Hair cell regeneration

Current Opinion in Neurobiology

Volumn 18, Issue 4, 2008, Pages 377-382

  Edge, Albert SB ^a,b,c   Chen, Zheng Yi ^a,b,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; GENE TARGETING; HAIR CELL; INNER EAR; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL TRANSDIFFERENTIATION; EAR, INNER; HAIR CELLS, AUDITORY; HUMANS; REGENERATION; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 55249116483     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2008.10.001     Document Type: Review

References (52)

1. Jorgensen J.M., and Mathiesen C. The avian inner ear. Continuous production of hair cells in vestibular sensory organs, but not in the auditory papilla. Naturwissenschaften 75 (1988) 319-320
2. Corwin J.T., and Cotanche D.A. Regeneration of sensory hair cells after acoustic trauma. Science 240 (1988) 1772-1774
3. Ryals B.M., and Rubel E.W. Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240 (1988) 1774-1776
4. Marean G.C., Burt J.M., Beecher M.D., and Rubel E.W. Hair cell regeneration in the European starling (Sturnus vulgaris): recovery of pure-tone detection thresholds. Hear Res 71 (1993) 125-136
5. Adler H.J., and Raphael Y. New hair cells arise from supporting cell conversion in the acoustically damaged chick inner ear. Neurosci Lett 205 (1996) 17-20
6. Stone J.S., and Cotanche D.A. Hair cell regeneration in the avian auditory epithelium. Int J Dev Biol 51 (2007) 633-647
7. Witte M.C., Montcouquiol M., and Corwin J.T. Regeneration in avian hair cell epithelia: identification of intracellular signals required for S-phase entry. Eur J Neurosci 14 (2001) 829-838
8. Li H., Liu H., Sage C., Huang M., Chen Z.Y., and Heller S. Islet-1 expression in the developing chicken inner ear. J Comp Neurol 477 (2004) 1-10
9. Brockes J.P., and Kumar A. Appendage regeneration in adult vertebrates and implications for regenerative medicine. Science 310 (2005) 1919-1923
10. Hu Z., and Corwin J.T. Inner ear hair cells produced in vitro by a mesenchymal-to-epithelial transition. Proc Natl Acad Sci U S A 104 (2007) 16675-16680
11. Ma E.Y., Rubel E.W., and Raible D.W. Notch signaling regulates the extent of hair cell regeneration in the zebrafish lateral line. J Neurosci 28 (2008) 2261-2273. In a detailed study on zebrafish neuromast hair cell regeneration after neomycin induced hair cell death, blockade of the Notch pathway by γ-secretase inhibitor DAPT resulted in an increase in the number of hair cells regenerated. In contrast to the mammalian inner ear, most of the regenerated neuromast hair cells were derived from the proliferation of supporting cells.
12. Hernandez P.P., Olivari F.A., Sarrazin A.F., Sandoval P.C., and Allende M.L. Regeneration in zebrafish lateral line neuromasts: expression of the neural progenitor cell marker sox2 and proliferation-dependent and -independent mechanisms of hair cell renewal. Dev Neurobiol 67 (2007) 637-654
13. Lopez-Schier H., and Hudspeth A.J. A two-step mechanism underlies the planar polarization of regenerating sensory hair cells. Proc Natl Acad Sci U S A 103 (2006) 18615-18620
14. 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., et al. Proliferation of functional hair cells in vivo in the absence of the retinoblastoma protein. Science 307 (2005) 1114-1118. We used a conditional knockout mouse model to demonstrate that Rb1 is required for cell cycle exit of inner ear sensory progenitor cells, and establishment of the postmitotic status of hair cells and supporting cells. We showed that hair cells without Rb1 could undergo differentiation and proliferation concurrently and the mitosis-derived hair cells were functional. This study suggested a strategy to achieve hair cell regeneration by blocking cell cycle inhibitors.
15. Stone J.S., and Rubel E.W. Temporal, spatial, and morphologic features of hair cell regeneration in the avian basilar papilla. J Comp Neurol 417 (2000) 1-16
16. Oshima K., Grimm C.M., Corrales C.E., Senn P., Martinez Monedero R., Geleoc G.S., Edge A., Holt J.R., and Heller S. Differential distribution of stem cells in the auditory and vestibular organs of the inner ear. J Assoc Res Otolaryngol 8 (2007) 18-31. The authors comprehensively quantified stem cells from a range of inner ear tissues throughout development. They showed that all the tissues sampled harbored stem cells that could differentiate into inner ear cell types such as hair cells and ganglion neurons. However, the number of stem cells decreased rapidly in the adult cochlea, in contrast to relatively abundant stem cells in the adult vestibular system. This observation may help to explain the lack of hair cell regeneration in the cochlea compared to the utricle.
17. Li H., Liu H., and Heller S. Pluripotent stem cells from the adult mouse inner ear. Nat Med 9 (2003) 1293-1299
18. Martinez-Monedero R., Yi E., Oshima K., Glowatzki E., and Edge A.S. Differentiation of inner ear stem cells to functional sensory neurons. Dev Neurobiol 68 (2008) 669-684
19. Qyang Y., Martin-Puig S., Chiravuri M., Chen S., Xu H., Bu L., Jiang X., Lin L., Granger A., Moretti A., et al. The renewal and differentiation of Isl1+ cardiovascular progenitors are controlled by a Wnt/beta-catenin pathway. Cell Stem Cell 1 (2007) 165-179
20. Lamba D., Karl M., and Reh T. Neural regeneration and cell replacement: a view from the eye. Cell Stem Cell 2 (2008) 538-549
21. 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. Math1: an essential gene for the generation of inner ear hair cells. Science 284 (1999) 1837-1841
22. Gubbels S.P., Woessner D.W., Mitchell J.C., Ricci A.J., and Brigande J.V. Functional auditory hair cells produced in the mammalian cochlea by in utero gene transfer. Nature 455 (2008) 537-541
23. Izumikawa M., Minoda R., Kawamoto K., Abrashkin K.A., Swiderski D.L., Dolan D.F., Brough D.E., and Raphael Y. Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat Med 11 (2005) 271-276. The authors overexpressed Atoh1 in deafened guinea pigs and observed the production of new hair cells as a consequence of the transdifferentiation of supporting cells to hair cells. Limited improvement in auditory thresholds was also observed in the ears overexpressing Atoh1.
24. Kelley M.W. Regulation of cell fate in the sensory epithelia of the inner ear. Nat Rev Neurosci 7 (2006) 837-849
25. Zheng J.L., and Gao W.Q. Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat Neurosci 3 (2000) 580-586
26. Lanford P.J., Lan Y., Jiang R., Lindsell C., Weinmaster G., Gridley T., and Kelley M.W. Notch signalling pathway mediates hair cell development in mammalian cochlea. Nat Genet 21 (1999) 289-292
27. Zine A., Aubert A., Qiu J., Therianos S., Guillemot F., Kageyama R., and de Ribaupierre F. Hes1 and Hes5 activities are required for the normal development of the hair cells in the mammalian inner ear. J Neurosci 21 (2001) 4712-4720
28. Kiernan A.E., Cordes R., Kopan R., Gossler A., and Gridley T. The Notch ligands DLL1 and JAG2 act synergistically to regulate hair cell development in the mammalian inner ear. Development 132 (2005) 4353-4362
29. Yamamoto N., Tanigaki K., Tsuji M., Yabe D., Ito J., and Honjo T. Inhibition of Notch/RBP-J signaling induces hair cell formation in neonate mouse cochleas. J Mol Med 84 (2006) 37-45
30. Jeon S.J., Fujioka M., and Edge A.S. Inhibition of Notch signaling increases differentiation of stem cells to hair cells through upregulation of Math1. Association for Research in Otolaryngology Thirty-First Midwinter Meeting (2008) Abstract 570
31. Li H., Corrales C.E., Wang Z., Zhao Y., Wang Y., Liu H., and Heller S. BMP4 signaling is involved in the generation of inner ear sensory epithelia. BMC Dev Biol 5 (2005) 16
32. Pujades C., Kamaid A., Alsina B., and Giraldez F. BMP-signaling regulates the generation of hair-cells. Dev Biol 292 (2006) 55-67
33. Driver E.C., Pryor S.P., Hill P., Turner J., Ruther U., Biesecker L.G., Griffith A.J., and Kelley M.W. Hedgehog signaling regulates sensory cell formation and auditory function in mice and humans. J Neurosci 28 (2008) 7350-7358
34. Stevens C.B., Davies A.L., Battista S., Lewis J.H., and Fekete D.M. Forced activation of Wnt signaling alters morphogenesis and sensory organ identity in the chicken inner ear. Dev Biol 261 (2003) 149-164
35. Chen P., and Segil N. p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126 (1999) 1581-1590
36. Mantela J., Jiang Z., Ylikoski J., Fritzsch B., Zacksenhaus E., and Pirvola U. The retinoblastoma gene pathway regulates the postmitotic state of hair cells of the mouse inner ear. Development 132 (2005) 2377-2388
37. Sage C., Huang M., Vollrath M.A., Brown M.C., Hinds P.W., Corey D.P., Vetter D.E., and Chen Z.Y. Essential role of retinoblastoma protein in mammalian hair cell development and hearing. Proc Natl Acad Sci U S A 103 (2006) 7345-7350
38. Forge A., Li L., Corwin J.T., and Nevill G. Ultrastructural evidence for hair cell regeneration in the mammalian inner ear. Science 259 (1993) 1616-1619
39. Warchol M.E., Lambert P.R., Goldstein B.J., Forge A., and Corwin J.T. Regenerative proliferation in inner ear sensory epithelia from adult guinea pigs and humans. Science 259 (1993) 1619-1622
40. White P.M., Doetzlhofer A., Lee Y.S., Groves A.K., and Segil N. Mammalian cochlear supporting cells can divide and trans-differentiate into hair cells. Nature 441 (2006) 984-987. The authors used a p27kip1 promoter-driven GFP transgenic mouse model and showed that purified early postnatal cochlear supporting cells have the potential to re-enter the cell cycle and differentiate into hair cells in vitro. However, this capacity was rapidly lost postnatally. Deletion of p27kip1 led to enhanced proliferation in early postnatal supporting cells.
41. Hume C.R., Bratt D.L., and Oesterle E.C. Expression of LHX3 and SOX2 during mouse inner ear development. Gene Expr Patterns 7 (2007) 798-807
42. Lopez I.A., Zhao P.M., Yamaguchi M., de Vellis J., and Espinosa-Jeffrey A. Stem/progenitor cells in the postnatal inner ear of the GFP-nestin transgenic mouse. Int J Dev Neurosci 22 (2004) 205-213
43. Sakaguchi H., Yaoi T., Suzuki T., Okano H., Hisa Y., and Fushiki S. Spatiotemporal patterns of Musashi1 expression during inner ear development. Neuroreport 15 (2004) 997-1001
44. Stone J.S., Shang J.L., and Tomarev S. cProx1 immunoreactivity distinguishes progenitor cells and predicts hair cell fate during avian hair cell regeneration. Dev Dyn 230 (2004) 597-614
45. Li H., Roblin G., Liu H., and Heller S. Generation of hair cells by stepwise differentiation of embryonic stem cells. Proc Natl Acad Sci U S A 100 (2003) 13495-13500
46. Coleman B., Fallon J.B., Pettingill L.N., de Silva M.G., and Shepherd R.K. Auditory hair cell explant co-cultures promote the differentiation of stem cells into bipolar neurons. Exp Cell Res 313 (2007) 232-243
47. Corrales C.E., Pan L., Li H., Liberman M.C., Heller S., and 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 66 (2006) 1489-1500
48. Shi F., Corrales C.E., Liberman M.C., and Edge A.S. BMP4 induction of sensory neurons from human embryonic stem cells and reinnervation of sensory epithelium. Eur J Neurosci 26 (2007) 3016-3023
49. Jeon S.J., Oshima K., Heller S., and Edge A.S. Bone marrow mesenchymal stem cells are progenitors in vitro for inner ear hair cells. Mol Cell Neurosci 34 (2007) 59-68
50. Doyle K.L., Kazda A., Hort Y., McKay S.M., and Oleskevich S. Differentiation of adult mouse olfactory precursor cells into hair cells in vitro. Stem Cells 25 (2007) 621-627
51. MacLaren R.E., Pearson R.A., MacNeil A., Douglas R.H., Salt T.E., Akimoto M., Swaroop A., Sowden J.C., and Ali R.R. Retinal repair by transplantation of photoreceptor precursors. Nature 444 (2006) 203-207
52. Hanna J., Markoulaki S., Schorderet P., Carey B.W., Beard C., Wernig M., Creyghton M.P., Steine E.J., Cassady J.P., Foreman R., et al. Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell 133 (2008) 250-264