Hair Cell Regeneration: Mechanisms Guiding Cellular Proliferation and Differentiation

  • Elizabeth C. Oesterle
  • Jennifer S. Stone
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 33)


Hair Cell Sensory Epithelium Hair Cell Loss Basilar Papilla Hair Cell Regeneration 


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  1. Aberg MAI, Aberg ND, Palmer TD, Alborn A-M, Carlsson-Skwirut C, Bang P, Rosengren LE, Olsson T, Gage FH, Ericksson PS (2003) IGF-1 has a direct proliferative effect in adult hippocampal progenitor cells. Mol Cell Neurosci. 24:23–40.PubMedGoogle Scholar
  2. 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.PubMedGoogle Scholar
  3. Adler HJ, Raphael Y (1996) New hair cells arise from supporting cell conversion in the acoustically damaged chick inner ear. Neurosci Lett 205:17–20.PubMedGoogle Scholar
  4. Adler HJ, Saunders JC (1995) Hair cell replacement in the avian inner ear following two exposures to intense sound. J Neurocytol 24:111–116.PubMedGoogle Scholar
  5. Artavanis-Tsakonas S, Simpson P (1991) Choosing a cell fate: a view from the Notch locus. Trends Genet 7:403–408.PubMedGoogle Scholar
  6. Avallone B, Balsamo G, Trapani S, Marmo F (2002) Apoptosis during chick inner ear development: some observations by TEM and TUNEL techniques. Eur J Histochem 46:53–59.PubMedGoogle Scholar
  7. Avallone B, Porritiello M, Esposito D, Mutone R, Balsamo G, Marmo F (2003) Evidence for hair cell regeneration in the crista ampullaris of the lizard Podarcis sicula. Hear Res 178:79–88.PubMedGoogle Scholar
  8. Baird RA, Torres MA, Schuff NR (1993) Hair cell regeneration in the bullfrog vestibular otolith organs following aminoglycoside toxicity. Hear Res 65:164–174.PubMedGoogle Scholar
  9. Baird RA, Steyger PS, Schuff N (1996) Mitotic and nonmitotic hair cell regeneration in the bullfrog vestibular otolith organs. Ann NY Acad Sci 781:59–70.PubMedGoogle Scholar
  10. Baird RA, Burton MD, Fashena DS, Naeger RA (2000) Hair cell recovery in mitotically blocked cultures of the bullfrog saccule. Proc Natl Acad Sci USA 97:11722–11729.PubMedGoogle Scholar
  11. Balak KJ, Corwin JT, Jones JE (1990) Regenerated hair cells can originate from supporting cell progeny: evidence from phototoxicity and laser ablation experiments in the lateral line system. J Neurosci 10:2502–2512.PubMedGoogle Scholar
  12. Barald KF, Kelley MW (2004) From placode to polarization: new tunes in inner ear development. Development 131:4119–4130.PubMedGoogle Scholar
  13. Bartolami S, Goodyear R, Richardson G (1991) Appearance and distribution of the 275 kD hair-cell antigen during development of the avian inner ear. J Comp Neurol 314:777–788.PubMedGoogle Scholar
  14. Beites CL, Kawauchi S, Crocker CE, Calof AL (2005) Identification and molecular regulation of neural stem cells in the olfactory epithelium. Exp Cell Res 306:309–316.PubMedGoogle Scholar
  15. Ben-Arie N, McCall AE, Berkman S, Eichele G, Bellen HJ, Zoghbi HY (1996) Evolutionary conservation of sequence and expression of the bHLH protein Atonal suggests a conserved role in neurogenesis. Hum Mol Genet 5:1207–1216.PubMedGoogle Scholar
  16. Ben-Arie N, Hassan BA, Bermingham NA, Malicki DM, Armstrong D, Matzuk M, Bellen HJ, Zoghbi HY (2000) Functional conservation of atonal and Math1 in the CNS and PNS. Development 127:1039–1048.PubMedGoogle Scholar
  17. 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.PubMedGoogle Scholar
  18. Bermingham-McDonogh O, Stone JS, Reh TA, Rubel EW (2001) FGFR3 expression during development and regeneration of the chick inner ear sensory epithelia. Dev Biol 238:247–259.PubMedGoogle Scholar
  19. Bertrand N, Castro DS, Guillemot F (2002) Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3:517–530.PubMedGoogle Scholar
  20. Bever MM, Fekete DM (1999) Ventromedial focus of cell death is absent during develop- ment of Xenopus and zebrafish inner ears. J Neurocytol 28:781–793.PubMedGoogle Scholar
  21. Bhave SA, Stone JS, Rubel EW, Coltrera MD (1995) Cell cycle progression in gentamicin-damaged avian cochleas. J Neurosci 15:4618–4628.PubMedGoogle Scholar
  22. Bhave SA, Oesterle EC, Coltrera MD (1998) Macrophage and microglia-like cells in the avian inner ear. J Comp Neurol 398:241–256.PubMedGoogle Scholar
  23. Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E (2004) Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118:635–648.PubMedGoogle Scholar
  24. Bohne B (1971) Scar Formation in the Inner Ear Following Acoustic Injury: Sequence of Changes from Early Signs of Damage to Healed Lesion. Ph. D. Thesis. St. Louis, MO: Washington University.Google Scholar
  25. Bone RC, Ryan AF (1978) Audiometric and histologic correlates of the interaction between kanamycin and subtraumatic levels of noise in the chinchilla. Otolaryngology 86: ORL400–4.PubMedGoogle Scholar
  26. Brooker R, Hozumi K, Lewis J (2006) Notch ligands with contrasting functions: Jagged1 and Delta1 in the mouse inner ear. Development 133:1277–1286.PubMedGoogle Scholar
  27. Brown JN, Miller JM, Altschuler RA, Nuttall AL (1993) Osmotic pump implant for chronic infusion of drugs into the inner ear. Hear Res 70:167–172.PubMedGoogle Scholar
  28. Bryant J, Goodyear RJ, Richardson GP (2002) Sensory organ development in the inner ear: molecular and cellular mechanisms. Br Med Bull 63:39–57.PubMedGoogle Scholar
  29. Cafaro J, Lee GS, Stone JS (2007) Atoh1 expression defines activated progenitors and differentiating hair cells during avian hair cell regeneration. Dev Dyn. 236 (1):156–170.PubMedGoogle Scholar
  30. Calof AL, Chikaraishi DM (1989) Analysis of neurogenesis in a mammalian neuroepithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron 3:115–127.PubMedGoogle Scholar
  31. Camarero G, Avendano C, Fernandez-Moreno C, Villar A, Contreras J, de Pable F, Pichel JG, Varela-Nieto I (2001) Delayed inner ear maturation and neuronal loss in postnatal Igf-1–deficient mice. J Neurosci 21:7630–7641.PubMedGoogle Scholar
  32. Cantos R, Cole LK, Acampora D, Simeone A, Wu DK (2000) Patterning of the mammalian cochlea. Proc Natl Acad Sci USA 97:11707–11713.PubMedGoogle Scholar
  33. Carnicero E, Garrido JJ, Alonso MT, Schimmang T (2001) Roles of fibroblast growth factor 2 during innervation of the avian inner ear. J Neurochem 77:786–795.PubMedGoogle Scholar
  34. Carnicero E, Zelarayan LC, Rüttiger L, Knipper M, Alvarez Y, Alonso MT, Schimmang T (2004) Differential roles of fibroblast growth factor-2 during development and maintenance of auditory sensory epithelial. J Neurosci Res 77:787–797.PubMedGoogle Scholar
  35. Chardin S, Romand R (1995) Regeneration and mammalian auditory hair cells. Science 267:707–711.PubMedGoogle Scholar
  36. Chen P, Segil N (1999) p27Kip1 links cell proliferation to morphogenesis in the developing organ of Corti. Development 126: 1581–1590.PubMedGoogle Scholar
  37. Chen ZY, Corey DP (2002) Understanding inner ear development with gene expression profiling. J Neurobiol. 5:276–285.Google Scholar
  38. 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.PubMedGoogle Scholar
  39. Chen P, Zindy F, Abdala C, Liu F, Li X, Roussel MF, Segil N (2003) Progressive hearing loss in mice lacking the cyclin-dependent kinase inhibitor Ink4d. Nature 5:422–426.Google Scholar
  40. Cho Y, Gong T-WL, Stöver T, Lomax MI, Altschuler RA (2001) Gene expression profiles of the rat cochlea, cochlear nucleus, and inferior colliculus. J Assoc Res Otolaryngol 3:54–67.Google Scholar
  41. 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.PubMedGoogle Scholar
  42. Collier JR, Monk NA, Maini PK, Lewis JH (1996) Pattern formation by lateral inhibition with feedback: a mathematical model of delta-notch intercellular signaling. J Theor Biol 183:429–446.PubMedGoogle Scholar
  43. Corwin JT (1981) Postembryonic production and aging in inner ear hair cells in sharks. J Comp Neurol 201:541–553.PubMedGoogle Scholar
  44. Corwin JT (1983) Postembryonic growth of the macula neglecta auditory detector in the ray, Raja clavata: continual increases in hair cell number, neural convergence, and physiological sensitivity. J Comp Neurol 217:345–345.PubMedGoogle Scholar
  45. Corwin JT (1985) Perpetual production of hair cells and maturational changes in hair cell ultrastructure accompany postembryonic growth in an amphibian ear. Proc Natl Acad Sci USA 82:3911–3915.PubMedGoogle Scholar
  46. Corwin JT, Cotanche DA (1988) Regeneration of sensory hair cells after acoustic trauma. Science 240:1772–1774.PubMedGoogle Scholar
  47. Corwin JT, Jones JE, Katayama A, Kelley MW, Warchol ME (1991) Hair cell regeneration: the identities of progenitor cells, potential triggers and instructive cues. Ciba Found Symp 160:103–120.PubMedGoogle Scholar
  48. Cotanche DA (1987a) Regeneration of hair cell stereociliary bundles in the chick cochlea following severe acoustic trauma. Hear Res 30:181–195.Google Scholar
  49. Cotanche DA (1987b) Regeneration of the tectorial membrane in the chick cochlea following severe acoustic trauma. Hear Res 30:197–206.Google Scholar
  50. Cotanche DA (1999) Structural recovery from sound and aminoglycoside damage in the avian cochlea. Audiol Neurootol 4:271–285.PubMedGoogle Scholar
  51. Cotanche DA, Sulik KK (1984) The development of stereociliary bundles in the cochlear duct of chick embryos. Brain Res 318(2):181–193.Google Scholar
  52. Cotanche DA, Petrell A, Picard DA (1991) Structural reorganization of hair cells and supporting cells during noise damage, recovery and regeneration in the chick cochlea. Ciba Found Symp 160:131–142.PubMedGoogle Scholar
  53. Cotanche DA, Messana EP, Ofsie MS (1995) Migration of hyaline cells into the chick basilar papilla during severe noise damage. Hear Res 91:148–159.PubMedGoogle Scholar
  54. Cristobal R, Popper P, Lopez I, Micevych P, De Vellis J, Honrubia V (2002) In vivo and in vitro localization of brain-derived neurotrophic factor, fibroblast growth factor-2 and their receptors in the bullfrog vestibular end organs. Mol Brain Res 102:83–99.PubMedGoogle Scholar
  55. Cruz RM, Lambert PR, Rubel EW (1987) Light microscopic evidence of hair cell regeneration after gentamicin toxicity in chick cochlea. Arch Otolaryngol Head Neck Surg 113:1058–1062.PubMedGoogle Scholar
  56. Cryns K, Van Camp G (2004) Deafness genes and their diagnostic applications. Audiol Neuro-Otol 9:2–22.Google Scholar
  57. Dabdoub A, Donohue MJ, Brennan A, Wolf V, Montcouquiol M, Sassoon DA, Hseih JC, Rubin JS, Salinas PC, Kelley MW (2003) Wnt signaling mediates reorientation of outer hair cell stereociliary bundles in the mammalian cochlea. Development 130:2375–2384.PubMedGoogle Scholar
  58. 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.PubMedGoogle Scholar
  59. Daudet N, Vago P, Ripoll C, Humbert G, Pujol R, Lenoir M (1998) Characterization of atypical cells in the juvenile rat organ of Corti after aminoglycoside ototoxicity. J Comp Neurol 401:145–162.PubMedGoogle Scholar
  60. Daudet N, Ripoll C, Lenoir M (2002) Transforming growth factor-α-induced cellular changes in organotypic cultures of juvenile, amikacin-treated rat organ of Corti. J Comp Neurol 442:6–22.PubMedGoogle Scholar
  61. Davis RL, Turner DL (2001) Vertebrate hairy and Enhancer of split related proteins: transcriptional repressors regulating cellular differentiation and embryonic patterning. Oncogene 20:8342–8357.PubMedGoogle Scholar
  62. Ding-Pfennigdorff D, Smolders JW, Muller M, Klinke R (1998) Hair cell loss and regeneration after severe acoustic overstimulation in the adult pigeon. Hear Res. 120:109–120.PubMedGoogle Scholar
  63. Doe CQ (1996) Asymmetric cell division and neurogenesis. Opin Genet Dev 6:562–566.Google Scholar
  64. Doe CQ, Chu-LaGraff Q, Wright DM, Scott MP (1991) The prospero gene specifies cell fates in the Drosophila central nervous system. Cell 65:451–464.PubMedGoogle Scholar
  65. Doetzlhofer A, White PM, Johnson JE, Segil N, Groves AK (2004) In vitro growth and differentiation of mammalian sensory hair cell progenitors for EGF and periotic mesenchyme. Dev Biol 272:432–447.PubMedGoogle Scholar
  66. Duckert LG, Rubel EW (1990) Ultrastructural observations on regenerating hair cells in the chick basilar papilla. Hear Res 48:161–182.PubMedGoogle Scholar
  67. Dye BJ, Frank TC, Newlands SD, Dickman JD (1999) Distribution and time course of hair cell regeneration in the pigeon utricle. Hear Res 13:17–26.Google Scholar
  68. Dyer MA, Livesey FJ, Cepko CL, Oliver G (2003) Prox1 function controls progenitor cell proliferation and horizontal cell genesis in the mammalian retina. Nat Genet 34:53–58.PubMedGoogle Scholar
  69. 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.PubMedGoogle Scholar
  70. Epstein JE, Cotanche DA (1995) Secretion of a new basal layer of tectorial membrane following gentamicin-induced hair cell loss. Hear Res 90:31–43.PubMedGoogle Scholar
  71. Fehon RG, Johansen K, Rebay I, Artavanis-Tsakonas S (1990) Complex cellular and subcellular regulation of notch expression during embryonic and imaginal development of Drosophila: implications for notch function. J Cell Biol 113:657–669.Google Scholar
  72. Fekete DM, Wu DK (2002) Revisiting cell fate specification in the inner ear. Curr Opin Neurobiol 12:35–42.PubMedGoogle Scholar
  73. Fekete DM, Muthukumar S, Karagogeos D (1998) Hair cells and supporting cells share a common progenitor in the avian inner ear. J Neurosci 18:7811–7821.PubMedGoogle Scholar
  74. Fischer AJ, Reh TA (2000) Identification of a proliferating marginal zone of retinal progenitors in postnatal chickens. Dev Biol 2000 220:197–210.Google Scholar
  75. Fischer AJ, Reh TA (2001) Muller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat Neurosci 4:247–252.PubMedGoogle Scholar
  76. Forge A (1985) Outer hair cell loss and supporting cell expansion following chronic gentamicin treatment. Hear Res 19:171–182.PubMedGoogle Scholar
  77. Forge A, Schacht J (2000) Aminoglycoside antibiotics. Audiol Neurootol 5:3–22.PubMedGoogle Scholar
  78. Forge A, Li L, Corwin JT, Nevill G (1993) Ultrastructural evidence for hair cell regeneration in the mammalian inner ear [see comments] Science 259:1616–1619.Google Scholar
  79. Forge A, Li L, Nevill G (1998) Hair cell recovery in the vestibular sensory epithelia of mature guinea pigs. J Comp Neurol 397:69–88.PubMedGoogle Scholar
  80. Fredelius L, Rask-Andersen H (1990) The role of macrophages in the disposal of degeneration products within the organ of corti after acoustic overstimulation. Acta Otolaryngol Stockh 109:76–82.PubMedGoogle Scholar
  81. Fritzsch B, Beisel KW, Bermingham NA (2000) Developmental evolutionary biology of the vertebrate ear: conserving mechanoelectric transductionand developmental pathways in diverging morphologies. NeuroReport 11:R35–44.PubMedGoogle Scholar
  82. Galderisi U, Jori FP, Giordano A (2003) Cell cycle regulation and neural differentiation. Oncogene 22:5208–5219.PubMedGoogle Scholar
  83. Gale JE, Meyers JR, Periasamy A, Corwin JT (2000) Survival of bundleless hair cells and subsequent bundle replacement in the bullfrog’s saccule. J Neurobiol 50:81–92.Google Scholar
  84. Gao W (2003) Hair cell development in higher vertebrates. Curr Top Dev Biol 57:293–319.PubMedGoogle Scholar
  85. Ginzberg RD, Gilula NB (1979) Modulation of cell junctions during differentiation of the chicken otocyst sensory epithelium. Dev Biol 68:110–129.PubMedGoogle Scholar
  86. Girod DA, Duckert LG, Rubel EW (1989) Possible precursors of regenerated hair cells in the avian cochlea following acoustic trauma. Hear Res 42:175–194.PubMedGoogle Scholar
  87. Girod DA, Tucci DL, Rubel EW (1991) Anatomical correlates of functional recovery in the avian inner ear following aminoglycoside ototoxicity. Laryngoscope 101:1139–1149.PubMedGoogle Scholar
  88. Gleich O, Dooling RJ, Manley GA (1994) Inner-ear abnormalities and their functional consequences in Belgian Waterslager canaries (Serinus canarius). Hear Res 79:123.PubMedGoogle Scholar
  89. Gleich O, Dooling RJ, Presson JC (1997) Evidence for supporting cell proliferation and hair cell differentiation in the basilar papilla of adult Belgian Waterslager canaries (Serinus canarius). J Comp Neurol 377:5–14.PubMedGoogle Scholar
  90. Go MJ, Eastman DS, Artavanis-Tsakonas S (1998) Cell proliferation control by Notch signaling in Drosophila development. Development 125:2031–2040.PubMedGoogle Scholar
  91. Goldstein BJ, Fang H, Youngentob SL, Schwob JE (1998) Transplantation of multipotent progenitors from the adult olfactory epithelium. NeuroReport 9:1611–1617.PubMedGoogle Scholar
  92. Goodyear RJ, Richardson GP (2002) Extracellular matrices associated with the apical surfaces of sensory epithelia in the inner ear: molecular and structural diversity. J Neurobiol 53:212–227.PubMedGoogle Scholar
  93. Goodyear R, Holley M, Richardson G (1995) Hair and supporting-cell differentiation during the development of the avian inner ear. J Comp Neurol 351:81–93.PubMedGoogle Scholar
  94. Goodyear R, Killick R, Legan PK, Richardson GP (1996) Distribution of beta-tectorin mRNA in the early posthatch and developing avian inner ear. Hear Res 96:167–178.PubMedGoogle Scholar
  95. Goodyear RJ, Gates R, Lukashkin AN, Richardson GP (1999) Hair-cell numbers continue to increase in the utricular macula of the early posthatch chick. J Neurocytol 28:851–861.PubMedGoogle Scholar
  96. Goodyear RJ, Kwan T, Oh SH, Raphael Y, Richardson GP (2001) The cell adhesion molecule BEN defines a prosensory patch in the developing avian otocyst. J Comp Neurol 434:275–288.PubMedGoogle Scholar
  97. Goodyear RJ, Legan PK, Wright MB, Marcotti W, Oganesian A, Coats SA, Booth CJ, Kros CJ, Seifert RA, Bowen-Pope DF, Richardson GP (2003) A receptor-like inositol lipid phosphatase is required for the maturation of developing cochlear hair bundles. J Neurosci 23:9208–9219.PubMedGoogle Scholar
  98. Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, Faravelli L, Morassutti DJ, Roisen F, Nickel DD et al. (1996) Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J. Neurosci 16:1091–1100.PubMedGoogle Scholar
  99. Gritti A, Frolichsthal-Schoeller P, Galli R, Parati EA, Cova L, Pagano SF, Bjornson CR and Vescovi AL (1999) Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J Neurosci 19:3287–3297.PubMedGoogle Scholar
  100. Hackett L, Davies D, Helyer R, Kennedy H, Kros C, Lawlor P, Rivolta MN, Holley M (2002) E-cadherin and the differentiation of mammalian vestibular hair cells. Exp Cell Res 278:19–30.PubMedGoogle Scholar
  101. Haddon C, Jiang YJ, Smithers L, Lewis J (1998) Delta-Notch signalling and the patterning of sensory cell differentiation in the zebrafish ear: evidence from the mind bomb mutant. Development125:4637–4644.PubMedGoogle Scholar
  102. Hall PA, Watt FM (1989) Stem cells: the generation and maintenance of cellular diversity. Development 106:619–633.PubMedGoogle Scholar
  103. Hamilton TA, Ohmori Y, Narumi S, Tannenbaum CS, eds (1993) Regulation of Diversity of Macrophage Activation. Ann Arbor: CRC Press.Google Scholar
  104. Harris JA, Cheng AG, Cunningham LL, MacDonald G, Raible DW, Rubel EW (2003) Neomycin-induced hair cell death and rapid regeneration in the lateral line of zebrafish (Danio rerio). J Assoc Res Otolaryngol 4:219–234.PubMedGoogle Scholar
  105. Hartenstein V, Posakony JW (1990) A dual function of the Notch gene in Drosophila sensillum development. Dev Biol 142:13–30.PubMedGoogle Scholar
  106. Hashino E, Salvi R (1993) Changing patterns of DNA replication in the noise-damaged chick cochlea. J Cell Sci 105:23–31.PubMedGoogle Scholar
  107. Hashino E, TinHan EK, Salvi RJ (1995) Base-to-apex gradient of cell proliferation in the chick cochlea following kanamycin-induced hair cell loss. Hear Res 88:156–168.PubMedGoogle Scholar
  108. Hashino E, Tanaka Y, Sokabe M (1991) Hair cell damage and recovery following chronic application of kanamycin in the chick cochlea. Hear Res 52:356–368.PubMedGoogle Scholar
  109. Hassan BA, Bellen HJ (2000) Doing the MATH: is the mouse a good model for fly development? Genes Dev 14:1852–1865.Google Scholar
  110. Hasson T, Gillespie PG, Garcia JA, MacDonald RB, Zhao Y, Yee AG, Mooseker MS, Corey DP (1997) Unconventional myosins in inner-ear sensory epithelia. J Cell Biol 137:1287–1307.PubMedGoogle Scholar
  111. Hawkins E (1976) Drug ototoxicity. In Keidel WD, Neff WD (eds) Auditory System. New York: Springer-Verlag, pp. 707–748.Google Scholar
  112. Hawkins RD, Bashiardes S, Helms CA, Hu L, Saccone NL, Warchol ME, Lovett M (2003) Gene expression differences in quiescent versus regenerating hair cells of avian sensory epithelia: implications for human hearing and balance disorders. Hum Mol Genet12:1261–1272.PubMedGoogle Scholar
  113. Henrique D, Hirsinger E, Adam J, Le Roux I, Pourquie O, Ish-Horowicz D, Lewis J (1997) Maintenance of neuroepithelial progenitor cells by Delta-Notch signalling in the embryonic chick retina. Curr Biol 7:661–670.PubMedGoogle Scholar
  114. Higgs DM, Souza MJ, Wilkins HR, Presson JC, Popper AN (2002) Age- and size-related changes in the inner ear and hearing ability of the adult zebrafish (Danio rerio). J Assoc Res Otolaryngol 3:222.Google Scholar
  115. Hirose K, Westrum LE, Cunningham DE, Rubel EW (2004) Electron microscopy of degenerative changes in the chick basilar papilla after gentamicin exposure. J Comp Neurol 470:164–180.PubMedGoogle Scholar
  116. Hong R, Chakravarti D (2003) The human proliferating cell nuclear antigen regulates transcriptional coactivator p300 activity and promotes transcriptional repression. J Biol Chem 278:44505–44513.PubMedGoogle Scholar
  117. Hoppe PE, Greenspan RJ (1986) Local function of the Notch gene for embryonic ectodermal pathway choice in Drosophila. Cell 46:773–783.PubMedGoogle Scholar
  118. Huard JM, Youngentob SL, Goldstein BJ, Luskin MB, Schwob JE (1998) Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. J Comp Neurol 400:469–486.PubMedGoogle Scholar
  119. Hume CR, Kirkegaard M, Oesterle EC (2003) ErbB expression: the mouse inner ear and maturation of the mitogenic response to heregulin. J Assoc Res Otolaryngol 4:422–443.PubMedGoogle Scholar
  120. Inglis-Broadgate SL, Thomson RE, Pellicano F, Tartaglia MA, Pontikis CC, Cooper JD, Iwata T (2005) FGFR3 regulates brain size by controlling progenitor cell proliferation and apoptosis during embryonic development. Dev Biol 279:73–85.PubMedGoogle Scholar
  121. Iso T, Kedes L, Hamamori Y (2003) HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol 194:237–255.PubMedGoogle Scholar
  122. Itoh M, Chitnis AB (2001) Expression of proneural and neurogenic genes in the zebrafish lateral line primordium correlates with selection of hair cell fate in neuromasts. Mech Dev 102:263–266.PubMedGoogle Scholar
  123. Itoh M, Kim CH, Palardy G, Oda T, Jiang YJ, Maust D, Yeo SY, Lorick K, Wright GJ, Ariza-McNaughton L, Weissman AM, Lewis J, Chandrasekharappa SC, Chitnis AB (2003) Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev Cell 4:67–82.PubMedGoogle Scholar
  124. 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.PubMedGoogle Scholar
  125. Jan YN, Jan LY (1998) Asymmetric cell division. Nature 392:775–778.PubMedGoogle Scholar
  126. Janas JD, Cotanche DA, Rubel EW (1995) Avian cochlear hair cell regeneration: stereological analyses of damage and recovery from a single high dose of gentamicin. Hear Res 92:17–29.PubMedGoogle Scholar
  127. Jarman AP, Grau Y, Jan LY, Jan YN (1993) atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73:1307–1321.PubMedGoogle Scholar
  128. Jiang YJ, Brand M, Heisenberg CP, Beuchle D, Furutani-Seiki M, Kelsh RN, Warga RM, Granato M, Haffter P, Hammerschmidt M, Kane DA, Mullins MC, Odenthal J, van Eeden FJ, Nusslein-Volhard C (1996) Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio. Development123:205–216.PubMedGoogle Scholar
  129. Johansson CB, Lothian C, Molin M, Okano H, Lendhal U (2002) Nestin enhance requirements for expression in normal and injured adult CNS. J Neurosci Res 69:784–794.PubMedGoogle Scholar
  130. Johnson LG, Hawkins JE Jr, Kingsley TC, Black FO, Matz GJ (1981) Aminoglycoside-induced cochlear pathology in man. Acta Otolaryngol 383(Suppl):1–19.Google Scholar
  131. Johnston LA, Edgar BA (1998) Wingless and Notch regulate cell-cycle arrest in the developing Drosophila wing. Nature 394:82–84.PubMedGoogle Scholar
  132. Jones JE, Corwin JT (1993) Replacement of lateral line sensory organs during tail regeneration in salamanders: identification of progenitor cells and analysis of leukocyte activity. J Neurosci 13:1022–1034.PubMedGoogle Scholar
  133. Jones JE, Corwin JT (1996) Regeneration of sensory cells after laser ablation in the lateral line system: hair cell lineage and macrophage behavior revealed by time-lapse video microscopy. J Neurosci 16:649–662.PubMedGoogle Scholar
  134. J⊝rgensen JM (1991) Regeneration of lateral line and inner ear vestibular cells. Ciba Found Symp 160:151–170.Google Scholar
  135. J⊝rgensen JM, Flock A (1976) Non-innervated sense organs of the lateral line: development in the regenerating tail of the salamander Ambystoma mexicanum. J Neurocytol 5:33–41.Google Scholar
  136. J⊝rgensen JM, Mathiesen C (1988) The avian inner ear. Continuous production of hair cells in vestibular sensory organs, but not in the auditory papilla. Naturwissenschaften 75:319–320.Google Scholar
  137. Jung KH, Chu K, Kim M, Jeong SW, Song YM, Lee ST, Kim JY, Lee SK, Roh JK (2004) Continuous cytosine-b-D-arabinofuranoside infusion reduces ectopic granule cells in adult rat hippocampus with attenuation of spontaneous recurrent seizures following pilocarpine-induced status epilepticus. Eur J Neurosci 19:3219–3226.PubMedGoogle Scholar
  138. Kageyama R, Ohtsuka T, Hatakeyama J, Ohsawa R (2005) Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res. 306:343–348.PubMedGoogle Scholar
  139. Kalinec F, Kalinec G, Boukhvalova M, Kachar B (1999) Establishment and characterization of conditionally immortalized organ of corti cell lines. Cell Biol Int 23:175–184.PubMedGoogle Scholar
  140. Katayama A, Corwin JT (1989) Cell production in the chicken cochlea. J Comp Neurol 281:129–135.PubMedGoogle Scholar
  141. Katayama A, Corwin JT (1993) Cochlear cytogenesis visualized through pulse labeling of chick embryos in culture. J Comp Neurol 333:28–40.PubMedGoogle Scholar
  142. 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.PubMedGoogle Scholar
  143. Kawauchi S, Beites CL, Crocker CE, Wu HH, Bonnin A, Murray R, Calof AL (2004) Molecular signals regulating proliferation of stem and progenitor cells in mouse olfactory epithelium. Dev Neurosci 26:166–180.PubMedGoogle Scholar
  144. Kelley MW (2003) Cell adhesion molecules during inner ear and hair cell development, including notch and its ligands. Curr Top Dev Biol 57:321–356.PubMedGoogle Scholar
  145. 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 15:3013–3026.PubMedGoogle Scholar
  146. Kevetter GA, Blumberg KR, Correia MJ (2000) Hair cell and supporting cell density and distribution in the normal and regenerating posterior crista ampullaris of the pigeon. Int J Dev Neurosci 18:855–867.PubMedGoogle Scholar
  147. Kiernan AE, Ahituv N, Fuchs H, Balling R, Avraham KB, Steel KP, Hrabe de Angelis (2001) The Notch ligand Jagged1 is required for inner ear sensory development. Proc Natl Acad Sci USA 98:3873–3878.PubMedGoogle Scholar
  148. Kiernan AE, Cordes R, Kopan R, Gossler A, Gridley T (2005) The Notch ligands DLL1 and JAG2 act synergistically to regulate hair cell development in the mammalian inner ear. Development 132:4353–4362. Epub 2005 Sept 1PubMedGoogle Scholar
  149. 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(1):e4. Epub 2006 Jan 13.Google Scholar
  150. Kil J, Warchol ME, Corwin JT (1997) Cell death, cell proliferation, and estimates of hair cell life spans in the vestibular organs of chicks. Hear Res 114:117–126.PubMedGoogle Scholar
  151. Kilpatrick TJ, Bartlett PF (1993) Cloning and growth of multipotential neural precursors: requirements for proliferation and differentiation. Neuron 10:255–265.PubMedGoogle Scholar
  152. Kirkegaard M, J⊝rgensen JM (2000) Continuous hair cell turnover in the inner ear vestibular organs of a mammal, the Daubenton’s bat (Myotis daubentonii). Naturwissenschaften 87:83–86.PubMedGoogle Scholar
  153. Kirkegaard M, J⊝rgensen JM (2001) The inner ear macular sensory epithelia of the Daubenton’s bat. J Comp Neurol 438:433–444.PubMedGoogle Scholar
  154. Klockars T, Perheentupa T, Dahl H-HM (2002) In silico analyses of mouse inner-ear transcripts. JARO 4:24–40.PubMedGoogle Scholar
  155. Kopke RD, Jackson RL, Li G, Rasmussen MD, Hoffer ME, Frenz DA, Costello M, Schultheiss P, Van de Water TR (2001) Growth factor treatment enhances vestibular hair cell renewal and results in improved vestibular function. Proc Natl Acad Sci USA 98:5886–5891.PubMedGoogle Scholar
  156. Kruger RP, Goodyear RJ, Legan PK, Warchol ME, Raphael Y, Cotanche DA, Richardson GP (1999) The supporting-cell antigen: a receptor-like protein tyrosine phosphatase expressed in the sensory epithelia of the avian inner ear. J Neurosci 19:4815–4827.PubMedGoogle Scholar
  157. Kuntz AL, Oesterle EC (1998a) Transforming growth factor alpha with insulin stimulates cell proliferation in vivo in adult rat vestibular sensory epithelium. J Comp Neurol 399:413–423.Google Scholar
  158. Kuntz AL, Oesterle EC (1998b) Transforming growth factor-alpha with insulin induces proliferation in rat utricular extrasensory epithelia. Otolaryngol Head Neck Surg 118:816–824.Google Scholar
  159. Lambert PR (1994) Inner ear hair cell regeneration in a mammal: identification of a triggering factor. Laryngoscope 104:701–718.PubMedGoogle Scholar
  160. Lambert PR, Gu R, Corwin JT (1997) Analysis of small hair bundles in the utricles of mature guinea pigs. Am J Otol 18:637–643.PubMedGoogle Scholar
  161. Lanford PJ, Lan Y, Jiang R, Lindsell C, Weinmaster G, Gridley T, Kelley MW (1999) Notch signalling pathway mediates hair cell development in mammalian cochlea. Nat Genet 21:289–292.PubMedGoogle Scholar
  162. 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.PubMedGoogle Scholar
  163. 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.PubMedGoogle Scholar
  164. Lee KH, Cotanche DA (1996) Potential role of bFGF and retinoic acid in the regeneration of chicken cochlear hair cells. Hear Res 94:1–13.PubMedGoogle Scholar
  165. Lefebvre PP, Malgrange B, Staecker H, Moonen G, Van de Water TR (1993) Retinoic acid stimulates regeneration of mammalian auditory hair cells [see comments]. Science 260:692–695.PubMedGoogle Scholar
  166. Lefebvre PP, Malgrange B, Thiry M, Van de Water TR, Moonen G (2000) Epidermal growth factor upregulates production of supernumerary hair cells in neonatal rat organ of Corti explants. Acta Otolaryngol 120:142–145.PubMedGoogle Scholar
  167. Lendahl U, Zimmerman LB, McKay RDG (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585–595.PubMedGoogle Scholar
  168. Lenoir M, Vago P (1996) Morphological indications of hair cell neodifferentiation in the organ of Corti of amikacin treated rat pups. CR Acad Sci 319:269–276.Google Scholar
  169. Lenoir M, Vago P (1997) Does the organ of Corti attempt to differentiate new hair cells after antibiotic intoxication in rat pups? Int J Dev Neurosci 15:487–495.PubMedGoogle Scholar
  170. León Y, Vazquez E, Sanz C, Vega JA, Mato JM, Giraldez F, Represa J,Varela-Nieto I (1995) Insulin-like growth factor-I regulates cell proliferation in the developing inner ear, activating glycosylphosphatidylinositol hydrolysis and Fos expression. Endocrinology 136:3494–3503.PubMedGoogle Scholar
  171. León Y, Sanz C, Giráldez F, Varela-Nieto I (1998) Induction of cell growth by insulin and insulin-like growth factor-I is associated with Jun expression in the otic vesicle. J Comp Neurol 398:323–332.PubMedGoogle Scholar
  172. León Y, Sanz C, Frago LM, Camarero G, Cañón S, Vazrela-Nieto I, Giráldez F (1999) Involvement of insulin-like growth factor-1 in inner ear organogenesis and regeneration. Horm Metab Res 31:126–132.PubMedGoogle Scholar
  173. Levenberg S, Yarden A, Kam Z, Geiger B (1999) p27 is involved in N-cadherin-mediated contact inhibition of cell growth and S-phase entry. Oncogene 18:869–876.PubMedGoogle Scholar
  174. Lewis J (1991) Rules for the production of sensory cells. Ciba Found Symp 160:25–39.PubMedGoogle Scholar
  175. Lewis J (1996) Neurogenic genes and vertebrate neurogenesis. Curr Opin Neurobiol 6:3–10.PubMedGoogle Scholar
  176. Lewis AK, Frantz GD, Carpenter DA, de Sauvage FJ, Gao WQ (1998) Distinct expression patterns of notch family receptors and ligands during development of the mammalian inner ear. Mech Dev 78:159–163.PubMedGoogle Scholar
  177. Li L, Forge A (1997) Morphological evidence for supporting cell to hair cell conversion in the mammalian utricular macula. Int J Dev Neurosci 15:433–446.PubMedGoogle Scholar
  178. Li L, Vaessin H (2000) Pan-neural Prospero terminates cell proliferation during Drosophila neurogenesis. Genes Dev 14:147–151.PubMedGoogle Scholar
  179. Li H, Liu H, Heller S (2003) Pluripotent stem cells from the adult mouse inner ear. Nat med 9:1293–1299.PubMedGoogle Scholar
  180. Lindsell CE, Boulter J, diSibio G, Gossler A, Weinmaster G (1996) Expression patterns of Jagged, Delta1, Notch1, Notch2, and Notch3 genes identify ligand-receptor pairs that may function in neural development. Mol Cell Neurosci 8:14–27.PubMedGoogle Scholar
  181. Lippe WR, Westbrook EW, Ryals BM (1991) Hair cell regeneration in the chicken cochlea following aminoglycoside toxicity. Hear Res 56:203–210.PubMedGoogle Scholar
  182. Lopez I, Honrubia V, Lee SC, Schoeman G, Beykirch K (1997) Quantification of the process of hair cell loss and recovery in the chinchilla crista ampullaris after gentamicin treatment. Int J Dev Neurosci 15:447–461.PubMedGoogle Scholar
  183. Lopez I, Honrubia V, Lee SC, Li G, Beykirch K (1998) Hair cell recovery in the chinchilla crista ampullaris after gentamicin treatment: a quantitative approach. Otolaryngol Head Neck Surg 119:255–262.PubMedGoogle Scholar
  184. Lopez IA, Zhao PM, Yamaguchi M, de Vellis J, Espinosa-Jeffrey A (2004) Stem/ progenitor cells in the postnatal inner ear of the GFP-nestin transgenic mouse. Int J Dev Neurosci 22:205–213.PubMedGoogle Scholar
  185. Löwenheim H, Furness DN, Kil J, Zinn C, Gültig K, Fero ML, Frost D, Gummer AW, Roberts JM, Rubel EW, Hackney CM, Zenner HP (1999) Proc Natl Acad Sci USA 96: 4084–4088.PubMedGoogle Scholar
  186. Malgrange B, Belachew S, Thiry M, Nguyen L, Rogister B, Alvarez M, Rigo J-M, Van De Water TR, Moonen G, Lefebvre PP (2002) Proliferative generation of mammalian auditory hair cells in culture. Mech Dev 112:79–88.PubMedGoogle Scholar
  187. 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.PubMedGoogle Scholar
  188. Marean GC, Cunningham D, Burt JM, Beecher MD, Rubel EW (1995) Regenerated hair cells in the European starling: are they more resistant to kanamycin ototoxicity than original hair cells? Hear Res 82:267–276.PubMedGoogle Scholar
  189. Marsh RR, Xu LR, Moy JP, Saunders JC (1990) Recovery of the basilar papilla following intense sound exposure in the chick. Hear Res 46:229–237.PubMedGoogle Scholar
  190. 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.PubMedGoogle Scholar
  191. Matsui JI, Oesterle EC, Stone JS, Rubel EW (2000) Characterization of damage and regeneration in cultured avian utricles. J Assoc Res Otolaryngol 1:46–63.PubMedGoogle Scholar
  192. Matsui JI, Ogilvie JM, Warchol ME (2002) Inhibition of caspases prevents ototoxic and ongoing hair cell death. J Neurosci 22:1218–1227.PubMedGoogle Scholar
  193. Matsunaga T, Davis JG, Greene MI (2001) Adult rat otic placode-derived neurons and sensory epithelium express all four erbB receptors: a role in regulating vestibular ganglion neuron viability. DNA Cell Biol 20:307–319.PubMedGoogle Scholar
  194. McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R (2003) Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 162:1135–1147.PubMedGoogle Scholar
  195. Montcouquiol M, Corwin JT (2001a) Brief treatments with forskolin enhance S-phase entry in balance epithelia from the ears of rats. J Neurosci 21:974–982.Google Scholar
  196. Montcouquiol M, Corwin JT (2001b) Intracellular signals that control cell proliferation in mammalian balance epithelia: key roles for phosphatidylinositol-3 kinase, mammalian target of rapamycin, and S6 kinases in preference to calcium, protein kinase C, and mitogen-activated protein kinase. J Neurosci 21:570–580.Google Scholar
  197. Montcouquiol M, Rachel RA, Lanford PJ, Copeland NG, Jenkins NA, Kelley MW (2003) Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423:173–177.PubMedGoogle Scholar
  198. Morest DK, Cotanche DA (2004) Regeneration of the inner ear as a model of neural plasticity. J Neurosci Res 78:455–460.PubMedGoogle Scholar
  199. Morrison A, Hodgetts C, Gossler A, Hrabe de Angelis M, Lewis J (1999) Expression of Delta1 and Serrate1 (Jagged1) in the mouse inner ear. Mech Dev 84:169–172.PubMedGoogle Scholar
  200. Mumm JS, Shou J, Calof AL (1996) Colony-forming progenitors from mouse olfactory epithelium: evidence for feedback regulation of neuron production. Proc Natl Acad Sci USA 93:11167–11172.PubMedGoogle Scholar
  201. Murray RC, Calof AL (1999) Neuronal regeneration: lessons from the olfactory system. Semin Cell Dev Biol 10:421–431.PubMedGoogle Scholar
  202. Nagaraj R, Banerjee U (2004) The little R cell that could. Int J Dev Biol 48:755–760.PubMedGoogle Scholar
  203. Navaratnam DS, Su HS, Scott S, Oberholtzer JC (1996) Proliferation in the auditory receptor epithelium mediated by a cyclic AMP-dependent signaling pathway. Nat Med 2:1136–1139.PubMedGoogle Scholar
  204. Nickel R, Becker D, Forge A (2006) Molecular and functional characterization of gap junctions in the avian inner ear. J Neurosci 26:6190–6199.PubMedGoogle Scholar
  205. Niemiec AJ, Raphael Y, Moody DB (1994) Return of auditory function following structural regeneration after acoustic trauma: behavioral measures from quail. Hear Res 79:1–16.PubMedGoogle Scholar
  206. Oesterle EC, Hume CR (1999) Growth factor regulation of the cell cycle in developing and mature inner ear sensory epithelia. J Neurocytol 28:877–887.PubMedGoogle Scholar
  207. Oesterle EC, Rubel EW (1993) Postnatal production of supporting cells in the chick cochlea. Hear Res 66:213–224.PubMedGoogle Scholar
  208. Oesterle EC, Cunningham DE, Rubel EW (1992) Ultrastructure of hyaline, border, and vacuole cells in chick inner ear. J Comp Neurol 318:64–82.PubMedGoogle Scholar
  209. Oesterle EC, Tsue TT, Reh TA, Rubel EW (1993) Hair-cell regeneration in organ cultures of the postnatal chicken inner ear. Hear Res 70:85–108.PubMedGoogle Scholar
  210. Oesterle EC, Tsue TT, Rubel EW (1997) Induction of cell proliferation in avian inner ear sensory epithelia by insulin-like growth factor-I and insulin. J Comp Neurol 380:262–274.PubMedGoogle Scholar
  211. Oesterle EC, Bhave SA, Coltrera MD (2000) Basic fibroblast growth factor inhibits cell proliferation in cultured avian inner ear sensory epithelia. J Comp Neurol 424:307–326.PubMedGoogle Scholar
  212. Oesterle EC, Cunningham DE, Westrum LE, Rubel EW (2003) Ultrastructural analysis of (3H)thymidine-labeled cells in the rat utricular macula. J Comp Neurol 463:177–195.PubMedGoogle Scholar
  213. Ogata Y, Slepecky NB, Takahashi M (1999) Study of the gerbil utricular macula following treatment with gentamicin, by use of bromodeoxyuridine and calmodulin immunohistochemical labelling. Hear Res 133:53–60.PubMedGoogle Scholar
  214. O’Halloran EK, Oesterle EC (2004) Characterization of leukocyte subtypes in chicken inner ear sensory epithelia. J Comp Neurol 475:340–360.PubMedGoogle Scholar
  215. Paquette AJ, Perez SE, Anderson DJ (2000) Constitutive expression of the neuron-restrictive silencer factor (NRSF)/REST in differentiating neurons disrupts neuronal gene expression and causes axon pathfinding errors in vivo. Proc Natl Acad Sci USA 97:12318–12323.PubMedGoogle Scholar
  216. Parietti C, Vago P, Humbert G, Lenoir M (1998) Attempt at hair cell neodifferentiation in developing and adult amikacin intoxicated rat cochleae. Brain Res 813:57–66.PubMedGoogle Scholar
  217. Parker MA, Cotanche DA (2004) The potential use of stem cells for cochlear repair. Audiol Neurootol 9:72–80.PubMedGoogle Scholar
  218. Pickles JO, van Heumen WRA (1997) The expression of messenger RNAs coding for growth factors, their receptors, and eph-class receptor tyrosine kinases in normal and ototoxically damaged chick cochleae. Developmental Neuroscience 19: 476–487.PubMedGoogle Scholar
  219. Pirvola U, Cao Y, Oellig C, Suoqiang Z, Pettersson RF, Ylikoski J (1995) The site of action of neuronal acidic fibroblast growth factor is the organ of Corti of the rat cochlea. Proc Natl Acad Sci USA 92:9269–9273.PubMedGoogle Scholar
  220. Platt C (1977) Hair cell distribution and orientation in goldfish otolith organs. J Comp Neurol 172:283–287.PubMedGoogle Scholar
  221. Popper AN, Hoxter B (1984) Growth of a fish ear: 1. Quantitative analysis of hair cell and ganglion cell proliferation. Hear Res 15:133–142.PubMedGoogle Scholar
  222. Presson JC, Popper AN (1990) Possible precursors to new hair cells, support cells, and Schwann cells in the ear of a post-embryonic fish. Hear Res 46:9–22.PubMedGoogle Scholar
  223. Presson JC, Smith T, Mentz L (1995) Proliferating hair cell precursors in the ear of a postembryonic fish are replaced after elimination by cytosine arabinoside. J Neurobiol 26:579–584.PubMedGoogle Scholar
  224. Presson JC, Lanford PJ, Popper AN (1996) Hair cell precursors are ultrastructurally indistinguishable from mature support cells in the ear of a postembryonic fish. Hear Res 100:10–20.PubMedGoogle Scholar
  225. Radtke F, Wilson A, MacDonald HR (2004) Notch signaling in T- and B-cell development. Curr Opin Immunol 6:174–179.Google Scholar
  226. Raphael Y (1992) Evidence for supporting cell mitosis in response to acoustic trauma in the avian inner ear. J Neurocytol 21:663–671.PubMedGoogle Scholar
  227. Raz Y, Kelley MW (1997) Effects of retinoid and thyroid receptors during development of the inner ear. Semin Cell Dev Biol 8:257–264.PubMedGoogle Scholar
  228. Raz Y, Kelley MW (1999) Retinoic acid signaling is necessary for the development of the organ of Corti. Dev Biol 213:180–193.PubMedGoogle Scholar
  229. Reddy GV, Rodrigues V (1999) Sibling cell fate in the Drosophila adult external sense organ lineage is specified by prospero function, which is regulated by Numb and Notch. Development126:2083–2092.PubMedGoogle Scholar
  230. Richards LJ, Kilpatrick TJ, Bartlett PF (1992) De novo generation of neuronal cells from the adult mouse brain. Proc Natl Acad Sci USA 89:8591–8595.PubMedGoogle Scholar
  231. Riley BB, Chiang M, Farmer L, Heck R (1999) The deltaA gene of zebrafish mediates lateral inhibition of hair cells in the inner ear and is regulated by pax2.1. Development 126:5669–5678.PubMedGoogle Scholar
  232. Rivolta MN, Grix N, Lawlor P, Ashmore JF, Jagger DJ, Holley MC (1998) Auditory hair cell precursors immortalized from the mammalian inner ear. Proc Biol Sci 265(1406):1595–1603.PubMedGoogle Scholar
  233. Rivolta MN, Grix N, Lawlor P, Ashmore JF, Jagger DJ, Holley MC (2003) Auditory hair cell precursors immortalized from the mammalian inner ear. Proc Biol Sci 265:1595–1603.Google Scholar
  234. Roberson DW, Rubel EW (1994) Cell division in the gerbil cochlea after acoustic trauma. Am J Otol 15:28–34.PubMedGoogle Scholar
  235. Roberson DW, Weisleder P, Bohrer PS, Rubel EW (1992) Ongoing production of sensory cells in the vestibular epithelium of the chick. Hear Res 57:166–174.PubMedGoogle Scholar
  236. Roberson DW, Kreig CS, Rubel EW (1996) Light microscopic evidence that direct transdifferentiation gives rise to new hair cells in regenerating avian auditory epithelium. Aud Neurosci 2:195–205.Google Scholar
  237. Roberson DW, Alosi JA, Mercola M, Cotanche DA (2002) REST mRNA expression in normal and regenerating avian auditory epithelium. Res 172:62–172.Google Scholar
  238. Roberson DW, Alosi JA, Cotanche DA (2004) Direct transdifferentiation gives rise to the earliest new hair cells in regenerating avian auditory epithelium. J Neurosci Res 78:461–471.PubMedGoogle Scholar
  239. Romand R, Chardin S, Le Calvez S (1996) The spontaneous appearance of hair cell-like cells in the mammalian cochlea following aminoglycoside ototoxicity. NeuroReport 8:133–137.PubMedGoogle Scholar
  240. Rosenfeld RG, Roberts CT Jr, eds (1999)The IGF System. Totowa, NJ: Humana Press.Google Scholar
  241. Rubel EW, Dew LA, Roberson DW (1995) Mammalian vestibular hair cell regeneration [letter; comment]. Science 267:701–707.PubMedGoogle Scholar
  242. Ruben RJ (1967) Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol Suppl 220:1–43.Google Scholar
  243. Ruben RJ (1969) The synthesis of DNA and RNA in the developing inner ear. Laryngoscope 79:1546–1556.Google Scholar
  244. Ryals BM, Rubel EW (1988) Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240:1774–1776.PubMedGoogle Scholar
  245. Saffer LD, Gu R, Corwin JT (1996) An RT-PCR analysis of mRNA for growth factor receptors in damaged and control sensory epithelia of rat utricles. Hear Res 94:14–23.PubMedGoogle Scholar
  246. Sage C, Huang M, Karimi K, Gutierrez G, Vollrath MA, Zhang D-S, García-Añoveros J, Hinds PW, Corwin JT, Corey DP, Chen Z-Y (2005) Proliferation of functional hair cells in vivo in the absence of the retinoblastoma protein. Science 307:1114–1118.PubMedGoogle Scholar
  247. Schoenherr CJ, Anderson DJ (1995) Silencing is golden: negative regulation in the control of neuronal gene transcription. Curr Opin Neurobiol 5(5): 566–571.Google Scholar
  248. Schwartz Levey M, Chikaraishi DM, Kauer JS (1991) Characterization of potential precursor populations in the mouse olfactory epithelium using immunocytochemistry and autoradiography. J Neurosci 11:3556–3564.PubMedGoogle Scholar
  249. Schwob JE (2002) Neural regeneration and the peripheral olfactory system. Anat Rec 269:33–49.PubMedGoogle Scholar
  250. Severinsen SA, J⊝rgensen JM, Nyengaard JR (2003) Structure and growth of the utricular macula in the inner ear of the slider turtle Trachemys scripta. J Assoc Res Otolaryngol 4:505–520.Google Scholar
  251. Shailam R, Lanford PJ, Dolinsky CM, Norton CR, Gridley T, Kelley MW (1999) Expression of proneural and neurogenic genes in the embryonic mammalian vestibular system. J Neurocytol 28:809–819.PubMedGoogle Scholar
  252. Shou J, Zheng JL, Gao WQ (2003) Robust generation of new hair cells in the mature mammalian inner ear by adenoviral expression of Hath1. Mol Cell Neurosci 23:169–179.PubMedGoogle Scholar
  253. Skeath JB, Carroll SB (1992) Regulation of proneural gene expression and cell fate during neuroblast segregation in the Drosophila embryo. Development 114:939–946.PubMedGoogle Scholar
  254. Sliwinska-Kowalska M, Rzadzinska A, Jedlinska U, Rajkowska E (2000) Hair cell regeneration in the chick basilar papilla after exposure to wide-band noise: evidence for ganglion cell involvement. Hear Res 148:197–212.PubMedGoogle Scholar
  255. Sobkowicz HM, Bereman B, Rose JE (1975) Organotypic development of the organ of Corti in culture. J Neurocytol 4:543–572.PubMedGoogle Scholar
  256. Sobkowicz HM, August BK, Slapnick SM (1992) Epithelial repair following mechanical injury of the developing organ of Corti in culture: an electron microscopic and autoradiographic study. Exp Neurol 115:44–49.PubMedGoogle Scholar
  257. Sobkowicz HM, August BK, Slapnick SM (1996) Post-traumatic survival and recovery of the auditory sensory cells in culture. Acta Oto-Laryngologica 116:257–262.PubMedGoogle Scholar
  258. Sobkowicz HM, August BK, Slapnick SM (1997) Cellular interactions as a response to injury in the organ of Corti in culture. Int J Dev Neurosci 15:463–485.PubMedGoogle Scholar
  259. Staecker H, Van de Water TR (1998) Factors controlling hair-cell regeneration/repair in the inner ear. Curr Opin Neurobiol 8:480–487.PubMedGoogle Scholar
  260. 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 261:149–164.PubMedGoogle Scholar
  261. Steyger PS, Burton M, Hawkins JR, Schuff NR, Baird RA (1997) Calbindin and parvalbumin are early markers of non-mitotically regenerating hair cells in the bullfrog vestibular otolith organs. Int J Dev Neurosci 15:417–432.PubMedGoogle Scholar
  262. Stone JS, Cotanche DA (1994) Identification of the timing of S phase and the patterns of cell proliferation during hair cell regeneration in the chick cochlea. J Comp Neurol 341:50–67.PubMedGoogle Scholar
  263. Stone JS, Rubel EW (1999) Delta1 expression during avian hair cell regeneration. Development 126:961–973.PubMedGoogle Scholar
  264. Stone JS, Rubel EW (2000a) Temporal, spatial, and morphologic features of hair cell regeneration in the avian basilar papilla. J Comp Neurol 417:1–16.Google Scholar
  265. Stone JS, Rubel EW (2000b) Cellular studies of auditory hair cell regeneration in birds. Proc Natl Acad Sci USA 97:11714–11721.Google Scholar
  266. Stone JS, Leano SG, Baker LP, Rubel EW (1996) Hair cell differentiation in chick cochlear epithelium after aminoglycoside toxicity: in vivo and in vitro observations. J Neurosci 16:6157–6174.PubMedGoogle Scholar
  267. Stone JS, Choi YS, Woolley SM, Yamashita H, Rubel EW (1999) Progenitor cell cycling during hair cell regeneration in the vestibular and auditory epithelia of the chick. J Neurocytol 28:863–876.PubMedGoogle Scholar
  268. Stone JS, Shang JL, Tomarev S (2003) Expression of Prox1 defines regions of the avian otocyst that give rise to sensory or neural cells. J Comp Neurol 460:487–502.PubMedGoogle Scholar
  269. Stone JS, Shang JL, Tomarev S (2004) cProx1 immunoreactivity distinguishes progenitor cells and predicts hair cell fate during avian hair cell regeneration. Dev Dyn 230:597–614.PubMedGoogle Scholar
  270. Tanaka K, Smith CA (1978) Structure of the chicken’s inner ear: SEM and TEM study. Am J Anat 153:251–271.PubMedGoogle Scholar
  271. Tang LS, Alger HM, Pereira FA (2006) COUP-TFI controls Notch regulation of hair cell and support cell differentiation. Development 133:3683–3693.PubMedGoogle Scholar
  272. Tanyeri H, Lopez I, Honrubia V (1995) Histological evidence for hair cell regeneration after ototoxic cell destruction with local application of gentamicin in the chinchilla crista ampullaris. Hear Res 89:194–202.PubMedGoogle Scholar
  273. Taylor RR, Forge A (2005) Hair cell regeneration in sensory epithelia from the inner ear of a urodele amphibian. J Comp Neurol 484:105–120.PubMedGoogle Scholar
  274. Torres M, Giraldez F (1998) The development of the vertebrate inner ear. Mech Dev 71:5–21.PubMedGoogle Scholar
  275. Tsai H, Hardisty RE, Rhodes C, Kiernan AE, Roby P, Tymowska-Lalanne Z, Mburu P, Rastan S, Hunter AJ, Brown SD, Steel KP (2001) The mouse slalom mutant demonstrates a role for Jagged1 in neuroepithelial patterning in the organ of Corti. Hum Mol Genet10:507–512.PubMedGoogle Scholar
  276. Tsue TT, Watling DL, Weisleder P, Coltrera MD, Rubel EW (1994a) Identification of hair cell progenitors and intermitotic migration of their nuclei in the normal and regenerating avian inner ear. J Neurosci 14:140–152.Google Scholar
  277. Tsue TT, Oesterle EC, Rubel EW (1994b) Diffusible factors regulate hair cell regeneration in the avian inner ear. Proc Natl Acad Sci USA 91:1584–1588.Google Scholar
  278. Turpin JA, Lopez-Berestein G, eds (1993) Differentiation, maturation, and activation of monocytes and macrophages: functional activity is controlled by a continum of maturation. In Lopez-Berestein G, Klostergaard J (eds) Mononuclear Phagocytes in Cell Biology. Ann Arbor: CRC Press, pp. 72–99.Google Scholar
  279. Umemoto M, Sakagam M, Fukazawa K, Ashida K, Kubo T, Senda T, Yoneda Y (1995) Hair cell regeneration in the chick inner ear following acoustic trauma: ultrastructural and immunohistochemical studies. Cell Tissue Res 281:435–443.PubMedGoogle Scholar
  280. Vaessin H, Grell E, Wolff E, Bier E, Jan LY, Jan YN (1991) prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell 67:941–953.PubMedGoogle Scholar
  281. Vago P, Humbert G, Lenoir M (1998) Amikacin intoxication induces apoptosis and cell proliferation in rat organ of Corti. NeuroReport 9:431–436.PubMedGoogle Scholar
  282. Varela-Nieto I, Morales-Garcia JA, Vigil P, Diaz-Casares A, Gorospe I, Sánchez-Galiano, Cañon S, Camarero G, Contreras J, Cediel R, Leon Y (2004) Trophic effects of insulin-like growth factor-I (IGF-1) in the inner ear. Hear Res 196:19–25.PubMedGoogle Scholar
  283. Wagers AJ, Weissman IL (2004) Plasticity of adult stem cells. Cell 116:639–648.PubMedGoogle Scholar
  284. Wang S, Barres BA (2000) Up a notch: instructing gliogenesis. Neuron 27:197–200.PubMedGoogle Scholar
  285. Warchol ME (1995) Supporting cells in isolated sensory epithelia of avian utricles proliferate in serum-free culture. NeuroReport 6:981–984.PubMedGoogle Scholar
  286. Warchol ME (1997) Macrophage activity in organ cultures of the avian cochlea: Demonstration of a resident population and recruitment to sites of hair cell lesions. J Neurobiol 33:724–734.PubMedGoogle Scholar
  287. Warchol ME (1999) Immune cytokines and dexamethasone influence sensory regeneration in the avian vestibular periphery. J Neurocytol 28:889–900.PubMedGoogle Scholar
  288. Warchol ME (2002) Cell density and N-cadherin interactions regulate cell proliferation in the sensory epithelia of the inner ear. J Neurosci 22:2607–2616.PubMedGoogle Scholar
  289. Warchol ME, Corwin JT (1996) Regenerative proliferation in organ cultures of the avian cochlea: identification of the initial progenitors and determination of the latency of the proliferative response. J Neurosci 16:5466–5477.PubMedGoogle Scholar
  290. Warchol ME, Lambert PR, Goldstein BJ, Forge A, Corwin JT (1993) Regenerative proliferation in inner ear sensory epithelia from adult guinea pigs and humans. Science 259:1619–1622.PubMedGoogle Scholar
  291. Watt FM, Hogan BL (2000) Out of Eden: stem cells and their niches. Science 287:1427–1430.PubMedGoogle Scholar
  292. Weisleder P, Rubel EW (1992) Hair cell regeneration in the avian vestibular epithelium. Exp Neurol 115:2–6.PubMedGoogle Scholar
  293. Weisleder P, Rubel EW (1993) Hair cell regeneration after streptomycin toxicity in the avian vestibular epithelium. J Comp Neurol 331:97–110.PubMedGoogle Scholar
  294. Weisleder P, Tsue TT, Rubel EW (1995) Hair cell replacement in avian vestibular epithelium: supporting cell to type I hair cell. Hear Res 82:125–133.PubMedGoogle Scholar
  295. Weissman IL, Anderson DJ, Gage F (2001) Stem and progenitor cells: origins, phenotypes, lineage commitments, and transdifferentiations. Annu Rev Cell Dev Biol 17:387–403.PubMedGoogle Scholar
  296. White PM, Doetzlhofer A, Lee YS, Groves AK, Segil N (2006) Mammalian cochlear supporting cells can divide and trans-differentiate into hair cells. Nature 441:984–987.PubMedGoogle Scholar
  297. Whitehead MC, Morest DK (1985) The development of innervation patterns in the avian cochlea. Neuroscience 14:255–276.PubMedGoogle Scholar
  298. Wigle JT, Chowdhury K, Gruss P, Oliver G (1999) Prox1 function is crucial for mouse lens-fibre elongation. Nat Genet 21:318–322.PubMedGoogle Scholar
  299. Wigle JT, Harvey N, Detmar M, Lagutina I, Grosveld G, Gunn MD, Jackson DG, Oliver G (2002) An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J 21:1505–1513.PubMedGoogle Scholar
  300. Wilkins HR, Presson JC, Popper AN (1999) Proliferation of vertebrate inner ear supporting cells. J Neurobiol 39:527–535.PubMedGoogle Scholar
  301. Williams JA, Holder N (2000) Cell turnover in neuromasts of zebrafish larvae. Hear Res 143:171–181.PubMedGoogle Scholar
  302. Witte MC, Montcouquiol M, Corwin JT (2001) Regeneration in avian hair cell epithelia: identification of intracellular signals required for S-phase entry. Eur J Neurosci 14:829–838.PubMedGoogle Scholar
  303. Woods C, Montcouquiol M, Kelley MW (2004) Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat Neurosci 1–9.Google Scholar
  304. Woolley SM, Rubel EW (1999) High-frequency auditory feedback is not required for adult song maintenance in Bengalese finches. J Neurosci 19:358–371.PubMedGoogle Scholar
  305. Wu H, Ivkovic S, Murray RC, Jaramillo S, Lyons KM, Johnson JE, Calof AL (2003) Autoregulation of neurogenesis by GDF-11. Neuron 37:197–207.PubMedGoogle Scholar
  306. Yamamoto N, Tanigaki K, Tsuji M, Yabe D, Ito J, Honjo T (2006) Inhibition of Notch/RBP-J signaling induces hair cell formation in neonate mouse cochleas. J Mol Med 84:37–45.PubMedGoogle Scholar
  307. Yamashita H, Oesterle EC (1995) Induction of cell proliferation in mammalian inner ear sensory epithelia by transforming growth factor-alpha and epidermal growth factor. Proc Natl Acad Sci USA 92: 3152–3155.PubMedGoogle Scholar
  308. Yang Q, Bermingham NA, Finegold MJ, Zoghbi HY (2001) Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 294:2155–2158.PubMedGoogle Scholar
  309. Zhang N, Martin GV, Kelley MW, Gridley T (2000) A mutation in the Lunatic fringe gene suppresses the effects of a Jagged2 mutation on inner hair cell development in the cochlea. Curr Biol 10:659–662.PubMedGoogle Scholar
  310. Zhang M, Ding D-L, Salvi R (2002) Expression of heregulin and erbB/HER receptors in the adult chinchilla cochlear and vestibular sensory epithelium. Hear Res 169:56–68.PubMedGoogle Scholar
  311. Zheng JL, Gao W-Q (1997) Analysis of rat vestibular hair cell development and regeneration using calretinin as an early marker. J Neurosci 17:8270–8282.PubMedGoogle Scholar
  312. Zheng JL, Gao W-Q (2000) Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat Neurosci 3:580–586.PubMedGoogle Scholar
  313. Zheng JL, Helbig C, Gao W-Q (1997) Induction of cell proliferation by fibroblast and insulin-like growth factors in pure rat inner ear epithelial cell cultures. J Neurosci 17:216–226.PubMedGoogle Scholar
  314. Zheng JL, Frantz G, Lewis AK, Sliwkowski M, Gao W-Q (1999) Heregulin enhances regenerative proliferation in postnatal rat utricular sensory epithelium after ototoxic damage. J Neurocytol 28:901–912.PubMedGoogle Scholar
  315. 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.PubMedGoogle Scholar
  316. Zine A (2003) Molecular mechanisms that regulate auditory hair-cell differentiation in the mammalian cochlea. Mol Neurobiol 27:223–238.PubMedGoogle Scholar
  317. Zine A, de Ribaupierre F (1998) Replacement of mammalian auditory hair cells. Neuro Report 9:263–268.Google Scholar
  318. Zine A, de Ribaupierre F (2002) Notch/Notch ligands and Math1 expression patterns in the organ of Corti of wild-type and Hes1 and Hes5 mutant mice. Hear Res 170:22–31.PubMedGoogle Scholar
  319. Zine A, Van De Water TR, de Ribaupierre F (2000) Notch signaling regulates the pattern of auditory hair cell differentiation in mammals. Development 127:3373–3383.PubMedGoogle Scholar
  320. 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.PubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Elizabeth C. Oesterle
  • Jennifer S. Stone

There are no affiliations available

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