Biotechnology in the treatment of sensorineural hearing loss: Foundations and future of hair cell regeneration

Journal of Speech, Language, and Hearing Research

Volumn 54, Issue 6, 2011, Pages 1709-1731

  Parker, Mark A ^a,b,c  

^a EMERSON COLLEGE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

Author keywords

Development; Gene therapy; Hair cell; Hearing loss; Regeneration; Stem cell

Indexed keywords

ANIMAL; BIOTECHNOLOGY; GENE THERAPY; HAIR CELL; HUMAN; NERVE REGENERATION; PATHOPHYSIOLOGY; PERCEPTION DEAFNESS; PHYSIOLOGY; REVIEW; STEM CELL TRANSPLANTATION;

ANIMALS; BIOTECHNOLOGY; GENE THERAPY; HAIR CELLS, AUDITORY; HEARING LOSS, SENSORINEURAL; HUMANS; NERVE REGENERATION; STEM CELL TRANSPLANTATION;

EID: 79960005201     PISSN: 10924388     EISSN: None     Source Type: Journal    
DOI: 10.1044/1092-4388(2011/10-0149)     Document Type: Article

References (189)

1. Abello, G., & Alsina, B. (2007). Establishment of a proneural field in the inner ear. The International Journal of Developmental Biology, 51, 483-493.
2. Akazawa, C., Ishibashi, M., Shimizu, C., Nakanishi, S., & Kageyama, R. (1995). A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. The Journal of Biological Chemistry, 270, 8730-8738.
3. Alberts, B., Johnson, A., Lewis, J., & Raff, M. (2007). Molecular biology of the cell (5th ed.). New York, NY: Garland Science.
4. Alford, B.R., & Ruben, R.J. (1963). Physiological, behavioral and anatomical correlates of the development of hearing in the mouse. Annals of Otology, Rhinology & Laryngology, 72, 237-247.
5. Alibardi, L. (2010). Morphological and cellular aspects of tail and limb regeneration in lizards. A model system with implications for tissue regeneration in mammals. Advances in Anatomy, Embryologyo, and Cell Biology, 207, 3, v-x, 1-109.
6. Alsina, B., Giraldez, F., & Pujades, C. (2009). Patterning and cell fate in ear development. The International Journal of Developmental Biology, 53, 1503-1513.
7. Anderson, D. J., Gage, F. H., & Weissman, I. L. (2001). Can stem cells cross lineage boundaries? Nature Medicine, 7, 935-939.
8. Anniko, M. (1983). Cytodifferentiation of cochlear hair cells. American Journal of Otolaryngology, 4, 375-388.
9. Anniko, M., Thornell, L. E., Gustavsson, H., & Virtanen, I. (1986). Intermediate filaments in the newborn inner ear of the mouse. ORL; Journal for Oto-rhino-laryngology and Its Related Specialties, 48, 98-106.
10. Anniko, M., & Wikstrom, S. O. (1984). Pattern formation of the otic placode and morphogenesis of the otocyst. American Journal of Otolaryngology, 5, 373-381.
11. Aposhian, H. V. (1970). The use of DNA for gene therapy-the need, experimental approach, and implications. Perspectives in Biology and Medicine, 14, 98-108.
12. Aposhian, H. V., Barr, S. M., & Keck, K. (1977). Experimental gene delivery systems for mammalian cells-the polyoma pseudovirus system. Advances in Enzyme Regulation, 16, 275-288.
13. Atar, O., & Avraham, K. B. (2005). Therapeutics of hearing loss: Expectations vs reality. Drug Discovery Today, 10, 1323-1330.
14. 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, 79-88.
15. 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, 164-174.
16. Barald, K. F., & Kelley, M. W. (2004). From placode to polarization: New tunes in inner ear development. Development, 131, 4119-4130.
17. Batts, S. A., & Raphael, Y. (2007). Transdifferentiation and its applicability for inner ear therapy. Hearing Research, 227, 41-47.
18. Beadle, E. A. R., McKinley, D. J., Nikolopoulos, T. P., Brough, J., O'Donoghue, G. M., & Archbold, S.M. (2005). Long-term functional outcomes and academic-occupational status in implanted children after 10 to 14 years of cochlear implant use. Otology & Neurotology, 26, 1152-1160.
19. Beisel, K., Hansen, L., Soukup, G., & Fritzsch, B. (2008). Regenerating cochlear hair cells: Quo vadis stem cell. Cell and Tissue Research, 333, 373-379.
20. Ben-Arie, N., Hassan, B. A., Bermingham, N. A., Malicki, D. M., Armstrong, D., Matzuk, M., Zoghbi, H.Y. (2000). Functional conservation of atonal and Math1 in the CNS and PNS. Development, 127, 1039-1048.
21. Berlin, C. I., Morlet, T., & Hood, L. J. (2003). Auditory neuropathy/dyssynchrony: Its diagnosis and management. Pediatric Clinics of North America, 50, 331-340, vii-viii.
22. Bermingham, N. A., Hassan, B. A., Price, S. D., Vollrath, M. A., Ben-Arie, N., Eatock, R. A., Zoghbi, H. Y. (1999, June 11). Math1: An essential gene for the generation of inner ear hair cells. Science, 284, 1837-1841.
23. McDonogh-Bermingham, O., Oesterle, E. C., Stone, J. S., Hume, C. R., Huynh, H. M., & Hayashi, T. (2006). Expression of Prox1 during mouse cochlear development. The Journal of Comparative Neurology, 496, 172-186.
24. Bernstein, A., & Breitman, M. (1989). Genetic ablation in transgenic mice. Molecular Biology & Medicine, 6, 523-530.
25. Blamey, P. J., Dooley, G. J., James, C. J., & Parisi, E. S. (2000). Monaural and binaural loudness measures in cochlear implant users with contralateral residual hearing. Ear and Hearing, 21, 6-17.
26. Boeda, B., Weil, D., & Petit, C. (2001). A specific promoter of the sensory cells of the inner ear defined by transgenesis. Human Molecular Genetics, 10, 1581-1589.
27. Breitman, M. L., Clapoff, S., Rossant, J., Tsui, L. C., Glode, L. M., Maxwell, I. H., & Bernstein, A. (1987, December 11). Genetic ablation: Targeted expression of a toxin gene causes microphthalmia in transgenic mice. Science, 238, 1563-1565.
28. Brigande, J.V., Gubbels, S.P., Woessner, D.W., Jungwirth, J. J., & Bresee, C. S. (2009). Electroporation-mediated gene transfer to the developing mouse inner ear. Methods in Molecular Biology, 493, 125-139.
29. Brigande, J. V., & Heller, S. (2009). Quo vadis, hair cell regeneration? Nature Neuroscience, 12, 679-685.
30. 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.
31. Cao, Q., Benton, R.L., & Whittemore, S. R.(2002). Stem cell repair of central nervous system injury. Journal of Neuro-science Research, 6, 501-510.
32. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W.W., & Prasher, D. C. (1994, February 11). Green fluorescent protein as a marker for gene expression. Science, 263, 802-805.
33. Chen, P., & Segil, N. (1999). p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development, 126, 1581-1590.
34. Chikar, J. A., Colesa, D. J., Swiderski, D. L., Di Polo, A., Raphael, Y., & Pfingst, B. E. (2008). Over-expression of BDNF by adenovirus with concurrent electrical stimulation improves cochlear implant thresholds and survival of auditory neurons. Hearing Research, 245, 24-34.
35. Clark, G. M. (1975). A surgical approach for a cochlear implant: An anatomical study. The Journal of Laryngology and Otology, 89, 9-15.
36. Clark, G. M. (2008). Personal reflections on the multichannel cochlear implant and a view of the future. Journal of Rehabilitation Research & Development, 45, 651-693.
37. Clark, G. M. (2009). The multi-channel cochlear implant: Past, present and future perspectives. Cochlear Implants International, 10(Suppl 1), 2-13.
38. Cohen, S. M., Labadie, R. F., Dietrich, M. S., & Haynes, D. S. (2004). Quality of life in hearing-impaired adults: The role of cochlear implants and hearing aids. Otolaryngology- Head and Neck Surgery, 131, 413-422.
39. Coleman, B., de Silva, M. G., & Shepherd, R. K. (2007). Concisereview: The potential ofstem cells for auditoryneuron generation and replacement. Stem Cells, 25, 2685-2694.
40. Connolly, J. B. (2002). Lentiviruses in gene therapy clinical research. Gene Therapy, 9, 1730-1734.
41. Corrales, C. E., Pan, L., Li, H., Liberman, M. C., Heller, S., & Edge, A. S. (2006). Engraftment and differentiation of embryonic stem cell-derived neural progenitor cells in the cochlear nerve trunk: Growth of processes into the organ of Corti. Journal of Neurobiology, 66, 1489-1500.
42. Corwin, J. T. (1981). Postembryonic production and aging in inner ear hair cells in sharks. The Journal of Comparative Neurology, 201, 541-553.
43. Corwin, J. T., & Cotanche, D. A. (1988, June 24). Regeneration of sensory hair cells after acoustic trauma. Science, 240, 1772-1774.
44. Cotanche, D. A. (1987a). Regenerationof hair cell stereociliary bundles in chick cochlea following severe acoustic trauma. Hearing Research, 30, 181-196.
45. Cotanche, D. A. (1987b). Regeneration of the tectorial membrane in the chick cochlea following severe acoustic trauma. Hearing Research, 30, 197-206.
46. Cotanche, D. A. (2008). Genetic and pharmacological intervention for treatment/prevention of hearing loss. Journal of Communication Disorders, 41, 421-443.
47. Cruz, R. M., Lambert, P. R., & Rubel, E. W. (1987). Light microscopicevidenceofhair cell regenerationaftergentamicin toxicity in chick cochlea. Archives of Otolaryngology-Head & Neck Surgery, 113, 1058-1062.
48. Das, S., & Buchman, C. A. (2005). Bilateral cochlear implantation: Current concepts. Current Opinion in Otolaryngology & Head and Neck Surgery, 13, 290-293.
49. Djourno, A., Eyries, C., & Vallancien, B. (1957). De l'excitation électrique du nerf cochléaire chez l'homme, par induction à distance, à l'aide d'un micro-bobinage inclus à demeure [Electric excitation of the cochlear nerve in man by induction at a distance with the aid of micro-coil included in the fixture]. Comptes Rendus des Séances de la Société de Biologie et de ses Filiales, 151, 423-425.
50. Doetzlhofer, A., Basch, M. L., Ohyama, T., Gessler, M., Groves, A. K., & Segil, N. (2009). Hey2 regulation by FGF provides a Notch-independent mechanism for maintaining pillar cell fate in the organ of Corti. Developmental Cell, 16, 58-69.
51. Donaldson, G. S., Chisolm, T. H., Blasco, G. P., Shinnick, L. J., Ketter, K. J., & Krause, J. C. (2009). BKB-SIN and ANL predict perceived communication ability in cochlear implant users. Ear and Hearing, 30, 401-410.
52. Driver, E. C., & Kelley, M. W. (2009). Specification of cell fate in the mammalian cochlea. Birth Defects Research. Part C, Embryo Today: Reviews, 87, 212-221.
53. Fassati, A., Takahara, Y., Walsh, F.S., & Dickson, G.(1994). Production of high titre helper-free recombinant retroviral vectorsby lipofection. Nucleic Acids Research, 22,1117-1118.
54. Feng, G., Mellor, R. H., Bernstein, M., Keller-Peck, C., Nguyen, Q.T., Wallace, M., Sanes, J. R.(2000). Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron, 28, 41-51.
55. Forge, A., & Schacht, J. (2000). Aminoglycoside antibiotics. Audiology & Neuro-Otology, 5, 3-22.
56. Friedmann, I. (1959). Electron microscope observations on in vitro cultures of the isolated fowl embryo otocyst. The Journal of Biophysical and Biochemical Cytology, 5, 263-268.
57. Fu, Q. J., Hsu, C. J., & Horng, M. J. (2004). Effects of speech processing strategyonChinese tone recognitionby nucleus-24 cochlear implant users. Ear and Hearing, 25, 501-508.
58. Fu, Q. J., Zeng, F. G., Shannon, R. V., & Soli, S. D. (1998). Importance of tonal envelope cues in Chinese speech recognition. The Journal of the Acoustical Society of America, 104, 505-510.
59. Fukuda, M., Okamura, K., Fujita, S., Bohm, N., Rohrbach, R., & Sandritter, W. (1978). The different stem cell populations in mouse epidermis and lingual epithelium. Pathology, Research and Practice, 163, 205-227.
60. Gage, F. H. (2000, February 25). Mammalian neural stem cells. Science, 287, 1433-1438.
61. Gazit, R., Krizhanovsky, V., & Ben-Arie, N. (2004). Math1 controls cerebellar granule cell differentiation by regulating multiple components of the Notch signaling pathway. Development, 131, 903-913.
62. Geers, A.E., Nicholas, J.G., & Sedey, A.L.(2003). Language skills of children with early cochlear implantation. Ear and Hearing, 24(1 Suppl.), 46S-58S.
63. Gfeller, K., Turner, C., Mehr, M., Woodworth, G., Fearn, R., Knutson, J. F., Stordahl, J. (2002). Recognition of familiar melodies by adult cochlear implant recipients and normal-hearing adults. Cochlear Implants International, 3, 29-53.
64. Gilbert, S. F. (2010). Developmental biology (9th ed.). Sunder-land, MA: Sinauer Associates.
65. Gillespie, P. G. (1995). Molecular machinery of auditory and vestibular transduction. Current Opinion in Neurobiology, 5, 449-455.
66. Gordon, J. W., & Ruddle, F. H. (1982). Germ line transmission in transgenic mice. Progress in Clinical and Biological Research, 85(Part B), 111-124.
67. Groves, A. K. (2010). The challenge of hair cell regeneration. Experimental Biology and Medicine, 235, 434-446.
68. Gubbels, S. P., Woessner, D. W., Mitchell, J. C., Ricci, A. J., & Brigande, J. V. (2008, September 25). Functional auditory hair cells produced in the mammalian cochlea by in utero gene transfer. Nature, 455, 537-541.
69. Hakuba, N., Hata, R., Morizane, I., Feng, G., Shimizu, Y., Fujita, K., Gyo, K. (2005). Neural stem cells suppress the hearing threshold shift caused by cochlear ischemia. NeuroReport, 16, 1545-1549.
70. Halliday, A. L., & Cepko, C. L. (1992). Generation and migration of cells in the developing striatum. Neuron, 9, 15-26.
71. Han, J. J., Mhatre, A. N., Wareing, M., Pettis, R., Gao, W. Q., Zufferey, R. N., Lalwani, A. K. (1999). Transgene expression in the guinea pig cochlea mediated by a lentivirus-derived gene transfer vector. Human Gene Therapy, 10, 1867-1873.
72. 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, 219-234.
73. Hartman, B.H., Reh, T.A., & Bermingham-McDonogh, O. (2010). Notch signaling specifies prosensory domains via lateral induction in the developing mammalian inner ear. Proceedings of the National Academy of Sciences, USA, 107, 15792-15797.
74. Hasson, T., Gillespie, P. G., Garcia, J. A., MacDonald, R. B., Zhao, Y.-D., Yee, A. G., Corey, D. P. (1997). Unconventional myosins in inner-ear sensory epithelia. The Journal of Cell Biology, 137, 1287-1307.
75. Hinojosa, R. (1977). A note on development of Corti's organ. Acta Oto-laryngologica, 84, 238-251.
76. Hoffmeister-Ullerich, S. A. (2007). Hydra-ancient model with modern outfit. Cellular and Molecular Life Sciences, 64, 3012-3016.
77. Holley, M. C. (2002). Application of new biological approaches to stimulate sensory repair and protection. British Medical Bulletin, 63, 157-169.
78. Hu, Z., Andang, M., Ni, D., & Ulfendahl, M. (2005). Neural cograft stimulates the survival and differentiation of embryonic stem cells in the adult mammalian auditory system. Brain Research, 1051, 137-144.
79. Iguchi, F., Nakagawa, T., Tateya, I., Kim, T. S., Endo, T., Taniguchi, Z., Ito, J. (2003). Trophic support of mouse inner ear by neural stem cell transplantation. NeuroReport, 14, 77-80.
80. Ito, J., Kojima, K., & Kawaguchi, S. (2001). Survival of neural stem cells in the cochlea. Acta Oto-laryngologica, 121, 140-142.
81. Izumikawa, M., Batts, S. A., Miyazawa, T., Swiderski, D. L., & Raphael, Y. (2008). Response of the flat cochlear epithelium to forced expression of Atoh1. Hearing Research, 240, 52-56.
82. Izumikawa, M., Minoda, R., Kawamoto, K., Abrashkin, K. A., Swiderski, D. L., Dolan, D. F., Raphael, Y. (2005). Auditory hair cell replacement and hearing improvement by atoh1 gene therapy in deaf mammals. Nature Medicine, 11, 271-276.
83. Jarman, A. P., Grau, Y., Jan, L. Y., & Jan, Y. N. (1993). Atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell, 73, 1307-1321.
84. Johnston, J. C, Durieux-Smith, A., Angus, D., O'Connor, A., & Fitzpatrick, E. (2009). Bilateral paediatric cochlear implants: A critical review. International Journal of Audiology, 48, 601-617.
85. Jones, F. W. (1952). The mandible and its relation to the otocyst and auditory organ. The Journal of Laryngology and Otology, 66, 473-479.
86. Jones, J. E., & Corwin, J. T. (1993). Replacement of lateral line sensory organs during tail regeneration in salamanders: Identification of progenitor cells and analysis of leukocyte activity. The Journal of Neuroscience, 13, 1022-1034.
87. Kandel, E., Schwartz, J., & Jessell, T. (2000). Principles of neural science. New York, NY: McGraw-Hill Medical.
88. Kawamoto, K., Ishimoto, S.-I., Minoda, R., Brough, D. E., & Raphael, Y. (2003). Math1 gene transfer generates new cochlear hair cells in mature guinea pigs in vivo. The Journal of Neuroscience, 23, 4395-4400.
89. Kelley, M. W. (2006). Hair cell development: Commitment through differentiation. Brain Research, 1091, 172-185.
90. Kelley, M. W., Talreja, D. R., & Corwin, J. T. (1995). Replacement of hair cells after laser microbeam irradiation in cultured organs of Corti from embryonic and neonatal mice. Journal of Neuroscience, 15, 3013-3026.
91. Kelley, M. W., Xu, X., Wagner, M., Warchol, M., & Corwin, J. T. (1993). The developing organ of Corti contains retinoic acid and forms supernumerary hair cells in response to exogenous retinoic acid in culture. Development, 119, 1041-1053.
92. Kelly, M. C., & Chen, P. (2009). Development of form and function in the mammalian cochlea. Current Opinion in Neurobiology, 19, 395-401.
93. Kessinger, A., Smith, D. M., Strandjord, S. E., Landmark, J. D., Dooley, D. C., Law, P., Armitage, J. O. (1989). Allogeneic transplantation of blood-derived, T cell-depleted hemopoietic stem cells after myeloablative treatment in a patient with acute lymphoblastic leukemia. Bone Marrow Transplantation, 4, 643-646.
94. Kidson, C., & Kirby, K. S. (1964, August 8). Selective alterations of mammalian messenger-RNA synthesis: Evidence for differential action of hormones on gene transcription. Nature, 203, 599-603.
95. Kikuchi, K., & Hilding, D. (1965). The development of the organ of Corti in the mouse. Acta Oto-laryngologica, 60, 207-222.
96. Kim, Y. H., & Raphael, Y. (2007). Cell division and maintenance of epithelial integrity in the deafened auditory epithelium. Cell Cycle, 6, 612-619.
97. Krizhanovsky, V., Golenser, E., & Ben-Arie, N. (2004). Genotype identification of Math1/LacZ knockout mice based on real-time PCR with SYBR Green I dye. Journal of Neuroscience Methods, 136, 187-192.
98. Lang, H., Schulte, B. A., Goddard, J. C., Hedrick, M., Schulte, J. B., Wei, L., & Schmiedt, R. A. (2008). Transplantation of mouse embryonic stem cells into the cochlea of an auditory-neuropathy animal model: Effects of timing after injury. Journal of The Association for Research in Otolaryngology, 9, 225-240.
99. Leblond, C. P., Clermont, Y., & Nadler, N. J. (1967). The pattern of stem cell renewal in three epithelia: (esophagus, intestine and testis). Proceedings, Canadian Cancer Conference, 7, 3-30.
100. Li, H., Liu, H., & Heller, S. (2003). Pluripotent stem cells from the adult mouse inner ear. Nature Medicine, 9, 1293-1299.
101. 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, 166-174.
102. Lowenheim, H., Furness, D.N., Kil, J., Zinn, C., Gultig, K., Fero, M. L., Zenner, H. P. (1999). Gene disruption of p27(Kip1) allows cell proliferation in the postnatal and adult organ of Corti. Proceedings of the National Academy of Sciences, USA, 96, 4084-4088.
103. Luo, X., & Fu, Q.-J. (2004). Enhancing Chinese tone recognition by manipulating amplitude envelope: Implications for cochlear implants. The Journal of the Acoustical Society of America, 116, 3659-3667.
104. Martinez-Monedero, R., Corrales, C.E., Cuajungco, M.P., Heller, S., & Edge, A. S. (2006). Reinnervation of hair cells by auditory neurons after selective removal of spiral ganglion neurons. Journal of Neurobiology, 66, 319-331.
105. Michael, C. T., Wei-Chung, C., Philip, W. B., & Marco, P. (2001). Molecular approach to echinoderm regeneration. Microscopy Research and Technique, 55, 474-485.
106. Mok, M., Grayden, D., Dowell, R. C., & Lawrence, D. (2006). Speech perception for adults who use hearing aids in conjunction with cochlear implants in opposite ears. Journal of Speech, Language, and Hearing Research, 49, 338-351.
107. Molea, D., Stone, J. S., & Rubel, E. W. (1999). Class III beta-tubulin expression in sensory and nonsensory regions of the developing avian inner ear. The Journal of Comparative Neurology, 406, 183-198.
108. Morsli, H., Choo, D., Ryan, A., Johnson, R., & Wu, D. K. (1998). Development of the mouse inner ear and origin of its sensory organs. The Journal of Neuroscience, 18, 3327-3335.
109. Neumann, E., Schaefer-Ridder, M., Wang, Y., & Hofschneider, P. H. (1982). Gene transfer into mouse lyoma cells by electroporation in high electric fields. The EMBO Journal, 1, 841-845.
110. National InstituteonDeafnessand OtherCommunication Disorders (NIDCD). (2003, October, 23). What is hearing loss? A common problem in older adults. NIH Senior Health. Retrieved from http://nihseniorhealth.gov/hearingloss/ hearinglossdefined/01.html.
111. NIDCD. (2008). Statistics about hearing, balance, ear infections, and deafness: Quick statistics. Retrieved from www.nidcd.nih.gov/health/statistics/quick.htm.
112. Nossal, G. J., & Makela, O. (1962). Autoradiographic studies on the immune response.I. The kinetics of plasma cell proliferation. The Journal of Experimental Medicine, 115, 209-230.
113. Okano, T., Nakagawa, T., Endo, T., Kim, T. S., Kita, T., Tamura, T., Ito, J. (2005). Engraftment of embryonic stem cell-derived neurons into the cochlear modiolus. NeuroReport, 16, 1919-1922.
114. Olson, A. D., & Shinn, J. B. (2008). A systematic review to determine the effectiveness of using amplification in conjunction with cochlear implantation. Journal of The American Academy of Audiology, 19, 657-671; quiz 735.
115. Oshima, K., Grimm, C. M., Corrales, C. E., Senn, P., Martinez Monedero, R., Géléoc, G. S. G., Heller, S. (2007). Differential distribution of stem cells in the auditory and vestibular organs of the inner ear. Journal of The Association for Research in Otolaryngology, 8, 18-31.
116. Oshima, K., Senn, P., & Heller, S. (2009). Isolation of sphere-forming stem cells from the mouse inner ear. Methods in Molecular Biology, 493, 141-162.
117. Oshima, K., Shin, K., Diensthuber, M., Peng, A. W., Ricci, A. J., & Heller, S. (2010). Mechanosensitive hair cell-like cells from embryonic and induced pluripotent stem cells. Cell, 141, 704-716.
118. Osterman, J.V., Waddell, A., & Aposhian, H. V.(1970). DNA and gene therapy: Uncoating of polyoma pseudovirus in mouse embryo cells. Proceedings of the National Academy of Sciences, USA, 67, 37-40.
119. Parker, M. A., Corliss, D. A., Anderson, J. K., Liberman, M. C., Snyder, E. Y., & Cotanche, D. A. (2003, February). Neural stem cell transdifferentiation into cochlear cell types. Paper presented at the Annual Meeting of The Association for Research in Otolaryngology, Daytona Beach, FL.
120. Parker, M. A., Corliss, D. A., Gray, B., Anderson, J. K., Bobbin, R. P., Snyder, E. Y., & Cotanche, D. A. (2007). Neural stem cells injected into the sound-damaged cochlea migrate throughout the cochlea and express markers of hair cells, supporting cells, and spiral ganglion cells. Hearing Research, 232, 29-43.
121. Parker, M. A., & Cotanche, D. A. (2004). The potential use of stem cells for cochlear repair. Audiology and Neurootology, 9, 72-80.
122. Parker, M. A., Jiang, K., Adams, J., & Edge, A. S. (2011). TAK1 expression in the cochlea: A specific marker for adult supporting cells. Journal of The Association for Research in Otolaryngology: JARO, 12, 471-483.
123. Parving, A.(2003). The hearing aid revolution: Fact or fiction? Acta Oto-laryngologica, 123, 245-248.
124. Patel, N. P., Mhatre, A. N., & Lalwani, A. K. (2004). Biological therapy for the inner ear. Expert Opinion on Biological Therapy, 4, 1811-1819.
125. Pathak, A., Patnaik, S., & Gupta, K.C.(2009). Recent trends in non-viral vector-mediated gene delivery. Biotechnology Journal, 4, 1559-1572.
126. Pattillo, R. A., Gey, G. O., Delfs, E., & Mattingly, R. F. (1968). In vitro identification of the trophoblastic stem cell of the human villous placenta. American Journal of Obstetrics and Gynecology, 100, 582-588.
127. Peng, S. C., Tomblin, J. B., Cheung, H., Lin, Y. S., & Wang, L. S. (2004). Perception and production of Mandarin tones in prelingually deaf children with cochlear implants. Ear and Hearing, 25, 251-264.
128. Plyler, P. N., Bahng, J., & von Hapsburg, D. (2008). The acceptance of background noise in adult cochlear implant users. Journal of Speech, Language, and Hearing Research, 51, 502-515.
129. Prasher, D., McCann, R. O., & Cormier, M. J. (1985). Cloning and expression of the cDNA coding for aequorin, a bioluminescent calcium-binding protein. Biochemical and Biophysical Research Communications, 126, 1259-1268.
130. Pujol, R., & Hilding, D. (1973). Anatomy and physiology of the onset of auditory function. Acta Oto-laryngologica, 76, 1-10.
131. Raphael, Y., & Altschuler, R. A. (2003). Structure and in-nervation of the cochlea [Review]. Brain Research Bulletin, 60, 397-422.
132. Raphael, Y., Kim, Y. H., Osumi, Y., and I zumikawa, M. (2007). Non-sensory cells in the deafened organ of Corti: Approaches for repair. The International Journal of Developmental Biology, 51, 649-654.
133. Rejali, D., Lee, V. A., Abrashkin, K. A., Humayun, N., Swiderski, D. L., & Raphael, Y. (2007). Cochlear implants and ex vivo BDNF gene therapy protect spiral ganglion neurons. Hearing Research, 228, 180-187.
134. Reynolds, B. A., & Weiss, S. (1992, March 27). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science, 255, 1707-1710.
135. Rio, C., Dikkes, P., Liberman, M. C., & Corfas, G. (2002). Glial fibrillary acidic protein expression and promoter activity in the inner ear of developing and adult mice. The Journal of Comparative Neurology, 442, 156-162.
136. Roberson, D. W., Alosi, J. A., & Cotanche, D. A. (2004). Direct transdifferentiation gives rise to the earliest new hair cells in regenerating avian auditory epithelium. Journal of Neuroscience Research, 78, 461-471.
137. Roy, S., & Gatien, S. (2008). Regenerationin axolotls:A model to aim for! Experimental Gerontology, 43, 968-973.
138. Ruben, R. J. (1967). Development of the inner ear of the mouse: A radioautographic study of terminal mitoses. Acta Oto-Laryngologica, 1967(Suppl. 220), 1-44.
139. Ryals, B. M., & Rubel, E. W. (1988, June 24). Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science, 240, 1774-1776.
140. Ryals, B. M., & Westbrook, E. W. (1994). TEM analysis of neural terminals on autoradiographically identified regenerated hair cells. Hearing Research, 72, 81-88.
141. Sahly, I., El-Amraoui, A., Abitbol, M., Petit, C., & Dufier, J. L. (1997). Expression of myosin VIIA during mouse embryogenesis. Anatomy and Embryology, 196, 159-170.
142. Sakamoto, T., Nakagawa, T., Endo, T., Kim, T. S., Iguchi, F., Naito, Y., Ito, J. (2004). Fates of mouse embryonic stem cells transplanted into the inner ears of adult mice and embryonic chickens. Acta Oto-Laryngologica, 2004(Suppl. 551), 48-52.
143. Saunders, S. S., Salvi, R. J., & Miller, K.M. (1995). Recovery of thresholds and temporal integration in adult chickens after high-level 525-Hz pure-tone exposure. The Journal of the Acoustical Society of America, 97, 1150-1164.
144. Schneider-Maunoury, S., & Pujades, C. (2007). Hindbrain signals in otic regionalization: Walk on the wild side. The International Journal of Developmental Biology, 51, 495-506.
145. Schwander, M., Kachar, B., & Muller, U. (2010). Review series: The cell biology of hearing. Journal of Cell Biology, 190, 9-20.
146. Senn, P., Oshima, K., Teo, D., Grimm, C., & Heller, S. (2007). Robust postmortem survival of murine vestibular and cochlear stem cells. Journal of the Association for Research in Otolaryngology, 8, 194-204.
147. Shi, F., Corrales, C. E., Liberman, M. C., & Edge, A. S. (2007). BMP4 induction of sensory neurons from human embryonic stem cells and reinnervation of sensory epithelium. The European Journal of Neuroscience, 26, 3016-3023.
148. Shihabuddin, L. S., Ray, J., & Gage, F. H. (1999). Stem cell technology for basic science and clinical applications. Archives of Neurology, 56, 29-32.
149. Shimizu, C., Akazawa, C., Nakanishi, S., & Kageyama, R. (1995). MATH-2, a mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal, is specifically expressed in the nervous system. European Journal of Biochemistry, 229, 239-248.
150. Shimomura, O., Johnson, F. H., & Saiga, Y. (1962). Extraction, purification and properties ofaequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. Journal of Cellular and Comparative Physiology, 59, 223-239.
151. Snyder, B. R., Boulis, N. M., & Federici, T. (2010). Viral vector-mediated gene transfer for CNS disease. Expert Opinion on Biological Therapy, 10, 381-394.
152. Snyder, E. Y., Yoon, C., Flax, J. D., & Macklis, J. D. (1997). Multipotent neural precursors can differentiate toward replacement of neurons undergoing targeted apoptotic degeneration in adult mouse neocortex. Proceedings of the National Academy of Sciences, USA, 94, 11663-11668.
153. Somerville, R. L., & Yanofsky, C. (1964). On the translation of the A gene region of tryptophan messenger RNA. Journal of Molecular Biology, 8, 616-619.
154. Srinivasan, R. S., Dillard, M. E., Lagutin, O. V., Lin, F. J., Tsai, S., Tsai, M. J., Oliver, G. (2007). Lineage tracing demonstrates the venous originof the mammalian lymphatic vasculature. Genes & Development, 21, 2422-2432.
155. Stewart, P. L., Fuller, S. D., & Burnett, R. M. (1993). Difference imaging of adenovirus: Bridging the resolution gap between X-ray crystallography and electron microscopy. The EMBO Journal, 12, 2589-2599.
156. Stone, J. S., & Cotanche, D. A. (1994). Identification of the timingof S phase and the patternsof cell proliferation during hair cell regeneration in the chick cochlea. The Journal of Comparative Neurology, 341, 50-67.
157. Stone, J. S., & Cotanche, D. A. (2007). Hair cell regeneration in the avian auditory epithelium. The International Journal of Developmental Biology, 51, 633-647.
158. Stone, J. S., & Rubel, E. W. (2000). Cellular studies of auditory hair cell regeneration in birds. Proceedings of the National Academy of Sciences, USA, 97, 11714-11721.
159. Streit, A. (2007). The preplacodal region: An ectodermal domain with multipotential progenitors that contribute to sense organs and cranial sensory ganglia. The International Journal of Developmental Biology, 51, 447-461.
160. Tan, B. T., Lee, M. M., & Ruan, R. (2008). Bone-marrow-derived cellsthathometoacoustic deafenedcochlea preserved their hematopoietic identity. The Journal of Comparative Neurology, 509, 167-179.
161. Tateya, I., Nakagawa, T., Iguchi, F., Kim, T. S., Endo, T., Yamada, S., Ito, J. (2003). Fate of neural stem cells grafted into injured inner ears of mice. NeuroReport, 14, 1677-1681.
162. Teng, Y. D., Lavik, E. B., Qu, X., Park, K. I., Ourednik, J., Zurakowski, D., Snyder, E. Y. (2002). Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proceedings of the National Academy of Sciences, USA, 99, 3024-3029.
163. Thelen, N., Breuskin, I., Malgrange, B., & Thiry, M. (2009). Early identification of inner pillar cells during rat cochlear development. Cell and Tissue Research, 337, 1-14.
164. Tritsch, N. X., Yi, E., Gale, J. E., Glowatzki, E., & Bergles, D. E. (2007, November 1). The origin of spontaneous activity in the developing auditory system. Nature, 450, 50-55.
165. Turner, C. W., Reiss, L. A., & Gantz, B. J. (2008). Combined acoustic and electric hearing: Preserving residual acoustic hearing. Hearing Research, 242, 164-171.
166. Uziel, A. S., Sillon, M., Vieu, A., Artieres, F., Piron, J.-P., Daures, J.-P., & Mondain, M. (2007). Ten-year follow-up of a consecutive series of children with multichannel cochlear implants. Otology & Neurotology, 28, 615-628.
167. Vuorialho, A., Karinen, P., & Sorri, M. (2006). Effect of hearing aids on hearing disability and quality of life in the elderly. International Journal of Audiology, 45, 400-405.
168. Waltzman, S. B., Cohen, N. L., & Shapiro, W. H. (1992). Sensory aids in conjunction with cochlear implants. The American Journal of Otology, 13, 308-312.
169. Wang, Y., Hirose, K., & Liberman, M. C. (2002). Dynamics of noise-induced cellular injury and repair in the mouse cochlea. Journal of The Association for Research in Otolar-yngology, 3, 248-268.
170. Warchol, M. E., Lambert, P. R., Goldstein, B. J., Forge, A., & Corwin, J. T. (1993, March 12). Regenerative proliferation in inner ear sensory epithelia from adult guinea pigs and humans. Science, 259, 1619-1622.
171. Wei, D., Levic, S., Nie, L., Gao, W. Q., Petit, C., Jones, E. G., & Yamoah, E. N. (2008). Cells of adult brain germinal zone have properties akin to hair cells and can be used to replace inner ear sensory cells after damage. Proceedings of the National Academy of Sciences, USA, 105, 21000-21005.
172. Weissman, I. L. (2000). Stem cells: Units of development, units of regeneration, and units in evolution. Cell, 100, 157-168.
173. Weissman, I. L., Anderson, D. J., & Gage, F. (2001). Stem and progenitor cells: Origins, phenotypes, lineage commitments, and transdifferentiations. Annual Review of Cell and Developmental Biology, 17, 387-403.
174. White, P. M., Doetzlhofer, A., Lee, Y. S., Groves, A. K., & Segil, N. (2006, June 22). Mammalian cochlear supporting cells can divide and trans-differentiate into hair cells. Nature, 441, 984-987.
175. Whitfield, T. T., & Hammond, K. L. (2007). Axial patterning in the developing vertebrate inner ear. The International Journal of Developmental Biology, 51, 507-520.
176. Wilhelm, J. M., Johnson, G., Haselkorn, R., & Geiduschek, E. P. (1972). Specific inhibition of bacteriophage SPO1 DNA-directed protein synthesis by the SPO1 transcription factor, TF 1. Biochemical and Biophysical Research Communications, 46, 1970-1977.
177. Wilson, B. S., & Dorman, M. F. (2008a). Cochlear implants: A remarkable past and a brilliant future. Hearing Research, 242, 3-21.
178. Wilson, B. S., & Dorman, M. F. (2008b). Cochlear implants: Current designs and future possibilities. Journal of Rehabilitation Research and Development, 45, 695-730.
179. Wilson, B. S., Lawson, D. T., Muller, J. M., Tyler, R. S., & Kiefer, J. (2003). Cochlear implants: Some likely next steps. Annual Review of Biomedical Engineering, 5, 207-249.
180. Wilson, D. R. (2002). Viral-mediated gene transfer for cancer treatment. Current Pharmaceutical Biotechnology, 3, 151-164.
181. Wislocki, G. B., & Ladman, A. J. (1955). Selective and histo-chemical staining of the otolithic membranes, cupulae and tectorial membrane of the inner ear. Journal of Anatomy, 89, 3-12.
182. Woods, C., Montcouquiol, M., & Kelley, M.W.(2004). Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nature Neuroscience, 7, 1310-1318.
183. Yagi, M., Kanzaki, S., Kawamoto, K., Shin, B., Shah, P. P., Magal, E., Raphael, Y. (2000). Spiral ganglion neurons are protected from degeneration by GDNF gene therapy. Journal of The Association for Research in Otolaryngology 1, 315-325.
184. Young, L. S., Searle, P. F., Onion, D., & Mautner, V. (2006). Viral gene therapy strategies: From basic science to clinical application. The Journal of Pathology, 208, 299-318.
185. Zhai, S., Shi, L., Wang, B. E., Zheng, G., Song, W., Hu, Y., Gao, W. Q. (2005). Isolation and culture of hair cell progenitors from postnatal rat cochleae. Journal of Neurobiology, 65, 282-293.
186. Zhang, Y., Zhai, S.-Q., Shou, J., Song, W., Sun, J.-H., Guo, W., & Gao, W. Q. (2007). Isolation, growth and differentiation of hair cell progenitors from the newborn rat cochlear greater epithelial ridge. Journal of Neuroscience Methods, 164, 271-279.
187. Zheng, J. L., & Gao, W. Q. (2000). Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nature Neuroscience, 3, 580-586.
188. Zheng, J. L., Lewis, A. K., & Gao, W. Q. (1998). Establishment of conditionally immortalized rat utricular epithelial cell lines usingaretrovirus-mediated gene transfer technique. Hearing Research, 117, 13-23.
189. Zine, A., Van De Water, T. R., & de Ribaupierre, F. (2000). Notch signaling regulates the pattern of auditory hair cell differentiation in mammals. Development, 127, 3373-3383.