Understanding the evolution and development of neurosensory transcription factors of the ear to enhance therapeutic translation

Cell and Tissue Research

Volumn 349, Issue 2, 2012, Pages 415-432

  Pan, Ning ^a   Kopecky, Benjamin ^a   Jahan, Israt ^a   Fritzsch, Bernd ^a  

^a E11 SSH   (United States)

Author keywords

Development; Hair cell; Inner ear; Restoration; Transcription factor

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR;

ANIMAL; CORTI ORGAN; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEARING IMPAIRMENT; HUMAN; INNER EAR; METABOLISM; MOLECULAR EVOLUTION; REVIEW;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; EAR, INNER; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEARING LOSS; HUMANS; ORGAN OF CORTI;

EID: 84871908093     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-012-1454-0     Document Type: Review

References (138)

1. Abrashkin KA, Izumikawa M, Miyazawa T, Wang CH, Crumling MA, Swiderski DL, Beyer LA, Gong TW, Raphael Y (2006) The fate of outer hair cells after acoustic or ototoxic insults. Hear Res 218:20-29
2. Abu-Daya A, Khokha MK, Zimmerman LB (2012) The hitchhiker's guide to Xenopus genetics. Genesis 50:164-175
3. Adam J, Myat A, Le Roux I, Eddison M, Henrique D, Ish-Horowicz D, Lewis J (1998) Cell fate choices and the expression of Notch, Delta and Serrate homologues in the chick inner ear: parallels with Drosophila sense-organ development. Development 125:4645-4654
4. Ahmed M, Wong EYM, Sun J, Xu J, Wang F, Xu P-X (2012a) Eya1- Six1 interaction is sufficient to induce hair cell fate in the cochlea by activating Atoh1 expression in cooperation with Sox2. Dev Cell 22:377-390
5. Ahmed M, Xu J, Xu PX (2012b) EYA1 and SIX1 drive the neuronal developmental program in cooperation with the SWI/SNF chromatin-remodeling complex and SOX2 in the mammalian inner ear. Development (in press)
6. Alam SA, Robinson BK, Huang J, Green SH (2007) Prosurvival and proapoptotic intracellular signaling in rat spiral ganglion neurons in vivo after the loss of hair cells. J Comp Neurol 503:832-852
7. Ali F, Hindley C, McDowell G, Deibler R, Jones A, Kirschner M, Guillemot F, Philpott A (2011) Cell cycle-regulated multi-site phosphorylation of Neurogenin 2 coordinates cell cycling with differentiation during neurogenesis. Development 138:4267-4277
8. Basch ML, Ohyama T, Segil N, Groves AK (2011) Canonical Notch signaling is not necessary for prosensory induction in the mouse cochlea: insights from a conditional mutant of RBPjkappa. J Neurosci 31:8046-8058
9. Batts SA, Shoemaker CR, Raphael Y (2009) Notch signaling and Hes labeling in the normal and drug-damaged organ of Corti. Hear Res 249:15-22
10. Belyantseva IA, Adler HJ, Curi R, Frolenkov GI, Kachar B (2000) Expression and localization of prestin and the sugar transporter GLUT-5 during development of electromotility in cochlear outer hair cells. J Neurosci 20:RC116
11. 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
12. Bok J, Dolson DK, Hill P, Ruther U, Epstein DJ, Wu DK (2007) Opposing gradients of Gli repressor and activators mediate Shh signaling along the dorsoventral axis of the inner ear. Development 134:1713-1722
13. Bouchard M, de Caprona D, Busslinger M, Xu P, Fritzsch B (2010) Pax2 and Pax8 cooperate in mouse inner ear morphogenesis and innervation. BMC Dev Biol 10:89
14. Brar GA, Yassour M, Friedman N, Regev A, Ingolia NT, Weissman JS (2011) High-resolution view of the yeast meiotic program revealed by ribosome profiling. Science
15. Bridgham JT, Carroll SM, Thornton JW (2006) Evolution of hormonereceptor complexity by molecular exploitation. Science 312:97-101
16. Brigande JV, Heller S (2009) Quo vadis, hair cell regeneration? Nat Neurosci 12:679-685
17. Brooker R, Hozumi K, Lewis J (2006) Notch ligands with contrasting functions: Jagged1 and Delta1 in the mouse inner ear. Development 133:1277-1286
18. Budelmann B (1992) Hearing in nonarthropod invertebrates. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 141-155
19. Burighel P, Caicci F, Manni L (2011) Hair cells in non-vertebrate models: lower chordates and molluscs. Hear Res 273:14-24
20. Cachero S, Simpson TI, Zur Lage PI, Ma L, Newton FG, Holohan EE, Armstrong JD, Jarman AP (2011) The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons. PLoS Biol 9:e1000568
21. Chang W, Lin Z, Kulessa H, Hebert J, Hogan BL, Wu DK (2008) Bmp4 is essential for the formation of the vestibular apparatus that detects angular head movements. PLoS Genet 4: e1000050
22. Chellappa R, Li S, Pauley S, Jahan I, Jin K, Xiang M (2008) Barhl1 regulatory sequences required for cell-specific gene expression and autoregulation in the inner ear and central nervous system. Mol Cell Biol 28:1905-1914
23. Chen P, Johnson JE, Zoghbi HY, Segil N (2002) The role of Math1 in inner ear development: Uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 129:2495-2505
24. Conway SJ, Firulli B, Firulli AB (2010) A bHLH code for cardiac morphogenesis. Pediatr Cardiol 31:318-324
25. Cotanche DA, Kaiser CL (2010) Hair cell fate decisions in cochlear development and regeneration. Hear Res 266:18-25
26. Crocker J, Tamori Y, Erives A (2008) Evolution acts on enhancer organization to fine-tune gradient threshold readouts. PLoS Biol 6:e263
27. Dabdoub A, Puligilla C, Jones JM, Fritzsch B, Cheah KS, Pevny LH, Kelley MW (2008) Sox2 signaling in prosensory domain specification and subsequent hair cell differentiation in the developing cochlea. Proc Natl Acad Sci USA 105:18396-18401
28. Dalgard CL, Zhou Q, Lundell TG, Doughty ML (2011) Altered gene expression in the emerging cerebellar primordium of Neurog1-/- mice. Brain Res 1388:12-21
29. Daudet N, Ariza-McNaughton L, Lewis J (2007) Notch signalling is needed to maintain, but not to initiate, the formation of prosensory patches in the chick inner ear. Development 134:2369-2378
30. Degnan BM, Vervoort M, Larroux C, Richards GS (2009) Early evolution of metazoan transcription factors. Curr Opin Genet Dev 19:591-599
31. Deol MS (1981) The inner ear in Bronx waltzer mice. Acta Otolaryngol 92:331-336
32. 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 16:58-69
33. Dominguez-Frutos E, Lopez-Hernandez I, Vendrell V, Neves J, Gallozzi M, Gutsche K, Quintana L, Sharpe J, Knoepfler PS, Eisenman RN, Trumpp A, Giraldez F, Schimmang T (2011) N-myc controls proliferation, morphogenesis, and patterning of the inner ear. J Neurosci 31:7178-7189
34. Duncan JS, Lim KC, Engel JD, Fritzsch B (2011) Limited inner ear morphogenesis and neurosensory development are possible in the absence of GATA3. Int J Dev Biol 55:297-303
35. Espinosa-Soto C, Martin OC, Wagner A (2011) Phenotypic plasticity can facilitate adaptive evolution in gene regulatory circuits. BMC Evol Biol 11:5
36. Fritzsch B, Wake MH (1988) The inner ear of gymnophione amphibians and its nerve supply: a comparative study of regressive events in a complex sensory system. Zoomorphology 108:210-217
37. Fritzsch B, Beisel KW, Bermingham NA (2000) Developmental evolutionary biology of the vertebrate ear: conserving mechanoelectric transduction and developmental pathways in diverging morphologies. Neuroreport 11:R35-44
38. Fritzsch B, Beisel KW, Jones K, Farinas I, Maklad A, Lee J, Reichardt LF (2002) Development and evolution of inner ear sensory epithelia and their innervation. J Neurobiol 53:143-156
39. Fritzsch B, Matei VA, Nichols DH, Bermingham N, Jones K, Beisel KW, Wang VY (2005) Atoh1 null mice show directed afferent fiber growth to undifferentiated ear sensory epithelia followed by incomplete fiber retention. Dev Dyn 233:570-583
40. Fritzsch B, Beisel KW, Hansen LA (2006) The molecular basis of neurosensory cell formation in ear development: a blueprint for hair cell and sensory neuron regeneration? Bioessays 28:1181-1193
41. Fritzsch B, Beisel KW, Pauley S, Soukup G (2007) Molecular evolution of the vertebrate mechanosensory cell and ear. Int J Dev Biol 51:663-678
42. Fritzsch B, Eberl DF, Beisel KW (2010) The role of bHLH genes in ear development and evolution: revisiting a 10-year-old hypothesis. Cell Mol Life Sci 67:3089-3099
43. Fritzsch B, Jahan I, Pan N, Kersigo J, Duncan J, Kopecky B (2011) Dissecting the molecular basis of organ of Corti development: Where are we now? Hear Res 276:16-26
44. Galliot B, Quiquand M (2011) A two-step process in the emergence of neurogenesis. Eur J Neurosci 34:847-862
45. Garcia-Bellido A, de Celis JF (2009) The complex tale of the achaetescute complex: a paradigmatic case in the analysis of gene organization and function during development. Genetics 182:631-639
46. Gazave E, Lapebie P, Richards GS, Brunet F, Ereskovsky AV, Degnan BM, Borchiellini C, Vervoort M, Renard E (2009) Origin and evolution of the Notch signalling pathway: an overview from eukaryotic genomes. BMC Evol Biol 9:249
47. Gowan K, Helms AW, Hunsaker TL, Collisson T, Ebert PJ, Odom R, Johnson JE (2001) Crossinhibitory activities of Ngn1 and Math1 allow specification of distinct dorsal interneurons. Neuron 31:219-232
48. Groves AK (2010) The challenge of hair cell regeneration. Exp Biol Med (Maywood) 235:434-446
49. Groves AK, Fekete DM (2012) Shaping sound in space: the regulation of inner ear patterning. Development 139:245-257
50. 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 127:1185-1196
51. 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 340:547-556
52. Huang M, Sage C, Tang Y, Lee SG, Petrillo M, Hinds PW, Chen ZY (2011) Overlapping and distinct pRb pathways in the mammalian auditory and vestibular organs. Cell Cycle 10:337-351
53. 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:e1001231
54. Izumikawa M, Minoda R, Kawamoto K, Abrashkin KA, Swiderski DL, Dolan DF, Brough DE, Raphael Y (2005) Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat Med 11:271-276
55. Izumikawa M, Batts SA, Miyazawa T, Swiderski DL, Raphael Y (2008) Response of the flat cochlear epithelium to forced expression of Atoh1. Hear Res 240:52-56
56. Jacques BE, Montcouquiol ME, Layman EM, Lewandoski M, Kelley MW (2007) Fgf8 induces pillar cell fate and regulates cellular patterning in the mammalian cochlea. Development 134:3021-3029
57. Jahan I, Kersigo J, Pan N, Fritzsch B (2010a) Neurod1 regulates survival and formation of connections in mouse ear and brain. Cell Tissue Res 341:95-110
58. Jahan I, Pan N, Kersigo J, Fritzsch B (2010b) Neurod1 suppresses hair cell differentiation in ear ganglia and regulates hair cell subtype development in the cochlea. PLoS One 5:e11661
59. Jahan I, Pan N, Kersigo J, Calisto LE, Morris KA, Kopecky B, Duncan JS, Beiseld KW, Fritzsch B (2012) Expression of Neurog1 instead of Atoh1 can partially rescue organ of Corti cell survival. PLoS One 7:e30853
60. Jeon SJ, Fujioka M, Kim SC, Edge AS (2011) Notch signaling alters sensory or neuronal cell fate specification of inner ear stem cells. J Neurosci 31:8351-8358
61. Jorgensen JM (1989) Evolution of octavolateralis sensory cells. In: Coombs S, Goerner P, Muenz H (eds) The mechanosensory lateral line. Neurobiology and evolution. Springer, New York, pp 99-115
62. Jungebluth P, Macchiarini P (2011) Stem cell-based therapy and regenerative approaches to diseases of the respiratory system. Br Med Bull 99:169-187
63. Jungebluth P, Alici E, Baiguera S, Le Blanc K, Blomberg P, Bozoky B, Crowley C, Einarsson O, Grinnemo KH, Gudbjartsson T, Le Guyader S, Henriksson G, Hermanson O, Juto JE, Leidner B, Lilja T, Liska J, Luedde T, Lundin V, Moll G, Nilsson B, Roderburg C, Stromblad S, Sutlu T, Teixeira AI, Watz E, Seifalian A, Macchiarini P (2011) Tracheobronchial transplantation with a stemcell-seeded bioartificial nanocomposite: a proof-of-concept study. Lancet 378:1997-2004
64. Karis A, Pata I, van Doorninck JH, Grosveld F, de Zeeuw CI, de Caprona D, Fritzsch B (2001) Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. J Comp Neurol 429:615-630
65. 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:e4
66. Kim WY, Fritzsch B, Serls A, Bakel LA, Huang EJ, Reichardt LF, Barth DS, Lee JE (2001) NeuroD-null mice are deaf due to a severe loss of the inner ear sensory neurons during development. Development 128:417-426
67. 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 108:3288-3293
68. Kopecky B, Fritzsch B (2011) Regeneration of hair cells: making sense of all the noise. Pharm (Basel) 4:848-879
69. Kopecky B, Santi P, Johnson S, Schmitz H, Fritzsch B (2011) Conditional deletion of N-Myc disrupts neurosensory and non-sensory development of the ear. Dev Dyn 240:1373-1390
70. Kozmik Z, Daube M, Frei E, Norman B, Kos L, Dishaw LJ, Noll M, Piatigorsky J (2003) Role of pax genes in eye evolution. A Cnidarian PaxB gene uniting Pax2 and Pax6 functions. Dev Cell 5:773-785
71. Kruger M, Schmid T, Kruger S, Bober E, Braun T (2006) Functional redundancy of NSCL-1 and NeuroD during development of the petrosal and vestibulocochlear ganglia. Eur J Neurosci 24:1581-1590
72. Laine H, Doetzlhofer A, Mantela J, Ylikoski J, Laiho M, Roussel MF, Segil N, Pirvola U (2007) p19(Ink4d) and p21(Cip1) collaborate to maintain the postmitotic state of auditory hair cells, their codeletion leading to DNA damage and p53-mediated apoptosis. J Neurosci 27:1434-1444
73. Lander AD (2011) Pattern, growth, and control. Cell 144:955-969
74. Lee MP, Yutzey KE (2011) Twist1 directly regulates genes that promote cell proliferation and migration in developing heart valves. PLoS One 6:e29758
75. Li HJ, Ray SK, Singh NK, Johnston B, Leiter AB (2011) Basic helixloop-helix transcription factors and enteroendocrine cell differentiation. Diabetes Obes Metab 13(Suppl 1):5-12
76. Liu Z, Zuo J (2008) Cell cycle regulation in hair cell development and regeneration in the mouse cochlea. Cell Cycle 7:2129-2133
77. Loponen H, Ylikoski J, Albrecht JH, Pirvola U (2011) Restrictions in cell cycle progression of adult vestibular supporting cells in response to ectopic cyclin D1 expression. PLoS One 6:e27360
78. 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
79. Ma Q, Chen Z, del Barco BI, de la Pompa JL, Anderson DJ (1998) neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 20:469-482
80. Ma Q, Anderson DJ, Fritzsch B (2000) Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. J Assoc Res Otolaryngol 1:129-143
81. Mantela J, Jiang Z, Ylikoski J, Fritzsch B, Zacksenhaus E, Pirvola U (2005) The retinoblastoma gene pathway regulates the postmitotic state of hair cells of the mouse inner ear. Development 132:2377-2388
82. Maricich SM, Xia A, Mathes EL, Wang VY, Oghalai JS, Fritzsch B, Zoghbi HY (2009) Atoh1-lineal neurons are required for hearing and for the survival of neurons in the spiral ganglion and brainstem accessory auditory nuclei. J Neurosci 29:11123-11133
83. Matei V, Pauley S, Kaing S, Rowitch D, Beisel KW, Morris K, Feng F, Jones K, Lee J, Fritzsch B (2005) Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Dev Dyn 234:633-650
84. Minoda R, Izumikawa M, Kawamoto K, Zhang H, Raphael Y (2007) Manipulating cell cycle regulation in the mature cochlea. Hear Res 232:44-51
85. Montcouquiol M, Kelley MW (2003) Planar and vertical signals control cellular differentiation and patterning in the mammalian cochlea. J Neurosci 23:9469-9478
86. Nichols DH, Pauley S, Jahan I, Beisel KW, Millen KJ, Fritzsch B (2008) Lmx1a is required for segregation of sensory epithelia and normal ear histogenesis and morphogenesis. Cell Tissue Res 334:339-358
87. Niwa H, Miyazaki J, Smith AG (2000) Quantitative expression of Oct- 3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24:372-376
88. O'Brien EK, Degnan B (2003) Expression of Pax258 in the gastropod statocyst: insights into the antiquity of metazoan geosensory organs. Evol Dev 5:572-578
89. Oesterle EC, Chien WM, Campbell S, Nellimarla P, Fero ML (2011) p27(Kip1) is required to maintain proliferative quiescence in the adult cochlea and pituitary. Cell Cycle 10:1237-1248
90. Ohyama T, Groves AK (2004) Expression of mouse Foxi class genes in early craniofacial development. Dev Dyn 231:640-646
91. Ohyama T, Basch ML, Mishina Y, Lyons KM, Segil N, Groves AK (2011) BMP signaling is necessary for patterning the sensory and nonsensory regions of the developing mammalian cochlea. J Neurosci 30:15044-15051
92. Ono K, Nakagawa T, Kojima K, Matsumoto M, Kawauchi T, Hoshino M, Ito J (2009) Silencing p27 reverses post-mitotic state of supporting cells in neonatal mouse cochleae. Mol Cell Neurosci 42:391-398
93. Oshima K, Shin K, Diensthuber M, Peng AW, Ricci AJ, Heller S (2010) Mechanosensitive hair cell-like cells from embryonic and induced pluripotent stem cells. Cell 141:704-716
94. Ozeki M, Hamajima Y, Feng L, Ondrey FG, Schlentz E, Lin J (2007) Id1 induces the proliferation of cochlear sensory epithelial cells via the nuclear factor-kappaB/cyclin D1 pathway in vitro. J Neurosci Res 85:515-524
95. Pan W, Jin Y, Stanger B, Kiernan AE (2010) Notch signaling is required for the generation of hair cells and supporting cells in the mammalian inner ear. Proc Natl Acad Sci USA 107:15798-15803
96. Pan N, Jahan I, Kersigo J, Kopecky B, Santi P, Johnson S, Schmitz H, Fritzsch B (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 275:66-80
97. Pan N, Jahan I, Kersigo J, Duncan J, Kopecky B, Fritzsch B (2012) A novel Atoh1 'self-terminating' mouse model reveals the necessity of proper Atoh1 expression level and duration for inner ear hair cell differentiation and viability. PLoS One 7:e30358
98. Pang ZP, Yang N, Vierbuchen T, Ostermeier A, Fuentes DR, Yang TQ, Citri A, Sebastiano V, Marro S, Sudhof TC, Wernig M (2011) Induction of human neuronal cells by defined transcription factors. Nature advance online publication
99. Pauley S, Wright TJ, Pirvola U, Ornitz D, Beisel K, Fritzsch B (2003) Expression and function of FGF10 in mammalian inner ear development. Dev Dyn 227:203-215
100. Pauley S, Lai E, Fritzsch B (2006) Foxg1 is required for morphogenesis and histogenesis of the mammalian inner ear. Dev Dyn 235:2470-2482
101. Pelet S, Rudolf F, Nadal-Ribelles M, de Nadal E, Posas F, Peter M (2011) Transient activation of the HOG MAPK pathway regulates bimodal gene expression. Science 332:732-735
102. Peter IS, Davidson EH (2011) Evolution of gene regulatory networks controlling body plan development. Cell 144:970-985
103. Pirvola U, Spencer-Dene B, Xing-Qun L, Kettunen P, Thesleff I, Fritzsch B, Dickson C, Ylikoski J (2000) FGF/FGFR-2(IIIb) signaling is essential for inner ear morphogenesis. J Neurosci 20:6125-6134
104. Puligilla C, Kelley MW (2009) Building the world's best hearing aid; regulation of cell fate in the cochlea. Curr Opin Genet Dev 19:368-373
105. Puligilla C, Feng F, Ishikawa K, Bertuzzi S, Dabdoub A, Griffith AJ, Fritzsch B, Kelley MW (2007) Disruption of fibroblast growth factor receptor 3 signaling results in defects in cellular differentiation, neuronal patterning, and hearing impairment. Dev Dyn 236:1905-1917
106. Quinones HI, Savage TK, Battiste J, Johnson JE (2010) Neurogenin 1 (Neurog1) expression in the ventral neural tube is mediated by a distinct enhancer and preferentially marks ventral interneuron lineages. Dev Biol 340:283-292
107. Raft S, Koundakjian EJ, Quinones H, Jayasena CS, Goodrich LV, Johnson JE, Segil N, Groves AK (2007) Cross-regulation of Ngn1 and Math1 coordinates the production of neurons and sensory hair cells during inner ear development. Development 134:4405-4415
108. Riccomagno MM, Martinu L, Mulheisen M, Wu DK, Epstein DJ (2002) Specification of the mammalian cochlea is dependent on Sonic hedgehog. Genes Dev 16:2365-2378
109. Riccomagno MM, Takada S, Epstein DJ (2005) Wnt-dependent regulation of inner ear morphogenesis is balanced by the opposing and supporting roles of Shh. Genes Dev 19:1612-1623
110. Rocha-Sanchez SM, Scheetz LR, Contreras M, Weston MD, Korte M, McGee J, Walsh EJ (2011) Mature mice lacking Rbl2/p130 gene have supernumerary inner ear hair cells and supporting cells. J Neurosci 31:8883-8893
111. Ronaghi M, Nasr M, Heller S (2012) Concise review: inner ear stem cellsan oxymoron, but why? Stem Cells 30:69-74
112. Rosa A, Brivanlou AH (2011) A regulatory circuitry comprised of miR-302 and the transcription factors OCT4 and NR2F2 regulates human embryonic stem cell differentiation. EMBO J 30:237-248
113. Sajan SA, Warchol ME, Lovett M (2007) Toward a systems biology of mouse inner ear organogenesis: gene expression pathways, patterns and network analysis. Genetics 177:631-653
114. Sajan SA, Rubenstein JL, Warchol ME, Lovett M (2011) Identification of direct downstream targets of Dlx5 during early inner ear development. Hum Mol Genet 20:1262-1273
115. Sansom SN, Griffiths DS, Faedo A, Kleinjan DJ, Ruan Y, Smith J, van Heyningen V, Rubenstein JL, Livesey FJ (2009) The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS Genet 5:e1000511
116. Schuldiner O, Eden A, Ben-Yosef T, Yanuka O, Simchen G, Benvenisty N (1996) ECA39, a conserved gene regulated by c-Myc in mice, is involved in G1/S cell cycle regulation in yeast. Proc Natl Acad Sci USA 93:7143-7148
117. Sebe-Pedros A, de Mendoza A, Lang BF, Degnan BM, Ruiz-Trillo I (2011) Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol Biol Evol 28:1241-1254
118. Seipel K, Yanze N, Schmid V (2004) Developmental and evolutionary aspects of the basic helix-loop-helix transcription factors Atonallike 1 and Achaete-scute homolog 2 in the jellyfish. Dev Biol 269:331-345
119. Seo S, Lim JW, Yellajoshyula D, Chang LW, Kroll KL (2007) Neurogenin and NeuroD direct transcriptional targets and their regulatory enhancers. EMBO J 26:5093-5108
120. Shibata SB, Budenz CL, Bowling SA, Pfingst BE, Raphael Y (2010) Nerve maintenance and regeneration in the damaged cochlea. Hear Res 281:56-64
121. Shroyer NF, Helmrath MA, Wang VY, Antalffy B, Henning SJ, Zoghbi HY (2007) Intestine-specific ablation of mouse atonal homolog 1 (Math1) reveals a role in cellular homeostasis. Gastroenterology 132:2478-2488
122. Simionato E, Ledent V, Richards G, Thomas-Chollier M, Kerner P, Coornaert D, Degnan BM, Vervoort M (2007) Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics. BMC Evol Biol 7:33
123. Simionato E, Kerner P, Dray N, Le Gouar M, Ledent V, Arendt D, Vervoort M (2008) atonal- and achaete-scute-related genes in the annelid Platynereis dumerilii: insights into the evolution of neural basic-Helix-Loop-Helix genes. BMC Evol Biol 8:170
124. Soukup GA, Fritzsch B, Pierce ML, Weston MD, Jahan I, McManus MT, Harfe BD (2009) Residual microRNA expression dictates the extent of inner ear development in conditional Dicer knockout mice. Dev Biol 328:328-341
125. Staecker H, Praetorius M, Brough DE (2011) Development of gene therapy for inner ear disease: using bilateral vestibular hypofunction as a vehicle for translational research. Hear Res 276:44-51
126. Sulg M, Kirjavainen A, Pajusola K, Bueler H, Ylikoski J, Laiho M, Pirvola U (2010) Differential sensitivity of the inner ear sensory cell populations to forced cell cycle re-entry and p53 induction. J Neurochem 112:1513-1526
127. Wagner A (2011) The origins of evolutionary innovations. Oxford University Press, Oxford
128. Wang VY, Hassan BA, Bellen HJ, Zoghbi HY (2002) Drosophila atonal fully rescues the phenotype of Math1 null mice: new functions evolve in new cellular contexts. Curr Biol 12:1611-1616
129. Weber T, Corbett MK, Chow LM, Valentine MB, Baker SJ, Zuo J (2008) Rapid cell-cycle reentry and cell death after acute inactivation of the retinoblastoma gene product in postnatal cochlear hair cells. Proc Natl Acad Sci USA 105:781-785
130. Xiang M, Maklad A, Pirvola U, Fritzsch B (2003) Brn3c null mutant mice show long-term, incomplete retention of some afferent inner ear innervation. BMC Neurosci 4:2
131. Yang S, Yalamanchili HK, Li X, Yao KM, Sham PC, Zhang MQ, Wang J (2011) Correlated evolution of transcription factors and their binding sites. Bioinformatics 27:2972-2978
132. Yang J, Bouvron S, Lv P, Chi F, Yamoah EN (2012) Functional features of trans-differentiated hair cells mediated by atoh1 reveals a primordial mechanism. J Neurosci 32:3712-3725
133. Yoo AS, Sun AX, Li L, Shcheglovitov A, Portmann T, Li Y, Lee-Messer C, Dolmetsch RE, Tsien RW, Crabtree GR (2011) MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476:228-231
134. Young SL, Diolaiti D, Conacci-Sorrell M, Ruiz-Trillo I, Eisenman RN, King N (2011) Premetazoan ancestry of the Myc-Max network. Mol Biol Evol 28:2961-2971
135. Yu Y, Weber T, Yamashita T, Liu Z, Valentine MB, Cox BC, Zuo J (2010) In vivo proliferation of postmitotic cochlear supporting cells by acute ablation of the retinoblastoma protein in neonatal mice. J Neurosci 30:5927-5936
136. Zheng JL, Gao WQ (1997) Analysis of rat vestibular hair cell development and regeneration using calretinin as an early marker. J Neurosci 17:8270-8282
137. Zine A, Aubert A, Qiu J, Therianos S, Guillemot F, Kageyama R, de Ribaupierre F (2001) Hes1 and Hes5 activities are required for the normal development of the hair cells in the mammalian inner ear. J Neurosci 21:4712-4720
138. Zou D, Erickson C, Kim EH, Jin D, Fritzsch B, Xu PX (2008) Eya1 gene dosage critically affects the development of sensory epithelia in the mammalian inner ear. Hum Mol Genet 17:3340-3356