Prospects for replacement of auditory neurons by stem cells

Hearing Research

Volumn 297, Issue , 2013, Pages 106-112

  Shi, Fuxin ^a   Edge, Albert S B ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACOUSTIC NERVE FIBER; ACTION POTENTIAL; CELL TRANSPLANTATION; ENGRAFTMENT; HUMAN; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SOUND DETECTION; STEM CELL TRANSPLANTATION; SYNAPTOGENESIS; VESTIBULOCOCHLEAR NERVE DISEASE;

ANIMALS; BRAIN STEM; COCHLEA; COCHLEAR NERVE; HAIR CELLS, AUDITORY; HEARING LOSS, SENSORINEURAL; HUMANS; MICE; NERVE REGENERATION; NEURONS; SPIRAL GANGLION; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84875374779     PISSN: 03785955     EISSN: 18785891     Source Type: Journal    
DOI: 10.1016/j.heares.2013.01.017     Document Type: Review

References (112)

1. Aldskogius H., Kozlova E.N. Strategies for repair of the deafferented spinal cord. Brain Res. Rev. 2002, 40:301-308.
2. Battisti A.C., Fekete D.M. Slits and robos in the developing chicken inner ear. Dev. Dyn. 2008, 237:476-484.
3. Bianchi L.M., Liu H. Comparison of ephrin-A ligand and EphA receptor distribution in the developing inner ear. Anat. Rec. 1999, 254:127-134.
4. Bianchi L.M., Gray N.A. EphB receptors influence growth of ephrin-B1-positive statoacoustic nerve fibers. Eur. J. Neurosci. 2002, 16:1499-1506.
5. Bjorklund A., Dunnett S.B., Brundin P., Stoessl A.J., Freed C.R., Breeze R.E., Levivier M., Peschanski M., Studer L., Barker R. Neural transplantation for the treatment of Parkinson's disease. Lancet Neurol. 2003, 2:437-445.
6. Bodmer D., Brors D., Pak K., Keithley E.M., Mullen L., Ryan A.F., Gloddek B. Inflammatory signals increase Fas ligand expression by inner ear cells. J. Neuroimmunol. 2002, 129:10-17.
7. Brugeaud A., Edge A.S.B. Characterization of in Vitro Regenerated Synapses between Auditory Neurons and Hair Cells 2009, ARO 32nd Annual Meeting Abstract #786.
8. Buchthal F., Kuhl V. Nerve conduction, tactile sensibility, and the electromyogram after suture or compression of peripheral nerve: a longitudinal study in man. J. Neurol. Neurosurg. Psychiatry 1979, 42:436-451.
9. Caiazzo M., Dell'Anno M.T., Dvoretskova E., Lazarevic D., Taverna S., Leo D., Sotnikova T.D., Menegon A., Roncaglia P., Colciago G., Russo G., Carninci P., Pezzoli G., Gainetdinov R.R., Gustincich S., Dityatev A., Broccoli V. Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 2011, 476:224-227.
10. Carney P.R., Silver J. Studies on cell migration and axon guidance in the developing distal auditory system of the mouse. J. Comp. Neurol. 1983, 215:359-369.
11. Chu K., Kim M., Jeong S.W., Kim S.U., Yoon B.W. Human neural stem cells can migrate, differentiate, and integrate after intravenous transplantation in adult rats with transient forebrain ischemia. Neurosci. Lett. 2003, 343:129-133.
12. Coleman B., Hardman J., Coco A., Epp S., de Silva M., Crook J., Shepherd R. Fate of embryonic stem cells transplanted into the deafened mammalian cochlea. Cell Transplant 2006, 15:369-380.
13. Corrales C.E., Pan L., Li H., Liberman M.C., Heller S., Edge A.S. 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. 2006, 66:1489-1500.
14. Crigler L., Robey R.C., Asawachaicharn A., Gaupp D., Phinney D.G. Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp. Neurol. 2006, 198:54-64.
15. Davies D. Temporal and spatial regulation of alpha6 integrin expression during the development of the cochlear-vestibular ganglion. J. Comp. Neurol. 2007, 502:673-682.
16. Echteler S.M. Developmental segregation in the afferent projections to mammalian auditory hair cells. Proc. Natl. Acad. Sci. USA 1992, 89:6324-6327.
17. Eybalin M., Norenberg M.D., Renard N. Glutamine synthetase and glutamate metabolism in the guinea pig cochlea. Hear. Res. 1996, 101:93-101.
18. Fekete D.M., Rouiller E.M., Liberman M.C., Ryugo D.K. The central projections of intracellularly labeled auditory nerve fibers in cats. J. Comp. Neurol. 1984, 229:432-450.
19. Fritzsch B., Tessarollo L., Coppola E., Reichardt L.F. Neurotrophins in the ear: their roles in sensory neuron survival and fiber guidance. Prog. Brain Res. 2004, 146:265-278.
20. Gage F.H. Mammalian neural stem cells. Science 2000, 287:1433-1438.
21. Goda Y., Davis G.W. Mechanisms of synapse assembly and disassembly. Neuron 2003, 40:243-264.
22. Grant L., Yi E., Glowatzki E. Two modes of release shape the postsynaptic response at the inner hair cell ribbon synapse. J. Neurosci. 2010, 30:4210-4220.
23. Hakuba N., Koga K., Gyo K., Usami S.I., Tanaka K. Exacerbation of noise-induced hearing loss in mice lacking the glutamate transporter GLAST. J. Neurosci. 2000, 20:8750-8753.
24. Harel N.Y., Strittmatter S.M. Can regenerating axons recapitulate developmental guidance during recovery from spinal cord injury?. Nat. Rev. Neurosci. 2006, 7:603-616.
25. Harris J.P., Ryan A.F. Fundamental immune mechanisms of the brain and inner ear. Otolaryngol. Head Neck Surg. 1995, 112:639-653.
26. Hata K., Fujitani M., Yasuda Y., Doya H., Saito T., Yamagishi S., Mueller B.K., Yamashita T. RGMa inhibition promotes axonal growth and recovery after spinal cord injury. J. Cell. Biol. 2006, 173:47-58.
27. Heinrich C., Gascon S., Masserdotti G., Lepier A., Sanchez R., Simon-Ebert T., Schroeder T., Gotz M., Berninger B. Generation of subtype-specific neurons from postnatal astroglia of the mouse cerebral cortex. Nat. Protoc. 2011, 6:214-228.
28. Huang L.C., Greenwood D., Thorne P.R., Housley G.D. Developmental regulation of neuron-specific P2X3 receptor expression in the rat cochlea. J. Comp. Neurol. 2005, 484:133-143.
29. Imitola J., Comabella M., Chandraker A.K., Dangond F., Sayegh M.H., Snyder E.Y., Khoury S.J. Neural stem/progenitor cells express costimulatory molecules that are differentially regulated by inflammatory and apoptotic stimuli. Am. J. Pathol. 2004, 164:1615-1625.
30. Jeon S.J., Fujioka M., Kim S.C., Edge A.S.B. Notch signaling alters sensory or neuronal cell fate specification of inner ear stem cells. J. Neurosci. 2011, 31:8351-8358.
31. Karis A., Pata I., van Doorninck J.H., Grosveld F., de Zeeuw C.I., de Caprona D., Fritzsch B. Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. J. Comp. Neurol. 2001, 429:615-630.
32. Kawase T., Liberman M.C. Spatial organization of the auditory nerve according to spontaneous discharge rate. J. Comp. Neurol. 1992, 319:312-318.
33. Kempfle J., Shi F., Edge A. Reciprocal Effect of BMP4 on Differentiation of Hair Cells and Neurons from Inner Ear Stem Cells 2010, ARO 33rd Annual Meeting Abstract #18.
34. Kim T.S., Nakagawa T., Kita T., Higashi T., Takebayashi S., Matsumoto M., Kojima K., Sakamoto T., Ito J. Neural connections between embryonic stem cell-derived neurons and vestibular hair cells in vitro. Brain Res. 2005, 1057:127-133.
35. Kim W.Y., Fritzsch B., Serls A., Bakel L.A., Huang E.J., Reichardt L.F., Barth D.S., Lee J.E. NeuroD-null mice are deaf due to a severe loss of the inner ear sensory neurons during development. Development 2001, 128:417-426.
36. Koundakjian E.J., Appler J.L., Goodrich L.V. Auditory neurons make stereotyped wiring decisions before maturation of their targets. J. Neurosci. 2007, 27:14078-14088.
37. Kujawa S.G., Liberman M.C. Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J. Neurosci. 2009, 29:14077-14085.
38. Kyoto A., Hata K., Yamashita T. Synapse formation of the cortico-spinal axons is enhanced by RGMa inhibition after spinal cord injury. Brain Res. 2007, 1186:74-86.
39. Lang H., Schulte B.A., Schmiedt R.A. Ouabain induces apoptotic cell death in type I spiral ganglion neurons, but not type II neurons. J. Assoc. Res. Otolaryngol. 2005, 6:63-74.
40. Lang H., Schulte B.A., Goddard J.C., Hedrick M., Schulte J.B., Wei L., Schmiedt R.A. Transplantation of mouse embryonic stem cells into the cochlea of an auditory-neuropathy animal model: effects of timing after injury. J. Assoc. Res. Otolaryngol. 2008, 9:225-240.
41. Lang H., Li M., Kilpatrick L.A., Zhu J., Samuvel D.J., Krug E.L., Goddard J.C. Sox2 up-regulation and glial cell proliferation following degeneration of spiral ganglion neurons in the adult mouse inner ear. J. Assoc. Res. Otolaryngol. 2011, 12:151-171.
42. Lang H., Ebihara Y., Schmiedt R.A., Minamiguchi H., Zhou D., Smythe N., Liu L., Ogawa M., Schulte B.A. Contribution of bone marrow hematopoietic stem cells to adult mouse inner ear: mesenchymal cells and fibrocytes. J. Comp. Neurol. 2006, 496:187-201.
43. Lawoko-Kerali G., Rivolta M.N., Lawlor P., Cacciabue-Rivolta D.I., Langton-Hewer C., van Doorninck J.H., Holley M.C. GATA3 and NeuroD distinguish auditory and vestibular neurons during development of the mammalian inner ear. Mech. Dev. 2004, 121:287-299.
44. Lee K.H., Warchol M.E. Promotion of neurite outgrowth and axon guidance in spiral ganglion cells by netrin-1. Arch. Otolaryngol. Head Neck Surg. 2008, 134:146-151.
45. Lerner-Natoli M., Ladrech S., Renard N., Puel J.L., Eybalin M., Pujol R. Protein kinase C may be involved in synaptic repair of auditory neuron dendrites after AMPA injury in the cochlea. Brain Res. 1997, 749:109-119.
46. Liberman M.C. Morphological differences among radial afferent fibers in the cat cochlea: an electron-microscopic study of serial sections. Hear. Res. 1980, 3:45-63.
47. Liberman M.C. Single-neuron labeling in the cat auditory nerve. Science 1982, 216:1239-1241.
48. Liberman M.C., Mulroy M.J. Acute and chronic effects of acoustic trauma: cochlear pathology and auditory nerve pathophysiology. New Perspectives on Noise-induced Hearing Loss 1982, 105-151. R.P. Hamernik (Ed.).
49. Lin H.W., Furman A.C., Kujawa S.G., Liberman M.C. Primary neural degeneration in the Guinea pig cochlea after reversible noise-induced threshold shift. J. Assoc. Res. Otolaryngol. 2011, 12:605-616.
50. Liu M., Pereira F.A., Price S.D., Chu M.J., Shope C., Himes D., Eatock R.A., Brownell W.E., Lysakowski A., Tsai M.J. Essential role of BETA2/NeuroD1 in development of the vestibular and auditory systems. Genes Dev. 2000, 14:2839-2854.
51. Lu C.C., Appler J.M., Houseman E.A., Goodrich L.V. Developmental profiling of spiral ganglion neurons reveals insights into auditory circuit assembly. J. Neurosci. 2011, 31:10903-10918.
52. Lunn J.S., Sakowski S.A., Hur J., Feldman E.L. Stem cell technology for neurodegenerative diseases. Ann. Neurol. 2011, 70:353-361.
53. Ma Q., Anderson D.J., Fritzsch B. Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. J. Assoc. Res. Otolaryngol. 2000, 1:129-143.
54. Ma Q., Chen Z., del Barco Barrantes I., de la Pompa J.L., Anderson D.J. Neurogenin 1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 1998, 20:469-482.
55. Makary C.A., Shin J., Kujawa S.G., Liberman M.C., Merchant S.N. Age-related primary cochlear neuronal degeneration in human temporal bones. J. Assoc. Res. Otolaryngol. 2011, 12:711-717.
56. Maklad A., Kamel S., Wong E., Fritzsch B. Development and organization of polarity-specific segregation of primary vestibular afferent fibers in mice. Cell. Tissue Res. 2010, 340:303-321.
57. Maricich S.M., Xia A., Mathes E.L., Wang V.Y., Oghalai J.S., Fritzsch B., Zoghbi H.Y. Atoh1-lineal neurons are required for hearing and for the survival of neurons in the spiral ganglion and brainstem accessory auditory nuclei. J. Neurosci. 2009, 29:11123-11133.
58. Marrs G.S., Spirou G.A. Embryonic assembly of auditory circuits: spiral ganglion and brainstem. J. Physiol. 2012, 590:2391-2408.
59. Martinez-Monedero R., Edge A.S. Stem cells for the replacement of inner ear neurons and hair cells. Int. J. Dev. Biol. 2007, 51:655-661.
60. Martinez-Monedero R., Corrales C.E., Cuajungco M.P., Heller S., Edge A.S. Reinnervation of hair cells by auditory neurons after selective removal of spiral ganglion neurons. J. Neurobiol. 2006, 66:319-331.
61. Martinez-Monedero R., Yi E., Oshima K., Glowatzki E., Edge A.S. Differentiation of inner ear stem cells to functional sensory neurons. Dev. Neurobiol. 2008, 68:669-684.
62. Matei V., Pauley S., Kaing S., Rowitch D., Beisel K.W., Morris K., Feng F., Jones K., Lee J., Fritzsch B. Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Dev. Dyn. 2005, 234:633-650.
63. Meyer A.C., Frank T., Khimich D., Hoch G., Riedel D., Chapochnikov N.M., Yarin Y.M., Harke B., Hell S.W., Egner A., Moser T. Tuning of synapse number, structure and function in the cochlea. Nat. Neurosci. 2009, 12:444-453.
64. Moser T., Neef A., Khimich D. Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. J. Physiol. 2006, 576:55-62.
65. Nayagam B.A., Edge A.S., Needham K., Hyakumura T., Leung J., Nayagam D.A., Dottori M. An in vitro model of developmental synaptogenesis using cocultures of human neural progenitors and cochlear explants. Stem Cells Dev 2012, Epub ahead of print.
66. Nishimura K., Nakagawa T., Ono K., Ogita H., Sakamoto T., Yamamoto N., Okita K., Yamanaka S., Ito J. Transplantation of mouse induced pluripotent stem cells into the cochlea. Neuroreport 2009, 20:1250-1254.
67. Okano T., Nakagawa T., Endo T., Kim T.S., Kita T., Tamura T., Matsumoto M., Ohno T., Sakamoto T., Iguchi F., Ito J. Engraftment of embryonic stem cell-derived neurons into the cochlear modiolus. Neuroreport 2005, 16:1919-1922.
68. Pasterkamp R.J., Verhaagen J. Semaphorins in axon regeneration: developmental guidance molecules gone wrong?. Philos. Trans. R Soc. Lond. B Biol. Sci. 2006, 361:1499-1511.
69. Pasterkamp R.J., De Winter F., Holtmaat A.J., Verhaagen J. Evidence for a role of the chemorepellent semaphorin III and its receptor neuropilin-1 in the regeneration of primary olfactory axons. J. Neurosci. 1998, 18:9962-9976.
70. Pickles J.O., Claxton C., Van Heumen W.R. Complementary and layered expression of Ephs and ephrins in developing mouse inner ear. J. Comp. Neurol. 2002, 449:207-216.
71. Pluchino S., Zanotti L., Rossi B., Brambilla E., Ottoboni L., Salani G., Martinello M., Cattalini A., Bergami A., Furlan R., Comi G., Constantin G., Martino G. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 2005, 436:266-271.
72. Praetorius M., Vicario I., Schimmang T. Efficient transfer of embryonic stem cells into the cochlea via a non-invasive vestibular route. Acta Otolaryngol. 2008, 128:720-723.
73. Puel J.L., Ruel J., Gervais d'Aldin C., Pujol R. Excitotoxicity and repair of cochlear synapses after noise-trauma induced hearing loss. Neuroreport 1998, 9:2109-2114.
74. Puel J.L., d'Aldin C., Ruel J., Ladrech S., Pujol R. Synaptic repair mechanisms responsible for functional recovery in various cochlear pathologies. Acta Otolaryngol. 1997, 117:214-218.
75. Reyes J.H., O'Shea K.S., Wys N.L., Velkey J.M., Prieskorn D.M., Wesolowski K., Miller J.M., Altschuler R.A. 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. 2008, 28:12622-12631.
76. Robertson D. Functional significance of dendritic swelling after loud sounds in the guinea pig cochlea. Hear. Res. 1983, 9:263-278.
77. Rodgers K.D., Barritt L., Miner J.H., Cosgrove D. The laminins in the murine inner ear: developmental transitions and expression in cochlear basement membranes. Hear. Res. 2001, 158:39-50.
78. Romand M.R., Romand R. The ultrastructure of spiral ganglion cells in the mouse. Acta Otolaryngol. 1987, 104:29-39.
79. Rotshenker S. Wallerian degeneration: the innate-immune response to traumatic nerve injury. J. Neuroinflammation 2011, 8:109.
80. Rutherford M.A., Chapochnikov N.M., Moser T. Spike encoding of neurotransmitter release timing by spiral ganglion neurons of the cochlea. J. Neurosci. 2012, 32:4773-4789.
81. Ryugo D.K. Projections of low spontaneous rate, high threshold auditory nerve fibers to the small cell cap of the cochlear nucleus in cats. Neuroscience 2008, 154:114-126.
82. Ryugo D.K., Fekete D.M. 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.
83. Ryugo D.K., Parks T.N. Primary innervation of the avian and mammalian cochlear nucleus. Brain Res. Bull. 2003, 60:435-456.
84. Ryugo D.K., Kretzmer E.A., Niparko J.K. Restoration of auditory nerve synapses in cats by cochlear implants. Science 2005, 310:1490-1492.
85. Ryugo D.K., Montey K.L., Wright A.L., Bennett M.L., Pongstaporn T. Postnatal development of a large auditory nerve terminal: the endbulb of Held in cats. Hear. Res. 2006, 216-217:100-115.
86. Schmiedt R.A., Okamura H.O., Lang H., Schulte B.A. Ouabain application to the round window of the gerbil cochlea: a model of auditory neuropathy and apoptosis. J. Assoc. Res. Otolaryngol. 2002, 3:223-233.
87. Sekiya, T., Kojima, K., Matsumoto, M., Holley, M.C., Ito, J., 2007. Rebuilding lost hearing using cell transplantation. Neurosurgery 60:417-433; discussion 433.
88. Sekiya T., Kojima K., Matsumoto M., Kim T.S., Tamura T., Ito J. Cell transplantation to the auditory nerve and cochlear duct. Exp. Neurol. 2006, 198:12-24.
89. Shi F., Kempfle J.S., Edge A.S. Wnt-responsive lgr5-expressing stem cells are hair cell progenitors in the cochlea. J. Neurosci. 2012, 32:9639-9648.
90. Shi F., Corrales C.E., Liberman M.C., Edge A.S. BMP4 induction of sensory neurons from human embryonic stem cells and reinnervation of sensory epithelium. Eur. J. Neurosci. 2007, 26:3016-3023.
91. Shnerson A., Devigne C., Pujol R. Age-related changes in the C57BL/6J mouse cochlea. II. Ultrastructural findings. Brain Res. 1981, 254:77-88.
92. Sobkowicz H.M., Rose J.E., Scott G.E., Slapnick S.M. Ribbon synapses in the developing intact and cultured organ of Corti in the mouse. J. Neurosci. 1982, 2:942-957.
93. Sobkowicz H.M., Rose J.E., Scott G.L., Levenick C.V. Distribution of synaptic ribbons in the developing organ of Corti. J. Neurocytol. 1986, 15:693-714.
94. Spoendlin H. Primary structural changes in the organ of Corti after acoustic overstimulation. Acta Otolaryngol. 1971, 71:166-176.
95. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
96. Tamura T., Nakagawa T., Iguchi F., Tateya I., Endo T., Kim T.S., Dong Y., Kita T., Kojima K., Naito Y., Omori K., Ito J. Transplantation of neural stem cells into the modiolus of mouse cochleae injured by cisplatin. Acta Otolaryngol. Suppl. 2004, 65-68.
97. Tan B.T., Lee M.M., Ruan R. Bone-marrow-derived cells that home to acoustic deafened cochlea preserved their hematopoietic identity. J. Comp. Neurol. 2008, 509:167-179.
98. Tang X.Q., Heron P., Mashburn C., Smith G.M. Targeting sensory axon regeneration in adult spinal cord. J. Neurosci. 2007, 27:6068-6078.
99. Tannemaat M.R., Korecka J., Ehlert E.M., Mason M.R., van Duinen S.G., Boer G.J., Malessy M.J., Verhaagen J. Human neuroma contains increased levels of semaphorin 3A, which surrounds nerve fibers and reduces neurite extension in vitro. J. Neurosci. 2007, 27:14260-14264.
100. Tashiro A., Sandler V.M., Toni N., Zhao C., Gage F.H. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 2006, 442:929-933.
101. Thonabulsombat C., Johansson S., Spenger C., Ulfendahl M., Olivius P. Implanted embryonic sensory neurons project axons toward adult auditory brainstem neurons in roller drum and Stoppini co-cultures. Brain Res. 2007, 1170:48-58.
102. Tokano, H., Shi, F., Liberman, M.C. Edge ASB Improvement in function after transplantation of ES cell-derived neural progenitors into the de-afferented cochlea, Submitted for publication.
103. Tong, M., Brugeaud, A., Edge, A.S.B. Regenerated synapses between postnatal hair cells and auditory neurons. J. Assoc. Res. Otolaryngol., in press.
104. Tritsch N.X., Bergles D.E. Developmental regulation of spontaneous activity in the Mammalian cochlea. J. Neurosci. 2010, 30:1539-1550.
105. Tritsch N.X., Yi E., Gale J.E., Glowatzki E., Bergles D.E. The origin of spontaneous activity in the developing auditory system. Nature 2007, 450:50-55.
106. Vierbuchen T., Ostermeier A., Pang Z.P., Kokubu Y., Sudhof T.C., Wernig M. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 2010, 463:1035-1041.
107. Wang J., Ding D., Salvi R.J. Carboplatin-induced early cochlear lesion in chinchillas. Hear. Res. 2003, 181:65-72.
108. Wang Q., Green S.H. Functional role of neurotrophin-3 in synapse regeneration by spiral ganglion neurons on inner hair cells after excitotoxic trauma in vitro. J. Neurosci. 2011, 31:7938-7949.
109. Whitlon D.S., Zhang X., Kusakabe M. Tenascin-C in the cochlea of the developing mouse. J. Comp. Neurol. 1999, 406:361-374.
110. Yuan Y., Mizutari K., Cheng Y., Lang H., Liberman C., Shi F., Edge A. Reinnervation of Hair Cells and Cochlear Nucleus by Engrafted Neurons Derived from Stem Cells 2012, ARO 35th Annual Meeting Abstract #355.
111. Zhang R., Zhang L., Zhang Z., Wang Y., Lu M., Lapointe M., Chopp M. A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann. Neurol. 2001, 50:602-611.
112. Zhou Y., Yuan J., Zhou B., Lee A.J., Ghawji M., Yoo T.J. The therapeutic efficacy of human adipose tissue-derived mesenchymal stem cells on experimental autoimmune hearing loss in mice. Immunology 2011, 133:133-140.