Inner ear protection and regeneration: A 'historical' perspective

Current Opinion in Otolaryngology and Head and Neck Surgery

Volumn 17, Issue 5, 2009, Pages 363-372

  Diaz, Rodney C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Direct transdifferentiation; Endocochlear potential; Gene therapy; Stem cells

Indexed keywords

AMINOGLYCOSIDE ANTIBIOTIC AGENT; CASPASE 3; CASPASE 9;

APOPTOSIS; CELL PROTECTION; CELL REGENERATION; EAR INJURY; EAR PROTECTION; ENZYME ACTIVATION; HAIR CELL; HUMAN; INNER EAR; METABOLIC REGULATION; NONHUMAN; OTOTOXICITY; PRIORITY JOURNAL; REHABILITATION CARE; REVIEW; SPIRAL GANGLION; STRIA VASCULARIS;

ANIMALS; APOPTOSIS; CASPASE 3; CASPASE 9; CELL DIFFERENTIATION; CELL SURVIVAL; EAR, INNER; EFLORNITHINE; ELECTRIC STIMULATION; ENZYME INHIBITORS; HAIR CELLS, AUDITORY, INNER; HUMANS; OXIDATIVE STRESS; REGENERATION; SPIRAL GANGLION;

EID: 70349669407     PISSN: 10689508     EISSN: None     Source Type: Journal    
DOI: 10.1097/MOO.0b013e3283303513     Document Type: Review

References (203)

1. McHaney VA, Thibadoux G, Hayes FA, et al. Hearing loss in children receiving cisplatin chemotherapy. J Pediatr 1983; 102:314-317. (Pubitemid 13194726)
2. Rybak LP. Drug ototoxicity. Annu Rev Pharmacol Toxicol 1986; 26:79-99.
3. Schacht J, Weiner N. Aminoglycoside-induced hearing loss: a molecular hypothesis. ORL J Otorhinolaryngol Relat Spec 1986; 48:116-123. (Pubitemid 16125829)
4. Schell MJ, McHaney VA, Green AA, et al. Hearing loss in children and young adults receiving cisplatin with or without prior cranial irradiation. J Clin Oncol 1989; 7:754-760.
5. Stennicke HR, Salvesen GS. Caspases: controlling intracellular signals by protease zymogen activation. Biochim Biophys Acta 2000; 1477:299-306.
6. Borner C. The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Mol Immunol 2003; 39:615-647. (Pubitemid 35454076)
7. Lindsten T, Zong WX, Thompson CB. Defining the role of the Bcl-2 family of proteins in the nervous system. Neuroscientist 2005; 11:10-15. (Pubitemid 40223086)
8. Gross A, Jockel J, Wei MC, et al. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J 1998; 17:3878-3885. (Pubitemid 28333974)
9. Slee EA, Adrain C, Martin SJ. Executioner caspase-3, -6, and -7 perform distinct, nonredundant roles during the demolition phase of apoptosis. J Biol Chem 2001; 276:7320-7326. (Pubitemid 37392038)
10. Cheng AG, Cunningham LL, Rubel EW. Mechanisms of hair cell death and protection. Curr Opin Otolaryngol Head Neck Surg 2005; 13:343-348. (Pubitemid 41682251)
11. Ip YT, Davis RJ. Signal transduction by the c-Jun N-terminal kinase (JNK): from inflammation to development. Curr Opin Cell Biol 1998; 10:205-219. (Pubitemid 28174763)
12. Zine A, van de Water TR. The MAPK/JNK signalling pathway offers potential therapeutic targets for the prevention of acquired deafness. Curr Drug Targets CNS Neurol Disord 2004; 3:325-332. (Pubitemid 39242918)
13. Hutchin T, Cortopassi G. Proposed molecular and cellular mechanism for aminoglycoside ototoxicity. Antimicrob Agents Chemother 1994; 38:2517-2520. (Pubitemid 24332579)
14. Dehne N, Rauen U, de Groot H, et al. Involvement of the mitochondrial permeability transition in gentamicin ototoxicity. Hear Res 2002; 169:47-55. (Pubitemid 34733018)
15. Perier C, Tieu K, Guegan C, et al. Complex I deficiency primes Bax-dependent neuronal apoptosis through mitochondrial oxidative damage. Proc Natl Acad Sci U S A 2005; 102:19126-19131. (Pubitemid 43049577)
16. Cunningham LL, Cheng AG, Rubel EW. Caspase activation in hair cells of the mouse utricle exposed to neomycin. J Neurosci 2002; 22:8532-8540.
17. Lee JE, Nakagawa T, Kim TS, et al. Signaling pathway for apoptosis of vestibular hair cells of mice due to aminoglycosides. Acta Otolaryngol Suppl 2004:69-74. (Pubitemid 38388644)
18. Cunningham LL, Matsui JI, Warchol ME, et al. Overexpression of Bcl-2 prevents neomycin-induced hair cell death and caspase-9 activation in the adult mouse utricle in vitro. J Neurobiol 2004; 60:89-100.
19. Pirvola U, Xing-Qun L, Virkkala J, et al. Rescue of hearing, auditory hair cells, and neurons by CEP-1347/KT7515, an inhibitor of c-Jun N-terminal kinase activation. J Neurosci 2000; 20:43-50. (Pubitemid 30220489)
20. Ylikoski J, Xing-Qun L, Virkkala J, et al. Blockade of c-Jun N-terminal kinase pathway attenuates gentamicin-induced cochlear and vestibular hair cell death. Hear Res 2002; 166:33-43. (Pubitemid 34626457)
21. Wang J, Van De Water TR, Bonny C, et al. A peptide inhibitor of c-Jun N-terminal kinase protects against both aminoglycoside and acoustic trauma-induced auditory hair cell death and hearing loss. J Neurosci 2003; 23:8596-8607. (Pubitemid 37158759)
22. Siddik ZH. Cisplatin: mode of cytotoxic action and molecular basis of resistance. Oncogene 2003; 22:7265-7279.
23. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000; 408:307-310.
24. Pozniak CD, Barnabe-Heider F, Rymar VV, et al. p73 is required for survival and maintenance of CNS neurons. J Neurosci 2002; 22:9800-9809. (Pubitemid 35332864)
25. Devarajan P, Savoca M, Castaneda MP, et al. Cisplatin-induced apoptosis in auditory cells: role of death receptor and mitochondrial pathways. Hear Res 2002; 174:45-54. (Pubitemid 35305031)
26. Wang J, Ladrech S, Pujol R, et al. Caspase inhibitors, but not c-Jun NH2- terminal kinase inhibitor treatment, prevent cisplatin-induced hearing loss. Cancer Res 2004; 64:9217-9224. (Pubitemid 39665538)
27. Zhang M, Liu W, Ding D, et al. Pifithrin-alpha suppresses p53 and protects cochlear and vestibular hair cells from cisplatin-induced apoptosis. Neuroscience 2003; 120:191-205. (Pubitemid 36782642)
28. Cotanche DA, Saunders JC, Tilney LG. Hair cell damage produced by acoustic trauma in the chick cochlea. Hear Res 1987; 25:267-286.
29. Barrenas ML. Hair cell loss from acoustic trauma in chloroquine-treated red, black and albino guinea pigs. Audiology 1997; 36:187-201. (Pubitemid 27348189)
30. Patuzzi R. Nonlinear aspects of outer hair cell transduction and the temporary threshold shifts after acoustic trauma. Audiol Neurootol 2002; 7:17-20. (Pubitemid 34253005)
31. Chen YS, Liu TC, Cheng CH, et al. Changes of hair cell stereocilia and threshold shift after acoustic trauma in guinea pigs: comparison between inner and outer hair cells. ORL J Otorhinolaryngol Relat Spec 2003; 65: 266-274.
32. Hu BH, Henderson D, Nicotera TM. Involvement of apoptosis in progression of cochlear lesion following exposure to intense noise. Hear Res 2002; 166:62-71. (Pubitemid 34626460)
33. Nicotera TM, Hu BH, Henderson D. The caspase pathway in noise-induced apoptosis of the chinchilla cochlea. J Assoc Res Otolaryngol 2003; 4:466-477. (Pubitemid 38112631)
34. Yang WP, Henderson D, Hu BH, et al. Quantitative analysis of apoptotic and necrotic outer hair cells after exposure to different levels of continuous noise. Hear Res 2004; 196:69-76. (Pubitemid 39298897)
35. Hu BH, Henderson D, Nicotera TM. Extremely rapid induction of outer hair cell apoptosis in the chinchilla cochlea following exposure to impulse noise. Hear Res 2006; 211:16-25. (Pubitemid 43112407)
36. Clerici WJ, DiMartino DL, Prasad MR. Direct effects of reactive oxygen species on cochlear outer hair cell shape in vitro. Hear Res 1995; 84:30-40.
37. Korsmeyer SJ, Yin XM, Oltvai ZN, et al. Reactive oxygen species and the regulation of cell death by the Bcl-2 gene family. Biochim Biophys Acta 1995; 1271:63-66.
38. Hirose K, Hockenbery DM, Rubel EW. Reactive oxygen species in chick hair cells after gentamicin exposure in vitro. Hear Res 1997; 104:1-14. (Pubitemid 27092045)
39. Henderson D, McFadden SL, Liu CC, et al. The role of antioxidants in protection from impulse noise. Ann N Y Acad Sci 1999; 884:368-380.
40. Ohlemiller KK, Wright JS, Dugan LL. Early elevation of cochlear reactive oxygen species following noise exposure. Audiol Neurootol 1999; 4:229-236.
41. Takumida M, Anniko M, Shimizu A, et al. Neuroprotection of vestibular sensory cells from gentamicin ototoxicity obtained using nitric oxide synthase inhibitors, reactive oxygen species scavengers, brain-derived neurotrophic factors and calpain inhibitors. Acta Otolaryngol 2003; 123:8-13. (Pubitemid 36216504)
42. Rybak LP, Husain K, Evenson L, et al. Protection by 4-methylthiobenzoic acid against cisplatin-induced ototoxicity: antioxidant system. Pharmacol Toxicol 1997; 81:173-179. (Pubitemid 27432572)
43. Husain K, Scott RB, Whitworth C, et al. Dose response of carboplatin-induced hearing loss in rats: antioxidant defense system. Hear Res 2001; 151:71-78.
44. Rybak LP, Husain K, Whitworth C, et al. Dose dependent protection by lipoic acid against cisplatin-induced ototoxicity in rats: antioxidant defense system. Toxicol Sci 1999; 47:195-202. (Pubitemid 29214827)
45. Somani SM, Husain K, Whitworth C, et al. Dose-dependent protection by lipoic acid against cisplatin-induced nephrotoxicity in rats: antioxidant defense system. Pharmacol Toxicol 2000; 86:234-241. (Pubitemid 30333651)
46. Sha SH, Zajic G, Epstein CJ, et al. Overexpression of copper/zinc-superoxide dismutase protects from kanamycin-induced hearing loss. Audiol Neurootol 2001; 6:117-123. (Pubitemid 32710231)
47. Hight NG, McFadden SL, Henderson D, et al. Noise-induced hearing loss in chinchillas pretreated with glutathione monoethylester and R-PIA. Hear Res 2003; 179:21-32. (Pubitemid 36547887)
48. Kawamoto K, Sha SH, Minoda R, et al. Antioxidant gene therapy can protect hearing and hair cells from ototoxicity. Mol Ther 2004; 9:173-181. (Pubitemid 38256543)
49. Lynch ED, Gu R, Pierce C, et al. Ebselen-mediated protection from single and repeated noise exposure in rat. Laryngoscope 2004; 114:333-337. (Pubitemid 38182634)
50. Husain K, Whitworth C, Somani SM, et al. Partial protection by lipoic acid against carboplantin-induced ototoxicity in rats. Biomed Environ Sci 2005; 18:198-206. (Pubitemid 41127548)
51. Canlon B, Borg E, Flock A. Protection against noise trauma by preexposure to a low level acoustic stimulus. Hear Res 1988; 34:197-200. (Pubitemid 18186290)
52. Subramaniam M, Henderson D, Spongr VP. Protection from noise induced hearing loss: is prolonged 'conditioning' necessary? Hear Res 1993; 65: 234-239.
53. Ryan AF, Bennett TM, Woolf NK, et al. Protection from noise-induced hearing loss by prior exposure to a nontraumatic stimulus: role of the middle ear muscles. Hear Res 1994; 72:23-28.
54. Canlon B. Protection against noise trauma by sound conditioning. Ear Nose Throat J 1997; 76:248-250; 253-1245 (Pubitemid 27181139)
55. McFadden SL, Zheng XY, Ding DL. Conditioning-induced protection from impulse noise in female and male chinchillas. J Acoust Soc Am 2000; 107: 2162-2168.
56. Niu X, Tahera Y, Canlon B. Protection against acoustic trauma by forward and backward sound conditioning. Audiol Neurootol 2004; 9:265-273. (Pubitemid 39370259)
57. Paz Z, Freeman S, Horowitz M, et al. Prior heat acclimation confers protection against noise-induced hearing loss. Audiol Neurootol 2004; 9:363-369. (Pubitemid 39482543)
58. Canlon B, Fransson A, Viberg A. Medial olivocochlear efferent terminals are protected by sound conditioning. Brain Res 1999; 850:253-260.
59. Le Prell CG, Dolan DF, Schacht J, et al. Pathways for protection from noise induced hearing loss. Noise Health 2003; 5:1-17. (Pubitemid 37236415)
60. Nishida A, Takahashi M, Tanihara H, et al. Incorporation and differentiation of hippocampus-derived neural stem cells transplanted in injured adult rat retina. Invest Ophthalmol Vis Sci 2000; 41:4268-4274.
61. Ito J, Kojima K, Kawaguchi S. Survival of neural stem cells in the cochlea. Acta Otolaryngol 2001; 121:140-142. (Pubitemid 32328554)
62. Iguchi F, Nakagawa T, Tateya I, et al. Trophic support of mouse inner ear by neural stem cell transplantation. Neuroreport 2003; 14:77-80. (Pubitemid 36160746)
63. Tateya I, Nakagawa T, Iguchi F, et al. Fate of neural stem cells grafted into injured inner ears of mice. Neuroreport 2003; 14:1677-1681. (Pubitemid 37323752)
64. Sakamoto T, Nakagawa T, Endo T, et al. Fates of mouse embryonic stem cells transplanted into the inner ears of adult mice and embryonic chickens. Acta Otolaryngol Suppl 2004:48-52. (Pubitemid 38388639)
65. Li H, Roblin G, Liu H, et al. Generation of hair cells by stepwise differentiation of embryonic stem cells. Proc Natl Acad Sci U S A 2003; 100:13495-13500. (Pubitemid 37444770)
66. Kojima K, Murata M, Nishio T, et al. Survival of fetal rat otocyst cells grafted into the damaged inner ear. Acta Otolaryngol Suppl 2004:53-55. (Pubitemid 38388640)
67. Barald KF, Lindberg KH, Hardiman K, et al. Immortalized cell lines from embryonic avian and murine otocysts: tools for molecular studies of the developing inner ear. Int J Dev Neurosci 1997; 15:523-540. (Pubitemid 27332103)
68. Rivolta MN, Grix N, Lawlor P, et al. Auditory hair cell precursors immortalized from the mammalian inner ear. Proc Biol Sci 1998; 265:1595-1603. (Pubitemid 28442081)
69. Malgrange B, Belachew S, Thiry M, et al. Proliferative generation of mammalian auditory hair cells in culture. Mech Dev 2002; 112:79-88. (Pubitemid 34163222)
70. Li H, Liu H, Heller S. Pluripotent stem cells from the adult mouse inner ear. Nat Med 2003; 9:1293-1299. (Pubitemid 37279853)
71. Taylor R, Forge A. Developmental biology. Life after deaf for hair cells? Science 2005; 307:1056-1058.
72. Cruz RM, Lambert PR, Rubel EW. Light microscopic evidence of hair cell regeneration after gentamicin toxicity in chick cochlea. Arch Otolaryngol Head Neck Surg 1987; 113:1058-1062.
73. Corwin JT, Cotanche DA. Regeneration of sensory hair cells after acoustic trauma. Science 1988; 240:1772-1774. (Pubitemid 18172313)
74. Ryals BM, Rubel EW. Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 1988; 240:1774-1776.
75. Jones JE, Corwin JT. Regeneration of sensory cells after laser ablation in the lateral line system: hair cell lineage and macrophage behavior revealed by time-lapse video microscopy. J Neurosci 1996; 16:649-662.
76. Taylor RR, Forge A. Hair cell regeneration in sensory epithelia from the inner ear of a urodele amphibian. J Comp Neurol 2005; 484:105-120. (Pubitemid 40315408)
77. Fekete DM, Muthukumar S, Karagogeos D. Hair cells and supporting cells share a common progenitor in the avian inner ear. J Neurosci 1998; 18: 7811-7821. (Pubitemid 28441021)
78. Girod DA, Duckert LG, Rubel EW. Possible precursors of regenerated hair cells in the avian cochlea following acoustic trauma. Hear Res 1989; 42:175-194.
79. Raphael Y. Evidence for supporting cell mitosis in response to acoustic trauma in the avian inner ear. J Neurocytol 1992; 21:663-671.
80. Raphael Y. Reorganization of the chick basilar papilla after acoustic trauma. J Comp Neurol 1993; 330:521-532. (Pubitemid 23113306)
81. Stone JS, Cotanche DA. Identification of the timing of S phase and the patterns of cell proliferation during hair cell regeneration in the chick cochlea. J Comp Neurol 1994; 341:50-67.
82. Stone JS, Choi YS, Woolley SM, et al. Progenitor cell cycling during hair cell regeneration in the vestibular and auditory epithelia of the chick. J Neurocytol 1999; 28:863-876.
83. Beresford WA. Direct transdifferentiation: can cells change their phenotype without dividing? Cell Differ Dev 1990; 29:81-93.
84. Adler HJ, Komeda M, Raphael Y. Further evidence for supporting cell conversion in the damaged avian basilar papilla. Int J Dev Neurosci 1997; 15:375-385. (Pubitemid 27332093)
85. Li L, Forge A. Morphological evidence for supporting cell to hair cell conversion in the mammalian utricular macula. Int J Dev Neurosci 1997; 15:433-446. (Pubitemid 27332097)
86. Baird RA, Burton MD, Fashena DS, et al. Hair cell recovery in mitotically blocked cultures of the bullfrog saccule. Proc Natl Acad Sci U S A 2000; 97:11722-11729.
87. Roberson DW, Alosi JA, Cotanche DA. Direct transdifferentiation gives rise to the earliest new hair cells in regenerating avian auditory epithelium. J Neurosci Res 2004; 78:461-471.
88. Carnicero E, Zelarayan LC, Ruttiger L, et al. Differential roles of fibroblast growth factor-2 during development and maintenance of auditory sensory epithelia. J Neurosci Res 2004; 77:787-797. (Pubitemid 39187063)
89. Zheng JL, Frantz G, Lewis AK, et al. Heregulin enhances regenerative proliferation in postnatal rat utricular sensory epithelium after ototoxic damage. J Neurocytol 1999; 28:901-912. (Pubitemid 30617136)
90. Hume CR, Kirkegaard M, Oesterle EC. ErbB expression: the mouse inner ear and maturation of the mitogenic response to heregulin. J Assoc Res Otolaryngol 2003; 4:422-443. (Pubitemid 37187821)
91. Bermingham-McDonogh O, Rubel EW. Hair cell regeneration: winging our way towards a sound future. Curr Opin Neurobiol 2003; 13:119-126. (Pubitemid 36197936)
92. Oesterle EC, Cunningham DE, Westrum LE, et al. Ultrastructural analysis of [3H]thymidine-labeled cells in the rat utricular macula. J Comp Neurol 2003; 463:177-195.
93. Navaratnam DS, Su HS, Scott SP, et al. Proliferation in the auditory receptor epithelium mediated by a cyclic AMP-dependent signaling pathway. Nat Med 1996; 2:1136-1139.
94. Montcouquiol M, Corwin JT. Brief treatments with forskolin enhance s-phase entry in balance epithelia from the ears of rats. J Neurosci 2001; 21:974-982. (Pubitemid 32163138)
95. Kim TS, Nakagawa T, Lee JE, et al. Induction of cell proliferation and betacatenin expression in rat utricles in vitro. Acta Otolaryngol Suppl 2004:22-25. (Pubitemid 38388633)
96. Cass LA, Summers SA, Prendergast GV, et al. Protein kinase A-dependent and -independent signaling pathways contribute to cyclic AMP-stimulated proliferation. Mol Cell Biol 1999; 19:5882-5891.
97. Parker SB, Eichele G, Zhang P, et al. p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells. Science 1995; 267:1024-1027.
98. Chen P, Segil N. p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 1999; 126:1581-1590. (Pubitemid 29204323)
99. Lowenheim H, Furness DN, Kil J, et al. Gene disruption of p27(Kip1) allows cell proliferation in the postnatal and adult organ of corti. Proc Natl Acad Sci U S A 1999; 96:4084-4088. (Pubitemid 29169040)
100. Lipinski MM, Jacks T. The retinoblastoma gene family in differentiation and development. Oncogene 1999; 18:7873-7882. (Pubitemid 30066233)
101. Frolov MV, Dyson NJ. Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J Cell Sci 2004; 117:2173-2181. (Pubitemid 38807486)
102. Sage C, Huang M, Karimi K, et al. Proliferation of functional hair cells in vivo in the absence of the retinoblastoma protein. Science 2005; 307:1114-1118. (Pubitemid 40262118)
103. Ito I, Ji L, Tanaka F, et al. Liposomal vector mediated delivery of the 3p FUS1 gene demonstrates potent antitumor activity against human lung cancer in vivo. Cancer Gene Ther 2004; 11:733-739. (Pubitemid 39488471)
104. Nguyen LT, Ishida T, Kiwada H. Gene expression in primary cultured mouse hepatocytes with a cationic liposomal vector, TFL-3: comparison with rat hepatocytes. Biol Pharm Bull 2005; 28:1472-1475.
105. Bermingham NA, Hassan BA, Price SD, et al. Math1: an essential gene for the generation of inner ear hair cells. Science 1999; 284:1837-1841. (Pubitemid 29275624)
106. Chen P, Johnson JE, Zoghbi HY, et al. The role of Math1 in inner ear development: uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 2002; 129:2495-2505. (Pubitemid 34863855)
107. Zheng JL, Gao WQ. Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat Neurosci 2000; 3:580-586.
108. Kawamoto K, Ishimoto S, Minoda R, et al. Math1 gene transfer generates new cochlear hair cells in mature guinea pigs in vivo. J Neurosci 2003; 23:4395-4400. (Pubitemid 36706168)
109. Shou J, Zheng JL, Gao WQ. Robust generation of new hair cells in the mature mammalian inner ear by adenoviral expression of Hath1. Mol Cell Neurosci 2003; 23:169-179. (Pubitemid 36705528)
110. Izumikawa M, Minoda R, Kawamoto K, et al. Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat Med 2005; 11:271-276. (Pubitemid 40460554)
111. Yamamoto N, Tanigaki K, Tsuji M, et al. Inhibition of Notch/RBP-J signaling induces hair cell formation in neonate mouse cochleas. J Mol Med 2006; 84:37-45. (Pubitemid 43099522)
112. Lanford PJ, Shailam R, Norton CR, et al. Expression of Math1 and HES5 in the cochleae of wildtype and Jag2 mutant mice. J Assoc Res Otolaryngol 2000; 1:161-171. (Pubitemid 32405385)
113. Webster M, Webster DB. Spiral ganglion neuron loss following organ of Corti loss: a quantitative study. Brain Res 1981; 212:17-30. (Pubitemid 11100780)
114. Spoendlin H. Factors inducing retrograde degeneration of the cochlear nerve. Ann Otol Rhinol Laryngol Suppl 1984; 112:76-82. (Pubitemid 14069994)
115. Zimmermann CE, Burgess BJ, Nadol JB Jr. Patterns of degeneration in the human cochlear nerve. Hear Res 1995; 90:192-201.
116. Zheng JL, Stewart RR, Gao WQ. Neurotrophin-4/5, brain-derived neurotrophic factor, and neurotrophin-3 promote survival of cultured vestibular ganglion neurons and protect them against neurotoxicity of ototoxins. J Neurobiol 1995; 28:330-340.
117. Fritzsch B, Silos-Santiago I, Bianchi LM, et al. The role of neurotrophic factors in regulating the development of inner ear innervation. Trends Neurosci 1997; 20:159-164. (Pubitemid 27116287)
118. Van De Water TR, Staecker H, Ernfors P, et al. Neurotrophic factors as pharmacological agents for the treatment of injured auditory neurons. Ciba Found Symp 1996; 196:149-162; discussion 162-1146 (Pubitemid 126788327)
119. Altschuler RA, Cho Y, Ylikoski J, et al. Rescue and regrowth of sensory nerves following deafferentation by neurotrophic factors. Ann N Y Acad Sci 1999; 884:305-311.
120. Staecker H, Li D, O'Malley BW Jr, et al. Gene expression in the mammalian cochlea: a study of multiple vector systems. Acta Otolaryngol 2001; 121:157-163. (Pubitemid 32328558)
121. Lalwani AK, Han JJ, Castelein CM, et al. In vitro and in vivo assessment of the ability of adeno-associated virus-brain-derived neurotrophic factor to enhance spiral ganglion cell survival following ototoxic insult. Laryngoscope 2002; 112:1325-1334.
122. Bianchi LM, Raz Y. Methods for providing therapeutic agents to treat damaged spiral ganglion neurons. Curr Drug Targets CNS Neurol Disord 2004; 3:195-199. (Pubitemid 38854914)
123. Leake PA, Hradek GT, Rebscher SJ, et al. Chronic intracochlear electrical stimulation induces selective survival of spiral ganglion neurons in neonatally deafened cats. Hear Res 1991; 54:251-271.
124. Leake PA, Snyder RL, Hradek GT, et al. Chronic intracochlear electrical stimulation in neonatally deafened cats: effects of intensity and stimulating electrode location. Hear Res 1992; 64:99-117.
125. Leake PA, Snyder RL, Hradek GT, et al. Consequences of chronic extracochlear electrical stimulation in neonatally deafened cats. Hear Res 1995; 82:65-80.
126. Leake PA, Hradek GT, Snyder RL. Chronic electrical stimulation by a cochlear implant promotes survival of spiral ganglion neurons after neonatal deafness. J Comp Neurol 1999; 412:543-562.
127. Hegarty JL, Kay AR, Green SH. Trophic support of cultured spiral ganglion neurons by depolarization exceeds and is additive with that by neurotrophins or cAMP and requires elevation of [Ca2+]i within a set range. J Neurosci 1997; 17:1959-1970.
128. Bok J, Zha XM, Cho YS, et al. An extranuclear locus of cAMP-dependent protein kinase action is necessary and sufficient for promotion of spiral ganglion neuronal survival by cAMP. J Neurosci 2003; 23:777-787. (Pubitemid 36206168)
129. Miller AL, Prieskorn DM, Altschuler RA, et al. Mechanism of electrical stimulation-induced neuroprotection: effects of verapamil on protection of primary auditory afferents. Brain Res 2003; 966:218-230.
130. Zappia JJ, Niparko JK, Oviatt DL, et al. Evaluation of the temporal bones of a multichannel cochlear implant patient. Ann Otol Rhinol Laryngol 1991; 100:914-921.
131. Marsh MA, Jenkins HA, Coker NJ. Histopathology of the temporal bone following multichannel cochlear implantation. Arch Otolaryngol Head Neck Surg 1992; 118:1257-1265.
132. Nadol JB Jr, Ketten DR, Burgess BJ. Otopathology in a case of multichannel cochlear implantation. Laryngoscope 1994; 104:299-303. (Pubitemid 24085927)
133. Nadol JB Jr, Shiao JY, Burgess BJ, et al. Histopathology of cochlear implants in humans. Ann Otol Rhinol Laryngol 2001; 110:883-891.
134. Khan AM, Handzel O, Damian D, et al. Effect of cochlear implantation on residual spiral ganglion cell count as determined by comparison with the contralateral nonimplanted inner ear in humans. Ann Otol Rhinol Laryngol 2005; 114:381-385. (Pubitemid 40676654)
135. Khan AM, Handzel O, Burgess BJ, et al. Is word recognition correlated with the number of surviving spiral ganglion cells and electrode insertion depth in human subjects with cochlear implants? Laryngoscope 2005; 115:672-677.
136. Ryugo DK, Fekete DM. Morphology of primary axosomatic endings in the anteroventral cochlear nucleus of the cat: a study of the endbulbs of Held. J Comp Neurol 1982; 210:239-257.
137. Lee DJ, Cahill HB, Ryugo DK. Effects of congenital deafness in the cochlear nuclei of Shaker-2 mice: an ultrastructural analysis of synapse morphology in the endbulbs of Held. J Neurocytol 2003; 32:229-243.
138. Carr CE. Processing of temporal information in the brain. Annu Rev Neurosci 1993; 16:223-243.
139. Shepherd RK, Baxi JH, Hardie NA. Response of inferior colliculus neurons to electrical stimulation of the auditory nerve in neonatally deafened cats. J Neurophysiol 1999; 82:1363-1380.
140. Shepherd RK, Hardie NA, Baxi JH. Electrical stimulation of the auditory nerve: single neuron strength-duration functions in deafened animals. Ann Biomed Eng 2001; 29:195-201.
141. Trussell LO. Modulation of transmitter release at giant synapses of the auditory system. Curr Opin Neurobiol 2002; 12:400-404.
142. Ryugo DK, Kretzmer EA, Niparko JK. Restoration of auditory nerve synapses in cats by cochlear implants. Science 2005; 310:1490-1492.
143. Snyder RL, Rebscher SJ, Cao KL, et al. Chronic intracochlear electrical stimulation in the neonatally deafened cat. I: expansion of central representation. Hear Res 1990; 50:7-33.
144. Snyder RL, Rebscher SJ, Leake PA, et al. Chronic intracochlear electrical stimulation in the neonatally deafened cat. II. Temporal properties of neurons in the inferior colliculus. Hear Res 1991; 56:246-264.
145. Snyder R, Leake P, Rebscher S, et al. Temporal resolution of neurons in cat inferior colliculus to intracochlear electrical stimulation: effects of neonatal deafening and chronic stimulation. J Neurophysiol 1995; 73: 449-467.
146. Leake PA, Snyder RL, Rebscher SJ, et al. Plasticity in central representations in the inferior colliculus induced by chronic single- vs. two-channel electrical stimulation by a cochlear implant after neonatal deafness. Hear Res 2000; 147:221-241.
147. Vollmer M, Leake PA, Beitel RE, et al. Degradation of temporal resolution in the auditory midbrain after prolonged deafness is reversed by electrical stimulation of the cochlea. J Neurophysiol 2005; 93:3339-3355. (Pubitemid 40720911)
148. Klinke R, Kral A, Heid S, et al. Recruitment of the auditory cortex in congenitally deaf cats by long-term cochlear electrostimulation. Science 1999; 285:1729-1733. (Pubitemid 29428872)
149. Beitel RE, Snyder RL, Schreiner CE, et al. Electrical cochlear stimulation in the deaf cat: comparisons between psychophysical and central auditory neuronal thresholds. J Neurophysiol 2000; 83:2145-2162. (Pubitemid 30198669)
150. Beitel RE, Vollmer M, Snyder RL, et al. Behavioral and neurophysiological thresholds for electrical cochlear stimulation in the deaf cat. Audiol Neurootol 2000; 5:31-38. (Pubitemid 30093593)
151. Klinke R, Hartmann R, Heid S, et al. Plastic changes in the auditory cortex of congenitally deaf cats following cochlear implantation. Audiol Neurootol 2001; 6:203-206. (Pubitemid 33033364)
152. Kral A, Hartmann R, Tillein J, et al. Hearing after congenital deafness: central auditory plasticity and sensory deprivation. Cereb Cortex 2002; 12:797-807. (Pubitemid 34803879)
153. von Bekesy G. DC potentials and energy balance of the cochlear partition. J Acoust Soc Am 1950; 22:576-582.
154. Davis H. Biophysics and physiology of the inner ear. Physiol Rev 1957; 37: 1-49.
155. Kuijpers W, Bonting SL. Studies on (Na+-K+)-activated ATPase. XXIV. Localization and properties of ATPase in the inner ear of the guinea pig. Biochim Biophys Acta 1969; 173:477-485.
156. Kikuchi T, Adams JC, Miyabe Y, et al. Potassium ion recycling pathway via gap junction systems in the mammalian cochlea and its interruption in hereditary nonsyndromic deafness. Med Electron Microsc 2000; 33:51-56. (Pubitemid 32164777)
157. Kimura RS, Schuknecht HF. The ultrastructure of the human stria vascularis. II. Acta Otolaryngol 1970; 70:301-318.
158. Kimura RS, Schuknecht HF. The ultrastructure of the human stria vascularis. I. Acta Otolaryngol 1970; 69:415-427.
159. Kuijpers W, Bonting SL. The cochlear potentials. I. The effect of ouabain on the cochlear potentials of the guinea pig. Pflugers Arch 1970; 320:348-358.
160. Kuijpers W, Bonting SL. The cochlear potentials. II. The nature of the cochlear endolymphatic resting potential. Pflugers Arch 1970; 320:359-372.
161. Takahashi T. The ultrastructure of the pathologic stria vascularis and spiral prominence in man. Ann Otol Rhinol Laryngol 1971; 80:721-735.
162. Jahnke K. The fine structure of freeze-fractured intercellular junctions in the guinea pig inner ear. Acta Otolaryngol Suppl 1975; 336:1-40.
163. Reale E, Luciano L, Franke K, et al. Intercellular junctions in the vascular stria and spiral ligament. J Ultrastruct Res 1975; 53:284-297.
164. Melichar I, Syka J. Electrophysiological measurements of the stria vascularis potentials in vivo. Hear Res 1987; 25:35-43. (Pubitemid 17201711)
165. Offner FF, Dallos P, Cheatham MA. Positive endocochlear potential: mechanism of production by marginal cells of stria vascularis. Hear Res 1987; 29:117-124.
166. Salt AN, Melichar I, Thalmann R. Mechanisms of endocochlear potential generation by stria vascularis. Laryngoscope 1987; 97:984-991. (Pubitemid 18022613)
167. Schulte BA, Adams JC. Distribution of immunoreactive Na+, K+-ATPase in gerbil cochlea. J Histochem Cytochem 1989; 37:127-134.
168. McGuirt JP, Schulte BA. Distribution of immunoreactive alpha- and beta-subunit isoforms of Na,K-ATPase in the gerbil inner ear. J Histochem Cytochem 1994; 42:843-853. (Pubitemid 2099530)
169. Marcus DC, Wu T, Wangemann P, et al. KCNJ10 (Kir4.1) potassium channel knockout abolishes endocochlear potential. Am J Physiol Cell Physiol 2002; 282:C403-C407. (Pubitemid 34663200)
170. Wangemann P, Itza EM, Albrecht B, et al. Loss of KCNJ10 protein expression abolishes endocochlear potential and causes deafness in Pendred syndrome mouse model. BMC Med 2004; 2:30. (Pubitemid 40251702)
171. Marcus DC, Marcus NY, Thalmann R. Changes in cation contents of stria vascularis with ouabain and potassium-free perfusion. Hear Res 1981; 4:149-160. (Pubitemid 11099723)
172. Steel KP, Barkway C. Another role for melanocytes: their importance for normal stria vascularis development in the mammalian inner ear. Development 1989; 107:453-463. (Pubitemid 20006085)
173. Carlisle L, Steel K, Forge A. Endocochlear potential generation is associated with intercellular communication in the stria vascularis: structural analysis in the viable dominant spotting mouse mutant. Cell Tissue Res 1990; 262:329-337. (Pubitemid 20344873)
174. Shugyo A, Mori N, Matsunaga T. A comparison of the reduction in the K+
175. O'Grady SM, Palfrey HC, Field M. Characteristics and functions of Na-K-Cl cotransport in epithelial tissues. Am J Physiol 1987; 253:C177-192. (Pubitemid 17155147)
176. Kinne RK. The Na-K-Cl cotransporter in the kidney. Ann N Y Acad Sci 1989; 574:63-74.
177. Haas M, Forbush B 3rd. The Na-K-Cl cotransporters. J Bioenerg Biomembr 1998; 30:161-172.
178. Hidaka H, Oshima T, Ikeda K, et al. The Na-K-Cl cotransporters in the rat cochlea: RT-PCR and partial sequence analysis. Biochem Biophys Res Commun 1996; 220:425-430. (Pubitemid 3044316)
179. Goto S, Oshima T, Ikeda K, et al. Expression and localization of the Na-K-2Cl cotransporter in the rat cochlea. Brain Res 1997; 765:324-326. (Pubitemid 27397629)
180. Takeuchi S, Ando M, Irimajiri A. Changes in the volume of marginal cells induced by isotonic 'Cl- depletion/restoration': involvement of the Cl- channel and Na+-K+-Cl- cotransporter. Hear Res 1997; 113:99-109.
181. Casimiro MC, Knollmann BC, Ebert SN, et al. Targeted disruption of the Kcnq1 gene produces a mouse model of Jervell and Lange-Nielsen syndrome. Proc Natl Acad Sci U S A 2001; 98:2526-2531.
182. Wangemann P. K+ cycling and the endocochlear potential. Hear Res 2002; 165:1-9.
183. Doyle KJ. Delayed, reversible hearing loss caused by difluoromethylornithine (DFMO). Laryngoscope 2001; 111:781-785.
184. Ficker E, Taglialatela M, Wible BA, et al. Spermine and spermidine as gating molecules for inward rectifier K+ channels. Science 1994; 266:1068-1072. (Pubitemid 24373730)
185. Taglialatela M, Ficker E, Wible B, et al. Pharmacological implications of inward rectifier K+ channels regulation by cytoplasmic polyamines. Pharmacol Res 1995; 32:335-344. (Pubitemid 26163043)
186. Taglialatela M, Ficker E, Wible BA, et al. C-terminus determinants for Mg2+ and polyamine block of the inward rectifier K+ channel IRK1. EMBO J 1995; 14:5532-5541.
187. Bianchi L, Roy ML, Taglialatela M, et al.Regulation by spermine of native inward rectifier K+ channels in RBL-1 cells. J Biol Chem 1996; 271:6114-6121. (Pubitemid 26095416)
188. Smith MC, Tinling S, Doyle KJ. Difluoromethylornithine-induced reversible hearing loss across a wide frequency range. Laryngoscope 2004; 114:1113-1117. (Pubitemid 38736527)
189. Nie L, Feng W, Diaz R, et al. Functional consequences of polyamine synthesis inhibition by L-alpha-difluoromethylornithine (DFMO): cellular mechanisms for DFMO-mediated ototoxicity. J Biol Chem 2005; 280:15097-15102. (Pubitemid 40562863)
190. Rybak LP, Morizono T. Effect of furosemide upon endolymph potassium concentration. Hear Res 1982; 7:223-231. (Pubitemid 12085188)
191. Rybak LP. Ototoxicity of loop diuretics. Otolaryngol Clin North Am 1993; 26:829-844.
192. Flagella M, Clarke LL, Miller ML, et al. Mice lacking the basolateral Na-K-2Cl cotransporter have impaired epithelial chloride secretion and are profoundly deaf. J Biol Chem 1999; 274:26946-26955. (Pubitemid 129520217)
193. Lee MP, Ravenel JD, Hu RJ, et al. Targeted disruption of the Kvlqt1 gene causes deafness and gastric hyperplasia in mice. J Clin Invest 2000; 106: 1447-1455.
194. Chouabe C, Neyroud N, Guicheney P, et al. Properties of KvLQT1 K+ channel mutations in Romano-Ward and Jervell and Lange-Nielsen inherited cardiac arrhythmias. EMBO J 1997; 16:5472-5479. (Pubitemid 27380154)
195. Neyroud N, Tesson F, Denjoy I, et al. A novel mutation in the potassium channel gene KVLQT1 causes the Jervell and Lange-Nielsen cardioauditory syndrome. Nat Genet 1997; 15:186-189. (Pubitemid 27061640)
196. Gratton MA, Schulte BA. Alterations in microvasculature are associated with atrophy of the stria vascularis in quiet-aged gerbils. Hear Res 1995;82:44-52.
197. Gratton MA, Schulte BA, Smythe NM. Quantification of the stria vascularis and strial capillary areas in quiet-reared young and aged gerbils. Hear Res 1997; 114:1-9.
198. Thomopoulos GN, Spicer SS, Gratton MA, et al. Age-related thickening of basement membrane in stria vascularis capillaries. Hear Res 1997; 111: 31-41.
199. Gratton MA, Meehan DT, Smyth BJ, et al. Strial marginal cells play a role in basement membrane homeostasis: in vitro and in vivo evidence. Hear Res 2002; 163:27-36.
200. Gratton MA, Smyth BJ, Schulte BA, et al. Na, K-ATPase activity decreases in the cochlear lateral wall of quiet-aged gerbils. Hear Res 1995; 83:43-50.
201. Gratton MA, Schmiedt RA, Schulte BA. Age-related decreases in endocochlear potential are associated with vascular abnormalities in the stria vascularis [corrected and republished article originally printed in Hear Res 1996 May;94(1-2):116-24]. Hear Res 1996; 102:181-190.
202. Gratton MA, Smyth BJ, Lam CF, et al. Decline in the endocochlear potential corresponds to decreased Na,K-ATPase activity in the lateral wall of quiet-aged gerbils. Hear Res 1997; 108:9-16.
203. Sakaguchi N, Crouch JJ, Lytle C, et al. Na-K-Cl cotransporter expression in the developing and senescent gerbil cochlea. Hear Res 1998; 118: 114-122. (Pubitemid 28212334)