Advertisement

Hearing Loss, Protection, and Regeneration in the Larval Zebrafish Lateral Line

  • Allison B. Coffin
  • Heather Brignull
  • David W. Raible
  • Edwin W. Rubel
Chapter
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 48)

Abstract

This chapter reviews how the larval zebrafish lateral line serves as a model system for studying hair cell death and regeneration. Drugs or vital dyes are rapidly taken up by lateral line hair cells and their effects can be quickly determined by visual assessment. Studies characterizing the death and robust regeneration of lateral line hair cells after exposure to a range of known toxins have established the lateral line as an in vivo model system for understanding these processes. The lateral line has also been the focus of several large-scale drug screens designed to identify novel ototoxins, protective compounds, and compounds that modulate hair cell regeneration. Genetic screens have also provided data about the genes contributing to toxin sensitivity and hair cell regeneration. The combination of rapid, quantitative assays with methods for in vivo visualization make the zebrafish lateral line a promising system for understanding fundamental processes underlying hair cell death and regeneration, and for identifying potential fruitful approaches to modulating these processes in other systems.

Keywords

Aminoglycoside Cell death Cisplatin Deafness Drug screen Fucoidin Gentamicin Genetic screen Hair cell Neomycin Ototoxicity Synthetic glucocorticoids 

References

  1. Akimenko, M. A., Mari-Beffa, M., Becerra, J., & Geraudie, J. (2003). Old questions, new tools, and some answers to the mystery of fin regeneration. Developmental Dynamics, 226(2), 190–201.PubMedGoogle Scholar
  2. Ashmore, J. (2008). Cochlear outer hair cell motility. Physiological Reviews, 88(1), 173–210.PubMedGoogle Scholar
  3. Avallone, B., Fascio, U., Balsamo, G., & Marmo, F. (2008). Gentamicin ototoxicity in the saccule of the lizard Podarcis sicula induces hair cell recovery and regeneration. Hearing Research, 235(1–2), 15–22.PubMedGoogle Scholar
  4. 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. Hearing Research, 178(1–2), 79–88.PubMedGoogle Scholar
  5. Baird, R. A., Torres, M. A., & Schuff, N. R. (1993). Hair cell regeneration in the bullfrog vestibular otolith organs following aminoglycoside toxicity. Hearing Research, 65(1–2), 164–174.PubMedGoogle Scholar
  6. Bang, P. I., Sewell, W. F., & Malicki, J. J. (2001). Morphology and cell type heterogeneities of the inner ear epithelia in adult and juvenile zebrafish (Danio rerio). Journal of Comparative Neurology, 438(2), 173–190.PubMedGoogle Scholar
  7. Barin, K., & Dodson, E. E. (2011). Dizziness in the elderly. Otolaryngologic Clinics of North America, 44(2), 437–454.PubMedGoogle Scholar
  8. Behra, M., Bradsher, J., Sougrat, R., Gallardo, V., Allende, M. L., & Burgess, S. M. (2009). Phoenix is required for mechanosensory hair cell regeneration in the zebrafish lateral line. PLoS Genetics, 5(4), e1000455.PubMedCentralPubMedGoogle Scholar
  9. Boguski, M. S., Mandl, K. D., & Sukhatme, V. P. (2009). Drug discovery: Repurposing with a difference. Science, 324(5933), 1394–1395.PubMedGoogle Scholar
  10. Brignull, H. R., Raible, D. W., & Stone, J. S. (2009). Feathers and fins: Non-mammalian models for hair cell regeneration. Brain Research, 1277, 12–23.PubMedCentralPubMedGoogle Scholar
  11. Brown, A. D., Mussen, T. D., Sisneros, J. A., & Coffin, A. B. (2011) Reevaluating the use of aminoglycoside antibiotics in behavioral studies of the lateral line. Hearing Research, 272(1–2), 1–4.PubMedCentralPubMedGoogle Scholar
  12. Burket, C. T., Montgomery, J. E., Thummel, R., Kassen, S. C., LaFave, M. C., Langenau, D. M., Zon, L. I., & Hyde, D. R. (2008). Generation and characterization of transgenic zebrafish lines using different ubiquitous promoters. Transgenic Research, 17(2), 265–279.PubMedCentralPubMedGoogle Scholar
  13. Cafaro, J., Lee, G. S., & Stone, J. S. (2007). Atoh1 expression defines activated progenitors and differentiating hair cells during avian hair cell regeneration. Developmental Dynamics, 236(1), 156–170.PubMedGoogle Scholar
  14. Chiu, L. L., Cunningham, L. L., Raible, D. W., Rubel, E. W., & Ou, H. C. (2008). Using the zebrafish lateral line to screen for ototoxicity. Journal of the Association for Research in Otolaryngology, 9(2), 178–190.PubMedCentralPubMedGoogle Scholar
  15. Chong, C. R., & Sullivan, D. J., Jr. (2007). New uses for old drugs. Nature, 448(7154), 645–646.PubMedGoogle Scholar
  16. Coffin, A. B., Dabdoub, A., Kelley, M. W., & Popper, A. N. (2007). Myosin VI and VIIa distribution among inner ear epithelia in diverse fishes. Hearing Research, 224(1–2), 15–26.PubMedCentralPubMedGoogle Scholar
  17. Coffin, A. B., Reinhart, K. E., Owens, K. N., Raible, D. W., & Rubel, E. W. (2009). Extracellular divalent cations modulate aminoglycoside-induced hair cell death in the zebrafish lateral line. Hearing Research, 253(1–2), 42–51.PubMedGoogle Scholar
  18. Coffin, A. B., Rubel, E. W, & Raible, D. W. (2013). Bax, Bcl2, and p53 differentially regulate neomycin- and gentamicin-induced hair cell death in the zebrafish lateral line. Journal of the Association for Research in Otolaryngology. doi:  10.1007/s10162-013-0404-1.
  19. Coombs, S., Görner, P., & Münz, H. (1989). The mechanosensory lateral line: Neurobiology and evolution. New York: Springer-Verlag.Google Scholar
  20. Coombs, S., Braun, C. B., & Donovan, B. (2001). The orienting response of Lake Michigan mottled sculpin is mediated by canal neuromasts. Journal of Experimental Biology, 204, 337–348.PubMedGoogle Scholar
  21. Corey, D. P., & Hudspeth, A. J. (1983). Kinetics of the receptor current in bullfrog saccular hair cells. Journal of Neuroscience, 3(5), 962–976.PubMedGoogle Scholar
  22. Corwin, J. T. (1992). Regeneration in the auditory system. Experimental Neurology, 115(1), 7–12.PubMedGoogle Scholar
  23. Corwin, J. T., & Cotanche, D. A. (1988). Regeneration of sensory hair cells after acoustic trauma. Science, 240(4860), 1772–1774.PubMedGoogle Scholar
  24. Cotanche, D. A., & Kaiser, C. L. (2010). Hair cell fate decisions in cochlear development and regeneration. Hearing Research, 266(1–2), 18–25.PubMedCentralPubMedGoogle Scholar
  25. Cunningham, L. L., Cheng, A. G., & Rubel, E. W. (2002). Caspase activation in hair cells of the mouse utricle exposed to neomycin. Journal of Neuroscience, 22(19), 8532–8540.PubMedGoogle Scholar
  26. Cunningham, L. L., Matsui, J. I., Warchol, M. E., & Rubel, E. W. (2004). Overexpression of Bcl-2 prevents neomycin-induced hair cell death and caspase-9 activation in the adult mouse utricle in vitro. Journal of Neurobiology, 60(1), 89–100.PubMedGoogle Scholar
  27. Dalton, D. S., Cruickshanks, K. J., Klein, B. E., Klein, R., Wiley, T. L., & Nondahl, D. M. (2003). The impact of hearing loss on quality of life in older adults. Gerontologist, 43(5), 661–668.PubMedGoogle Scholar
  28. Daudet, N., Gibson, R., Shang, J., Bernard, A., Lewis, J., & Stone, J. (2009). Notch regulation of progenitor cell behavior in quiescent and regenerating auditory epithelium of mature birds. Developmental Biology, 326(1), 86–100.PubMedCentralPubMedGoogle Scholar
  29. David, N. B., Sapede, D., Saint-Etienne, L., Thisse, C., Thisse, B., Dambly-Chaudiere, C., Rosa, F. M., & Ghysen, A. (2002). Molecular basis of cell migration in the fish lateral line: Role of the chemokine receptor CXCR4 and of its ligand, SDF1. Proceedings of the National Academy of Sciences of the USA, 99(25), 16297–16302.PubMedGoogle Scholar
  30. Ding, D., He, J., Allman, B. L., Yu, D., Jiang, H., Seigel, G. M., & Salvi, R. J. (2011). Cisplatin ototoxicity in rat cochlear organotypic cultures. Hearing Research.Google Scholar
  31. Doyon, Y., McCammon, J. M., Miller, J. C., Faraji, F., Ngo, C., Katibah, G. E., Amora, R., Hocking, T. D., Zhang, L., Rebar, E. J., Gregory, P. D., Urnov, F. D., & Amacher, S. L. (2008). Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nature Biotechnology, 26(6), 702–708.PubMedCentralPubMedGoogle Scholar
  32. Dufourcq, P., Roussigne, M., Blader, P., Rosa, F., Peyrieras, N., & Vriz, S. (2006). Mechano-sensory organ regeneration in adults: The zebrafish lateral line as a model. Molecular and Cellular Neurosciences, 33(2), 180–187.PubMedGoogle Scholar
  33. Engeszer, R. E., Patterson, L. B., Rao, A. A., & Parichy, D. M. (2007). Zebrafish in the wild: A review of natural history and new notes from the field. Zebrafish, 4(1), 21–40.PubMedGoogle Scholar
  34. Eppsteiner, R. W., & Smith, R. J. (2011). Genetic disorders of the vestibular system. Current Opinion in Otolaryngology & Head and Neck Surgery, 19(5), 397–402.Google Scholar
  35. Ernest, S., Rauch, G. J., Haffter, P., Geisler, R., Petit, C., & Nicolson, T. (2000). Mariner is defective in myosin VIIA: A zebrafish model for human hereditary deafness. Human Molecular Genetics, 9(14), 2189–2196.PubMedGoogle Scholar
  36. Faucher, K., Aas-Hansen, O., Damsgard, B., Laukli, E., & Stenklev, N. C. (2009). Damage and functional recovery of the Atlantic cod (Gadus morhua) inner ear hair cells following local injection of gentamicin. International Journal of Audiology, 48(7), 456–464.PubMedGoogle Scholar
  37. Flock, Å., & Wersäll, J. (1962). A study of the orientation of the sensory hairs of the receptor cells in the lateral line organ of fish, with special reference to the function of the receptors. Journal of Cell Biology, 15, 19–27.PubMedGoogle Scholar
  38. Foley, J. E., Yeh, J. R., Maeder, M. L., Reyon, D., Sander, J. D., Peterson, R. T., & Joung, J. K. (2009). Rapid mutation of endogenous zebrafish genes using zinc finger nucleases made by Oligomerized Pool ENgineering (OPEN). PLoS One, 4(2), e4348.PubMedCentralPubMedGoogle Scholar
  39. Gates, G. A., Couropmitree, N. N., & Myers, R. H. (1999). Genetic associations in age-related hearing thresholds. Archives of Otolaryngology - Head and Neck Surgery, 125(6), 654–659.PubMedGoogle Scholar
  40. Germana, A., Abbate, F., Gonzalez-Martinez, T., del Valle, M. E., de Carlos, F., Germana, G., & Vega, J. A. (2004). S100 protein is a useful and specific marker for hair cells of the lateral line system in postembryonic zebrafish. Neuroscience Letters, 365(3), 186–189.PubMedGoogle Scholar
  41. Ghysen, A., & Dambly-Chaudiere, C. (2004). Development of the zebrafish lateral line. Current Opinion in Neurobiology, 14(1), 67–73.PubMedGoogle Scholar
  42. Giari, L., Dezfuli, B. S., Astolfi, L., & Martini, A. (2011). Ultrastructural effects of cisplatin on the inner ear and lateral line system of zebrafish (Danio rerio) larvae. Journal of Applied Toxicology.Google Scholar
  43. Gibson, F., Walsh, J., Mburu, P., Varela, A., Brown, K. A., Antonio, M., Beisel, K. W., Steel, K. P., & Brown, S. D. (1995). A type VII myosin encoded by the mouse deafness gene shaker-1. Nature, 374(6517), 62–64.PubMedGoogle Scholar
  44. Gorden, N. T., Arts, H. H., Parisi, M. A., Coene, K. L., Letteboer, S. J., van Beersum, S. E., Mans, D. A., Hikida, A., Eckert, M., Knutzen, D., Alswaid, A. F., Ozyurek, H., Dibooglu, S., Otto, E. A., Liu, Y., Davis, E. E., Hutter, C. M., Bammler, T. K., Farin, F. M., Dorschner, M., Topcu, M., Zackai, E. H., Rosenthal, P., Owens, K. N., Katsanis, N., Vincent, J. B., Hildebrandt, F., Rubel, E. W., Raible, D. W., Knoers, N. V., Chance, P. F., Roepman, R., Moens, C. B., Glass, I. A., & Doherty, D. (2008). CC2D2A is mutated in Joubert syndrome and interacts with the ciliopathy-associated basal body protein CEP290. American Journal of Human Genetics, 83(5), 559–571.PubMedCentralPubMedGoogle Scholar
  45. Granato, M., van Eeden, F. J., Schach, U., Trowe, T., Brand, M., Furutani-Seiki, M., Haffter, P., Hammerschmidt, M., Heisenberg, C. P., Jiang, Y. J., Kane, D. A., Kelsh, R. N., Mullins, M. C., Odenthal, J., & Nusslein-Volhard, C. (1996). Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development, 123, 399–413.PubMedGoogle Scholar
  46. Grunwald, D. J., & Eisen, J. S. (2002). Headwaters of the zebrafish -- emergence of a new model vertebrate. Nature Reviews: Genetics, 3(9), 717–724.Google Scholar
  47. Guan, M. X., Fischel-Ghodsian, N., & Attardi, G. (2000). A biochemical basis for the inherited susceptibility to aminoglycoside ototoxicity. Human Molecular Genetics, 9(12), 1787–1793.PubMedGoogle Scholar
  48. Haffter, P., Granato, M., Brand, M., Mullins, M. C., Hammerschmidt, M., Kane, D. A., Odenthal, J., van Eeden, F. J., Jiang, Y. J., Heisenberg, C. P., Kelsh, R. N., Furutani-Seiki, M., Vogelsang, E., Beuchle, D., Schach, U., Fabian, C., & Nusslein-Volhard, C. (1996). The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development, 123, 1–36.PubMedGoogle Scholar
  49. Harris, J. A., Cheng, A. G., Cunningham, L. L., MacDonald, G., Raible, D. W., & Rubel, E. W. (2003). Neomycin-induced hair cell death and rapid regeneration in the lateral line of zebrafish (Danio rerio). Journal of the Association for Research in Otolaryngology, 4(2), 219–234.PubMedCentralPubMedGoogle Scholar
  50. Hernandez, P. P., Moreno, V., Olivari, F. A., & Allende, M. L. (2006). Sub-lethal concentrations of waterborne copper are toxic to lateral line neuromasts in zebrafish (Danio rerio). Hearing Research, 213(1–2), 1–10.PubMedGoogle Scholar
  51. Hirose, K., Westrum, L. E., Stone, J. S., Zirpel, L., & Rubel, E. W. (1999). Dynamic studies of ototoxicity in mature avian auditory epithelium. Annals of the New York Academy of Sciences, 884, 389–409.PubMedGoogle Scholar
  52. Hirose, Y., Simon, J. A., & Ou, H. C. (2011). Hair cell toxicity in anti-cancer drugs: Evaluating an anti-cancer drug library for independent and synergistic toxic effects on hair cells using the zebrafish lateral line. Journal of the Association for Research in Otolaryngology, 12(6), 719–728.PubMedCentralPubMedGoogle Scholar
  53. Jiang, H., Sha, S. H., Forge, A., & Schacht, J. (2006). Caspase-independent pathways of hair cell death induced by kanamycin in vivo. Cell Death and Differentiation, 13(1), 20–30.PubMedCentralPubMedGoogle Scholar
  54. Jørgensen, J. M. (1991). Regeneration of lateral line and inner ear vestibular cells. Ciba Foundation Symposium, 160, 151–163.PubMedGoogle Scholar
  55. Jørgensen, J. M., & Mathiesen, C. (1988). The avian inner ear. Continuous production of hair cells in vestibular sensory organs, but not in the auditory papilla. Naturwissenschaften, 75(6), 319–320.PubMedGoogle Scholar
  56. Kaufman, C. K., White, R. M., & Zon, L. (2009). Chemical genetic screening in the zebrafish embryo. Nature Protocols, 4(10), 1422–1432.PubMedCentralPubMedGoogle Scholar
  57. Kaus, S. (1987). The effect of aminoglycoside antibiotics on the lateral line organ of Aplocheilus lineatus (Cyprinodontidae). Acta Oto-Laryngologica, 103(5–6), 291–298.Google Scholar
  58. Kaus, S. (1992). The influence of calcium on the ototoxicity of aminoglycosides. Acta Oto-Laryngologica, 112(1), 83–87.PubMedGoogle Scholar
  59. Kawakami, K., Takeda, H., Kawakami, N., Kobayashi, M., Matsuda, N., & Mishina, M. (2004). A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Developmental Cell, 7(1), 133–144.PubMedGoogle Scholar
  60. Keats, B. J. B., Fay, R. R., & Popper, A. N. (2002). Genetics of Auditory Disorders. New York: Springer-Verlag.Google Scholar
  61. Kerstetter, A. E., Azodi, E., Marrs, J. A., & Liu, Q. (2004). Cadherin-2 function in the cranial ganglia and lateral line system of developing zebrafish. Developmental Dynamics, 230(1), 137–143.PubMedGoogle Scholar
  62. Kim, C. H., Kang, S. U., Pyun, J., Lee, M. H., Hwang, H. S., & Lee, H. (2008). Epicatechin protects auditory cells against cisplatin-induced death. Apoptosis, 13(9), 1184–1194.PubMedGoogle Scholar
  63. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., & Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Developmental Dynamics, 203(3), 253–310.PubMedGoogle Scholar
  64. Kral, A., & O'Donoghue, G. M. (2010). Profound deafness in childhood. New England Journal of Medicine, 363(15), 1438–1450.PubMedGoogle Scholar
  65. Kroese, A., & van den Bercken, J. (1980). Dual action of ototoxic antibiotics on sensory hair cells. Nature, 283(5745), 395–397.PubMedGoogle Scholar
  66. Kroese, A., & van den Bercken, J. (1982). Effects of ototoxic antibiotics on sensory hair cell functioning. Hearing Research, 6(2), 183–197.PubMedGoogle Scholar
  67. Kusaykin, M., Bakunina, I., Sova, V., Ermakova, S., Kuznetsova, T., Besednova, N., Zaporozhets, T., & Zvyagintseva, T. (2008). Structure, biological activity, and enzymatic transformation of fucoidans from the brown seaweeds. Biotechnology Journal, 3(7), 904–915.PubMedGoogle Scholar
  68. Lanford, P. J., Presson, J. C., & Popper, A. N. (1996). Cell proliferation and hair cell addition in the ear of the goldfish, Carassius auratus. Hearing Research, 100(1–2), 1–9.PubMedGoogle Scholar
  69. Linbo, T. L., Stehr, C. M., Incardona, J. P., & Scholz, N. L. (2006). Dissolved copper triggers cell death in the peripheral mechanosensory system of larval fish. Environmental Toxicology and Chemistry, 25(2), 597–603.PubMedGoogle Scholar
  70. Liu, X. Z., Walsh, J., Mburu, P., Kendrick-Jones, J., Cope, M. J., Steel, K. P., & Brown, S. D. (1997a). Mutations in the myosin VIIA gene cause non-syndromic recessive deafness. Nature Genetics, 16(2), 188–190.PubMedGoogle Scholar
  71. Liu, X. Z., Walsh, J., Tamagawa, Y., Kitamura, K., Nishizawa, M., Steel, K. P., & Brown, S. D. (1997b). Autosomal dominant non-syndromic deafness caused by a mutation in the myosin VIIA gene. Nature Genetics, 17(3), 268–269.PubMedGoogle Scholar
  72. Lombarte, A., & Popper, A. N. (1994). Quantitative analyses of postembryonic hair cell addition in the otolithic endorgans of the inner ear of the European hake, Merluccius merluccius (Gadiformes, Teleostei). Journal of Comparative Neurology, 345(3), 419–428.PubMedGoogle Scholar
  73. Lombarte, A., Yan, H. Y., Popper, A. N., Chang, J. S., & Platt, C. (1993). Damage and regeneration of hair cell ciliary bundles in a fish ear following treatment with gentamicin. Hearing Research, 64(2), 166–174.PubMedGoogle Scholar
  74. Lopez-Schier, H., & Hudspeth, A. J. (2006). A two-step mechanism underlies the planar polarization of regenerating sensory hair cells. Proceedings of the National Academy of Sciences of the USA, 103(49), 18615–18620.PubMedGoogle Scholar
  75. Lopez-Schier, H., Starr, C. J., Kappler, J. A., Kollmar, R., & Hudspeth, A. J. (2004). Directional cell migration establishes the axes of planar polarity in the posterior lateral-line organ of the zebrafish. Developmental Cell, 7(3), 401–412.PubMedGoogle Scholar
  76. Lord, E. M., & Gates, W. H. (1929). Shaker, a new mutation of the house mouse. . American Naturalist, 63(688), 435–442.Google Scholar
  77. Ma, E. Y., Rubel, E. W., & Raible, D. W. (2008). Notch signaling regulates the extent of hair cell regeneration in the zebrafish lateral line. Journal of Neuroscience, 28(9), 2261–2273.PubMedGoogle Scholar
  78. Malicki, J., Schier, A. F., Solnica-Krezel, L., Stemple, D. L., Neuhauss, S. C., Stainier, D. Y., Abdelilah, S., Rangini, Z., Zwartkruis, F., & Driever, W. (1996). Mutations affecting development of the zebrafish ear. Development, 123, 275–283.PubMedGoogle Scholar
  79. Mangiardi, D. A., McLaughlin-Williamson, K., May, K. E., Messana, E. P., Mountain, D. C., & Cotanche, D. A. (2004). Progression of hair cell ejection and molecular markers of apoptosis in the avian cochlea following gentamicin treatment. Journal of Comparative Neurology, 475(1), 1–18.PubMedGoogle Scholar
  80. Marcotti, W., van Netten, S. M., & Kros, C. J. (2005). The aminoglycoside antibiotic dihydrostreptomycin rapidly enters mouse outer hair cells through the mechano-electrical transducer channels. Journal of Physiology, 567(Pt 2), 505–521.PubMedGoogle Scholar
  81. Marean, G. C., Burt, J. M., Beecher, M. D., & Rubel, E. W. (1993). Hair cell regeneration in the European starling (Sturnus vulgaris): Recovery of pure-tone detection thresholds. Hearing Research, 71(1–2), 125–136.PubMedGoogle Scholar
  82. Marean, G. C., Burt, J. M., Beecher, M. D., & Rubel, E. W. (1998). Auditory perception following hair cell regeneration in European starling (Sturnus vulgaris): Frequency and temporal resolution. Journal of the Acoustical Society of America, 103(6), 3567–3580.PubMedGoogle Scholar
  83. Marot, M., Uziel, A., & Romand, R. (1980). Ototoxicity of kanamycin in developing rats: Relationship with the onset of the auditory function. Hearing Research, 2(2), 111–113.PubMedGoogle Scholar
  84. Mathew, L. K., Sengupta, S., Kawakami, A., Andreasen, E. A., Lohr, C. V., Loynes, C. A., Renshaw, S. A., Peterson, R. T., & Tanguay, R. L. (2007). Unraveling tissue regeneration pathways using chemical genetics. Journal of Biological Chemistry, 282(48), 35202–35210.PubMedGoogle Scholar
  85. Matsui, J. I., Gale, J. E., & Warchol, M. E. (2004). Critical signaling events during the aminoglycoside-induced death of sensory hair cells in vitro. Journal of Neurobiology, 61(2), 250–266.PubMedGoogle Scholar
  86. McDermott, B. M., Jr., Asai, Y., Baucom, J. M., Jani, S. D., Castellanos, Y., Gomez, G., McClintock, J. M., Starr, C. J., & Hudspeth, A. J. (2010). Transgenic labeling of hair cells in the zebrafish acousticolateralis system. Gene Expression Patterns, 10(2–3), 113–118.PubMedCentralPubMedGoogle Scholar
  87. McHenry, M. J., Feitl, K. E., Strother, J. A., & Van Trump, W. J. (2009). Larval zebrafish rapidly sense the water flow of a predator's strike. Biology Letters, 5(4), 477–479.PubMedCentralPubMedGoogle Scholar
  88. Meng, X., Noyes, M. B., Zhu, L. J., Lawson, N. D., & Wolfe, S. A. (2008). Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nature Biotechnology, 26(6), 695–701.PubMedCentralPubMedGoogle Scholar
  89. Metcalfe, W. K., Kimmel, C. B., & Schabtach, E. (1985). Anatomy of the posterior lateral line system in young larvae of the zebrafish. Journal of Comparative Neurology, 233(3), 377–389.PubMedGoogle Scholar
  90. Meyers, J. R., MacDonald, R. B., Duggan, A., Lenzi, D., Standaert, D. G., Corwin, J. T., & Corey, D. P. (2003). Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. Journal of Neuroscience, 23(10), 4054–4065.PubMedGoogle Scholar
  91. Montgomery, J. C., Baker, C. F., & Carton, A. G. (1997). The lateral line can mediate rheotaxis in fish. Nature, 389, 960–963.Google Scholar
  92. Moon, I. S., So, J. H., Jung, Y. M., Lee, W. S., Kim, E. Y., Choi, J. H., Kim, C. H., & Choi, J. Y. (2011). Fucoidan promotes mechanosensory hair cell regeneration following amino glycoside-induced cell death. Hearing Research, 282(1–2), 236–42.PubMedGoogle Scholar
  93. More, S. S., Akil, O., Ianculescu, A. G., Geier, E. G., Lustig, L. R., & Giacomini, K. M. (2010). Role of the copper transporter, CTR1, in platinum-induced ototoxicity. Journal of Neuroscience, 30(28), 9500–9509.PubMedCentralPubMedGoogle Scholar
  94. Mullins, M. C., Hammerschmidt, M., Haffter, P., & Nusslein-Volhard, C. (1994). Large-scale mutagenesis in the zebrafish: In search of genes controlling development in a vertebrate. Current Biology, 4(3), 189–202.PubMedGoogle Scholar
  95. Murakami, S. L., Cunningham, L. L., Werner, L. A., Bauer, E., Pujol, R., Raible, D. W., & Rubel, E. W. (2003). Developmental differences in susceptibility to neomycin-induced hair cell death in the lateral line neuromasts of zebrafish (Danio rerio). Hearing Research, 186(1–2), 47–56.PubMedGoogle Scholar
  96. Nagiel, A., Andor-Ardo, D., & Hudspeth, A. J. (2008). Specificity of afferent synapses onto plane-polarized hair cells in the posterior lateral line of the zebrafish. Journal of Neuroscience, 28(34), 8442–8453.PubMedCentralPubMedGoogle Scholar
  97. Namdaran, P., Reinhart, K. E., Owens, K. N., Raible, D. W., & Rubel, E. W. (2012). Identification of modulators of hair cell regeneration in the zebrafish lateral line. Journal of Neuroscience, 32(10), 3516–3528.PubMedCentralPubMedGoogle Scholar
  98. Nasevicius, A., & Ekker, S. C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nature Genetics, 26(2), 216–220.PubMedGoogle Scholar
  99. Nicolson, T. (2005). The genetics of hearing and balance in zebrafish. Annual Review of Genetics, 39, 9–22.PubMedGoogle Scholar
  100. Nicolson, T., Rusch, A., Friedrich, R. W., Granato, M., Ruppersberg, J. P., & Nusslein-Volhard, C. (1998). Genetic analysis of vertebrate sensory hair cell mechanosensation: The zebrafish circler mutants. Neuron, 20(2), 271–283.PubMedGoogle Scholar
  101. Obholzer, N., Wolfson, S., Trapani, J. G., Mo, W., Nechiporuk, A., Busch-Nentwich, E., Seiler, C., Sidi, S., Sollner, C., Duncan, R. N., Boehland, A., Nicolson, T. (2008). Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells. Journal of Neuroscience, 28(9), 2110–2118.PubMedGoogle Scholar
  102. Odelberg, S. J. (2005). Cellular plasticity in vertebrate regeneration. Anatomical Record. Part B, New anatomist., 287(1), 25–35.Google Scholar
  103. Oesterle, E.C., & Rubel, E.W (1993). Postnatal production of supporting cells in the chick cochlea. Hearing Research 66(2), 213224Google Scholar
  104. Olivari, F. A., Hernandez, P. P., & Allende, M. L. (2008). Acute copper exposure induces oxidative stress and cell death in lateral line hair cells of zebrafish larvae. Brain Research, 1244, 1–12.PubMedGoogle Scholar
  105. Ou, H. C., Raible, D. W., & Rubel, E. W. (2007). Cisplatin-induced hair cell loss in zebrafish (Danio rerio) lateral line. Hearing Research, 233(1–2), 46–53.PubMedCentralPubMedGoogle Scholar
  106. Ou, H. C., Cunningham, L. L., Francis, S. P., Brandon, C. S., Simon, J. A., Raible, D. W., & Rubel, E. W. (2009). Identification of FDA-approved drugs and bioactives that protect hair cells in the zebrafish (Danio rerio) lateral line and mouse (Mus musculus) utricle. Journal of the Association for Research in Otolaryngology, 10(2), 191–203.PubMedCentralPubMedGoogle Scholar
  107. Owens, K. N., Cunningham, D. E., MacDonald, G., Rubel, E. W., Raible, D. W., & Pujol, R. (2007). Ultrastructural analysis of aminoglycoside-induced hair cell death in the zebrafish lateral line reveals an early mitochondrial response. Journal of Comparative Neurology, 502(4), 522–543.PubMedGoogle Scholar
  108. Owens, K. N., Santos, F., Roberts, B., Linbo, T., Coffin, A. B., Knisely, A. J., Simon, J. A., Rubel, E. W., & Raible, D. W. (2008). Identification of genetic and chemical modulators of zebrafish mechanosensory hair cell death. PLoS Genetics, 4(2), e1000020.PubMedCentralPubMedGoogle Scholar
  109. Owens, K. N., Coffin, A. B., Hong, L. S., Bennett, K. O., Rubel, E. W., & Raible, D. W. (2009). Response of mechanosensory hair cells of the zebrafish lateral line to aminoglycosides reveals distinct cell death pathways. Hearing Research, 253(1–2), 32–41.PubMedCentralPubMedGoogle Scholar
  110. Parinov, S., Kondrichin, I., Korzh, V., & Emelyanov, A. (2004). Tol2 transposon-mediated enhancer trap to identify developmentally regulated zebrafish genes in vivo. Developmental Dynamics, 231(2), 449–459.PubMedGoogle Scholar
  111. Peterson, R. T., Link, B. A., Dowling, J. E., & Schreiber, S. L. (2000). Small molecule developmental screens reveal the logic and timing of vertebrate development. Proceedings of the National Academy of Sciences of the USA, 97(24), 12965–12969.PubMedGoogle Scholar
  112. Postlethwait, J. H., Johnson, S. L., Midson, C. N., Talbot, W. S., Gates, M., Ballinger, E. W., Africa, D., Andrews, R., Carl, T., Eisen, J. S., Horne, S., Kimmel, C. B., Mutchinson, M., Johnson, M., & Rodriguez, A. (1994). A genetic linkage map for the zebrafish. Science, 264(5159), 699–703.PubMedGoogle Scholar
  113. Prezant, R. T., Shohat, M., Jaber, L., Pressman, S., & Fischel-Ghodsian, N. (1992). Biochemical characterization of a pedigree with mitochondrially inherited deafness. American Journal of Medical Genetics, 44(4), 465–472.PubMedGoogle Scholar
  114. Raible, D. W., & Kruse, G. J. (2000). Organization of the lateral line system in embryonic zebrafish. Journal of Comparative Neurology, 421(2), 189–198.PubMedGoogle Scholar
  115. Raviv, D., Dror, A. A., & Avraham, K. B. (2010). Hearing loss: A common disorder caused by many rare alleles. Annals of the New York Academy of Sciences, 1214, 168–179.PubMedCentralPubMedGoogle Scholar
  116. Ricci, A. J., & Fettiplace, R. (1998). Calcium permeation of the turtle hair cell mechanotransducer channel and its relation to the composition of endolymph. Journal of Physiology, 506 (Pt 1), 159–173.PubMedGoogle Scholar
  117. Richardson, G. P., Forge, A., Kros, C. J., Fleming, J., Brown, S. D., & Steel, K. P. (1997). Myosin VIIA is required for aminoglycoside accumulation in cochlear hair cells. Journal of Neuroscience, 17(24), 9506–9519.PubMedGoogle Scholar
  118. Rihel, J., Prober, D. A., Arvanites, A., Lam, K., Zimmerman, S., Jang, S., Haggarty, S. J., Kokel, D., Rubin, L. L., Peterson, R. T., & Schier, A. F. (2010). Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science, 327(5963), 348–351.PubMedCentralPubMedGoogle Scholar
  119. Ruben, R. J. (2000). Redefining the survival of the fittest: Communication disorders in the 21st century. Laryngoscope, 110(2 Pt 1), 241–245.PubMedGoogle Scholar
  120. Ryals, B. M., & Rubel, E. W. (1988). Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science, 240(4860), 1774–1776.PubMedGoogle Scholar
  121. Rybak, L. P., & Ramkumar, V. (2007). Ototoxicity. Kidney International, 72(8), 931–935.PubMedGoogle Scholar
  122. Salvi, R. J., Popper, A. N., & Fay, R. R. (2008). Hair Cell Regeneration, Repair, and Protection. New York: Springer.Google Scholar
  123. Santos, F., MacDonald, G., Rubel, E. W., & Raible, D. W. (2006). Lateral line hair cell maturation is a determinant of aminoglycoside susceptibility in zebrafish (Danio rerio). Hearing Research, 213(1–2), 25–33.PubMedGoogle Scholar
  124. Schacht, J., & Hawkins, J. E. (2006). Sketches of otohistory. Part 11: Ototoxicity: Drug-induced hearing loss. Audiology and Neuro-Otology, 11(1), 1–6.PubMedGoogle Scholar
  125. Schacht, J., Popper, A. N., & Fay, R. R. (2008). Auditory Trauma, Protection, and Repair. New York: Springer.Google Scholar
  126. Schier, A. F., Neuhauss, S. C., Harvey, M., Malicki, J., Solnica-Krezel, L., Stainier, D. Y., Zwartkruis, F., Abdelilah, S., Stemple, D. L., Rangini, Z., Yang, H., & Driever, W. (1996). Mutations affecting the development of the embryonic zebrafish brain. Development, 123, 165–178.PubMedGoogle Scholar
  127. Seiler, C., Ben-David, O., Sidi, S., Hendrich, O., Rusch, A., Burnside, B., Avraham, K. B., & Nicolson, T. (2004). Myosin VI is required for structural integrity of the apical surface of sensory hair cells in zebrafish. Developmental Biology, 272(2), 328–338.PubMedGoogle Scholar
  128. Self, T., Mahony, M., Fleming, J., Walsh, J., Brown, S. D., & Steel, K. P. (1998). Shaker-1 mutations reveal roles for myosin VIIA in both development and function of cochlear hair cells. Development, 125(4), 557–566.PubMedGoogle Scholar
  129. Seligmann, H., Podoshin, L., Ben-David, J., Fradis, M., & Goldsher, M. (1996). Drug-induced tinnitus and other hearing disorders. Drug Safety, 14(3), 198–212.PubMedGoogle Scholar
  130. Sha, S. H., & Schacht, J. (2000). Antioxidants attenuate gentamicin-induced free radical formation in vitro and ototoxicity in vivo D-Methionine is a potential protectant. Hearing Research, 142(1–2), 34–40.PubMedGoogle Scholar
  131. Smith, M. E., Coffin, A. B., Miller, D. L., & Popper, A. N. (2006). Anatomical and functional recovery of the goldfish (Carassius auratus) ear following noise exposure. Journal of Experimental Biology, 209(Pt 21), 4193–4202.PubMedGoogle Scholar
  132. Solnica-Krezel, L., Stemple, D. L., Mountcastle-Shah, E., Rangini, Z., Neuhauss, S. C., Malicki, J., Schier, A. F., Stainier, D. Y., Zwartkruis, F., Abdelilah, S., & Driever, W. (1996). Mutations affecting cell fates and cellular rearrangements during gastrulation in zebrafish. Development, 123, 67–80.PubMedGoogle Scholar
  133. Song, J., Yan, H. Y., & Popper, A. N. (1995). Damage and recovery of hair cells in fish canal (but not superficial) neuromasts after gentamicin exposure. Hearing Research, 91(1–2), 63–71.PubMedGoogle Scholar
  134. Speidel, C. C. (1947). Correlated studies of sense organs and nerves of the lateral-line in living frog tadpoles. Journal of Comparative Neurology, 87, 29–55.PubMedGoogle Scholar
  135. Stemple, D. L., Solnica-Krezel, L., Zwartkruis, F., Neuhauss, S. C., Schier, A. F., Malicki, J., Stainier, D. Y., Abdelilah, S., Rangini, Z., Mountcastle-Shah, E., & Driever, W. (1996). Mutations affecting development of the notochord in zebrafish. Development, 123, 117–128.PubMedGoogle Scholar
  136. Steyger, P. S., Peters, S. L., Rehling, J., Hordichok, A., & Dai, C. F. (2003). Uptake of gentamicin by bullfrog saccular hair cells in vitro. Journal of the Association for Research in Otolaryngology, 4(4), 565–578.PubMedCentralPubMedGoogle Scholar
  137. Stone, J. S., & Cotanche, D. A. (2007). Hair cell regeneration in the avian auditory epithelium. International Journal of Developmental Biology, 51(6–7), 633–647.PubMedGoogle Scholar
  138. Stone, L. (1933). The development of lateral-line sense organs in amphibians observed in living and vital-stained preparations. Journal of Comparative Neurology, 57, 507–540.Google Scholar
  139. Stone, L. (1937). Further experimental studies of the development of lateral-line sense organs in amphibians observed in living preparations. Journal of Comparative Neurology, 68, 83–115.Google Scholar
  140. Suli, A., Watson, G. M., Rubel, E. W., & Raible, D. W. (2012). Rheotaxis in larval zebrafish is mediated by lateral line mechanosensory hair cells. PLoS One, 7(2), e29727.PubMedCentralPubMedGoogle Scholar
  141. Suster, M. L., Kikuta, H., Urasaki, A., Asakawa, K., & Kawakami, K. (2009). Transgenesis in zebrafish with the tol2 transposon system. Methods in Molecular Biology, 561, 41–63.PubMedGoogle Scholar
  142. Ton, C., & Parng, C. (2005). The use of zebrafish for assessing ototoxic and otoprotective agents. Hearing Research, 208(1–2), 79–88.PubMedGoogle Scholar
  143. Trapani, J. G., & Nicolson, T. (2011). Mechanism of spontaneous activity in afferent neurons of the zebrafish lateral-line organ. Journal of Neuroscience, 31(5), 1614–1623.PubMedCentralPubMedGoogle Scholar
  144. Van Trump, W. J., Coombs, S., Duncan, K., & McHenry, M. J. (2010). Gentamicin is ototoxic to all hair cells in the fish lateral line system. Hearing Research, 261 (1–2), 42–50.PubMedGoogle Scholar
  145. Wang, J., Ladrech, S., Pujol, R., Brabet, P., Van De Water, T. R., & Puel, J. L. (2004). Caspase inhibitors, but not c-Jun NH2–terminal kinase inhibitor treatment, prevent cisplatin-induced hearing loss. Cancer Research, 64(24), 9217–9224.Google Scholar
  146. Warchol, M. E. (2011). Sensory regeneration in the vertebrate inner ear: Differences at the levels of cells and species. Hearing Research, 273(1–2), 72–79.PubMedGoogle Scholar
  147. Webb, J. F., Montgomery, J. C., & Mogdans, J. (2008). Bioacoustics and the lateral line system of fishes. In J. F. Webb, R. R. Fay, & A. N. Popper (Eds.), Fish bioacoustics (pp. 145–182). New York: Springer.Google Scholar
  148. Weil, D., Blanchard, S., Kaplan, J., Guilford, P., Gibson, F., Walsh, J., Mburu, P., Varela, A., Levilliers, J., Weston, M. D., Kelley, P. M., Kimberling, W. J., Wagenaar, M., Levi-Acobas, F., Larget-Piet, D., Munnich, A., Steel, K. P., Brown, S. D. M., & Petit, C. (1995). Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature, 374(6517), 60–61.PubMedGoogle Scholar
  149. Weisleder, P., & Rubel, E. W. (1993). Hair cell regeneration after streptomycin toxocity in the avian vestibular epithelium. Journal of Comparative Neurology, 331(1), 97–110.PubMedGoogle Scholar
  150. Wersäll, J., & Flock, Å. (1964). Suppression and restoration of the microphonic output from the lateral line organ after local application of streptomycin. Life Sciences, 3, 1151–1155.Google Scholar
  151. Whitfield, T. T. (2002). Zebrafish as a model for hearing and deafness. Journal of Neurobiology, 53(2), 157–171.PubMedGoogle Scholar
  152. Whitfield, T. T., Granato, M., van Eeden, F. J., Schach, U., Brand, M., Furutani-Seiki, M., Haffter, P., Hammerschmidt, M., Heisenberg, C. P., Jiang, Y. J., Kane, D. A., Kelsh, R. N., Mullins, M. C., Odenthal, J., & Nusslein-Volhard, C. (1996). Mutations affecting development of the zebrafish inner ear and lateral line. Development, 123, 241–254.PubMedGoogle Scholar
  153. Whitfield, T. T., Riley, B. B., Chiang, M. Y., & Phillips, B. (2002). Development of the zebrafish inner ear. Developmental Dynamics, 223(4), 427–458.PubMedGoogle Scholar
  154. Wibowo, I., Pinto-Teixeira, F., Satou, C., Higashijima, S., & Lopez-Schier, H. (2011). Compartmentalized Notch signaling sustains epithelial mirror symmetry. Development, 138(6), 1143–1152.PubMedGoogle Scholar
  155. Williams, J. A., & Holder, N. (2000). Cell turnover in neuromasts of zebrafish larvae. Hearing Research, 143(1–2), 171–181.PubMedGoogle Scholar
  156. World Health Organization (2012). Deafness and Hearing Impairment Fact Sheet, 2012. Retrieved from http://www.who.int/mediacentre/factsheets/fs300/en/ (Accessed March 15, 2012).
  157. Wright, M. R. (1947). Regeneration and degeneration experiments on lateral line nerves and sense organs in anurans. Journal of Experimental Zoology, 105, 221–257.PubMedGoogle Scholar
  158. Xiao, T., Roeser, T., Staub, W., & Baier, H. (2005). A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection. Development, 132(13), 2955–2967.PubMedGoogle Scholar
  159. Zingler, V. C., Cnyrim, C., Jahn, K., Weintz, E., Fernbacher, J., Frenzel, C., Brandt, T., & Strupp, M. (2007). Causative factors and epidemiology of bilateral vestibulopathy in 255 patients. Annals of Neurology, 61(6), 524–532.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, New York 2013

Authors and Affiliations

  1. 1.Neuroscience ProgramWashington State UniversityVancouverUSA
  2. 2.Department of Biological StructureUniversity of WashingtonSeattleUSA
  3. 3.Virginia Merrill Bloedel Hearing Research CenterUniversity of WashingtonSeattleUSA

Personalised recommendations