Wang L, Li W, Zoghbi HY. 2011. In vivo Atoh1 targetome reveals how a proneural transcription factor regulates cerebellar development. Proc. Natl. Acad. Sci. USA 108:3288-933
66. Kloosterman WP, Plasterk RH. 2006. The diverse functions ofmicroRNAs in animal development and disease. Dev. Cell 11:441-500
67. Kosik KS. 2006. The neuronal microRNA system. Nat. Rev. Neurosci. 7:911-200
68. Kuhn S, Johnson SL, Furness DN, Chen J, Ingham N, et al. 2011. miR-96 regulates the progression of differentiation in mammalian cochlear inner and outer hair cells. Proc. Natl. Acad. Sci. USA 108:2355-600
69. Lai HC, Klisch TJ, Roberts R, Zoghbi HY, Johnson JE. 2011. In vivo neuronal subtype-specific targets of Atoh1 (Math1) in dorsal spinal cord. J. Neurosci. 31:10859-711
70. Lee YS, Liu F, Segil N. 2006. A morphogenetic wave of p27Kip1 transcription directs cell cycle exit during organ of Corti development. Development 133:2817-266
71. Lewis BP, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15-200
72. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. 2003. Prediction of mammalian microRNA targets. Cell 115:787-988
73. Lewis MA, Quint E, Glazier AM, Fuchs H, De Angelis MH, et al. 2009. An ENU-induced mutation of miR-96 associated with progressive hearing loss in mice. Nat. Genet. 41:614-188
74. Lewis MA, Steel KP. 2010. MicroRNAs in mouse development and disease. Semin. Cell Dev. Biol. 21:774-800
75. Lewis RM, Hume CR, Stone JS. 2012. Atoh1 expression and function during auditory hair cell regeneration in post-hatch chickens. Hear. Res. 289:74-855
76. Li H, Corrales CE, Wang Z, Zhao Y, Wang Y, et al. 2005. BMP4 signaling is involved in the generation of inner ear sensory epithelia. BMC Dev. Biol. 5:166
77. Li H, Kloosterman W, Fekete DM. 2010a. MicroRNA-183 family members regulate sensorineural fates in the inner ear. J. Neurosci. 30:3254-633
78. Li J, Fu H, Xu C, Tie Y, Xing R, et al. 2010b. miR-183 inhibits TGF-beta1-induced apoptosis by downregulation of PDCD4 expression in human hepatocellular carcinoma cells. BMC Cancer 10:3544
79. Lin H, Dai T, Xiong H, Zhao X, Chen X, et al. 2010. Unregulated miR-96 induces cell proliferation in human breast cancer by downregulating transcriptional factor FOXO3a. PLoS One 5:e157977
80. Lin V, Golub JS, Nguyen TB, Hume CR, Oesterle EC, Stone JS. 2011. Inhibition of Notch activity promotes nonmitotic regeneration of hair cells in the adult mouse utricles. J. Neurosci. 31:15329-399
81. Liu X, Fortin K, Mourelatos Z. 2008. MicroRNAs: biogenesis and molecular functions. Brain Pathol. 18:113-211
82. Liu Z, Dearman JA, Cox BC, Walters BJ, Zhang L, et al. 2012a. Age-dependent in vivo conversion of mouse cochlear pillar and Deiters' cells to immature hair cells by Atoh1 ectopic expression. J. Neurosci. 32:6600-100
83. Liu Z, Liu J, Segura MF, Shao C, Lee P, et al. 2012b. MiR-182 overexpression in tumourigenesis of high-grade serous ovarian carcinoma. J. Pathol. 228:204-155
84. Lowenheim H, Furness DN, Kil J, Zinn C, Gultig K, et al. 1999. Gene disruption of p27(Kip1) allows cell proliferation in the postnatal and adult organ of Corti. Proc. Natl. Acad. Sci. USA 96:4084-888
85. Lowery AJ, Miller N, Dwyer RM, Kerin MJ. 2010. Dysregulated miR-183 inhibits migration in breast cancer cells. BMC Cancer 10:5022
86. Lujan E, Chanda S, Ahlenius H, Sudhof TC, Wernig M. 2012. Direct conversion of mouse fibroblasts to self-renewing, tripotent neural precursor cells. Proc. Natl. Acad. Sci. USA 109:2527-322
87. Lumpkin EA, Collisson T, Parab P, Omer-Abdalla A, Haeberle H, et al. 2003. Math1-driven GFP expression in the developing nervous system of transgenic mice. Gene Expr. Patterns 3:389-955
88. Ma EY, Raible DW. 2009. Signaling pathways regulating zebrafish lateral line development. Curr. Biol. 19:R381-866
89. Ma EY, Rubel EW, Raible DW. 2008. Notch signaling regulates the extent of hair cell regeneration in the zebrafish lateral line. J. Neurosci. 28:2261-733
90. Matei V, Pauley S, Kaing S, Rowitch D, Beisel KW, et al. 2005. Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Dev. Dyn. 234:633-500
91. May-Simera H, Kelley MW. 2012. Planar cell polarity in the inner ear. Curr. Top. Dev. Biol. 101:111-400
92. Mencia A, Modamio-Høybjør S, Redshaw N, Morin M, Mayo-Merino F, et al. 2009. Mutations in the seed region of human miR-96 are responsible for nonsyndromic progressive hearing loss. Nat. Genet. 41:609-133
93. Mihelich BL, Khramtsova EA, Arva N, Vaishnav A, Johnson DN, et al. 2011. miR-183-96-182 cluster is overexpressed in prostate tissue and regulates zinc homeostasis in prostate cells. J. Biol. Chem. 286:44503-111
94. Montcouquiol M, Crenshaw EB 3rd, Kelley MW. 2006. Noncanonical Wnt signaling and neural polarity. Annu. Rev. Neurosci. 29:363-866
95. Montcouquiol M, Kelley MW. 2003. Planar and vertical signals control cellular differentiation and patterning in the mammalian cochlea. J. Neurosci. 23:9469-788
96. Moskwa P, Buffa FM, Pan Y, Panchakshari R, Gottipati P, et al. 2011. miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol. Cell 41:210-200
97. Mulvaney J, Dabdoub A. 2012. Atoh1, an essential transcription factor in neurogenesis and intestinal and inner ear development: function, regulation, and context dependency. J. Assoc. Res. Otolaryngol. 13:281-933
98. Mutoh H, Sakamoto H, Hayakawa H, Arao Y, Satoh K, et al. 2006. The intestine-specific homeobox gene Cdx2 induces expression of the basic helix-loop-helix transcription factor Math1. Differentiation 74:313-211
99. Neves J, Uchikawa M, Bigas A, Giraldez F. 2012. The prosensory function of Sox2 in the chicken inner ear relies on the direct regulation of Atoh1. PLoS One 7:e308711
100. Ohyama T, Basch ML, Mishina Y, Lyons KM, Segil N, Groves AK. 2010. BMP signaling is necessary for patterning the sensory and nonsensory regions of the developing mammalian cochlea. J. Neurosci. 30:15044-511
101. Oshima K, Grimm CM, Corrales CE, Senn P, Martinez Monedero R, et al. 2007. Differential distribution of stem cells in the auditory and vestibular organs of the inner ear. J. Assoc. Res. Otolaryngol. 8:18-311
102. Pan N, Jahan I, Kersigo J, Kopecky B, Santi P, et al. 2011. Conditional deletion of Atoh1 using Pax2-Cre results in viable mice without differentiated cochlear hair cells that have lost most of the organ of Corti. Hear. Res. 275:66-800
103. Pirvola U, Ylikoski J, Trokovic R, Hebert JM, McConnell SK, Partanen J. 2002. FGFR1 is required for the development of the auditory sensory epithelium. Neuron 35:671-800
104. Pujades C, Kamaid A, Alsina B, Giraldez F. 2006. BMP-signaling regulates the generation of hair-cells. Dev. Biol. 292:55-677
105. Puligilla C, Dabdoub A, Brenowitz SD, Kelley MW. 2010. Sox2 induces neuronal formation in the developing mammalian cochlea. J. Neurosci. 30:714-222
106. Puligilla C, Feng F, Ishikawa K, Bertuzzi S, Dabdoub A, et al. 2007. Disruption of fibroblast growth factor receptor 3 signaling results in defects in cellular differentiation, neuronal patterning, and hearing impairment. Dev. Dyn. 236:1905-177
107. Puligilla C, Kelley MW. 2009. Building the world's best hearing aid; regulation of cell fate in the cochlea. Curr. Opin. Genet. Dev. 19:368-733
108. Raft S, Koundakjian EJ, Quinones H, Jayasena CS, Goodrich LV, et al. 2007. Cross-regulation of Ngn1 and Math1 coordinates the production of neurons and sensory hair cells during inner ear development. Development 134:4405-155
109. Rida PC, Chen P. 2009. Line up and listen: planar cell polarity regulation in the mammalian inner ear. Semin. Cell Dev. Biol. 20:978-855
110. Riester A, Issler O, Spyroglou A, Rodrig SH, Chen A, Beuschlein F. 2012. ACTH-dependent regulation of microRNA as endogenous modulators of glucocorticoid receptor expression in the adrenal gland. Endocrinology 153:212-222
111. Roberson DF, Weisleder P, Bohrer PS, Rubel EW. 1992. Ongoing production of sensory cells in the vestibular epithelium of the chick. Hear. Res. 57:166-744
112. Roberson DW, Rubel EW. 1994. Cell division in the gerbil cochlea after acoustic trauma. Am. J. Otol. 15:28-344
113. Ruben RJ. 1967. Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol. 220(Suppl. ):1-444
114. Rudnicki A, Avraham KB. 2012. microRNAs: the art of silencing in the ear. EMBO Mol. Med. 4:849-599
115. Ryals BM, Rubel EW. 1988. Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240:1774-766
116. Sacheli R, Nguyen L, Borgs L, Vandenbosch R, Bodson M, et al. 2009. Expression patterns of miR-96, miR-182 and miR-183 in the development inner ear. Gene Expr. Patterns 9:364-700
117. Sarver AL, Li L, Subramanian S. 2010. MicroRNA miR-183 functions as an oncogene by targeting the transcription factor EGR1 and promoting tumor cell migration. Cancer Res. 70:9570-800
118. Saus E, Soria V, Escaramis G, Vivarelli F, Crespo JM, et al. 2010. Genetic variants and abnormal processing of pre-miR-182, a circadian clock modulator, in major depression patients with late insomnia. Hum. Mol. Genet. 19:4017-255
119. Segura MF, Hanniford D, Menendez S, Reavie L, Zou X, et al. 2009. Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor. Proc. Natl. Acad. Sci. USA 106:1814-199
120. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455:58-633
121. Shi F, Cheng YF, Wang XL, Edge AS. 2010. Beta-catenin up-regulates Atoh1 expression in neural progenitor cells by interaction with an Atoh1 3′ enhancer. J. Biol. Chem. 285:392-4000
122. Solda G, Robusto M, Primignani P, Castorina P, Benzoni E, et al. 2012. A novel mutation within the MIR96 gene causes non-syndromic inherited hearing loss in an Italian family by altering pre-miRNA processing. Hum. Mol. Genet. 21:577-855
123. Soukup GA. 2009. Little but loud: Small RNAs have a resounding affect on ear development. Brain Res. 1277:104-144
124. Soukup GA, Fritzsch B, Pierce ML, Weston MD, Jahan I, et al. 2009. Residual microRNA expression dictates the extent of inner ear development in conditional Dicer knockout mice. Dev. Biol. 328:328-411
125. Stevens CB, Davies AL, Battista S, Lewis JH, Fekete DM. 2003. Forced activation of Wnt signaling alters morphogenesis and sensory organ identity in the chicken inner ear. Dev. Biol. 261:149-644
126. Stone JS, Cotanche DA. 2007. Hair cell regeneration in the avian auditory epithelium. Int. J. Dev. Biol. 51:633-477
127. Stone JS, Rubel EW. 1999. Delta1 expression during avian hair cell regeneration. Development 126:961-733
128. Straube WL, Tanaka EM. 2006. Reversibility of the differentiated state: regeneration in amphibians. Artif. Organs 30:743-555
129. Sun Y, Fang R, Li C, Li L, Li F, et al. 2010. Hsa-mir-182 suppresses lung tumorigenesis through down regulation of RGS17 expression in vitro. Biochem. Biophys. Res. Commun. 396:501-77
130. Takacs CM, Giraldez AJ. 2010. MicroRNAs as genetic sculptors: fishing for clues. Semin. Cell Dev. Biol. 21:760-677
131. Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Sudhof TC, Wernig M. 2010. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463:1035-411
132. Wang J, Li J, Shen J, Wang C, Yang L, Zhang X. 2012a. MicroRNA-182 downregulates metastasis suppressor 1 and contributes to metastasis of hepatocellular carcinoma. BMC Cancer 12:2277
133. Wang XR, Zhang XM, Du J, Jiang H. 2012b. MicroRNA-182 regulates otocyst-derived cell differentiation and targets T-box1 gene. Hear. Res. 286:55-633
134. Wang Y, Huang JW, Calses P, Kemp CJ, Taniguchi T. 2012c. MiR-96 downregulates REV1 and RAD51 to promote cellular sensitivity to cisplatin and PARP inhibition. Cancer Res. 72:4037-466
135. Weston MD, Pierce ML, Jensen-Smith HC, Fritzsch B, Rocha-Sanchez S, et al. 2011. MicroRNA-183 family expression in hair cell development and requirement of microRNAs for hair cell maintenance and survival. Dev. Dyn. 240:808-199
136. Weston MD, Pierce ML, Rocha-Sanchez S, Beisel KW, Soukup GA. 2006. MicroRNA gene expression in the mouse inner ear. Brain Res. 1111:95-1044
137. Weston MD, Soukup GA. 2009. MicroRNAs sound off. Genome Med. 1:599
138. White PM, Doetzlhofer A, Lee YS, Groves AK, Segil N. 2006. Mammalian cochlear supporting cells can divide and trans-differentiate into hair cells. Nature 441:984-877
139. Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E, et al. 2005. MicroRNA expression in zebrafish embryonic development. Science 309:310-111
140. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. 2009. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat. Cell Biol. 11:228-344
141. Xu S, Witmer PD, Lumayag S, Kovacs B, Valle D. 2007. MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster. J. Biol. Chem. 282:25053-666
142. Yamasoba T, Kondo K. 2006. Supporting cell proliferation after hair cell injury in mature guinea pig cochlea in vivo. Cell Tissue Res. 325:23-311
143. Yan D, Dong XD, Chen X, Yao S, Wang L, et al. 2012. Role of microRNA-182 in posterior uveal melanoma: regulation of tumor development through MITF, BCL2 and cyclin D2. PLoS One 7:e409677
144. Yang N, Ng YH, Pang ZP, Sudhof TC, Wernig M. 2011. Induced neuronal cells: how to make and define a neuron. Cell Stem Cell 9:517-255
145. Yu S, Lu Z, Liu C, Meng Y, Ma Y, et al. 2010. miRNA-96 suppresses KRAS and functions as a tumor suppressor gene in pancreatic cancer. Cancer Res. 70:6015-255
146. Zheng JL, Gao WQ. 2000. Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat. Neurosci. 3:580-866
147. Zhu Q, Sun W, Okano K, Chen Y, Zhang N, et al. 2011. Sponge transgenic mouse model reveals important roles for the microRNA-183 (miR-183)/96/182 cluster in postmitotic photoreceptors of the retina. J. Biol. Chem. 286:31749-600