Cell- and gene-therapy approaches to inner ear repair

Histology and Histopathology

Volumn 26, Issue 7, 2011, Pages 923-940

  de Felipe, M M Conde ^a   Redondo, A Feijoo ^a   Garcia Sancho J ^a   Schimmang, T ^a   Alonso, M B Durán ^a  

^a UNIVERSITY OF VALLADOLID   (Spain)

Author keywords

Auditory neurons; Cochlea; Hair c ells; Hearing loss

Indexed keywords

NERVE GROWTH FACTOR;

ANIMAL; CELL SURVIVAL; CELL TRANSDIFFERENTIATION; GENE THERAPY; HUMAN; INJURY; INNER EAR; METHODOLOGY; NERVE CELL; PATHOLOGY; PERCEPTION DEAFNESS; REGENERATION; REVIEW; SPIRAL GANGLION; STEM CELL TRANSPLANTATION;

ANIMALS; CELL SURVIVAL; CELL TRANSDIFFERENTIATION; EAR, INNER; GENE THERAPY; HEARING LOSS, SENSORINEURAL; HUMANS; NERVE GROWTH FACTORS; NEURONS; REGENERATION; SPIRAL GANGLION; STEM CELL TRANSPLANTATION;

MAMMALIA; VERTEBRATA;

EID: 79960676965     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (173)

1. 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, 355-367.
2. Alam S.A., Robinson B.K., Huang J. and Green S.H. (2007). Prosurvival and proapoptotic intracellular signaling in rat spiral ganglion neurons in vivo after the loss of hair cells. J. Comp. Neurol. 503, 832-852.
3. Altschuler R.A., Cho Y., Ylikoski J., Pirvola U., Magal E. and Miller J.M. (1999). Rescue and regrowth of sensory nerves following deafferentation by neurotrophic factors. Ann. N. Y. Acad. Sci. 884, 305-311.
4. Altschuler R.A., O'Shea K.S. and Miller J.M. (2008). Stem cell transplantation for auditory nerve replacement. Hear. Res. 242, 110-116.
5. Batts S.A., Shoemaker C.R. and Raphael Y. (2009). Notch signaling and Hes labeling in the normal and drug-damaged organ of Corti. Hear. Res. 249, 15-22.
6. 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, 1837-1841.
7. Bermingham-McDonogh O. and Rubel E.W. (2003). Hair cell regeneration: winging our way towards a sound future. Curr. Opin. Neurobiol. 13, 119-126.
8. Bitner-Glindzicz M., Osei-Lah V., Colvin I., Sirimanna T., Lucas D., Mac Ardle B., Webb D., Shankar A., Kingston J., Jenkins L. and Rahman S. (2010). Aminoglycoside-induced deafness during treatment of acute leukaemia. Arch. Dis. Child. 95, 153-155.
9. Brigande J.V. and Heller S. (2009). Quo vadis, hair cell regeneration? Nat. Neurosci. 12, 679-685.
10. Brignull H.R., Raible D.W. and Stone J.S. (2009). Feathers and fins: non-mammalian models for hair cell regeneration. Brain Res. 1277, 12-23.
11. Burns J., Christophel J.J., Collado M.S., Magnus C., Carfrae M. and Corwin J.T. (2008). Reinforcement of cell junctions correlates with the absence of hair cell regeneration in mammals and its occurrence in birds. J. Comp. Neurol. 511, 396-414.
12. Caddick J., Kingham P.J., Gardiner N.J., Wiberg M. and Terenghi G. (2006). Phenotypic and functional characteristics of mesenchymal stem cells differentiated along a Schwann cell lineage. Glia 54, 840-849.
13. Chen H.C., Ma H.I., Sytwu H.K., Wang H.W., Chen C.C., Liu S.C., Chen C.H., Chen H.K. and Wang C.H. (2010). Neural stem cells secrete factors that promote auditory cell proliferation via a leukemia inhibitory factor signaling pathway. J. Neurosci. Res. 88, 3308-3318.
14. Chen P., Zindy F., Abdala C., Liu F., Li X., Roussel M.F. and Segil N. (2003). Progressive hearing loss in mice lacking the cyclindependent kinase inhibitor Ink4d. Nat. Cell Biol. 5, 422-426.
15. Chen W., Cacciabue-Rivolta D.I., Moore H.D. and Rivolta M.N. (2007). The human fetal cochlea can be a source for auditory progenitors/stem cells isolation. Hear. Res. 233, 23-29.
16. 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, 1196-1204.
17. 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, 232-243.
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, 369-380.
19. Corrales C.E., Pan L., Li H., Liberman M.C., Heller S. and Edge A.S. (2006). Engraftment and differentiation of embryonic stem cellderived neural progenitor cells in the cochlear nerve trunk: growth of processes into the organ of Corti. J. Neurobiol. 66, 1489-1500.
20. Cotanche D.A. (2008). Genetic and pharmacological intervention for treatment/prevention of hearing loss. J. Commun. Disord. 41, 421- 443.
21. Cotanche D.A. and Kaiser C.L. (2010). Hair cell fate decisions in cochlear development and regeneration. Hear. Res. 266, 18-25.
22. Daudet N. and Lewis J. (2005). Two contrasting roles for Notch activity in chick inner ear development: specification of prosensory patches and lateral inhibition of hair-cell differentiation. Development 132, 541-551.
23. Deng W., Obrocka M., Fischer I. and Prockop D.J. (2001). In vitro differentiation of human marrow stromal cells into early progenitors of neural cells by conditions that increase intracellular cyclic AMP. Biochem. Biophys. Res. Commun. 282, 148-152.
24. Doetzlhofer A., Basch M.L., Ohyama T., Gessler M., Groves A.K. and Segil N. (2009). Hey2 regulation by FGF provides a Notchindependent mechanism for maintaining pillar cell fate in the organ of Corti. Dev. Cell. 16, 58-69.
25. Doyle K.L., Kazda A., Hort Y., McKay S.M. and Oleskevich S. (2007). Differentiation of adult mouse olfactory precursor cells into hair cells in vitro. Stem Cells 25, 621-627.
26. Dror A.A. and Avraham K.B. (2010). Hearing impairment: a panoply of genes and functions. Neuron 68, 293-308.
27. Erdo F., Buhrle C., Blunk J., Hoehn M., Xia Y., Fleischmann B., Focking M., Kustermann E., Kolossov E., Hescheler J., Hossmann K.A. and Trapp T. (2003). Host-dependent tumorigenesis of embryonic stem cell transplantation in experimental stroke. J. Cereb. Blood Flow Metab. 23, 780-785.
28. Fekete D.M. and Wu D.K. (2002). Revisiting cell fate specification in the inner ear. Curr. Opin. Neurobiol. 12, 35-42.
29. Fransson A., Maruyama J., Miller J.M. and Ulfendahl M. (2010). Posttreatment effects of local GDNF administration to the inner ears of deafened guinea pigs. J. Neurotrauma 27, 1745-1751.
30. Gillespie L.N. and Shepherd R.K. (2005). Clinical application of neurotrophic factors: the potential for primary auditory neuron protection. Eur. J. Neurosci. 22, 2123-2133.
31. Gillespie L.N., Clark G.M., Bartlett P.F. and Marzella P.L. (2003). BDNFinduced survival of auditory neurons in vivo: Cessation of treatment leads to accelerated loss of survival effects. J. Neurosci. Res. 71, 785-790.
32. Gillespie L.N., Clark G.M. and Marzella P.L. (2004). Delayed neurotrophin treatment supports auditory neuron survival in deaf guinea pigs. Neuroreport 15, 1121-1125.
33. Groves A.K. (2010). The challenge of hair cell regeneration. Exp. Biol. Med. (Maywood) 235, 434-446.
34. Gubbels S.P., Woessner D.W., Mitchell J.C., Ricci A.J. and Brigande J.V. (2008). Functional auditory hair cells produced in the mammalian cochlea by in utero gene transfer. Nature 455, 537-541.
35. Hakuba N., Hata R., Morizane I., Feng G., Shimizu Y., Fujita K., Yoshida T., Sakanaka M. and Gyo K. (2005). Neural stem cells suppress the hearing threshold shift caused by cochlear ischemia. Neuroreport 16, 1545-1549.
36. 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, 426-433.
37. 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, 490-496.
38. Hansen M.R., Vijapurkar U., Koland J.G. and Green S.H. (2001). Reciprocal signaling between spiral ganglion neurons and Schwann cells involves neuregulin and neurotrophins. Hear. Res. 161, 87-98.
39. 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.
40. 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, 341-354.
41. Hildebrand M.S., Newton S.S., Gubbels S.P., Sheffield A.M., Kochhar A., de Silva M.G., Dahl H.H., Rose S.D., Behlke M.A. and Smith R.J. (2008). Advances in molecular and cellular therapies for hearing loss. Mol. Ther. 16, 224-236.
42. Hilgert N., Smith R.J. and Van Camp G. (2009). Function and expression pattern of nonsyndromic deafness genes. Curr. Mol. Med. 9, 546-564.
43. Hori R., Nakagawa T., Sakamoto T., Matsuoka Y., Takebayashi S. and Ito J. (2007). Pharmacological inhibition of Notch signaling in the mature guinea pig cochlea. Neuroreport 18, 1911-1914.
44. Hu Z., Ulfendahl M. and Olivius N.P. (2004). Central migration ofneuronal tissue and embryonic stem cells following transplantation along the adult auditory nerve. Brain Res. 1026, 68-73.
45. Hu Z., Andang M., Ni D. and Ulfendahl M. (2005a). Neural cograft stimulates the survival and differentiation of embryonic stem cells in the adult mammalian auditory system. Brain Res. 1051, 137-144.
46. Hu Z., Ulfendahl M. and Olivius N.P. (2005b). NGF stimulates extensive neurite outgrowth from implanted dorsal root ganglion neurons following transplantation into the adult rat inner ear. Neurobiol. Dis. 18, 184-192.
47. Hu Z., Wei D., Johansson C.B., Holmstrom N., Duan M., Frisen J. and Ulfendahl M. (2005c). Survival and neural differentiation of adult neural stem cells transplanted into the mature inner ear. Exp. Cell Res. 302, 40-47.
48. Hurley F.M., Costello D.J. and Sullivan A.M. (2004). Neuroprotective effects of delayed administration of growth/differentiation factor-5 in the partial lesion model of Parkinson's disease. Exp. Neurol. 185, 281-289.
49. Iguchi F., Nakagawa T., Tateya I., Kim T.S., Endo T., Taniguchi Z., Naito Y. and Ito J. (2003). Trophic support of mouse inner ear by neural stem cell transplantation. Neuroreport 14, 77-80.
50. Ito J., Kojima K. and Kawaguchi S. (2001). Survival of neural stem cells in the cochlea. Acta Otolaryngol. 121, 140-142.
51. 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, 271-276.
52. 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, 52-56.
53. Jeon S.J., Oshima K., Heller S. and Edge A.S. (2007). Bone marrow mesenchymal stem cells are progenitors in vitro for inner ear hair cells. Mol. Cell. Neurosci. 34, 59-68.
54. Jiang Y., Jahagirdar B.N., Reinhardt R.L., Schwartz R.E., Keene C.D., Ortiz-Gonzalez X.R., Reyes M., Lenvik T., Lund T., Blackstad M., Du J., Aldrich S., Lisberg A., Low W.C., Largaespada D.A. and Verfaillie C.M. (2002a). Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418, 41-49.
55. Jiang Y., Vaessen B., Lenvik T., Blackstad M., Reyes M. and Verfaillie C.M. (2002b). Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp. Hematol. 30, 896-904.
56. Jin K., Mao X.O., Batteur S., Sun Y. and Greenberg D.A. (2003). Induction of neuronal markers in bone marrow cells: differential effects of growth factors and patterns of intracellular expression. Exp. Neurol. 184, 78-89.
57. Jongkamonwiwat N., Zine A. and Rivolta M.N. (2010). Stem cell based therapy in the inner ear: appropriate donor cell types and routes for transplantation. Curr. Drug Targets 11, 888-897.
58. Kanzaki S., Stover T., Kawamoto K., Prieskorn D.M., Altschuler R.A., Miller J.M. and Raphael Y. (2002). Glial cell line-derived neurotrophic factor and chronic electrical stimulation prevent VIII cranial nerve degeneration following denervation. J. Comp. Neurol. 454, 350-360.
59. 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, 4395-4400.
60. Kelley M.W., Talreja D.R. and Corwin J.T. (1995). Replacement of hair cells after laser microbeam irradiation in cultured organs of corti from embryonic and neonatal mice. J. Neurosci. 15, 3013-3026.
61. Kiernan A.E., Cordes R., Kopan R., Gossler A. and Gridley T. (2005). The Notch ligands DLL1 and JAG2 act synergistically to regulate hair cell development in the mammalian inner ear. Development 132, 4353-4362.
62. Kim Y.H. and Raphael Y. (2007). Cell division and maintenance of epithelial integrity in the deafened auditory epithelium. Cell. Cycle 6, 612-619.
63. Kondo T., Johnson S.A., Yoder M.C., Romand R. and Hashino E. (2005). Sonic hedgehog and retinoic acid synergistically promote sensory fate specification from bone marrow-derived pluripotent stem cells. Proc. Natl. Acad. Sci. USA 102, 4789-4794.
64. Konishi M., Kawamoto K., Izumikawa M., Kuriyama H. and Yamashita T. (2008). Gene transfer into guinea pig cochlea using adenoassociated virus vectors. J. Gene Med. 10, 610-618.
65. Krabbe C., Zimmer J. and Meyer M. (2005). Neural transdifferentiation of mesenchymal stem cells--a critical review. APMIS 113, 831-844.
66. Kuroda Y., Kitada M., Wakao S., Nishikawa K., Tanimura Y., Makinoshima H., Goda M., Akashi H., Inutsuka A., Niwa A., Shigemoto T., Nabeshima Y., Nakahata T., Nabeshima Y., Fujiyoshi Y. and Dezawa M. (2010). Unique multipotent cells in adult human mesenchymal cell populations. Proc. Natl. Acad. Sci. USA 107, 8639-8643.
67. Laine H., Doetzlhofer A., Mantela J., Ylikoski J., Laiho M., Roussel M.F., Segil N. and Pirvola U. (2007). p19(Ink4d) and p21(Cip1) collaborate to maintain the postmitotic state of auditory hair cells, their codeletion leading to DNA damage and p53-mediated apoptosis. J. Neurosci. 27, 1434-1444.
68. Lang H., Ebihara Y., Schmiedt R.A., Minamiguchi H., Zhou D., Smythe N., Liu L., Ogawa M. and Schulte B.A. (2006). Contribution of bone marrow hematopoietic stem cells to adult mouse inner ear: mesenchymal cells and fibrocytes. J. Comp. Neurol. 496, 187-201.
69. Lang H., Schulte B.A., Goddard J.C., Hedrick M., Schulte J.B., Wei L. and Schmiedt R.A. (2008). Transplantation of mouse embryonic stem cells into the cochlea of an auditory-neuropathy animal model: effects of timing after injury. J. Assoc. Res. Otolaryngol. 9, 225-240.
70. Li H., Liu H. and Heller S. (2003a). Pluripotent stem cells from the adult mouse inner ear. Nat. Med. 9, 1293-1299.
71. Li H., Roblin G., Liu H. and Heller S. (2003b). Generation of hair cells by stepwise differentiation of embryonic stem cells. Proc. Natl. Acad. Sci. USA 100, 13495-13500.
72. Liu Q., Ye J., Yu H., Li H., Dai C., Gu Y., Zhu Y. and Zhang Z. (2010). Survival-enhancing of spiral ganglion cells under influence of olfactory ensheathing cells by direct cellular contact. Neurosci. Lett. 478, 37-41.
73. Liu Y., Okada T., Sheykholeslami K., Shimazaki K., Nomoto T., Muramatsu S., Kanazawa T., Takeuchi K., Ajalli R., Mizukami H., Kume A., Ichimura K. and Ozawa K. (2005). Specific and efficient transduction of Cochlear inner hair cells with recombinant adenoassociated virus type 3 vector. Mol. Ther. 12, 725-733.
74. Liu Y., Okada T., Shimazaki K., Sheykholeslami K., Nomoto T., Muramatsu S., Mizukami H., Kume A., Xiao S., Ichimura K. and Ozawa K. (2008). Protection against aminoglycoside-induced ototoxicity by regulated AAV vector-mediated GDNF gene transfer into the cochlea. Mol. Ther. 16, 474-480.
75. Lu P., Blesch A. and Tuszynski M.H. (2004). Induction of bone marrow stromal cells to neurons: differentiation, transdifferentiation, or artifact? J. Neurosci. Res. 77, 174-191.
76. Malgrange B., Belachew S., Thiry M., Nguyen L., Rogister B., Alvarez M.L., Rigo J.M., Van De Water T.R., Moonen G. and Lefebvre P.P. (2002). Proliferative generation of mammalian auditory hair cells in culture. Mech. Dev. 112, 79-88.
77. Martinez-Monedero R., Corrales C.E., Cuajungco M.P., Heller S. and Edge A.S. (2006). Reinnervation of hair cells by auditory neurons after selective removal of spiral ganglion neurons. J. Neurobiol. 66, 319-331.
78. Martinez-Monedero R., Oshima K., Heller S. and Edge A.S. (2007). The potential role of endogenous stem cells in regeneration of the inner ear. Hear. Res. 227, 48-52.
79. 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, 669-684.
80. Maruyama J., Yamagata T., Ulfendahl M., Bredberg G., Altschuler R.A. and Miller J.M. (2007). Effects of antioxidants on auditory nerve function and survival in deafened guinea pigs. Neurobiol. Dis. 25, 309-318.
81. 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.
82. Marzella P.L., Gillespie L.N., Clark G.M., Bartlett P.F. and Kilpatrick T.J. (1999). The neurotrophins act synergistically with LIF and members of the TGF-beta superfamily to promote the survival of spiral ganglia neurons in vitro. Hear. Res. 138, 73-80.
83. 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, 3075-3085.
84. Matsuoka A.J., Kondo T., Miyamoto R.T. and Hashino E. (2006). In vivo and in vitro characterization of bone marrow-derived stem cells in the cochlea. Laryngoscope 116, 1363-1367.
85. Matsuoka A.J., Kondo T., Miyamoto R.T. and Hashino E. (2007). Enhanced survival of bone-marrow-derived pluripotent stem cells in an animal model of auditory neuropathy. Laryngoscope 117, 1629- 1635.
86. Meen E., Blakley B. and Quddusi T. (2009). Brain-derived nerve growth factor in the treatment of sensorineural hearing loss. Laryngoscope 119, 1590-1593.
87. Meyers J.R. and Corwin J.T. (2007). Shape change controls supporting cell proliferation in lesioned mammalian balance epithelium. J. Neurosci. 27, 4313-4325.
88. Miller J. and Altschuler R. (2004). Neurotrophic factor and electrical stimulation promotes auditory nerve survival and regrowth following deafness. ARO Midwinter meeting, 90.
89. Miller J., Prieskorn D., Lee S., Kim J., Mitchell A. and Altschuler R. (2006). Auditory nerve survival remains enhanced four weeks following cessation of treatment with glial cell-line derived neurotrophic factor. ARO Midwinter meeting, Abstract 891.
90. Miller J.M., Le Prell C.G., Prieskorn D.M., Wys N.L. and Altschuler R.A. (2007). Delayed neurotrophin treatment following deafness rescues spiral ganglion cells from death and promotes regrowth of auditory nerve peripheral processes: effects of brain-derived neurotrophic factor and fibroblast growth factor. J. Neurosci. Res. 85, 1959-1969.
91. Minoda R., Izumikawa M., Kawamoto K., Zhang H. and Raphael Y. (2007). Manipulating cell cycle regulation in the mature cochlea. Hear. Res. 232, 44-51.
92. Naito Y., Nakamura T., Nakagawa T., Iguchi F., Endo T., Fujino K., Kim T.S., Hiratsuka Y., Tamura T., Kanemaru S., Shimizu Y. and Ito J. (2004). Transplantation of bone marrow stromal cells into the cochlea of chinchillas. Neuroreport 15, 1-4.
93. 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, 135-143.
94. Nicholl A.J., Kneebone A., Davies D., Cacciabue-Rivolta D.I., Rivolta M.N., Coffey P. and Holley M.C. (2005). Differentiation of an auditory neuronal cell line suitable for cell transplantation. Eur. J. Neurosci. 22, 343-353.
95. Nishimura K., Nakagawa T., Ono K., Ogita H., Sakamoto T., Yamamoto N., Okita K., Yamanaka S. and Ito J. (2009). Transplantation of mouse induced pluripotent stem cells into the cochlea. Neuroreport 20, 1250-1254.
96. Noushi F., Richardson R.T., Hardman J., Clark G. and O'Leary S. (2005). Delivery of neurotrophin-3 to the cochlea using alginate beads. Otol. Neurotol. 26, 528-533.
97. Oesterle E.C. and Campbell S. (2009). Supporting cell characteristics in long-deafened aged mouse ears. J. Assoc. Res. Otolaryngol. 10, 525-544.
98. Oesterle E.C., Campbell S., Taylor R.R., Forge A. and Hume C.R. (2008). Sox2 and JAGGED1 expression in normal and drugdamaged adult mouse inner ear. J. Assoc. Res. Otolaryngol. 9, 65- 89.
99. Ogita H., Nakagawa T., Sakamoto T., Inaoka T. and Ito J. (2010). Transplantation of bone marrow-derived neurospheres into guinea pig cochlea. Laryngoscope 120, 576-581.
100. Okano T., Nakagawa T., Endo T., Kim T.S., Kita T., Tamura T., Matsumoto M., Ohno T., Sakamoto T., Iguchi F. and Ito J. (2005). Engraftment of embryonic stem cell-derived neurons into the cochlear modiolus. Neuroreport 16, 1919-1922.
101. Okano T., Nakagawa T., Kita T., Endo T. and Ito J. (2006). Cell-gene delivery of brain-derived neurotrophic factor to the mouse inner ear. Mol. Ther. 14, 866-871.
102. Ono K., Nakagawa T., Kojima K., Matsumoto M., Kawauchi T., Hoshino M. and Ito J. (2009). Silencing p27 reverses post-mitotic state of supporting cells in neonatal mouse cochleae. Mol. Cell. Neurosci. 42, 391-398.
103. Oshima K., Grimm C.M., Corrales C.E., Senn P., Martinez Monedero R., Geleoc G.S., Edge A., Holt J.R. and Heller S. (2007). Differential distribution of stem cells in the auditory and vestibular organs of the inner ear. J. Assoc. Res. Otolaryngol. 8, 18-31.
104. Oshima K., Senn P. and Heller S. (2009). Isolation of sphere-forming stem cells from the mouse inner ear. Methods Mol. Biol. 493, 141-162.
105. 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, 704-716.
106. Othman M., Lu C., Klueber K., Winstead W. and Roisen F. (2005). Clonal analysis of adult human olfactory neurosphere forming cells. Biotech. Histochem. 80, 189-200.
107. Ourednik J., Ourednik V., Lynch W.P., Schachner M. and Snyder E.Y. (2002). Neural stem cells display an inherent mechanism for rescuing dysfunctional neurons. Nat. Biotechnol. 20, 1103-1110.
108. 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.
109. 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, 1138-1148.
110. 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, 821-828.
111. Poirrier A.L., Pincemail J., Van Den Ackerveken P., Lefebvre P.P. and Malgrange B. (2010). Oxidative stress in the cochlea: an update. Curr. Med. Chem. 17, 3591-3604.
112. Pollock K., Stroemer P., Patel S., Stevanato L., Hope A., Miljan E., Dong Z., Hodges H., Price J. and Sinden J.D. (2006). A conditionally immortal clonal stem cell line from human cortical neuroepithelium for the treatment of ischemic stroke. Exp. Neurol. 199, 143-155.
113. Prayle A. and Smyth A.R. (2010). Aminoglycoside use in cystic fibrosis: therapeutic strategies and toxicity. Curr. Opin. Pulm. Med. 16, 604-610.
114. Puligilla C. and Kelley M.W. (2009). Building the world's best hearing aid; regulation of cell fate in the cochlea. Curr. Opin. Genet. Dev. 19, 368-373.
115. Rask-Andersen H., Bostrom M., Gerdin B., Kinnefors A., Nyberg G., Engstrand T., Miller J.M. and Lindholm D. (2005). Regeneration of human auditory nerve. In vitro/in video demonstration of neural progenitor cells in adult human and guinea pig spiral ganglion. Hear. Res. 203, 180-191.
116. Regala C., Duan M., Zou J., Salminen M. and Olivius P. (2005). Xenografted fetal dorsal root ganglion, embryonic stem cell and adult neural stem cell survival following implantation into the adult vestibulocochlear nerve. Exp. Neurol. 193, 326-333.
117. 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, 12622-12631.
118. Richardson R.T., O'Leary S., Wise A., Hardman J. and Clark G. (2005). A single dose of neurotrophin-3 to the cochlea surrounds spiral ganglion neurons and provides trophic support. Hear. Res. 204, 37-47.
119. Rivolta M.N. (2010). Stem cells and cell lines from the human auditory organ: applications, hurdles and bottlenecks in the development of regenerative therapies for deafness. Drug Discov. Today 15, 283-286.
120. Roberson D.W., Alosi J.A. and Cotanche D.A. (2004). Direct transdifferentiation gives rise to the earliest new hair cells in regenerating avian auditory epithelium. J. Neurosci. Res. 78, 461-471.
121. Roisen F.J., Klueber K.M., Lu C.L., Hatcher L.M., Dozier A., Shields C.B. and Maguire S. (2001). Adult human olfactory stem cells. Brain Res. 890, 11-22.
122. Roy S., Johnston A.H., Newman T.A., Glueckert R., Dudas J., Bitsche M., Corbacella E., Rieger G., Martini A. and Schrott-Fischer A. (2010). Cell-specific targeting in the mouse inner ear using nanoparticles conjugated with a neurotrophin-derived peptide ligand: potential tool for drug delivery. Int. J. Pharm. 390, 214-224.
123. Sage C., Huang M., Karimi K., Gutierrez G., Vollrath M.A., Zhang D.S., Garcia-Anoveros J., Hinds P.W., Corwin J.T., Corey D.P. and Chen Z.Y. (2005). Proliferation of functional hair cells in vivo in the absence of the retinoblastoma protein. Science 307, 1114-1118.
124. Sage C., Huang M., Vollrath M.A., Brown M.C., Hinds P.W., Corey D.P., Vetter D.E. and Chen Z.Y. (2006). Essential role of retinoblastoma protein in mammalian hair cell development and hearing. Proc. Natl. Acad. Sci. USA 103, 7345-7350.
125. Sanchez-Ramos J., Song S., Cardozo-Pelaez F., Hazzi C., Stedeford T., Willing A., Freeman T.B., Saporta S., Janssen W., Patel N., Cooper D.R. and Sanberg P.R. (2000). Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp. Neurol. 164, 247-256.
126. Savary E., Hugnot J.P., Chassigneux Y., Travo C., Duperray C., Van De Water T. and Zine A. (2007). Distinct population of hair cell progenitors can be isolated from the postnatal mouse cochlea using side population analysis. Stem Cells 25, 332-339.
127. Savary E., Sabourin J.C., Santo J., Hugnot J.P., Chabbert C., Van De Water T., Uziel A. and Zine A. (2008). Cochlear stem/progenitor cells from a postnatal cochlea respond to Jagged1 and demonstrate that notch signaling promotes sphere formation and sensory potential. Mech. Dev. 125, 674-686.
128. Scheper V., Paasche G., Miller J.M., Warnecke A., Berkingali N., Lenarz T. and Stover T. (2009). Effects of delayed treatment with combined GDNF and continuous electrical stimulation on spiral ganglion cell survival in deafened guinea pigs. J. Neurosci. Res. 87, 1389-1399.
129. Schimmang T., Tan J., Muller M., Zimmermann U., Rohbock K., Kopschall I., Limberger A., Minichiello L. and Knipper M. (2003). Lack of Bdnf and TrkB signalling in the postnatal cochlea leads to a spatial reshaping of innervation along the tonotopic axis and hearing loss. Development 130, 4741-4750.
130. Sekiya T., Holley M.C., Kojima K., Matsumoto M., Helyer R. and Ito J. (2007). Transplantation of conditionally immortal auditory neuroblasts to the auditory nerve. Eur. J. Neurosci. 25, 2307-2318.
131. Sekiya T., Kojima K., Matsumoto M., Kim T.S., Tamura T. and Ito J. (2006). Cell transplantation to the auditory nerve and cochlear duct. Exp. Neurol. 198, 12-24.
132. Sell S. (2004). Stem cell origin of cancer and differentiation therapy. Crit. Rev. Oncol. Hematol. 51, 1-28.
133. Shepherd R.K., Roberts L.A. and Paolini A.G. (2004). Long-term sensorineural hearing loss induces functional changes in the rat auditory nerve. Eur. J. Neurosci. 20, 3131-3140.
134. Shepherd R.K., Coco A., Epp S.B. and Crook J.M. (2005). Chronic depolarization enhances the trophic effects of brain-derived neurotrophic factor in rescuing auditory neurons following a sensorineural hearing loss. J. Comp. Neurol. 486, 145-158.
135. 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, 100-109.
136. 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, 3016-3023.
137. Shibata S.B. and Raphael Y. (2010). Future approaches for inner ear protection and repair. J. Commun. Disord. 43, 295-310.
138. Shinohara T., Bredberg G., Ulfendahl M., Pyykko I., Olivius N.P., Kaksonen R., Lindstrom B., Altschuler R. and Miller J.M. (2002). Neurotrophic factor intervention restores auditory function in deafened animals. Proc. Natl. Acad. Sci. USA 99, 1657-1660.
139. Shoji F., Miller A.L., Mitchell A., Yamasoba T., Altschuler R.A. and Miller J.M. (2000a). Differential protective effects of neurotrophins in the attenuation of noise-induced hair cell loss. Hear. Res. 146, 134-142.
140. Shoji F., Yamasoba T., Magal E., Dolan D.F., Altschuler R.A. and Miller J.M. (2000b). Glial cell line-derived neurotrophic factor has a dose dependent influence on noise-induced hearing loss in the guinea pig cochlea. Hear. Res. 142, 41-55.
141. Shou J., Zheng J.L. and Gao W.Q. (2003). Robust generation of new hair cells in the mature mammalian inner ear by adenoviral expression of Hath1. Mol. Cell. Neurosci. 23, 169-179.
142. Song B.N., Li Y.X. and Han D.M. (2008). Effects of delayed brainderived neurotrophic factor application on cochlear pathology and auditory physiology in rats. Chin. Med. J. (Engl) 121, 1189-1196.
143. Song S. and Sanchez-Ramos J. (2003). Brain as the Sea of Marrow. Exp. Neurol. 184, 54-60.
144. Stevanato L., Corteling R.L., Stroemer P., Hope A., Heward J., Miljan E.A. and Sinden J.D. (2009). c-MycERTAM transgene silencing in a genetically modified human neural stem cell line implanted into MCAo rodent brain. BMC Neurosci. 10, 86.
145. Stone J.S. and Cotanche D.A. (2007). Hair cell regeneration in the avian auditory epithelium. Int. J. Dev. Biol. 51, 633-647.
146. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K. and Yamanaka S. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872.
147. Takahashi K. and Yamanaka S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676.
148. Talaska A.E., Schacht J. and Fischel-Ghodsian N. (2006). Molecular and genetic aspects of aminoglycoside-induced hearing loss. Drug Discovery Today: Disease Mechanisms 3, 119-124.
149. Tan B.T., Lee M.M. and Ruan R. (2008). Bone-marrow-derived cells that home to acoustic deafened cochlea preserved their hematopoietic identity. J. Comp. Neurol. 509, 167-179.
150. 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, 1677-1681.
151. Tessarollo L., Coppola V. and Fritzsch B. (2004). NT-3 replacement with brain-derived neurotrophic factor redirects vestibular nerve fibers to the cochlea. J. Neurosci. 24, 2575-2584.
152. Tondreau T., Lagneaux L., Dejeneffe M., Massy M., Mortier C., Delforge A. and Bron D. (2004). Bone marrow-derived mesenchymal stem cells already express specific neural proteins before any differentiation. Differentiation 72, 319-326.
153. Tsuji O., Miura K., Okada Y., Fujiyoshi K., Mukaino M., Nagoshi N., Kitamura K., Kumagai G., Nishino M., Tomisato S., Higashi H., Nagai T., Katoh H., Kohda K., Matsuzaki Y., Yuzaki M., Ikeda E., Toyama Y., Nakamura M., Yamanaka S. and Okano H. (2010). Therapeutic potential of appropriately evaluated safe-induced pluripotent stem cells for spinal cord injury. Proc. Natl. Acad. Sci. USA 107, 12704-12709.
154. Ulfendahl M., Hu Z., Olivius P., Duan M. and Wei D. (2007). A cell therapy approach to substitute neural elements in the inner ear. Physiol. Behav. 92, 75-79.
155. Warchol M.E. (2011). Sensory regeneration in the vertebrate inner ear: Differences at the levels of cells and species. Hear. Res. 273, 72-79.
156. Weber T., Corbett M.K., Chow L.M., Valentine M.B., Baker S.J. and Zuo J. (2008). Rapid cell-cycle reentry and cell death after acute inactivation of the retinoblastoma gene product in postnatal cochlear hair cells. Proc. Natl. Acad. Sci. USA 105, 781-785.
157. Wei D., Levic S., Nie L., Gao W.Q., Petit C., Jones E.G. and 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. Proc. Natl. Acad. Sci. USA 105, 21000-21005.
158. White P.M., Doetzlhofer A., Lee Y.S., Groves A.K. and Segil N. (2006). Mammalian cochlear supporting cells can divide and transdifferentiate into hair cells. Nature 441, 984-987.
159. Whitlon D.S., Ketels K.V., Coulson M.T., Williams T., Grover M., Edpao W. and Richter C.P. (2006). Survival and morphology of auditory neurons in dissociated cultures of newborn mouse spiral ganglion. Neuroscience 138, 653-662.
160. Whitlon D.S., Tieu D., Grover M., Reilly B. and Coulson M.T. (2009). Spontaneous association of glial cells with regrowing neurites in mixed cultures of dissociated spiral ganglia. Neuroscience 161, 227- 235.
161. 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, 147-165.
162. Woodbury D., Schwarz E.J., Prockop D.J. and Black I.B. (2000). Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res. 61, 364-370.
163. Woods C., Montcouquiol M. and Kelley M.W. (2004). Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat. Neurosci. 7, 1310-1318.
164. 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, 315-325.
165. Yamagata T., Miller J.M., Ulfendahl M., Olivius N.P., Altschuler R.A., Pyykko I. and Bredberg G. (2004). Delayed neurotrophic treatment preserves nerve survival and electrophysiological responsiveness in neomycin-deafened guinea pigs. J. Neurosci. Res. 78, 75-86.
166. Yamamoto N., Tanigaki K., Tsuji M., Yabe D., Ito J. and Honjo T. (2006). Inhibition of Notch/RBP-J signaling induces hair cell formation in neonate mouse cochleas. J. Mol. Med. 84, 37-45.
167. Yamasoba T. and Kondo K. (2006). Supporting cell proliferation after hair cell injury in mature guinea pig cochlea in vivo. Cell Tissue Res. 325, 23-31.
168. Yoshida T., Hakuba N., Morizane I., Fujita K., Cao F., Zhu P., Uchida N., Kameda K., Sakanaka M., Gyo K. and Hata R. (2007). Hematopoietic stem cells prevent hair cell death after transient cochlear ischemia through paracrine effects. Neuroscience 145, 923-930.
169. Yu Y., Weber T., Yamashita T., Liu Z., Valentine M.B., Cox B.C. and Zuo J. (2010). In vivo proliferation of postmitotic cochlear supporting cells by acute ablation of the retinoblastoma protein in neonatal mice. J. Neurosci. 30, 5927-5936.
170. Zhai S., Shi L., Wang B.E., Zheng G., Song W., Hu Y. and Gao W.Q. (2005). Isolation and culture of hair cell progenitors from postnatal rat cochleae. J. Neurobiol. 65, 282-293.
171. Zheng J.L. and Gao W.Q. (2000). Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat. Neurosci. 3, 580-586.
172. Zheng J.L., Shou J., Guillemot F., Kageyama R. and Gao W.Q. (2000). Hes1 is a negative regulator of inner ear hair cell differentiation. Development 127, 4551-4560.
173. Zine A., Van De Water T.R. and de Ribaupierre F. (2000). Notch signaling regulates the pattern of auditory hair cell differentiation in mammals. Development 127, 3373-3383.