Treating hearing disorders with cell and gene therapy

Journal of Neural Engineering

Volumn 11, Issue 6, 2014, Pages

  Gillespie, Lisa N ^a,b   Richardson, Rachael T ^a,b   Nayagam, Bryony A ^a,b   Wise, Andrew K ^a,b  

^a Bionics Institute   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

cell therapy; cochlear implant; gene therapy; hearing loss; neurotrophins; stem cell therapy

Indexed keywords

CELLS; COCHLEAR IMPLANTS; CYTOLOGY; GENE THERAPY; GENES; NEURONS; STEM CELLS;

CELL THERAPY; CLINICAL TRANSLATION; EMERGING TECHNOLOGIES; HEARING LOSS; NEUROTROPHINS; STEM CELL THERAPY; THERAPEUTIC AGENTS; THERAPEUTIC STRATEGY;

AUDITION;

VIRUS VECTOR;

ARTICLE; CELL REGENERATION; CELL THERAPY; CELL TYPE; DRUG DELIVERY SYSTEM; GENE THERAPY; GENE TRANSFER; HEARING DISORDER; HUMAN; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; SENSORY NERVE CELL; STEM CELL TRANSPLANTATION; ANIMAL; BIOLOGICAL THERAPY; COCHLEA; DRUG EFFECTS; HEARING LOSS; PATHOLOGY; PROCEDURES; TREATMENT OUTCOME; TRENDS;

ANIMALS; CELL- AND TISSUE-BASED THERAPY; COCHLEA; DRUG DELIVERY SYSTEMS; GENETIC THERAPY; HEARING LOSS; HUMANS; STEM CELL TRANSPLANTATION; TREATMENT OUTCOME;

EID: 84913533914     PISSN: 17412560     EISSN: 17412552     Source Type: Journal    
DOI: 10.1088/1741-2560/11/6/065001     Document Type: Article

References (128)

1. Aebischer P et al 1996 Intrathecal delivery of CNTF using encapsulated genetically modified xenogeneic cells in amyotrophic lateral sclerosis patients Nat. Med. 2 696-9
2. Agterberg M J, Versnel H, van Dijk L M, de Groot J C and Klis S F 2009 Enhanced survival of spiral ganglion cells after cessation of treatment with brain-derived neurotrophic factor in deafened guinea pigs J. Assoc. Res. Otolaryngol. 10 355-67
3. Albers K 2012 Hearing loss and dementia: new insights Minn. Med. 95 52-4
4. Angeli S, Lin X and Liu X Z 2012 Genetics of hearing and deafness Anat Rec. (Hoboken) 295 1812-29
5. Atkinson P J, Wise A K, Flynn B O, Nayagam B A and Richardson R T 2014a Viability of long-term gene therapy in the cochlea Sci. Rep. 4 4733
6. Atkinson P J, Wise A K, Flynn B O, Nayagam B A and Richardson R T 2014b Hair cell regeneration after ATOH1 gene therapy in the cochlea of profoundly deaf adult guinea pigs PLoS One 9 e102077
7. Avraham K B and Raphael Y 2003 Prospects for gene therapy in hearing loss J. Basic Clin. Physiol. Pharmacol. 14 77-83
8. Bankiewicz K S et al 2006 Long-term clinical improvement in MPTP-lesioned primates after gene therapy with AAV-hAADC Mol. Ther. 14 564-70
9. Bermingham N A, Hassan B A, Price S D, Vollrath M A, Ben-Arie N, Eatock R A, Bellen H J, Lysakowski A and Zoghbi H Y 1999 Math1: an essential gene for the generation of inner ear hair cells Science 284 1837-41
10. Blits B, Kitay B M, Farahvar A, Caperton C V, Dietrich W D and Bunge M B 2005 Lentiviral vector-mediated transduction of neural progenitor cells before implantation into injured spinal cord and brain to detect their migration, deliver neurotrophic factors and repair tissue Restor. Neurol. Neurosci. 23 313-24
11. Bramhall N F, Shi F, Arnold K, Hochedlinger K and Edge A S 2014 Lgr5-positive supporting cells generate new hair cells in the postnatal cochlea Stem Cell Reports 2 311-22
12. Calafiore R, Basta G, Luca G, Lemmi A, Montanucci M P, Calabrese G, Racanicchi L, Mancuso F and Brunetti P 2006 Microencapsulated pancreatic islet allografts into nonimmunosuppressed patients with type 1 diabetes: first two cases Diabetes Care 29 137-8
13. Carlson M L, Archibald D J, Gifford R H, Driscoll C L and Beatty C W 2012 Reimplantation with a conventional length electrode following residual hearing loss in four hybrid implant recipients Cochlear Implants Int. 13 148-55
14. Chen W, Johnson S L, Marcotti W, Andrews P W, Moore H D and Rivolta M N 2009 Human fetal auditory stem cells can be expanded in vitro and differentiate into functional auditory neurons and hair cell-like cells Stem Cells 27 1196-204
15. Chen W et al 2012 Restoration of auditory evoked responses by human ES-cell-derived otic progenitors Nature 490 278-82
16. Chen Y et al 2013 Cotransfection of Pax2 and Math1 promote in situ cochlear hair cell regeneration after neomycin insult Sci. Rep. 3 2996
17. Clinical Trials 2012 Open-label Investigation of the Safety and Clinical Effects of NTCELL in Patients With Parkinson's Disease Accessed September 2014 (http://clinicaltrials.gov/show/NCT01734733)
18. Coleman B, Hardman J, Coco A, Epp S, de Silva M, Crook J and Shepherd R 2006 Fate of embryonic stem cells transplanted into the deafened mammalian cochlea Cell Transplant 15 369-80
19. Coleman B, Fallon J B, Pettingill L N, de Silva M G and Shepherd R K 2007 Auditory hair cell explant co-cultures promote the differentiation of stem cells into bipolar neurons Exp. Cell Res. 313 232-43
20. Corrales C E, Pan L, Li H, Liberman M C, Heller S and 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 J. Neurobiol. 66 1489-5000
21. Cotanche D A, Lee K H, Stone J S and Picard D A 1994 Hair cell regeneration in the bird cochlea following noise damage or ototoxic drug damage Anat. Embryol. (Berl) 189 1-18
22. Eastwood H, Pinder D, James D, Chang A, Galloway S, Richardson R and O'Leary S 2010 Permanent and transient effects of locally delivered n-acetyl cysteine in a guinea pig model of cochlear implantation Hear. Res. 259 24-30
23. Eberling J L, Jagust W J, Christine C W, Starr P, Larson P, Bankiewicz K S and Aminoff M J 2008 Results from a phase I safety trial of hAADC gene therapy for Parkinson disease Neurology 70 1980-3
24. Evans A J, Thompson B C, Wallace G G, Millard R, O'Leary S J, Clark G M, Shepherd R K and Richardson R T 2009 Promoting neurite outgrowth from spiral ganglion neuron explants using polypyrrole/BDNF-coated electrodes J. Biomed. Mater Res. A 91 241-50
25. Flores-Otero J, Xue H Z and Davis R L 2007 Reciprocal regulation of presynaptic and postsynaptic proteins in bipolar spiral ganglion neurons by neurotrophins J. Neurosci. 27 14023-34
26. Fu X and Xu Y 2011 Self-renewal and scalability of human embryonic stem cells for human therapy Regen. Med. 6 327-34
27. Fu X and Xu Y 2012 Challenges to the clinical application of pluripotent stem cells: towards genomic and functional stability Genome. Med. 4 55
28. Gabaizadeh R, Staecker H, Liu W, Kopke R, Malgrange B, Lefebvre P P and Van de Water T R 1997 Protection of both auditory hair cells and auditory neurons from cisplatin induced damage Acta Otolaryngol. 117 232-8
29. Gantz B J, Turner C, Gfeller K E and Lowder M W 2005 Preservation of hearing in cochlear implant surgery: advantages of combined electrical and acoustical speech processing Laryngoscope 115 796-802
30. Gantz B J, Hansen M, Turner C W, Oleson J J, Reiss L A and Parkinson A J 2009 Hybrid 10 clinical trial: preliminary results Audiol Neurootol. 14 32-8 Suppl 1
31. Gillespie L N, Clark G M, Bartlett P F and Marzella P L 2003 BDNF-induced survival of auditory neurons in vivo: Cessation of treatment leads to an accelerated loss of survival effects J. Neurosci Res. 71 785-90
32. Gillespie L N, Zanin M P and Shepherd R K 2013 Cell-based neurotrophin delivery for auditory neuron survival in deafness Proc. Australian Neuroscience Soc. (Melbourne, 3-6 February) p 29
33. Green S H, Bailey E, Wang Q and Davis R L 2012 The Trk A, B, C's of neurotrophins in the cochlea Anat Rec. (Hoboken) 295 1877-95
34. Gstoettner W K, Helbig S, Maier N, Kiefer J, Radeloff A and Adunka O F 2006 Ipsilateral electric acoustic stimulation of the auditory system: results of long-term hearing preservation Audiol. Neurootol. 11 49-56 Suppl 1
35. Gunewardene N, Dottori M and Nayagam B A 2012 The convergence of cochlear implantation with induced pluripotent stem cell therapy Stem Cell Rev. 8 741-54
36. Gunewardene N, Bergen N V, Crombie D, Needham K, Dottori M and Nayagam B A 2014 Directing human induced pluripotent stem cells into a neurosensory lineage for auditory neuron replacement Biores. Open Access 3 162-75
37. Gupta V, Sikka K, Kumar R and Deka R C 2012 Inner ear infections as cause of perinatal deafness Indian Journal of Otology 18 193-5
38. Hadaczek P, Eberling J L, Pivirotto P, Bringas J, Forsayeth J and Bankiewicz K S 2010 Eight years of clinical improvement in MPTP-lesioned primates after gene therapy with AAV2-hAADC Mol. Ther. 18 1458-61
39. Hakuba N, Watabe K, Hyodo J, Ohashi T, Eto Y, Taniguchi M, Yang L, Tanaka J, Hata R and Gyo K 2003 Adenovirus-mediated overexpression of a gene prevents hearing loss and progressive inner hair cell loss after transient cochlear ischemia in gerbils Gene. Ther. 10 426-33
40. Han Z, Yang J M, Chi F L, Cong N, Huang Y B, Gao Z and Li W 2010 Survival and fate of transplanted embryonic neural stem cells by Atoh1 gene transfer in guinea pigs cochlea Neuroreport. 21 490-6
41. Hardie N A and Shepherd R K 1999 Sensorineural hearing loss during development: morphological and physiological response of the cochlea and auditory brainstem Hear. Res. 128 147-65
42. Hata K, Fujitani M, Yasuda Y, Doya H, Saito T, Yamagishi S, Mueller B K and Yamashita T 2006 RGMa inhibition promotes axonal growth and recovery after spinal cord injury J. Cell Biol. 173 47-58
43. Henderson D, Bielefeld E C, Harris K C and Hu B H 2006 The role of oxidative stress in noise-induced hearing loss Ear Hear 27 1-19
44. Hildebrand M S, Dahl H H, Hardman J, Coleman B, Shepherd R K and de Silva M G 2005 Survival of partially differentiated mouse embryonic stem cells in the scala media of the guinea pig cochlea J. Assoc Res. Otolaryngol. 6 341-54
45. Hu Y, Leaver S G, Plant G W, Hendriks W T, Niclou S P, Verhaagen J, Harvey A R and Cui Q 2005 Lentiviral-mediated transfer of CNTF to schwann cells within reconstructed peripheral nerve grafts enhances adult retinal ganglion cell survival and axonal regeneration Mol. Ther. 11 906-15
46. Iguchi F et al 2004 Surgical techniques for cell transplantation into the mouse cochlea Acta Otolaryngol Suppl. 55 43-7
47. Ito J, Kojima K and Kawaguchi S 2001 Survival of neural stem cells in the cochlea Acta Otolaryngol. 121 140-2
48. Izumikawa M, Minoda R, Kawamoto K, Abrashkin K A, Swiderski D L, Dolan D F, Brough D E and Raphael Y 2005 Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals Nat. Med. 11 271-6
49. Izumikawa M, Batts S A, Miyazawa T, Swiderski D L and Raphael Y 2008 Response of the flat cochlear epithelium to forced expression of Atoh1 Hear. Res. 240 52-6
50. Kaplitt M G et al 2007 Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial Lancet 369 2097-105
51. Kawamoto K, Oh S H, Kanzaki S, Brown N and Raphael Y 2001 The functional and structural outcome of inner ear gene transfer via the vestibular and cochlear fluids in mice Mol. Ther. 4 575-85
52. Kawamoto K, Ishimoto S, Minoda R, Brough D E and Raphael Y 2003 Math1 gene transfer generates new cochlear hair cells in mature guinea pigs in vivo J. Neurosci. 23 4395-400
53. Kelly M C, Chang Q, Pan A, Lin X and Chen P 2012 Atoh1 directs the formation of sensory mosaics and induces cell proliferation in the postnatal mammalian cochlea in vivo J. Neurosci. 32 6699-710
54. Kiefer J, Pok M, Adunka O, Sturzebecher E, Baumgartner W, Schmidt M, Tillein J, Ye Q and Gstoettner W 2005 Combined electric and acoustic stimulation of the auditory system: results of a clinical study Audiol Neurootol 10 134-44
55. Koehler K R, Mikosz A M, Molosh A I, Patel D and Hashino E 2013 Generation of inner ear sensory epithelia from pluripotent stem cells in 3D culture Nature 500 217-21
56. Kujawa S G and Liberman M C 2009 Adding insult to injury: cochlear nerve degeneration after 'temporary' noise-induced hearing loss J. Neurosci. 29 14077-85
57. Kyoto A, Hata K and Yamashita T 2007 Synapse formation of the cortico-spinal axons is enhanced by RGMa inhibition after spinal cord injury Brain Res. 1186 74-86
58. Lalwani A K, Han J J, Castelein C M, Carvalho G J and Mhatre A N 2002 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 112 1325-34
59. LeWitt P A et al 2011 AAV2-GAD gene therapy for advanced Parkinson's disease: a double-blind, sham-surgery controlled, randomised trial Lancet Neurol 10 309-19
60. Lin F R, Metter E J, O'Brien R J, Resnick S M, Zonderman A B and Ferrucci L 2011 Hearing loss and incident dementia Arch. Neurol. 68 214-20
61. Liu Y, Okada T, Nomoto T, Ke X, Kume A, Ozawa K and Xiao S 2007 Promoter effects of adeno-associated viral vector for transgene expression in the cochlea in vivo Exp. Mol. Med. 39 170-5
62. Liu Y et al 2008 Protection against aminoglycoside-induced ototoxicity by regulated AAV vector-mediated GDNF gene transfer into the cochlea Mol. Ther. 16 474-80
63. Liu Z, Dearman J A, Cox B C, Walters B J, Zhang L, Ayrault O, Zindy F, Gan L, Roussel M F and Zuo J 2012 Age-dependent in vivo conversion of mouse cochlear pillar and Deiters' cells to immature hair cells by Atoh1 ectopic expression J. Neurosci. 32 6600-10
64. Luebke A E, Foster P K, Muller C D and Peel A L 2001 Cochlear function and transgene expression in the guinea pig cochlea, using adenovirus- and adeno-associated virus-directed gene transfer Hum Gene Ther. 12 773-81
65. Makar T K et al 2009 Brain-derived neurotrophic factor gene delivery in an animal model of multiple sclerosis using bone marrow stem cells as a vehicle J. Neuroimmunol. 210 40-51
66. Martinez-Monedero R, Yi E, Oshima K, Glowatzki E and Edge A S 2008 Differentiation of inner ear stem cells to functional sensory neurons Dev Neurobiol. 68 669-84
67. Maruyama J, Miller J M and Ulfendahl M 2008 Glial cell line-derived neurotrophic factor and antioxidants preserve the electrical responsiveness of the spiral ganglion neurons after experimentally induced deafness Neurobiol. Dis. 29 14-21
68. Matsumoto M, Nakagawa T, Kojima K, Sakamoto T, Fujiyama F and Ito J 2008 Potential of embryonic stem cell-derived neurons for synapse formation with auditory hair cells J. Neurosci. Res. 86 3075-85
69. Mizutari K, Fujioka M, Hosoya M, Bramhall N, Okano H J, Okano H and Edge A S 2013 Notch inhibition induces cochlear hair cell regeneration and recovery of hearing after acoustic trauma Neuron 77 58-69
70. Muramatsu S et al 2010 A phase I study of aromatic L-amino acid decarboxylase gene therapy for Parkinson's disease Mol. Ther. 18 1731-5
71. Murua A, Portero A, Orive G, Hernandez R M, de Castro M and Pedraz J L 2008 Cell microencapsulation technology: towards clinical application J. Control Release 132 76-83
72. Nakaizumi T, Kawamoto K, Minoda R and Raphael Y 2004 Adenovirus-mediated expression of brain-derived neurotrophic factor protects spiral ganglion neurons from ototoxic damage Audiol. Neurootol. 9 135-43
73. Nathwani A C et al 2011 Adenovirus-associated virus vector-mediated gene transfer in hemophilia B N. Engl. J. Med. 365 2357-65
74. Nayagam B A, Backhouse S S, Cimenkaya C and Shepherd R K 2012 Hydrogel limits stem cell dispersal in the deaf cochlea: implications for cochlear implants J. Neural. Eng. 9 065001
75. Nayagam B A, Edge A S, Needham K, Hyakumura T, Leung J, Nayagam D A and Dottori M 2013 An in vitro model of developmental synaptogenesis using cocultures of human neural progenitors and cochlear explants Stem Cells Dev. 22 901-12
76. Needham K, Hyakumura T, Gunewardene N, Dottori M and Nayagam B A 2014 Electrophysiological properties of neurosensory progenitors derived from human embryonic stem cells Stem Cell Res. 12 241-9
77. Okano T and Kelley M W 2012 Stem cell therapy for the inner ear: recent advances and future directions Trends Amplif. 16 4-18
78. Oshima K, Shin K, Diensthuber M, Peng A W, Ricci A J and Heller S 2010 Mechanosensitive hair cell-like cells from embryonic and induced pluripotent stem cells Cell 141 704-16
79. Pan N, Jahan I, Kersigo J, Kopecky B, Santi P, Johnson S, Schmitz H and Fritzsch B 2011 Conditional deletion of Atoh1 using Pax2-Cre results in viable mice without differentiated cochlear hair cells that have lost most of the organ of Corti Hear. Res. 275 66-80
80. Park Y H, Wilson K F, Ueda Y, Tung Wong H, Beyer L A, Swiderski D L, Dolan D F and Raphael Y 2014 Conditioning the cochlea to facilitate survival and integration of exogenous cells into the auditory epithelium Mol. Ther. 22 873-80
81. Parker M A, Corliss D A, Gray B, Anderson J K, Bobbin R P, Snyder E Y and 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 Hear. Res. 232 29-43
82. Pettingill L N, Richardson R T, Wise A K, O'Leary S J and Shepherd R K 2007 Neurotrophic factors and neural prostheses: potential clinical applications based upon findings in the auditory system IEEE Trans. Biomed. Eng. 54 1138-48
83. Pettingill L N, Minter R L and Shepherd R K 2008 Schwann cells genetically modified to express neurotrophins promote spiral ganglion neuron survival in vitro Neuroscience 152 821-8
84. Pettingill L N, Wise A K, Geaney M S and Shepherd R K 2011 Enhanced auditory neuron survival following cell-based BDNF treatment in the deaf guinea pig PLoS One 6 e18733
85. Pinyon J L, Tadros S F, Froud K E, AC Y W, Tompson I T, Crawford E N, Ko M, Morris R, Klugmann M and Housley G D 2014 Close-field electroporation gene delivery using the cochlear implant electrode array enhances the bionic ear Sci. Transl. Med. 6 233ra54
86. Podskarbi-Fayette R, Pilka A and Skarzynski H 2010 Electric stimulation complements functional residual hearing in partial deafness Acta Otolaryngol 130 888-96
87. Ramekers D, Versnel H, Grolman W and Klis S F 2012 Neurotrophins and their role in the cochlea Hear. Res. 288 19-33
88. Rejali D, Lee V A, Abrashkin K A, Humayun N, Swiderski D L and Raphael Y 2007 Cochlear implants and ex vivo BDNF gene therapy protect spiral ganglion neurons Hear. Res. 228 180-7
89. Reubinoff B E, Pera M F, Fong C Y, Trounson A and Bongso A 2000 Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro Nat. Biotechnol. 18 399-404
90. Reyes J H, O'Shea K S, Wys N L, Velkey J M, Prieskorn D M, Wesolowski K, Miller J M and Altschuler R A 2008 Glutamatergic neuronal differentiation of mouse embryonic stem cells after transient expression of neurogenin 1 and treatment with BDNF and GDNF: in vitro and in vivo studies J. Neurosci. 28 12622-31
91. Sakamoto T, Nakagawa T, Endo T, Kim T S, Iguchi F, Naito Y, Sasai Y and Ito J 2004 Fates of mouse embryonic stem cells transplanted into the inner ears of adult mice and embryonic chickens Acta Otolaryngol. Suppl. 551 48-52
92. Sangro B et al 2010 A phase I clinical trial of thymidine kinase-based gene therapy in advanced hepatocellular carcinoma Cancer Gene Ther. 17 837-43
93. Schacht J, Talaska A E and Rybak L P 2012 Cisplatin and aminoglycoside antibiotics: hearing loss and its prevention Anat. Rec. (Hoboken) 295 1837-50
94. Seyyedi M, Viana L M and Nadol J B Jr 2014 Within-subject comparison of word recognition and spiral ganglion cell count in bilateral cochlear implant recipients Otol. Neurotol. 35 1446-50
95. Shepherd R K and Javel E 1997 Electrical stimulation of the auditory nerve. I. Correlation of physiological responses with cochlear status Hear. Res. 108 112-44
96. Shepherd R K, Coco A, Epp S B and Crook J M 2005 Chronic depolarisation enhances the trophic effects of BDNF in rescuing auditory neurons following a sensorineural hearing loss J. Comp. Neurol. 486 145-58
97. Shepherd R K, Coco A and Epp S B 2008 Neurotrophins and electrical stimulation for protection and repair of spiral ganglion neurons following sensorineural hearing loss Hear. Res. 242 100-9
98. Shepherd R K 2011 Rescuing the cochlea: the challenges ENT & audiology news 19 49-52
99. Shi F, Corrales C E, Liberman M C and Edge A S 2007 BMP4 induction of sensory neurons from human embryonic stem cells and reinnervation of sensory epithelium Eur. J. Neurosci. 26 3016-23
100. Shibata S B, Cortez S, Beyer L A, Wiler J A, Di Polo A, Pfingst B E and Raphael Y 2010 Transgenic BDNF induces nerve fiber regrowth into the auditory epithelium in deaf cochleae Exp. Neurol. 223 464-72
101. Shibata S B, Cortez S, Wiler J A, Swiderski D L and Raphael Y 2012 Hyaluronic acid enhances gene delivery into the cochlea Hum Gene Ther 23 302-10
102. Shoji F, Miller A L, Mitchell A, Yamasoba T, Altschuler R A and Miller J M 2000 Differential protective effects of neurotrophins in the attenuation of noise-induced hair cell loss Hear. Res. 146 134-42
103. Sieving P A, Caruso R C, Tao W, Coleman H R, Thompson D J, Fullmer K R and Bush R A 2006 Ciliary neurotrophic factor (CNTF) for human retinal degeneration: phase I trial of CNTF delivered by encapsulated cell intraocular implants Proc. Natl. Acad. Sci. USA 103 3896-901
104. Singh B, Xu Q G, Franz C K, Zhang R, Dalton C, Gordon T, Verge V M, Midha R and Zochodne D W 2012 Accelerated axon outgrowth, guidance, and target reinnervation across nerve transection gaps following a brief electrical stimulation paradigm J. Neurosurg. 116 498-512
105. Staecker H, Gabaizadeh R, Federoff H and Van De Water T R 1998 Brain-derived neurotrophic factor gene therapy prevents spiral ganglion degeneration after hair cell loss Otolaryngol Head Neck Surg. 119 7-13
106. Stankovic K, Rio C, Xia A, Sugawara M, Adams J C, Liberman M C and Corfas G 2004 Survival of adult spiral ganglion neurons requires erbB receptor signaling in the inner ear J. Neurosci. 24 8651-61
107. Stone I M, Lurie D I, Kelley M W and Poulsen D J 2005 Adeno-associated virus-mediated gene transfer to hair cells and support cells of the murine cochlea Mol. Ther. 11 843-8
108. Stover T, Yagi M and Raphael Y 1999 Cochlear gene transfer: round window versus cochleostomy inoculation Hear. Res. 136 124-30
109. Takahashi K and Yamanaka S 2006 Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 663-76
110. Tamir S, Ferrary E, Borel S, Sterkers O and Bozorg Grayeli A 2012 Hearing preservation after cochlear implantation using deeply inserted flex atraumatic electrode arrays Audiol. Neurootol. 17 331-7
111. Tateya I, Nakagawa T, Iguchi F, Kim T S, Endo T, Yamada S, Kageyama R, Naito Y and Ito J 2003 Fate of neural stem cells grafted into injured inner ears of mice Neuroreport 14 1677-81
112. Thanos C G and Emerich D F 2008 On the use of hydrogels in cell encapsulation and tissue engineering system Recent Pat. Drug Deliv. Formul. 2 19-24
113. Thomson J A, Itskovitz-Eldor J, Shapiro S S, Waknitz M A, Swiergiel J J, Marshall V S and Jones J M 1998 Embryonic stem cell lines derived from human blastocysts Science 282 1145-7
114. Turner C W, Reiss L A and Gantz B J 2008 Combined acoustic and electric hearing: preserving residual acoustic hearing Hear. Res. 242 164-71
115. Wahlberg L U et al 2012 Targeted delivery of nerve growth factor via encapsulated cell biodelivery in Alzheimer disease: a technology platform for restorative neurosurgery J. Neurosurg. 117 340-7
116. Warnecke A et al 2012 Stable release of BDNF from the fibroblast cell line NIH3T3 grown on silicone elastomers enhances survival of spiral ganglion cells in vitro and in vivo Hear. Res. 289 86-97
117. Winn S, Lindner M D, Lee A, Haggett G, Francis J M and Emerich D F 1996 Polymer-encapsulated genetically modified cells continue to secrete human nerve growth factor for over one year in rat ventricles: behavioral and anatomical consequences Exp. Neurol. 140 126-38
118. Wise A K, Richardson R, Hardman J, Clark G and O'Leary S 2005 Resprouting and survival of guinea pig cochlear neurons in response to the administration of the neurotrophins brain-derived neurotrophic factor and neurotrophin-3 J. Comp. Neurol. 487 147-65
119. Wise A K, Hume C R, Flynn B O, Jeelall Y S, Suhr C L, Sgro B E, O'Leary S J, Shepherd R K and Richardson R T 2010 Effects of localized neurotrophin gene expression on spiral ganglion neuron resprouting in the deafened cochlea Mol. Ther. 18 1111-22
120. Wise A K, Fallon J B, Neil A J, Pettingill L N, Geaney M S, Skinner S J and Shepherd R K 2011a Combining cell-based therapies and neural prostheses to promote neural survival Neurotherapeutics 8 774-87
121. Wise A K, Tu T, Atkinson P J, Flynn B O, Sgro B E, Hume C, O'Leary S J, Shepherd R K and Richardson R T 2011b The effect of deafness duration on neurotrophin gene therapy for spiral ganglion neuron protection Hear. Res. 278 69-76
122. Yagi M, Magal E, Sheng Z, Ang K A and Raphael Y 1999 Hair cell protection from aminoglycoside ototoxicity by adenovirus-mediated overexpression of glial cell line-derived neurotrophic factor Hum. Gene. Ther. 10 813-23
123. Yagi M, Kanzaki S, Kawamoto K, Shin B, Shah P P, Magal E, Sheng J and Raphael Y 2000 Spiral ganglion neurons are protected from degeneration by GDNF gene therapy J. Assoc. Res. Otolaryngol. 1 315-25
124. Yang S M, Chen W, Guo W W, Jia S, Sun J H, Liu H Z, Young W Y and He D Z 2012 Regeneration of stereocilia of hair cells by forced Atoh1 expression in the adult mammalian cochlea PLoS One 7 e46355
125. Zanin M P, Pettingill L N, Harvey A R, Emerich D F, Thanos C G and Shepherd R K 2012 The development of encapsulated cell technologies as therapies for neurological and sensory diseases J. Control Release 160 3-13
126. Zanin M P, Hellström M, Shepherd R K, Harvey A R and Gillespie L N 2014 Development of a cell-based treatment for long-term neurotrophin expression and spiral ganglion neuron survival Neuroscience 277 690-9
127. Zhai S Q, Guo W, Hu Y Y, Yu N, Chen Q, Wang J Z, Fan M and Yang W Y 2010 Protective effects of brain-derived neurotrophic factor on the noise-damaged cochlear spiral ganglion J. Laryngol. Otol. 1-6
128. Zimmermann H, Shirley S G and Zimmermann U 2007 Alginate-based encapsulation of cells: past, present, and future Curr. Diab. Rep. 7 314-20