Early Development of the Vertebrate Inner Ear

Anatomical Record

Volumn 295, Issue 11, 2012, Pages 1775-1790

  Magariños, Marta ^a,b,c   Contreras, Julio ^a,b,d   Aburto, María R ^a,b   Varela Nieto, Isabel ^a,b,e  

^a INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^e HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

Author keywords

Apoptosis; Autophagy; Deafness; IGF I; MiRNA; Notch signaling; Otic precursors; SOX2

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE; NEUROGENIN 1; NOTCH RECEPTOR; RAF PROTEIN; SOMATOMEDIN C; TRANSCRIPTION FACTOR SOX2;

APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DIFFERENTIATION; CELL FATE; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TYPE; CORTI ORGAN; GENE INACTIVATION; HAIR CELL; HEARING IMPAIRMENT; INNER EAR; MEMBRANE VESICLE; MULTIPOTENT STEM CELL; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; VERTEBRATE; VESTIBULAR DISORDER;

ANIMALS; CELL DIFFERENTIATION; EAR, INNER; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; SIGNAL TRANSDUCTION; VERTEBRATES;

VERTEBRATA;

EID: 84867901043     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.22575     Document Type: Article

References (172)

1. Aberg MAI, Aberg ND, Palmer TD, Alborn A-M, Carlsson-Skwirut C, Bang P, Rosengren LE, Olsson T, Gage FH, Eriksson PS. 2003. IGF-I has a direct proliferative effect in adult hippocampal progenitor cells. Mol Cell Neurosci 24: 23-40.
2. Aburto MR, Magariños M, Leon Y, Varela-Nieto I, Sánchez-Calderón H. 2012. AKT signaling mediates IGF-I survival actions on otic neural progenitors. PLoS ONE. e 30790.
3. Aburto MR, Sánchez-Calderón H, Hurlé JM, Varela-Nieto I, Magariños M. In press. Early otic development depends on autophagy for apoptotic cell clearance and neural differentiation. Cell Death Di.
4. 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.
5. Alvarez IS, Martín-Partido G, Rodríguez-Gallardo L, González-Ramos C, Navascués J. 1989. Cell proliferation during early development of the chick embryo otic anlage: quantitative comparison of migratory and non-migratory regions of the otic epithelium. J Comp Neurol 290: 278-288.
6. Anniko M. 1983. Cytodifferentiation of cochlear hair cells. Am J Otolaryngol 4: 375-388.
7. Appler JM, Goodrich LV. 2011. Connecting the ear to the brain: Molecular mechanisms of auditory circuit assembly. Prog Neurobiol 93: 488-508.
8. Arsenijevic Y, Weiss S, Schneider B, Aebischer P. 2001. Insulin-like growth factor-I is necessary for neural stem cell proliferation and demonstrates distinct actions of epidermal growth factor and fibroblast growth factor-2. J Neurosci 21: 7194-7202.
9. Bartel DP. 2009. MicroRNAs: Target recognition and regulatory functions. Cell 136: 215-233.
10. 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.
11. Battisti AC, Fekete DM. 2008. Slits and Robos in the developing chicken inner ear. Dev Dyn 237: 476-484.
12. Bell D, Streit A, Gorospe I, Varela-Nieto I, Alsina B, Giraldez F. 2008. Spatial and temporal segregation of auditory and vestibular neurons in the otic placode. Dev Biol 322: 109-120.
13. 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.
14. Bruce LL, Kingsley J, Nichols DH, Fritzsch B. 1997. The development of vestibulocochlear efferents and cochlear afferents in mice. Int J Dev Neurosci 15: 671-692.
15. Brumwell CL, Hossain WA, Morest DK, Bernd P. 2000. Role for basic fibroblast growth factor (FGF-2) in tyrosine kinase (TrkB) expression in the early development and innervation of the auditory receptor: In vitro and in situ studies. Exp Neurol 162: 121-145.
16. Bylund M, Andersson E, Novitch BG, Muhr J. 2003. Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat Neurosci 6: 1162-1168.
17. Camarero G, Leon Y, Gorospe I, De Pablo F, Alsina B, Giraldez F, Varela-Nieto I. 2003. Insulin-like growth factor 1 is required for survival of transit-amplifying neuroblasts and differentiation of otic neurons. Dev Biol 262: 242-253.
18. Camarero G, Villar MA, Contreras J, Fernández-Moreno C, Pichel JG, Avendaño C, Varela-Nieto I. 2002. Cochlear abnormalities in insulin-like growth factor-1 mouse mutants. Hear Res 170: 2-11.
19. Carney PR, Silver J. 1983. Studies on cell migration and axon guidance in the developing distal auditory system of the mouse. J Comp Neurol 215: 359-369.
20. Cediel R, Riquelme R, Contreras J, Díaz A, Varela-Nieto I. 2006. Sensorineural hearing loss in insulin-like growth factor I-null mice: A new model of human deafness. Eur J Neurosci 23: 587-590.
21. Chae JH, Stein GH, Lee JE. 2004. NeuroD: The predicted and the surprising. Mol Cells 18: 271-288.
22. Chambard J-C, Lefloch R, Pouysségur J, Lenormand P. 2007. ERK implication in cell cycle regulation. Biochim Biophys Acta 1773: 1299-1310.
23. Chang Q, Tang W, Ahmad S, Zhou B, Lin X. 2008. Gap junction mediated intercellular metabolite transfer in the cochlea is compromised in connexin30 null mice. PLoS ONE 3: e4088.
24. Chang W, ten Dijke P, Wu DK. 2002. BMP pathways are involved in otic capsule formation and epithelial-mesenchymal signaling in the developing chicken inner ear. Dev Biol 251: 380-394.
25. Chatterjee S, Kraus P, Lufkin T. 2010. A symphony of inner ear developmental control genes. BMC Genetics 11: 68.
26. 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.
27. Cohen-Salmon M, Regnault B, Cayet N, Caille D, Demuth K, Hardelin JP, Janel N, Meda P, Petit C. 2007. Connexin30 deficiency causes instrastrial fluid-blood barrier disruption within the cochlear stria vascularis. Proc Natl Acad Sci USA 104: 6229-6234.
28. Cole LK, Le Roux I, Nunes F, Laufer E, Lewis J, Wu DK. 2000. Sensory organ generation in the chicken inner ear: Contributions of bone morphogenetic protein 4, serrate1, and lunatic fringe. J Comp Neurol 424: 509-520.
29. D'Amico-Martel A, Noden DM. 1983. Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. Am J Anat 166: 445-468.
30. Dabdoub A, Puligilla C, Jones JM, Fritzsch B, Cheah KSE, 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.
31. Darnell DK, Kaur S, Stanislaw S, Konieczka JH, Yatskievych TA, Antin PB. 2006. MicroRNA expression during chick embryo development. Dev Dyn 235: 3156-3165.
32. Daudet N, Lewis J. 2005. Two contrasting roles for Notch activity in chick inner ear development: Specification of prosensory patches and lateral inhibition of hair-cell differentiation. Development 132: 541-551.
33. Davies D. 2007. Temporal and spatial regulation of alpha6 integrin expression during the development of the cochlear-vestibular ganglion J Comp Neurol 502: 673-682.
34. Davies D. 2011. Cell-extracellular matrix versus cell-cell interactions during the development of the cochlear-vestibular ganglion. J Neurosci Res 89: 1375-1387.
35. 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.
36. Driver EC, Kelley MK. 2009. Specification of cell fate in the mammalian cochlea. Birth Defects Res C Embryo Today 87: 212-221.
37. Eddison M, Le Roux I, Lewis J. 2000. Notch signaling in the development of the inner ear: Lessons from Drosophila. Proc Natl Acad Sci USA 97: 11692-11699.
38. Eisen MD, Ryugo DK. 2007. Hearing molecules: Contributions from genetic deafness. Cell Mol Life Sci 64: 566-580.
39. Ekker M, Akimenko MA, Bremiller R, Westerfield M. 1992. Regional expression of three homeobox transcripts in the inner ear of zebrafish embryos. Neuron 9: 27-35.
40. Fantetti KN, Fekete DM. 2011. Members of the BMP, Shh and FGF morphogen families promote chicken statoacoustic ganglion neurite outgrowth and neuron survival in vitro. Dev Neurobiol 72: 1213-1228.
41. Fariñas I, Jones KR, Tessarollo L, Vigers AJ, Huang E, Kirstein M, de Caprona DC, Coppola V, Backus C, Reichardt LF, Fritzsch B. 2001a. Spatial shaping of cochlear innervation by temporally regulated neurotrophin expression. J Neurosci 21: 6170-6180.
42. Fariñas I, Jones KR, Tessarollo L, Vigers AJ, Huang E, Kirstein M, de Caprona DC, Coppola V, Backus C, Reichardt LF, Fritzsch B. 2001b. Spatial shaping of cochlear innervation by temporally regulated neurotrophin expression. J Neurosci 21: 6170-6180.
43. Fekete DM, Campero AM. 2007. Axon guidance in the inner ear. Int J Dev Biol 51: 549-556.
44. Fetoni AR, Picciotti PM, Paludetti G, Troiani D. 2011. Pathogenesis of presbycusis in animal models: A review. Exp Gerontol 46: 413-425.
45. Forge A, Wright T. 2002. The molecular architecture of the inner ear. BMB 63: 5-24.
46. Frago LM, Cañón S, de la Rosa EJ, León Y, Varela-Nieto I. 2003. Programmed cell death in the developing inner ear is balanced by nerve growth factor and insulin-like growth factor I. J Cell Sci 116: 475-486.
47. Frago LM, León Y, de la Rosa EJ, Gómez-Muñoz A, Varela-Nieto I. 1998. Nerve growth factor and ceramides modulate cell death in the early developing inner ear. J Cell Sci 111 ( Pt 5): 549-556.
48. Friedman LM, Dror AA, Mor E, Tenne T, Toren G, Satoh T, Biesemeier DJ, Shomron N, Fekete DM, Hornstein E, Avraham KB. 2009. MicroRNAs are essential for development and function of inner ear hair cells in vertebrates. Proc Natl Acad Sci USA 106: 7915-7920.
49. 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.
50. 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.
51. Fritzsch B, Tessarollo L, Coppola E, Reichardt LF. 2004. Neurotrophins in the ear: Their roles in sensory neuron survival and fiber guidance. Prog Brain Res 146: 265-278.
52. Glick D, Barth S, Macleod KF. 2010. Autophagy: Cellular and molecular mechanisms. J Pathol 221: 3-12.
53. Goldberg JM. 1991. The vestibular end organs: morphological and physiological diversity of afferents. Curr Opin Neurobiol 1: 229-235.
54. Graham V, Khudyakov J, Ellis P, Pevny L. 2003. SOX2 functions to maintain neural progenitor identity. Neuron 39: 749-765.
55. Groves AK, Bronner-Fraser M. 2000. Competence, specification and commitment in otic placode induction. Development 127: 3489-3499.
56. Haddon C, Lewis J. 1996. Early ear development in the embryo of the zebrafish, Danio rerio. J Comp Neurol 365: 113-128.
57. Hartman BH, Hayashi T, Nelson BR, Bermingham-McDonogh O, Reh TA. 2007. Dll3 is expressed in developing hair cells in the mammalian cochlea. Dev Dyn 236: 2875-2883.
58. Hartman BH, Reh TA, Bermingham-McDonogh O. 2010. Notch signaling specifies prosensory domains via lateral induction in the developing mammalian inner ear. Proc Natl Acad Sci USA 107: 15792-15797.
59. Hayashi T, Kokubo H, Hartman BH, Ray CA, Reh TA, Bermingham-McDonogh O. 2008. Hesr1 and Hesr2 may act as early effectors of Notch signaling in the developing cochlea. Dev Biol 316: 87-99.
60. Hemond SG, Morest DK. 1991. Ganglion formation from the otic placode and the otic crest in the chick embryo: Mitosis, migration, and the basal lamina. Anat Embryol 184: 1-13.
61. Highstein SM, Fay RR. 2004. The vestibular system. Springer handbook of auditory research. Vol. 19. New York: Springer.
62. Hobert O, Westphal H. 2000. Functions of LIM-homeobox genes. Trends Genet 16: 75-83.
63. Hodge RD, D'Ercole AJ, O'Kusky JR. 2004. Insulin-like growth factor-I accelerates the cell cycle by decreasing G1 phase length and increases cell cycle reentry in the embryonic cerebral cortex. J Neurosci 24: 10201-10210.
64. Hudspeth AJ. 2008. Making an effort to listen: Mechanical amplification in the ear. Neuron 59: 530-545.
65. Jin Z, Mannströn P, Järlebark L, Ulfendahl M. 2007. Malformation of stria vascularis in the developing inner ear of the German waltzing guinea pig. Cell Tissue Res 328: 257-270.
66. Jin Z, Ulfendahl M, Järlebark L. 2008. Spatiotemporal loss of K+ transport proteins in the developing cochlear lateral wall of guinea pigs with hereditary deafness. Eur J Neurosci 27: 145-154.
67. Jones JM, Montcouquiol M, Dabdoub A, Woods C, Kelley MW. 2006. Inhibitors of differentiation and DNA binding (Ids) regulate Math1 and hair cell formation during the development of the organ of Corti. J Neurosci 26: 550-558.
68. Kawamoto K, Ishimoto S-I, Minoda R, Brough DE, Raphael Y. 2003. Math1 gene transfer generates new cochlear hair cells in mature guinea pigs in vivo. J Neurosci 23: 4395-4400.
69. Kelley MW. 2006. Regulation of cell fate in the sensory epithelia of the inner ear. Nat Rev Neurosci 7: 837-849.
70. Kelley MW. 2007. Cellular commitment and differentiation in the organ of Corti. Int J Dev Biol 51: 571-583.
71. Kelly MC, Chen P. 2009. Development of form and function in the mammalian cochlea. Curr Opin Neurobiol 19: 395-401.
72. Kiernan AE, Pelling AL, Leung KKH, Tang ASP, Bell DM, Tease C, Lovell-Badge R, Steel KP, Cheah KS. 2005. Sox2 is required for sensory organ development in the mammalian inner ear. Nature 434: 1031-1035.
73. 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.
74. Kimura RS. 1975. The ultrastructure of the organ of Corti. Int Rev Cytol 42: 173-222.
75. Kloosterman WP, Plasterk RHA. 2006. The diverse functions of microRNAs in animal development and disease. Dev Cell 11: 441-450.
76. Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, Waguri S, Kawahara N, Kuida K, Nagata S, Kominami E, Tanaka K, Uchiyama Y. 2008. Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 172: 454-469.
77. Kong D, Yamori T. 2008. Phosphatidylinositol 3-kinase inhibitors: Promising drug candidates for cancer therapy. Cancer Sci 99: 1734-1740.
78. Koundakjian EJ, Appler JL, Goodrich LV. 2007. Auditory neurons make stereotyped wiring decisions before maturation of their targets. J Neurosci 27: 14078-14088.
79. Kwan T, White PM, Segil N. 2009. Development and regeneration of the inner ear. Ann N Y Acad Sci 1170: 28-33.
80. Lanford PJ, Lan Y, Jiang R, Lindsell C, Weinmaster G, Gridley T, Kelley MK. 1999. Notch signalling pathway mediates hair cell development in mammalian cochlea. Nat Genet 21: 289-292.
81. Lanford PJ, Shailam R, Norton CR, Gridley T, Kelley MW. 2000. Expression of Math1 and HES5 in the cochleae of wildtype and Jag2 mutant mice. J Assoc Res Otolaryngol 1: 161-171.
82. Lang H, Bever MM, Fekete DM. 2000. Cell proliferation and cell death in the developing chick inner ear: Spatial and temporal patterns. J Comp Neurol 417: 205-220.
83. Laviola L, Natalicchio A, Perrini S, Giorgino F. 2008. Abnormalities of IGF-I signaling in the pathogenesis of diseases of the bone, brain, and fetoplacental unit in humans. Am J Physiol Endocrinol Metab 295: E991-999.
84. Lefebvre PP, Van de Water TR. 2000. Connexins, hearing and deafness: Clinical aspects of mutations in the connexin 26 gene. Brain Res 32: 159-162.
85. Léger S, Brand M. 2002. Fgf8 and Fgf3 are required for zebrafish ear placode induction, maintenance and inner ear patterning. Mech Dev 119: 91-108.
86. León Y, Sánchez-Galiano S, Gorospe I. 2004. Programmed cell death in the development of the vertebrate inner ear. Apoptosis 9: 255-264.
87. LeRoith D, Werner H, Beitner-Johnson D, Roberts CT, Jr. 1995. Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr Rev 16: 143-163.
88. Levine B, Klionsky DJ. 2004. Development by self-digestion: Molecular mechanisms and biological functions of autophagy. Dev Cell 6: 463-477.
89. Lewis MA, Quint E, Glazier AM, Fuchs H, De Angelis MH, Langford C, van Dongen S, Abreu-Goodger C, Piipari M, Redshaw N, Dalmay T, Moreno-Pelayo MA, Enright AJ, Steel KP. 2009. An ENU-induced mutation of miR-96 associated with progressive hearing loss in mice. Nat Genet 41: 614-618.
90. Lewis MA, Steel KP. 2010. MicroRNAs in mouse development and disease. Semin Cell Dev Biol 21: 774-780.
91. Li H, Corrales CE, Wang Z, Zhao Y, Wang Y, Liu H, Heller S. 2005. BMP4 signaling is involved in the generation of inner ear sensory epithelia. BMC Dev Biol 5: 16.
92. Li H, Costantini C, Scrable H, Weindruch R, Puglielli L. 2009. Egr-1 and Hipk2 are required for the TrkA to p75(NTR) switch that occurs downstream of IGF-1-R. Neurobiol Aging. 30: 2010-2020.
93. Li H, Fekete DM. 2010. MicroRNAs in hair cell development and deafness. Curr Opin Otolaryngol Head Neck Surg 18: 459-465.
94. Li H, Liu H, Sage C, Huang M, Chen Z, Heller S. 2004. Islet-1 expression in the developing chicken inner ear. J Comp Neurol 477: 1-10.
95. Li S, Mark S, Radde-Gallwitz K, Schlisner R, Chin MT, Chen P. 2008. Hey2 functions in parallel with Hes1 and Hes5 for mammalian auditory sensory organ development. BMC Dev Biol 8: 20.
96. Liu D, Chu H, Maves L, Yan YL, Morcos PA, Postlethwait JH, Westerfield M. 2003. Fgf3 and Fgf8 dependent and independent transcription factors are required for otic placode specification. Development 130: 2213-2224.
97. Liu XZ, Yan D. 2007. Ageing and hearing loss. J Pathol 211: 188-197.
98. 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.
99. Magariños M, Aburto MR, Sánchez-Calderón H, Muñoz-Agudo C, Rapp UR, Varela-Nieto I. 2010. RAF kinase activity regulates neuroepithelial cell proliferation and neuronal progenitor cell differentiation during early inner ear development. PLoS ONE 5: e14435.
100. Mairet-Coello G, Tury A, DiCicco-Bloom E. 2009. Insulin-like growth factor-1 promotes G(1)/S cell cycle progression through bidirectional regulation of cyclins and cyclin-dependent kinase inhibitors via the phosphatidylinositol 3-kinase/Akt pathway in developing rat cerebral cortex. J Neurosci 29: 775-788.
101. Mariño G, Fernández AF, Cabrera S, Lundberg YW, Cabanillas R, Rodríguez F, Salvador-Montoliu N, Vega JA, Germanà A, Fueyo A, Freije JM, López-Otín C. 2010. Autophagy is essential for mouse sense of balance. J Clin Invest 120: 2331-2344.
102. Maroon H, Walshe J, Mahmood R, Kiefer P, Dickson C, Mason I. 2002. Fgf3 and Fgf8 are required together for formation of the otic placode and vesicle. Development 129: 2099-2108.
103. Mencía A, Modamio-Høybjør S, Redshaw N, Morín M, Mayo-Merino F, Olavarrieta L, Aguirre LA, del Castillo I, Steel KP, Dalmay T, Moreno F, Moreno-Pelayo MA. 2009. Mutations in the seed region of human miR-96 are responsible for nonsyndromic progressive hearing loss. Nat Genet 41: 609-613.
104. Millimaki BB, Sweet EM, Dhason MS, Riley BB. 2007. Zebrafish atoh1 genes: Classic proneural activity in the inner ear and regulation by Fgf and Notch. Development 134: 295-305.
105. Millimaki BB, Sweet EM, Riley BB. 2010. Sox2 is required for maintenance and regeneration, but not initial development, of hair cells in the zebrafish inner ear. Dev Biol 338: 262-269.
106. Mizushima N, Levine B. 2010. Autophagy in mammalian development and differentiation. Nat Cell Biol 12: 823-830.
107. Moelling K, Schad K, Bosse M, Zimmermann S, Schweneker M. 2002. Regulation of Raf-Akt Cross-talk. J Biol Chem 277: 31099-31106.
108. Montero JA, Hurlé JM. 2010. Sculpturing digit shape by cell death. Apoptosis 15: 365-375.
109. Morrison A, Hodgetts C, Gossler A, Hrabé de Angelis M, Lewis J. 1999. Expression of Delta1 and Serrate1 (Jagged1) in the mouse inner ear. Mech Dev 84: 169-172.
110. Murata J, Tokunaga A, Okano H, Kubo T. 2006. Mapping of notch activation during cochlear development in mice: Implications for determination of prosensory domain and cell fate diversification. J Comp Neurol 497: 502-518.
111. Murillo-Cuesta S, Camarero G, González-Rodríguez A, Rodríguez-de la Rosa L, Burks DJ, Avendaño C, Valverde A, Varela-Nieto I. 2012. IRS2-deficient mice show sensorineural hearing loss before the onset of diabetes that is delayed by concomitant PTP1B loss of function. Mol Med 18: 260-269.
112. Murillo-Cuesta S, Contreras J, Zurita E, Cediel R, Cantero R, Varela-Nieto I, Montoliu L. 2010. Melanin precursors prevent premature age-related and noise-induced hearing loss in albino mice. Pigment Cell Melanoma Res 23: 72-83.
113. Murillo-Cuesta S, Rodríguez-de la Rosa L, Cediel R, Lassaletta L, Varela-Nieto I. 2011. The role of insulin-like growth factor-I in the physiopathology of hearing. Front Mol Neurosci 4: 11.
114. Nayagam BA, Muniak MA, Ryugo DK. 2011. The spiral ganglion: Connecting the peripheral and central auditory systems. Hear Res 278: 2-20.
115. Neves J, Kamaid A, Alsina B, Giraldez F. 2007. Differential expression of Sox2 and Sox3 in neuronal and sensory progenitors of the developing inner ear of the chick. J Comp Neurol 503: 487-500.
116. Nicholl AJ, Kneebone A, Davies D, Cacciabue-Rivolta DI, Rivolta MN, Coffey P, Holley MC. 2005. Differentiation of an auditory neuronal cell line suitable for cell transplantation. Eur J Neurosci 22: 343-353.
117. Norton JD. 2000. ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J Cell Sci 113 ( Pt 22): 3897-3905.
118. Ogura K-I, Goshima Y. 2006. The autophagy-related kinase UNC-51 and its binding partner UNC-14 regulate the subcellular localization of the Netrin receptor UNC-5 in Caenorhabditis elegans. Development 133: 3441-3450.
119. Oh SH, Johnson R, Wu DK. 1996. Differential expression of bone morphogenetic proteins in the developing vestibular and auditory sensory organs. J Neurosci 16: 6463-6475.
120. Patuzzi R. 2011. Ion flow in stria vascularis and the production and regulation of cochlear endolymph and the endolymphatic potential. Hear Res 277: 4-19.
121. Perron M, Opdecamp K, Butler K, Harris WA, Bellefroid EJ. 1999. X-ngnr-1 and Xath3 promote ectopic expression of sensory neuron markers in the neurula ectoderm and have distinct inducing properties in the retina. Proc Natl Acad Sci USA 96: 14996-15001.
122. Pierce ML, Weston MD, Fritzsch B, Gabel HW, Ruvkun G, Soukup GA. 2008. MicroRNA-183 family conservation and ciliated neurosensory organ expression. Evol Dev 10: 106-113.
123. Pirvola U, Hallböök F, Xing-Qun L, Virkkala J, Saarma M, Ylikoski J. 1997. Expression of neurotrophins and Trk receptors in the developing, adult, and regenerating avian cochlea. J Neurobiol 33: 1019-1033.
124. Pirvola U, Ylikoski J, Trokovic R, Hébert JM, McConnell SK, Partanen J. 2002. FGFR1 is required for the development of the auditory sensory epithelium. Neuron 35: 671-680.
125. Plowey ED, Cherra SJ, III, Liu Y-J, Chu CT. 2008. Role of autophagy in G2019S-LRRK2-associated neurite shortening in differentiated SH-SY5Y cells. J Neurochem 105: 1048-1056.
126. Pujades C, Kamaid A, Alsina B, Giraldez F. 2006. BMP-signaling regulates the generation of hair-cells. Dev Biol 292: 55-67.
127. Puligilla C, Dabdoub A, Brenowitz SD, Kelley MW. 2010. Sox2 induces neuronal formation in the developing mammalian cochlea. J Neurosci 30: 714-722.
128. Qu X, Zou Z, Sun Q, Luby-Phelps K, Cheng P, Hogan RN, Gilpin C, Levine B. 2007. Autophagy gene-dependent clearance of apoptotic cells during embryonic development. Cell 128: 931-946.
129. 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.
130. Raphael Y, Altschuler RA. 2003. Structure and innervation of the cochlea. Brain Res Bull 60: 397-422.
131. Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, Massey DC, Menzies FM, Moreau K, Narayanan U, Renna M, Siddiqi FH, Underwood BR, Winslow AR, Rubinsztein DC. 2010. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 90: 1383-1435.
132. Raviv D, Dror AA, Avraham KB. 2010. Hearing loss: A common disorder caused by many rare alleles. Ann N Y Acad Sci 1214: 168-179.
133. Rex M, Orme A, Uwanogho D, Tointon K, Wigmore PM, Sharpe PT, Scotting PJ. 1997. Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue. Dev Dyn 209: 323-332.
134. Riquelme R, Cediel R, Contreras J, la Rosa Lourdes R-de, Murillo-Cuesta S, Hernàndez-Sànchez C, Zubeldia JM, Cerdan S, Varela-Nieto I. 2010. A comparative study of age-related hearing loss in wild type and insulin-like growth factor I deficient mice. Front Neuroanat 4: 27.
135. Rodríguez-Muela N, Germain F, Mariño G, Fitze PS, Boya P. 2012. Autophagy promotes survival of retinal ganglion cells after optic nerve axotomy in mice. Cell Death Differ 19: 162-169.
136. Rubel EW, Fritzsch B. 2002. Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci 25: 51-101.
137. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ. 2007. Potential therapeutic applications of autophagy. Nat Rev Drug Discov 6: 304-312.
138. Sacheli R, Nguyen L, Borgs L, Vandenbosch R, Bodson M, Lefebvre P, Malgrange B. 2009. Expression patterns of miR-96, miR-182 and miR-183 in the development inner ear. Gene Expr Patterns 9: 364-370.
139. Sanchez-Calderon H, Milo M, Leon Y, Varela-Nieto I. 2007. A network of growth and transcription factors controls neuronal differentation and survival in the developing ear. Int J Dev Biol 51: 557-570.
140. Sanchez-Calderon H, Rodriguez-de la Rosa L, Milo M, Pichel JG, Holley M, Varela-Nieto I. 2010. RNA microarray analysis in prenatal mouse cochlea reveals novel IGF-I target genes: Implication of MEF2 and FOXM1 transcription factors. PLoS ONE 5: e8699.
141. Santi P, Tsuprun V. 2001. Cochlear microanatomy and ultrastructure. In: Physiology of the Ear. Jahn, AF, Santos-Sacchi J, editors. San Diego, CA: Singular Publishing. p 256-283.
142. Sanz C, León Y, Troppmair J, Rapp UR, Varela-Nieto I. 1999. Strict regulation of c-Raf kinase levels is required for early organogenesis of the vertebrate inner ear. Oncogene 18: 429-437.
143. Satoh T, Fekete DM. 2005. Clonal analysis of the relationships between mechanosensory cells and the neurons that innervate them in the chicken ear. Development 132: 1687-1697.
144. Schimmang T. 2007. Expression and functions of FGF ligands during early otic development. Int J Dev Biol 51: 473-481.
145. Schreck R, Rapp UR. 2006. Raf kinases: Oncogenesis and drug discovery. Int J Cancer 119: 2261-2271.
146. Solomon KS, Fritz A. 2002. Concerted action of two dlx paralogs in sensory placode formation. Development 129: 3127-3136.
147. Soukup GA. 2009. Little but loud: small RNAs have a resounding affect on ear development. Brain Res 1277: 104-114.
148. 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.
149. Streit A. 2007. The preplacodal region: an ectodermal domain with multipotential progenitors that contribute to sense organs and cranial sensory ganglia. Int J Dev Biol 51: 447-461.
150. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
151. Takeuchi S, Ando M, Kakigi A. 2000. Mechanism generating endocochlear potential: Role played by intermediate cells in stria vascularis. Biophys J 79: 2572-2582.
152. Taylor RR, Nevill G, Forge A. 2008. Rapid hair cell loss: A mouse model for cochlear lesions. J Assoc Res Otolaryngol 9: 44-64.
153. Varela-Nieto I, de la Rosa EJ, Valenciano AI, León Y. 2003. Cell death in the nervous system: Lessons from insulin and insulin-like growth factors. Mol Neurobiol 28: 23-50.
154. Varela-Nieto I, Morales-Garcia JA, Vigil P, Diaz-Casares A, Gorospe I, Sánchez-Galiano S, Cañon S, Camarero G, Contreras J, Cediel R, Leon Y. 2004. Trophic effects of insulin-like growth factor-I (IGF-I) in the inner ear. Hear Res 196: 19-25.
155. Walenkamp MJE, Wit JM. 2006. Genetic disorders in the growth hormone-insulin-like growth factor-I axis. Horm Res 66: 221-230.
156. Wangemann P. 2006. Supporting sensory transduction: Cochlear fluid homeostasis and the endocochlear potential. J Physiol 576: 11-21.
157. Webber A, Raz Y. 2006. Axon guidance cues in auditory development. Anat Rec A Discov Mol Cell Evol Biol 288: 390-396.
158. Webster DB, Popper AN, Fay RR. 1992. The mammalian auditory pathway: Neuroanatomy. Springer handbook of auditory research. Vol 1. New York: Springer.
159. Wegner M, Stolt CC. 2005. From stem cells to neurons and glia: A Soxist's view of neural development. Trends Neurosci 28: 583-588.
160. Wei D, Jin Z, Järlebark L, Scarfone E, Ulfendahl M. 2007. Survival, synaptogenesis, and regeneration of adult mouse spiral ganglion neurons in vitro. Dev Neurobiol 67: 108-122.
161. Weston MD, Pierce ML, Rocha-Sanchez S, Beisel KW, Soukup GA. 2006. MicroRNA gene expression in the mouse inner ear. Brain Res 1111: 95-104.
162. Whitehead MC, Morest DK. 1985. The development of innervation patterns in the avian cochlea. Neuroscience 14: 255-276.
163. Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E, de Bruijn E, Horvitz HR, Kauppinen S, Plasterk RH. 2005. MicroRNA expression in zebrafish embryonic development. Science 309: 310-311.
164. Woods C, Montcouquiol M, Kelley MW. 2004. Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat Neurosci 7: 1310-1318.
165. Wright TJ, Mansour SL. 2003. FGF signaling in ear development and innervation. Curr Top Dev Biol 57: 225-259.
166. Wu DK, Oh SH. 1996. Sensory organ generation in the chick inner ear. J Neurosci 16: 6454-6462.
167. Yang Y, Fukui K, Koike T, Zheng X. 2007. Induction of autophagy in neurite degeneration of mouse superior cervical ganglion neurons. Eur J Neurosci 26: 2979-2988.
168. Ye P, D'Ercole AJ. 2006. Insulin-like growth factor actions during development of neural stem cells and progenitors in the central nervous system. J Neurosci Res 83: 1-6.
169. Zheng JL, Gao WQ. 2000. Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat Neurosci 3: 580-586.
170. Zheng JL, Shou J, Guillemot F, Kageyama R, Gao WQ. 2000. Hes1 is a negative regulator of inner ear hair cell differentiation. Development 127: 4551-4560.
171. Zhong J, Li X, McNamee C, Chen AP, Baccarini M, Snider WD. 2007. Raf kinase signaling functions in sensory neuron differentiation and axon growth in vivo. Nat Neurosci 10: 598-607.
172. 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.