Regeneration of Auditory Hair Cells: A Potential Treatment for Hearing Loss on the Horizon
DOI:
https://doi.org/10.29105/ingenierias23.87-2Keywords:
Cochlea, Organ of Corti, regeneration, hair cellsAbstract
Hearing requires good health of the hair cells to ensure that the sound is detected and processed correctly. They degenerate and die due to age or exposition to high intensity sound, among other causes, and usually they do not regenerate. Some research results about possible regeneration of cochlear hair cells that suggest the possibility of treatment for hearing impairment due to this disease are presented in this paper..
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Bredberg, G. (1967). The human cochlea during development and ageing. Journal of Laryngology and Otology 81, 739–758.
McLean,W.J.,Smith,K.A.,Glowatzki,E.,andPyott,S.J.(2009).Distribution of the Na,K-ATPase a subunit in the rat spiral ganglion and organ of Corti. Journal of the Association for Research in Otolaryngology 10, 37–49.
Warchol, M.E. (2011) . Sensory Regeneration in the vertebrate inner ear: Differences at the levels of cells and species. Hearing Research 273, 72 – 79.
GrovesA.K.,Zhang,K.D.,andFekete,D.M.(2013).Thegeneticsofhaircell development and regeneration. Annual Review of Neuroscience 36, 361-381.
Rubel, E. W, Furrer, S. A., and Stone, J. S. (2013). A brief history of hair cell regeneration research and speculations on the future. Hearing Research 297, 42–51.
Cotanche,D.A.(1987).Regenerationofhaircellstereociliarybundlesinthechick cochlea following severe acoustic trauma. Hearing Research 30, 181–195.
Cruz, R. M., Lambert, P. R., and Rubel, E.W, (1987). Light microscopic evidence of hair cell regeneration after gentamicin toxicity in chick cochlea. Archives of Otolaryngology—Head & Neck Surgery 113, 1058–1062.
Jørgensen, J. M., and Mathiesen, C. (1988). The avian inner ear. Continuous production of hair cells in vestibular sensory organs, but not in the auditory papilla. Naturwissenscha_en 75, 319–320.
Corwin, J. T., and Cotanche, D. A. (1988). Regeneration of sensory hair cells after acoustic trauma. Science 240, 1772–1774.
Ryals, B. M., and Rubel, E. E. (1988). Hail cell regeneration after acustic trauma in adult Coturnix quail. Science 240, 1774 – 1776.
Roberson, D. W., Kreig, S., and Rubel, E. W. (1996). Light microscopic evidence that direct transdi_erentation gives rise to new hair cells in regenerating avian auditory epithelium. Auditory Neuroscience 2, 195– 205.
Roberson, D. W., and Rubel, E. W. (1994). Cell division in the gerbil cochlea after acoustic trauma. American Journal of Otolaryngology 15, 28–34.
Chardin, S., and Romand, R. (1995). Regeneration and mammalian auditorym hair cells. Science 267, 707–711.
Forge, A., Li, L., and Nevill, G. (1998). Hair cell recovery in the vestibular sensory epithelia of mature guinea pigs. Journal of Comparative Neurology 397, 69–88.
Kawamoto, K., Izumikawa, M., Beyer, L. A., Atkin, G. M., and Raphael, Y. (2009). Spontaneous hair cell regeneration in the mouse utricle following gentamicin ototoxicity. Hearing Research 247, 17–26.
Golub, J. S., Tong, L., Ngyuen, T. B., Hume, C. R., Palmiter, R. D., Rubel, E. W, and Stone, J. S. (2012). Hair cell replacement in adult mouse utricles a_er targeted ablation of hair cells with diphtheria toxin. Journal of Neuroscience 32, 15093–15105.
Li, L., and Forge, A. (1997). Morphological evidence for supporting cell to hair cell conversion in the mammalian utricular macula. International Journal of Developmental Neuroscience 15, 433–446.
Kuntz, A. L., and Oesterle, E. C. (1998). Transforming growth factor a with insulin stimulates cell proliferation in vivo in adult rat vestibular sensory epithelium. Journal of Comparative Neurology 399, 413-423.
Oesterle, E. C., Cunningham, D. E., Westrum, L. E., and Rubel, E. W. (2003). Ultrastructural analysis of [3H]thymidine-labeled cells in the rat utricular macula. Journal of Comparative Neurology 463, 177–195.
Oshima, K., Grimm, C. M., Corrales, C. E., Senn, P., Martinez Monedero, R., Géléoc, G. S. G., Edge, A., Holt, J. R., and Heller, S. (2007). Differential distribution of stem cells in the auditory and vestibular organs of the innerear. Journal of the Association for Research in Otolaryngology 8, 18–31.
White, P. M., Doetzlhofer, A., Lee, Y. S., Groves, A. K., and Segil, N. (2006). Mammalian cochlear supporting cells can divide and trans- differentiate into hair cells. Nature 441, 984 – 987.
Cox, B. C., Chai R., Lenoir A., Liu Z., Zhang L., Nguyen D. H., Chalasani K., Steigelman K. A., Fang, J., Rubel, E.W, Cheng A. G., and Zuo, J. (2014). Spontaneous hair cell regeneration in the neonatal mouse cochlea in vivo. Development 141, 816-829.
Cai, T., Jen, H.-I., Kang, H., Klisch, T. J., Zoghbi, H. Y., and Groves, A. K. (2015). Characterization of the transcriptome of nascent hair cells and identification of direct targets of the Atoh1 transcription factor. Journal of Neuroscience 35, 5870–5883.
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.
Cafaro, J., Lee, G. S., and Stone, J. S. (2007). Atoh1 expression defines activated progenitors and differentiating hair cells during avian hair cell regeneration. Developmental Dynamics 236, 156–170.
Wang, G.-P., Chatterjee, I., Batts, S. A., Wong, H. T., Gong, T.-W., Gong, S.-S., and Raphael, Y. (2010). Notchsignaling and Atoh 1 expression during hair cell regeneration in the mouse utricle. Hearing Research 267, 61 – 70.
Lin, V., Golub, J. S., Nguyen, T. B., Hume, C. R., Oesterle, E. C., and Stone, J. S. (2011). Inhibition of Notch activity promotes nonmitotic regeneration of hair cells in the adult mouse utricles. Journal of Neuroscience 31, 15329–15339.
Lewis, R. M., Hume, C. R., and Stone, J. S. (2012). Atoh1 expression and function during auditory hair cell regeneration in post-hatch chickens. Hearing Research 289, 74-85.
Zheng, J. L., and Gao, W. Q. (2000). Overexpression of Math 1 induces robust production of extra hair cells in postnatal rat inner ears. Nature Neuroscience 3, 580 – 586.
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.
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. Nature Medicine 11, 271–276.
Schlecker, C., Praetorius, M., Brough, D. E., Presler, R. G., Hsu, C., Plinkert, P. K., and Staecker, H. (2011). Selective atonal gene delivery improves balance function in a mouse model of vestibular disease. Gene Therapy 18, 884 – 890.
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. Journal of Neuroscience 32, 6600–6610.
Atkinson, P. J., Huarcaya Najarro, E., Sayyid, Z. N., and Cheng, A. G. (2015). Sensory hair cell development and regeneration: Similarities and differences. Development 142, 1561–1571.
Lewis, J. (1998). Notch signalling and the control of cell fate choices in vertebrates. Seminars in Cell and Developmental Biology 9, 583-589.
Kelley, M. W. (2006). Regulation of cell fate in the sensory epithelia of the inner ear. Nature Reviews Neuroscience 7, 837–849.
Lanford, P. J., Shailam, R., Norton, C. R., Gridley, T., and Kelley, M. W. (2000). Expression of Math1 and HES5 in the cochleae of wildtype and Jag2 mutant mice. Journal of the Association for Research in Otolaryngology 1, 161–171.
Hayashi, T., Kokubo, H., Hartman B. H., Ray, C. A., Reh, T. A., Bermingham- McDonogh, O. (2008). Hesr1 and Hesr2 may act as early effectors of Notch signaling in the developing cochlea. Developmental Biology 316, 87-99.
Doetzlhofer, A., Basch, M. L., Ohyama, T., Gessler, M., Groves, A. K., and Segil, N. (2009). Hey2 regulation by FGF provides a Notch-independent mechanism for maintaining pillar cell fate in the organ of Corti. Developmental Cell 16, 58–69.
Ma, E. Y., Rubel, E. W, and Raible, D. W. (2008). Notch signaling regulates the extent of hair cell regeneration in the zebrafish lateral line. Journal of Neuroscience 28, 2261–2273.
Daudet, N., Gibson, R., Shang, J., Bernard, A., Lewis, J., and Stone, J. (2009). Notch regulation of progenitor cell behavior in quiescent and regenerating auditory epithelium of mature birds. Developmental Biology 326, 86–100.
Mizutari, K., Fujioka, M., Hosoya, M., Bramhall, N., Okano, H. J., Okano, H., and Edge, A. S. B. (2013). Notch inhibition induces cochlear hair cell regeneration and recovery of hearing after acoustic trauma. Neuron 77, 58–69.
Maass, J. C., Gu, R., Basch, M. L., Waldhaus, J., Lopez, E. M., Xia, A., Oghalai, J. S., Heller, S., and Groves, A. K. (2015). Changes in the regulation of the Notch signaling pathway are temporally correlated with regenerative failure in the mouse cochlea. Frontiers in Cellular Neuroscience 9, 110.
Chen, P., and Segil, N. (1999). p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126, 1581–1590.
Löwenheim, H., Furness, D.N., Kil, J., Zinn, C., Gültig, K., Fero, M. L., Frost, D., Gummer, A. W., Roberts, J. M., Rubel, E.W, Hackney, C. M., and_ Zenner, H.-P. (1999). Gene disruption of p27Kip1 allows cell proliferation in the postnatal and adult organ of Corti. Proceedings of the National Academy of Sciences of the United States of America 96, 4084–4088.
Oesterle, E. C., Chien, W.-M., Campbell, S., Nellimarla, P., and Fero, M. L. (2011). p27Kip1 is required to maintain proliferative quiescence in the adult cochlea and pituitary. Cell Cycle 10, 1237–1248.
Jansson, L., Kim, G. S., and Cheng, A. G. (2015). Making sense of Wnt signaling- linking hair cell regeneration to development. Frontiers in Cellular Neuroscience 9, 66.
Shi, F., Hu, L., Jacques, B. E., Mulvaney, J. F., Dabdoub, A., and Edge, A.S. B. (2014). –Catenin is required for hair-cell differentiation in the cochlea. Journal of Neuroscience 34, 6470 – 6479.
Chai, R., Kuo, B., Wang, T., Liaw, E. J., Xia, A., Jan, T. A., Liu, Z., Taketo, M. M., Oghalai, J. S., Nusse, R., Zuo, J, and_Cheng, A. G. (2012). Wnt signaling induces proliferation of sensory precursors in the postnatal mouse cochlea. Proceedings of the National Academy of Sciences of the United States of America 109, 8167-8172
Shi, F., Hu, L., and Edge, A. S. B. (2013). Generation of hair cells in neonatal mice by –catenin overexpression in Lgr5-positive cochlear progenitors. Proceedings ok the National Academy of Sciences of the United States of America 110, 13851 – 13856.
Head, J. R., Gacioch, L., Pennisi, M., and Meyers, J. R. (2013). Activation of canonical Wnt/-catenin signaling stimulates proliferation in neuromasts in the zebrafish posterior lateral line. Developmental Dynamics 242, 832–846.
Jacques, B. E., Montgomery, W. H., Uribe, P. M., Yatteau, A., Asuncion, J. D., Resendiz, G., Matsui, J. I., and Dabdoub, A. (2014). The role of Wnt/- catenin signaling in proliferation and regeneration of the developing basilar papilla and lateral line. Developmental Neurobiology 74, 438–456.
White, P. M., Stone, J. S., Groves, A. K., and Segil, N. (2012). EGFR signaling is required for regenerative proliferation in the cochlea: conservation in birds and mammals. Developmental Biology 363, 191 – 200.
Lefebvre, P. P., Malgrange, B., _iry, M., Van De Water, T.R., and Moonen, G. (2000). Epidermal growth factor upregulates production of supernumerary hair cells in neonatal rat organ of corti explants. Acta Oto-laryngologica 120, 142–145.
Hume C. R., Kirkegaard M., Oesterle E. C. (2003). ErbB expression: The mouse inner ear and maturation of the mitogenic response to heregulin. Journal of the Association for Research in Otolaryngology 4(3), 422-443.
Zhao, L.-D., Guo, W.-W., Lin, C., Li, L.X-., Sun, J.-H., Wu, N., Ren, L.-L., Li, X.-X., Liu, H.-Z., Young, W.-Y., Gao, W. Q., and Yang, S. M. (2011). Effects of DAPT and Atoh 1 overexpression on hair cell production and hair bundle orientation in cultured Organ of Corti from neonatal rats. PLos One 6, e23729.
Kuo, B. R., Baldwin, E. M., Layman, W. S., Taketo, M. M., and Zuo, J. (2015). In vivo cochlear hair cell generation and survival by coactivation of -catenin and Atoh1. Journal of Neuroscience 35, 10786–10798.
Li, H., Roblin, G., Liu, H., and Heller, S. (2003). Generation of hair cells by stepwise differentiation of embryonic stem cells. Proceedings of the National Academy of Sciences 100, 13495–13500.
Fujino, K., Kim, T.-S., Nishida, A. T., Nakagawa, T., Omori, K., Naito, Y., and Ito, J. (2004). Transplantation of neural stem cells into explants of rat inner ear. Acta Oto-Laryngologica Supplementum 124(551), 31–33.
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.
Ronaghi, M., Nasr, M., Ealy, M., Durruthy-Durruthy, R., Waldhaus, J., Diaz, G. H., Joubert, L.-M., Oshima, K., and Heller, S. (2014). Inner ear hair cell like cells from human embryonic stem cells. Stem Cells and Development 23, 1275 – 1284.
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 Transplantation 15, 369–380.
Hildebrand, M. S., Dahl, H.-H.M., 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. Journal of the Association for Research in Otolaryngology 6, 341–354.
Parker, M. A., Corliss, D. A., Gray, B., Anderson, J. K., Bobbin, R. P., Snyder, E. Y., Cotanche, D. A. (2007). Neural stem cells injected into the sounddamaged cochlea migrate throughout the cochlea and express markers of hair cells, supporting cells, and spiral ganglion cells. Hearing Research 232, 29-43.