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Anatomy and Embryology

, Volume 189, Issue 1, pp 1–18 | Cite as

Hair cell regeneration in the bird cochlea following noise damage or ototoxic drug damage

  • Douglas A. Cotanche
  • Kenneth H. Lee
  • Jennifer S. Stone
  • Daniel A. Picard
Review Article

Abstract

Hair cells are sensory cells that transduce motion into neural signals. In the cochlea, they are used to detect sound waves in the environment and turn them into auditory signals that can be processed in the brain. Hair cells in the cochlea of birds and mammals were thought to be produced only during embryogenesis and, once made, they were expected to last throughout the lifetime of the animal. Thus, any loss of hair cells due to trauma or disease was thought to lead to permanent impairment of auditory function. Recently, however, studies from a number of laboratories have shown that hair cells in the avian cochlea can be regenerated after acoustic trauma or ototoxic drug damage. This regeneration is accompanied by a repair of the sensory organ and associated tissues and results in a recovery of auditory function. In this review, we examine and compare the structural events that lead to hair cell loss after noise damage and ototoxic drug damage as well as the processes involved in the recovery of the epithelium and the regeneration of the hair cells. Moreover, we examine functional recovery and how it relates to the structural recovery. Finally, we investigate the evidence for the hypothesis that supporting cells in the basilar papilla act as the progenitor cells for the regenerated hair cells and examine the cellular events required to stimulate the progenitor cells to leave the quiescent state, re-enter the cell cycle, and divide.

Key words

Hair cell Regeneration Avian Progenitor cells Basilar papilla 

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References

  1. Adler HJ, Kenealy JFX, DeDio RM, Saunders JC (1992) Threshold shift, hair cell loss, and hair bundle stiffness following exposure to 120 and 125 dB pure tones in the neonatal chick. Acta Otolaryngol (Stockh) 112:444–454Google Scholar
  2. Adler HJ, Poje CP, Saunders JC (1993) Recovery of auditory function and structure in the chick after two intense pure tone exposures. Hear Res (in press)Google Scholar
  3. Anderson GJ, Legreid RJ, Saunders JC, Marsh RR (1989) Basilar papilla damage during intense sound exposure in the chick cochlea. Assoc Res Otolaryngol Abstr 12:219–220Google Scholar
  4. 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 10:2502–2512Google Scholar
  5. Baserga R (1985) The biology of cell reproduction. Harvard University Press, Cambridge, MassGoogle Scholar
  6. Becker H, Stanners CP, Kudlow JE (1971) Control of macromolecular synthesis in proliferating and resting Syrian hamster cells in monolayer culture. J Cell Physiol 77:43–50Google Scholar
  7. Bohne BA (1976) Mechanisms of noise damage in the inner ear. In: Henderson D, Hamernik RP, Dosanjh DS, Mills JH (eds) Effects of noise on hearing. Raven Press, New York, pp 41–68Google Scholar
  8. Brooks RF (1976) Regulation of the fibroblast cell cycle by serum. Nature 260:248–250Google Scholar
  9. Campisi J, Pardee AB (1984) Post-translational control of the onset of DNA synthesis by an insulin-like growth factor. Mol Cell Biol 4:1807–1814Google Scholar
  10. Cohen YE, Saunders JC (1993) The effects of sound overexposure on the spectral response patterns of nucleus magnocellularis in the neonatal chick. Exp Brain Res 95:202–212Google Scholar
  11. Corwin JT (1981) Postembryonic production and aging of inner ear hair cells in sharks. J Comp Neurol 201:541–533Google Scholar
  12. 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 217:345–356Google Scholar
  13. 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 82:3911–3915Google Scholar
  14. Corwin JT, Cotanche DA (1988) Regeneration of sensory hair cells after acoustic trauma. Science 240:1772–1774Google Scholar
  15. Corwin JT, Jones JE, Katayama A, Kelley MW, Warchol ME (1991) Hair cell regeneration: the identities of progenitor cells, potential triggers and instructive cues. In: Bock GR, Whelan J (eds) Regeneration of vertebrate sensory cells. Ciba Foundation Symposium 160. Wiley, New York, pp 103–130Google Scholar
  16. Cotanche DA (1987a) Hair cell stereocilia regeneration in the chick cochlea after severe acoustic trauma. Assoc Res Otolaryngol Abstr 10:56Google Scholar
  17. Cotanche DA (1987b) Regeneration of hair cell stereociliary bundles in the chick cochlea following severe acoustic trauma. Hear Res 30:181–196Google Scholar
  18. Cotanche DA (1987c) Regeneration of the tectorial membrane in the chick cochlea following severe acoustic trauma. Hear Res 30:197–206Google Scholar
  19. Cotanche DA (1992) Video-enhanced DIG images of the noise-damaged and regenerated chick tectorial membrane. Exp Neurol 115:23–26Google Scholar
  20. Cotanche DA, Corwin JT (1991) Stereociliary bundles reorient during hair cell development and regeneration in the chick cochlea. Hear Res 52:379–402Google Scholar
  21. Cotanche DA, Dopyera CEJ (1990) Hair cell and supporting cell response to acoustic trauma in the chick cochlea. Hear Res 46:29–40Google Scholar
  22. Cotanche DA, Picard DA (1992) Progression of damage to the chick tectorial membrane with increased length of noise exposure. Assoc Res Otolaryngol Abstr 15:116Google Scholar
  23. Cotanche DA, Sulik KK (1984) The development of stereociliary bundles in the cochlear duct of chick embryos. Dev Brain Res 16:181–193Google Scholar
  24. Cotanche DA, Saunders JC, Tilney LG (1986) Hair cell recovery after severe acoustic trauma to the chick basilar papilla. Assoc Res Otolaryngol Abstr 9:14Google Scholar
  25. Cotanche DA, Saunders JC, Tilney LG (1987) Hair cell damage produced by acoustic trauma in the chick cochlea. Hear Res 25:267–286Google Scholar
  26. 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. In: Bock GR, Whelan J (eds) Regeneration of vertebrate sensory cells. Ciba Foundation Symposium 160. Wiley, New York, pp 131–150Google Scholar
  27. Covell WP (1953) Histological changes in the organ of Corti with intense sound. J Comp Neurol 99:43–60Google Scholar
  28. Cruz RM, Lambert PR, Rubel EW (1985) Temporal patterns of gentamicin-induced hair cell loss in the chick basilar papilla. Otolaryngol Head Neck Surg 93[Special issue]:31Google Scholar
  29. Cruz RM, Lambert PM, Rubel EW (1987) Light microscopic evidence of hair cell regeneration after gentamicin toxicity in chick cochlea. Arch Otolaryngol Head Neck Surg 113:1058–1062Google Scholar
  30. Davis H, Derbyshire AJ, Kemp EH, Lurie MH, Upton M (1935) Experimental stimulation deafness. Science 81:101–103Google Scholar
  31. Denhart DT, Edwards DR, Parfett CLJ (1986) Gene expression during the mammalian cell cycle. Biochim Biophys Acta 865:83–125Google Scholar
  32. Duckert LG, Rubel EW (1990) Ultrastructural observations on regenerating hair cells in the chick basilar papilla. Hear Res 48:161–182Google Scholar
  33. Duckert LG, Rubel EW (1993) Morphological correlates of functional recovery in the chicken inner ear after gentamicin treatment. J Comp Neurol 331:75–96Google Scholar
  34. Eldredge DH, Covell WP (1958) A laboratory method for the study of acoustic trauma. Laryngoscope 68:465–486Google Scholar
  35. Fischer FP (1992) Quantitative analysis of the innervation of the chicken basilar papilla. Hear Res 61:167–178Google Scholar
  36. Fischer FP (1993) Quantitative TEM analysis of the barn owl basilar papilla. Hear Res (in press)Google Scholar
  37. Forge A, Li L, Corwin JT, Nevill G (1993) Ultrastructural evidence for hair cell regeneration in the mammalian inner ear. Science 259:1616–1619PubMedGoogle Scholar
  38. Girod DA, Duckert LG, Rubel EW (1989) Possible precursors of regenerated hair cells in the avian cochlea following acoustic trauma. Hear Res 42:175–194Google Scholar
  39. Girod DA, Tucci DL, Rubel EW (1991) Anatomical correlates of functional recovery in the avian inner ear following aminoglycoside ototoxicity. Laryngoscope 101:1139–1149Google Scholar
  40. Gratzner HG (1982) Monoclonal antibody to 5-bromo-2-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218:474–475Google Scholar
  41. Hashino E, Sokabe M (1989) Kanamycin induced low-frequency hearing loss in the budgerigar (Melopsittacus undulatus). J Acoust Soc Am 85:289–294Google Scholar
  42. Hashino E, Sokabe M, Miyamoto K (1988) Frequency-specific susceptibility to acoustic trauma in the budgerigar (Melopsittacus undulatus) J Acoust Soc Am 83:2450–2453Google Scholar
  43. Hashino E, Tanaka Y, Sokabe M (1991) Hair cell damage and recovery following chronic application of kanamycin in the chick cochlea. Hear Res 52:356–368Google Scholar
  44. Hashino E, TinHan E, Salvi RJ (1993) Base-to-apex gradient of DNA replication in the chick cochlear epithelium during kanamycin poisoning. Assoc Res Otolaryngol Abstr 16:104Google Scholar
  45. Hashino E, Tanaka Y, Salvi RJ, Sokabe M (1992) Hair cell regeneration in the adult budgerigar after kanamycin ototoxicity. Hear Res 59:46–58Google Scholar
  46. Henry WJ, Makaretz M, Saunders JC, Schneider ME, Vrettakos P (1988) Hair cell loss and regeneration after exposure to intense sound in neonatal chicks. Otolaryngol Head Neck Surg 98:607–611Google Scholar
  47. Iurato S (1967) Vestibular labyrinth. In: Iurato S (eds) Submicroscopic structure of the inner ear. Pergamon Press, Oxford, pp 169–233Google Scholar
  48. Janas JD, Cotanche DA, Rubel EW (1992) Avian cochlear hair cell regeneration: early response to aminoglycoside ototoxicity. Otolaryngol Head Neck Surg 107:233Google Scholar
  49. 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 13:1022–1034Google Scholar
  50. Katayama A, Corwin JT (1989) Cell production in the chicken cochlea. J Comp Neurol 281:129–135Google Scholar
  51. Lajtha H (1963) On the concept of the cell cycle. J Cell Comp Physiol [Suppl] 62:143–145Google Scholar
  52. LeFebvre PP, Malgrange B, Staecker H, Moonen G, Van De Water TR (1993) Retinoic acid stimulates regeneration of mammalian auditory hair cells. Science 260:692–695Google Scholar
  53. Leof EB, Wyk JJ van, O'Keefe EJ, Pledger WJ (1983) Epidermal growth factor (EGF) is required only during the traverse of early G1 in PDGF-stimulated density-arrested BALB/c-3T3 cells. Exp Cell Res 147:202–208Google Scholar
  54. Linzenbold A, Dooling RJ, Ryals BM (1993) A behavioral audibility curve for the Japanese quail (Coturnix coturnix japonica) Assoc Res Otolaryngol Abstr 16:53Google Scholar
  55. Lippe WR, Westbrook EW, Ryals BM (1991) Hair cell regeneration in the chicken cochlea following aminoglycoside toxicity. Hear Res 56:203–210Google Scholar
  56. Lombarte A, Yan HY, Popper AN, Chang JS, Platt C (1993) Damage and regeneration of hair cell ciliary bundles in a fish ear following treatment with gentamicin. Hear Res 64:166–174Google Scholar
  57. Marean GC, Burt JM, Beecher MD, Rubel EW (1993) Hair cell regeneration in the European starling (Sturnus vulgaris): recovery of pure-tone detection thresholds. Hear Res (in press)Google Scholar
  58. Marsh RR, Xu L, Moy JP, Saunders JC (1990) Recovery of the basilar papilla following intense sound exposure in the chick. Hear Res 46:229–238Google Scholar
  59. McFadden EA, Saunders JC (1989) Recovery of auditory function following intense sound exposure in the neonatal chick. Hear Res 41:205–216Google Scholar
  60. Niemiec AJ, Raphael Y, Moody DB (1993) Return of auditory function following structural regeneration after acoustic trauma: behavioral measures from quail. Hear Res (in press)Google Scholar
  61. Oesterle EC, Cunningham DE, Rubel EW (1992) Ultrastructure of hyaline, border, and vacuole cells in chick inner ear. J Comp Neurol 318:64–82Google Scholar
  62. Pardee AB (1974) A restriction point for control of normal animal cell proliferation. Proc Natl Acad Sci USA 71:1286–1290Google Scholar
  63. Pardee AB (1987) Molecules involved in proliferation of normal and cancer cells. Presidential address. Cancer Res 47:1488–1491Google Scholar
  64. Pardee AB (1989) G1 events and regulation of cell proliferation. Science 246:603–608Google Scholar
  65. Picard DA, Cotanche DA (1990) Tall hair cells in the chick cochlea show hypersensitivity to anoxia, as revealed by localized apical blebbing during fixation. Assoc Res Otolaryngol Abstr 13:384Google Scholar
  66. Pines J (1992) Cell proliferation and control. Curr Opin Cell Biol 4:144–148Google Scholar
  67. Pledger WJ, Stiles CD, Antoniades HN, Scher CD (1977) Induction of DNA synthesis in BALB/c 3T3 cells by serum components: reevaluation of the commitment process. Proc Natl Acad Sci USA 74:4481–4485Google Scholar
  68. Pledger WJ, Stiles CD, Antoniades HN, Scher CD (1978) An ordered sequence of events is required before BALB/c-3T3 cells become committed to DNA synthesis. Proc Natl Acad Sci USA 75:2839–2843Google Scholar
  69. Pugliano FA, Pribitikin E, Adler HJ, Saunders JC (1993a) Growth of evoked potential amplitude in neonatal chicks exposed to intense sound. Acta Otolaryngol 113:18–25Google Scholar
  70. Pugliano FA, Wilcox TO, Rossiter J, Saunders JC (1993b) Recovery of auditory structure and function in neonatal chicks exposed to intense sound for 8 days. Neurosci Lett 151:214–218Google Scholar
  71. Raphael Y (1991) Damage to the tectorial membrane may protect chick hair cells from noise overstimulation. Hear Res 53:173–184Google Scholar
  72. Raphael Y (1992) Evidence for supporting cell mitosis in response to acoustic trauma in the avian inner ear. J Neurocytol 21:663–671Google Scholar
  73. Raphael Y (1993) Reorganization of the chick basilar papilla after acoustic trauma. J Comp Neurol 330:521–532Google Scholar
  74. Roberson DW, Rubel EW (1993) Autoradiographic labeling in the regenerating avian cochlea after continuous intralabyrinthine infusion of tritiated thymidine. Assoc Res Otolaryngol Abstr 16:104Google Scholar
  75. Rossow PW, Riddle VGH, Pardee AB (1979) Synthesis of labile, serum-dependent protein in early G1 controls animal cell growth. Proc Natl Acad Sci USA 76:4446–4450Google Scholar
  76. Rubel EW, Ryals BM (1982) Patterns of hair cell loss in chick basilar papilla after intense auditory stimulation. Acta Otolaryngol (Stockh) 93:31–41Google Scholar
  77. Rubel EW, Ryals BM (1983) Development of the place principle: acoustic trauma. Science 219:512–514Google Scholar
  78. Rubel EW, Oesterle EC, Weisleder P (1991) Hair cell regeneration in the avian inner ear. In: Bock GR, Whelan J (eds) Regeneration of vertebrate sensory cells. Ciba Foundation Symposium 160. Wiley, New York, pp 77–102Google Scholar
  79. Ruben RJ (1967) Development of the inner ear of the mouse. A radioautographic study of terminal mitosis. Acta Otolaryngol (Stockh) [Suppl] 220:1–44Google Scholar
  80. Ryals BM, Rubel EW (1982) Patterns of hair cell loss in the chick basilar papilla after intense auditory stimulation: frequency organization. Acta Otolaryngol (Stockh) 93:205–210Google Scholar
  81. Ryals BM, Rubel EW (1988) Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240:1774–1776Google Scholar
  82. Ryals BM, Westbrook EW (1990) Hair cell regeneration in senescent quail. Hear Res 50:87–96Google Scholar
  83. Ryals BM, Westbrook EW (1993) TEM analysis of neural terminals on autoradiographically identified regenerated hair cells. Hear Res (in press)Google Scholar
  84. Ryals BM, Westbrook EW, Stoots S, Spencer RF (1992) Changes in the acoustic nerve after hair cell regeneration. Exp Neurol 115:18–22Google Scholar
  85. Saunders JC, Dear SD, Schneider ME (1985) The anatomical consequences of acoustic injury: a review and tutorial. J Acoust Soc Am 78:833–860Google Scholar
  86. Saunders JC, Adler HJ, Pugliano FA (1992) The structural and functional aspects of hair cell regeneration in the chick as a result of exposure to intense sound. Exp Neurol 115:13–17Google Scholar
  87. Saunders JC, Torsiglieri AJ, DeDio RM (1993) The growth of hearing loss in neonatal chicks exposed to intense pure tones. Hear Res 69:25–34Google Scholar
  88. Saunders SS, Salvi RJ, Chen L, Turgen N (1993) Psychacoustic measures of recovery from noise-induced hearing loss in adult chickens. Assoc Res Otolaryngol Abstr 16:152Google Scholar
  89. Stiles CD, Isberg RR, Pledger WJ, Antoniades HN, Scher CD (1979) Control of the BALB/c-3T3 cell cycle by nutrients and serum growth factors: analysis using platelet-derived growth factor and platelet-poor plasma. J Cell Physiol 99:395–406Google Scholar
  90. Stone JS, Cotanche DA (1992) Synchronization of hair cell regeneration in the chick cochlea following noise damage. J Cell Sci 102:671–680Google Scholar
  91. Stone JS, Cotanche DA (1993a) Identification of the timing of S phase and the patterns of cell proliferation during hair cell regeneration in the chick cochlea. J Comp Neurol (in press)Google Scholar
  92. Stone JS, Cotanche DA (1993b) Patterns of cell division during hair cell regeneration in the chick cochlea. Assoc Res Otolaryngol Abstr 16:104Google Scholar
  93. Takasaka T, Smith CA (1971) The structure and innervation of the pigeon's basilar papilla. J Ultrastruct Res 35:20–65Google Scholar
  94. Tanaka K, Smith CA (1978) Structure of the chicken's inner ear: SEM and TEM study. Am J Anat 153:251–272Google Scholar
  95. Tilney LG, Saunders JC (1983) Actin filaments, stereocilia and hair cells of the bird cochlea. I. The length, number, width and distribution of stereocilia of each hair cell are related to the position of the hair cell on the cochlea. J Cell Biol 96:807–821Google Scholar
  96. Tilney LG, Tilney MS, Saunders JC, DeRosier DJ (1986) Actin filaments, stereocilia, and hair cells of the bird cochlea. III. The development and differentiation of hair cells and stereocilia in embryos. Dev Biol 116:100–118Google Scholar
  97. Tilney LG, Tilney MS, Cotanche DA (1988) Actin filaments, stereocilia and hair cells of the bird cochlea. V. How the staircase pattern of stereociliary lengths is generated. J Cell Biol 106:355–365Google Scholar
  98. Tucci DL, Rubel EW (1990) Physiological status of regenerated hair cells in the avian inner ear following aminoglycoside ototoxicity. Otolaryngol Head Neck Surg 103:443–450Google Scholar
  99. Warchol ME, Corwin JT (1992) Hair cell regeneration in vitro: determination of the latency and pattern of cell proliferation. Assoc Res Otolaryngol Abstr 15:106Google Scholar
  100. 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 259:1619–1622PubMedGoogle Scholar
  101. Weisleder P, Rubel EW (1993) Hair cell regeneration after streptomycin toxicity in the avian vestibular epithelium. J Comp Neurol 331:97–110Google Scholar
  102. Wharton W, Leof E, Pledger WJ, O'Keefe EJ (1982) Modulation of the epidermal growth factor receptor by platelet-derived growth factor and choleragen: effects on mitogenesis. Proc Natl Acad Sci USA 79:5567–5571Google Scholar
  103. Yang HC, Pardee AB (1986) Insulin-like growth factor I regulation of transcription and replicating enzyme induction necessary for DNA synthesis. J Cell Physiol 127:410–416Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Douglas A. Cotanche
    • 1
  • Kenneth H. Lee
    • 1
  • Jennifer S. Stone
    • 1
  • Daniel A. Picard
    • 1
  1. 1.Department of Anatomy and NeurobiologyBoston University School of MedicineBostonUSA

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