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Microarrays  2013 

The Transcriptomics to Proteomics of Hair Cell Regeneration: Looking for a Hair Cell in a Haystack

DOI: 10.3390/microarrays2030186

Keywords: hair cell, regeneration, gene expression, microarray, transcriptomics, proteomics, microRNA, growth factors, inner ear

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Abstract:

Mature mammals exhibit very limited capacity for regeneration of auditory hair cells, while all non-mammalian vertebrates examined can regenerate them. In an effort to find therapeutic targets for deafness and balance disorders, scientists have examined gene expression patterns in auditory tissues under different developmental and experimental conditions. Microarray technology has allowed the large-scale study of gene expression profiles (transcriptomics) at whole-genome levels, but since mRNA expression does not necessarily correlate with protein expression, other methods, such as microRNA analysis and proteomics, are needed to better understand the process of hair cell regeneration. These technologies and some of the results of them are discussed in this review. Although there is a considerable amount of variability found between studies owing to different species, tissues and treatments, there is some concordance between cellular pathways important for hair cell regeneration. Since gene expression and proteomics data is now commonly submitted to centralized online databases, meta-analyses of these data may provide a better picture of pathways that are common to the process of hair cell regeneration and lead to potential therapeutics. Indeed, some of the proteins found to be regulated in the inner ear of animal models (e.g., IGF-1) have now gone through human clinical trials.

References

[1]  Lim, D.J. Ultrastructural cochlear changes following acoustic hyperstimulation and ototoxicity. Ann. Otol. Rhinol. Laryngol. 1976, 85, 740–751.
[2]  Lindeman, H.H.; Bredberg, G. Scanning electron microscopy of the organ of Corti after intense auditory stimulation: Effects on stereocilia and cuticular surface of hair cells. Arch. Ohren Nasen Kehlkopfheilkd. 1972, 203, 1–15.
[3]  Stockwell, C.W.; Ades, H.W.; Engstr?m, H. Patterns of hair cell damage after intense auditory stimulation. Ann. Otol. Rhinol. Laryngol. 1969, 78, 1144–1168.
[4]  Theopold, H.M. Comparative surface studies of ototoxic effects of various aminoglycoside antibiotics on the organ of Corti in the guinea pig. A scanning electron microscopic study. Acta Otolaryngol. 1977, 84, 57–64, doi:10.3109/00016487709123942.
[5]  Keithley, E.M.; Feldman, M.L. Hair cell counts in an age-graded series of rat cochleas. Hear. Res. 1982, 8, 249–262, doi:10.1016/0378-5955(82)90017-X.
[6]  Lombarte, A.; Yan, H.Y.; Popper, A.N.; Chang, J.S.; Platt, C. Damage and regeneration of the hair cell ciliary bundles in a fish ear following treatment with gentamicin. Hear. Res. 1993, 64, 166–174, doi:10.1016/0378-5955(93)90002-I.
[7]  Harris, J.A.; Cheng, A.G.; Cunningham, L.L.; MacDonald, G.; Raible, D.W.; Rubel, E.W. Neomycin-induced hair cell death and rapid regeneration in the lateral line of zebrafish (Danio rerio). J. Assoc. Res. Otolaryngol. 2003, 4, 219–234, doi:10.1007/s10162-002-3022-x.
[8]  Smith, M.E.; Coffin, A.B.; Miller, D.L.; Popper, A.N. Anatomical and functional recovery of the goldfish (Carassius auratus) ear following noise exposure. J. Exp. Biol. 2006, 209, 4193–4202.
[9]  Schuck, J.B.; Smith, M.E. Cell proliferation follows acoustically-induced hair cell bundle loss in the zebrafish saccule. Hear. Res. 2009, 253, 67–76.
[10]  Jones, J.E.; Corwin, J.T. Regeneration of sensory cells after laser ablation in the lateral line system: Hair cell lineage and macrophage behavior revealed by time-lapse video microscopy. J. Neurosci. 1996, 16, 649–662.
[11]  Taylor, R.R.; Forge, A. Hair cell regeneration in sensory epithelia from the inner ear of a urodele amphibian. J. Comp. Neurol. 2005, 484, 105–120, doi:10.1002/cne.20450.
[12]  Avallone, B.; Porritiello, M.; Esposito, D.; Mutone, R.; Balsamo, G.; Marmo, F. Evidence of hair cell regeneration in the crista ampullaris of the lizard Podarcis sicula. Hear. Res. 2003, 178, 79–88.
[13]  Cotanche, D.A. Regeneration of hair cell stereociliary bundles in the chick cochlea following severe acoustic trauma. Hear. Res. 1987, 30, 181–195, doi:10.1016/0378-5955(87)90135-3.
[14]  Corwin, J.T.; Cotanche, D.A. Regeneration of sensory hair cells after acoustic trauma. Science 1988, 240, 1772–1774.
[15]  Ryals, B.M.; Rubel, E.W. Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 1988, 240, 1774–1776.
[16]  Weisleder, M.E.; Rubel, E.W. Hair cell regeneration after streptomycin toxicity in the avian vestibular epithelium. J. Comp. Neurol. 1993, 331, 97–110, doi:10.1002/cne.903310106.
[17]  Oesterle, E.C.; Stone, J.S. Hair Cell Regeneration: Mechanisms Guiding Cellular Proliferation and Differention. In Hair Cell Regeneration, Repair, and Protection; Salvi, R.J., Popper, A.N., Fay, R.R., Eds.; Springer: New York, NY, USA, 2008; pp. 141–197.
[18]  Stone, L. The development of the lateral line sense organs in the amphibian observed in living and vital-stained preparations. J. Comp. Neurol. 1933, 57, 507–540.
[19]  Stone, L. Further experimental studies of the development of lateral-line sense organs in the amphibians observed in living preparations. J. Comp. Neurol. 1937, 68, 83–115, doi:10.1002/cne.900680105.
[20]  Corwin, J.T. Postembryonic production and aging in inner ear hair cells in sharks. J. Comp. Neurol. 1981, 201, 541–553.
[21]  Corwin, J.T. Postembryonic growth of the macular neglecta auditory detector in the ray, Raja clavata; continued increases in hair cell number, neural convergence, and physiological sensitivity. J. Comp. Neurol. 1983, 217, 345–356, doi:10.1002/cne.902170309.
[22]  Popper, A.N.; Hoxter, B. Growth of a fish ear: Quantitative analysis of hair cell and ganglion cell proliferation. Hear. Res. 1984, 15, 133–142.
[23]  Cruz, R.M.; Lambert, P.R.; Rubel, E.W. Light microscopic evidence of hair cell regeneration after gentamicin toxicity in chick cochlea. Arch. Otolaryngol. Head Neck Surg. 1987, 113, 1058–1062, doi:10.1001/archotol.1987.01860100036017.
[24]  Hawkins, R.D.; Bashiardes, S.; Powder, K.E.; Sajan, S.A.; Bhonagiri, V.; Speck, J.; Warchol, M.E.; Lovett, M. Large scale gene expression profiles of regenerating inner ear sensory epithelia. PLoS One 2007, 2, e525, doi:10.1371/journal.pone.0000525.
[25]  Schuck, J.B.; Sun, H.; Penberthy, W.T.; Cooper, N.G.F.; Li, X.; Smith, M.E. Transcriptomic analysis of the zebrafish inner ear points to growth hormone mediated regeneration following acoustic trauma. BMC Neurosci. 2011, 12, 88, doi:10.1186/1471-2202-12-88.
[26]  Alvarado, D.M.; Hawkins, D.R.; Bashiardes, S.; Veile, R.A.; Ku, Y-C.K.; Powder, K.E.; Spriggs, M.K.; Speck, J.D.; Warchol, M.E.; Lovett, M. An RNA interference-based screen of transcription factor genes identifies pathways necessary for sensory regeneration in the avian inner ear. J. Neurosci. 2011, 31, 4535–4543.
[27]  Hawkins, R.D.; Bashiardes, S.; Helms, C.A.; Hu, L.; Saccone, N.L.; Warchol, M.E.; Lovett, M. Gene expression differences in quiescent versus regenerating hair cells of avian sensory epithelia: Implications for human hearing and balance disorders. Hum. Mol. Genet. 2003, 12, 1261–1272.
[28]  Cristobal, R.; Wackym, P.A.; Cioffi, J.A.; Erbe, C.B.; Roche, J.P.; Popper, P. Assessment of differential gene expression in vestibular epithelia cell types using microarray analysis. Mol. Brain Res. 2005, 133, 19–36, doi:10.1016/j.molbrainres.2004.10.001.
[29]  Hertzano, R.; Elkon, R. High throughput gene expression analysis of the inner ear. Hear. Res. 2012, 288, 77–88, doi:10.1016/j.heares.2012.01.002.
[30]  Thalmann, I. Inner ear proteomics: A fad or hear to stay. Brain Res. 2006, 1091, 103–112.
[31]  Zhou, J.; Thompson, D.K. Microarray technology and applications in environmental microbiology. Adv. Agron. 2004, 82, 183–270.
[32]  Rivolta, M.N.; Holley, M.C. Gene Arrays, Cell Lines, Stem Cells, and Sensory Regeneration in Mammalian Ears. In Hair Cell Regeneration, Repair, and Protection; Salvi, R.J., Popper, A.N., Fay, R.R., Eds.; Springer: New York, NY, USA, 2008; Volume 33, pp. 257–307.
[33]  Goulter, A.B.; Harmer, D.W.; Clark, K.L. Evaluation of low density array technology for quantitative parallel measurement of multiple genes in human tissue. BMC Genomics 2006, 7, 1–10, doi:10.1186/1471-2164-7-1.
[34]  Horan, M.P. Application of serial analysis of gene expression to the study of human genetic disease. Hum. Genet. 2009, 126, 605–614.
[35]  Mardis, E.R. The impact of next-generation sequencing technology on genetics. Trends Genet. 2008, 24, 133–141.
[36]  Liu, L.; Li, Y.; Li, S.; Hu, N.; He, Y.; Pong, R.; Lin, D.; Lu, L.; Law, M. Comparison of next-generation sequencing systems. J. Biomed. Biotechnol. 2012, 2012, doi:10.1155/2012/251364.
[37]  Friedman, L.M.; Avraham, K.B. MicroRNAs and epigenetic regulation in the mammalian ear: Implications for deafness. Mamm. Genome 2009, 20, 581–603.
[38]  Chen, Z.-Y.; Corey, D.P. An inner ear gene expression database. JARO 2001, 3, 140–148, doi:10.1007/s101620020029.
[39]  Chen, Z-Y.; Corey, D.P. Understanding inner ear development with gene expression profiling. J. Neurobiol. 2002, 53, 276–285, doi:10.1002/neu.10125.
[40]  Rivolta, M.N.; Halsall, A.; Johnson, C.M.; Tones, M.A.; Holley, M.C. Transcript profiling of functionally related groups of genes during conditional differentiation of a mammalian cochlear cell line. Genome Res. 2002, 12, 1091–1099, doi:10.1101/gr.225602.
[41]  Sajan, S.A.; Warchol, M.E.; Lovett, M. Towards a systems biology of mouse inner ear organogenesis: Gene expression pathways, patterns and network analysis. Genetics 2007, 177, 631–653, doi:10.1534/genetics.107.078584.
[42]  Smeti, I.; Assou, S.; Savary, E.; Masmoudi, S.; Zine, A. Transcriptomic analysis of the developing and adult cochlear sensory epithelia. PLoS One 2012, 7, e42987, doi:10.1371/journal.pone.0042987.
[43]  McDermott, B.M.; Baucom, J.M.; Hudspeth, A.J. Analysis and functional evaluation of the hair cell transcriptome. Proc. Natl. Acad. Sci. USA 2007, 104, 11820–11825, doi:10.1073/pnas.0704476104.
[44]  Liang, J.; Wang, D.; Renaud, G.; Wolfsberg, T.G.; Wilson, A.F.; Burgess, S.M. The stat3/socs3a pathway: Regulator of hair cell regeneration. J. Neurosci. 2012, 32, 10662–10673.
[45]  Roberson, D.W.; Rubel, E.W. Cell division in the gerbil cochlea after acoustic trauma. Am. J. Otol. 1994, 15, 28–34.
[46]  Sobkowicz, H.M.; August, B.W.; Slapnick, S.M. Cellular interactions as a response to injury in the organ of Corti in culture. Int. J. Dev. Neurosci. 1997, 15, 463–485, doi:10.1016/S0736-5748(96)00104-9.
[47]  Warchol, M.E.; Corwin, J.T. Supporting cells in avian vestibular organs proliferate in serum-free culture. Hear. Res. 1993, 71, 28–36, doi:10.1016/0378-5955(93)90018-V.
[48]  Forge, A.; Li, L.; Corwin, J.T.; Nevill, G. Ultrastructural evidence for hair cell regeneration in the mammalian inner ear. Science 1993, 259, 1616–1619.
[49]  Forge, A.; Nevill, G. Hair cell recovery in the vestibular sensory epithelia of mature guinea pigs. J. Comp. Neurol. 1998, 397, 69–88, doi:10.1002/(SICI)1096-9861(19980720)397:1<69::AID-CNE6>3.0.CO;2-G.
[50]  Zheng, Q.; Rozanas, C.; Thalmann, I.; Chance, M.; Alagramam, K. Inner ear proteomics of mouse models for deafness, a discovery strategy. Brain Res. 2006, 1091, 113–121.
[51]  Glokler, J.; Angenendt, P. Protein and antibody microarray technology. J. Chromatogr. B 2003, 797, 229–240, doi:10.1016/j.jchromb.2003.08.034.
[52]  Kusnezow, W.; Hoheisel, J. Antibody microarrays: Promises and problems. Biotechniques 2002, 33, S14–S23.
[53]  Jamesdaniel, S.; Ding, D.; Kermany, M.; Davidson, B.; Knight, P., III; Salvi, R.; Coling, D.E. Proteomic analysis of the balance between survival and cell death responses in cisplatin-mediated ototoxicity. J. Proteome Res. 2008, 7, 3516–3524.
[54]  Jamesdaniel, S.; Hu, B.; Kermany, M.; Jiang, H.; Ding, D.; Coling, D.; Salvi, R. Noise induced changes in the expression of p38/MAPK signaling proteins in the sensory epithelium of the inner ear. J. Proteomics 2011, 75, 410–424, doi:10.1016/j.jprot.2011.08.007.
[55]  Peng, H.; Liu, M.; Pecka, J.; Beisel, K.; Ding, S.-J. Proteomic analysis of the organ of Corti using nanoscale liquid chromatography coupled with tandem mass spectrometry. Int. J. Mol. Sci. 2012, 13, 8171–8188, doi:10.3390/ijms13078171.
[56]  Shin, J.-B.; Streijger, F.; Beynon, A.; Peters, T.; Gadzala, L.; McMillen, D.; Bystrom, C.; van der Zee, C.E.E.M.; Wallimann, T.; Gillespie, P.G. Hair bundles are specialized for ATP delivery via creatine kinase. Neuron 2007, 53, 371–386.
[57]  Spinelli, K.; Klimek, J.; Wilmarth, P.; Shin, J.-B.; Choi, D.; David, L.; Gillespie, P.G. Distinct energy metabolism of auditory and vestibular sensory epithelia revealed by quantitative mass spectrometry using MS2 intensity. Proc. Natl. Acad. Sci. USA 2012, 109, E268–E277.
[58]  Cho, Y.; Gong, T.-W.L.; St?ver, T.; Lomax, M.I.; Altschuler, R.A. Gene expression profiles of the rat cochlea, cochlear nucleus, and inferior colliculus. JARO 2001, 3, 54–67, doi:10.1088/1464-4258/3/4/359.
[59]  Kil, J.; Warchol, M.E.; Corwin, J.T. Cell death, cell proliferation, and estimates of hair cell life spans in the vestibular organs of chicks. Hear. Res. 1997, 114, 117–126, doi:10.1016/S0378-5955(97)00166-4.
[60]  Stone, J.S.; Oesterle, E.C.; Rubel, E.W. Recent insights into regeneration of auditory and vestibular hair cells. Curr. Opin. Neurol. 1998, 11, 17–24, doi:10.1097/00019052-199802000-00004.
[61]  Goodyear, R.J.; Gates, R.; Lukashkin, A.N.; Richardson, G.P. Hair cell numbers continue to increase in utricular macula of the early posthatch chick. J. Neurocytol. 1999, 28, 851–861, doi:10.1023/A:1007070121751.
[62]  Wilkins, H.R.; Presson, J.C.; Popper, A.N. Proliferation of vertebrate inner ear supporting cells. J. Neurobiol. 1999, 39, 527–535, doi:10.1002/(SICI)1097-4695(19990615)39:4<527::AID-NEU6>3.0.CO;2-K.
[63]  Oesterle, E.C.; Rubel, E.W. Postnatal production of supporting cells in the chick cochlea. Hear. Res. 1993, 66, 213–224, doi:10.1016/0378-5955(93)90141-M.
[64]  Lawoko-Kerali, G.; Rivolta, M.N.; Holley, M. Expression of the transcription factors GATA3 and Pax2 during development of the mammalian inner ear. J. Comp. Neurol. 2002, 442, 378–391, doi:10.1002/cne.10088.
[65]  Sun, H.; Lin, C.-H.; Smith, M.E. Growth hormone promotes hair cell regeneration in the zebrafish (Danio rerio) inner ear following acoustic trauma. PLoS One 2011, 6, e28372, doi:10.1371/journal.pone.0028372.
[66]  Camarero, G.; Avendano, C.; Fernandez-Moreno, C.; Villar, A.; Contreras, J.; de Pablo, F.; Pichel, J.G.; Varela-Nieto, I. Delayed inner ear maturation and neuronal loss in postnatal IGF-1 deficient mice. J. Neurosci. 2001, 21, 7630–7641.
[67]  Reznik, S.I.; Jaramillo, A.; Zhang, L.; Patterson, G.A.; Cooper, J.D.; Monhanakumar, T. Anti-HLA antibody binding to HAL class I molecules induces proliferation of airway epithelial cells: A potential mechanism for brochiolitis obliterans syndrome. J. Thorac. Cariovasc. Surg. 2000, 119, 39–45, doi:10.1016/S0022-5223(00)70215-7.
[68]  Herrington, J.; Carter-Su, C. Signaling pathways activated by the growth hormone receptor. Trends Endocrinol. Metabol. 2001, 12, 252–257, doi:10.1016/S1043-2760(01)00423-4.
[69]  Friedman, R.C.; Farh, K.K.-H.; Burge, C.B.; Bartel, D.P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009, 19, 92–105.
[70]  Bartel, D.P. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004, 116, 281–297, doi:10.1016/S0092-8674(04)00045-5.
[71]  Lewis, M.A.; Quint, E.; Glazier, A.M.; Fuchs, H.; de Angelis, M.H.; Langford, C.; van Dongen, S.; Abreu-Goodger, C.; Piipari, M.; Redshaw, N.; et al. An ENU-induced mutation of miR-96 associated with progressive hearing loss in mice. Nat. Genet. 2009, 41, 614–618, doi:10.1038/ng.369.
[72]  Brennecke, J.; Hipfner, D.R.; Stark, A.; Russell, R.; Cohen, S.M. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 2003, 113, 25–36, doi:10.1016/S0092-8674(03)00231-9.
[73]  Friedman, L.M.; Dror, A.A.; Mor, E.; Tenne, T.; Toren, G.; Satoh, T.; Biesemeier, D.J.; Shomron, N.; Fekete, D.M.; Hornstein, E.; Avraham, K.B. MicroRNAs are essential for development and function of inner ear hair cells in vertebrates. Proc. Natl. Acad. Sci. USA 2009, 106, 7915–7920, doi:10.1073/pnas.0812446106.
[74]  Weinholds, E.; Kloosterman, W.P.; Miska, E.; Alvarez-Saavedra, E.; Berezikov, E.; de Bruijn, E.; Horvitz, H.R.; Kauppinen, S.; Plasterk, R.H.A. MicroRNA expression in zebrafish embryonic development. Science 2005, 309, 310–311, doi:10.1126/science.1114519.
[75]  Lagos-Quintana, M.; Rauhut, R.; Lendeckel, W.; Tuschl, T. Identification of novel genes coding for small expressed RNAs. Science 2001, 294, 853–858, doi:10.1126/science.1064921.
[76]  Lim, L.P.; Lau, N.C.; Weinstein, E.G.; Abdelhakim, A.; Yekta, S.; Rhoades, M.W.; Burge, C.B.; Bartel, D.P. The microRNAs of Caenorhabditis elegans. Gene Dev. 2003, 17, 991–1008, doi:10.1101/gad.1074403.
[77]  Li, H.; Kloosterman, W.; Fekete, D.M. MicroRNA-183 family members regulate sensorineural fates in the inner ear. J. Neurosci. 2010, 30, 3254–3263, doi:10.1523/JNEUROSCI.4948-09.2010.
[78]  Weston, M.D.; Pierce, M.L.; Rocha-Sanchez, S.; Beisel, K.W.; Soukup, G.A. MicroRNA gene expression in the mouse inner ear. Brain Res. 2006, 1111, 95–104.
[79]  Wang, X.-R.; Zhang, X.-M.; Zhen, J.; Zhang, P.-X.; Xu, G.; Jiang, H. MicroRNA expression in the embryonic mouse inner ear. Neuroreport 2010, 21, 611–617, doi:10.1097/WNR.0b013e328338864b.
[80]  Yan, D.; Xing, Y.; Ouyang, X.; Zhu, J.; Chen, Z.-Y.; Lang, H.; Liu, X.Z. Analysis of miR-376 RNA cluster members in the mouse inner ear. Int. J. Exp. Pathol. 2012, 93, 450–457.
[81]  Soukup, G.A.; Fritzsch, B.; Pierce, M.L.; Weston, M.D.; Jahan, I.; McManus, M.T.; Harfe, B.D. Residual microRNA expression dictates the extent of inner ear development in conditional Dicer knockout mice. Dev. Biol. 2009, 328, 328–341, doi:10.1016/j.ydbio.2009.01.037.
[82]  Zhang, Q.; Liu, H.; McGee, J.; Walsh, E.; Soukup, G.; He, D. Identifying microRNAs involved in degeneration of the organ of Corti during age-related hearing loss. PLoS One 2013, 8, e62786, doi:10.1371/journal.pone.0062786.
[83]  Patel, M.; Cai, Q.; Ding, D.; Salvi, R.; Hu, Z.; Hu, B.H. The miR-183/Taok1 target pair is implicated in cochlear responses to acoustic trauma. PLoS One 2013, 8, e58471, doi:10.1371/journal.pone.0058471.
[84]  Frucht, C.; Uduman, M.; Duke, J.; Kleinstein, S.; Santos-Sacchi, J.; Navaratnam, D. Gene expression analysis of forskolin treated basilar papillae identifies microRNA181a as a mediator of proliferation. PLoS One 2010, 5, e11502, doi:10.1371/journal.pone.0011502.
[85]  Frucht, C.; Santos-Sacchi, J.; Navaratnam, D. MicroRNA181a plays a key role in hair cell regeneration in the avian auditory epithelium. Neurosci. Lett. 2011, 493, 44–48, doi:10.1016/j.neulet.2011.02.017.
[86]  Tsonis, P.A.; Call, M.K.; Grogg, M.W.; Sartor, M.A.; Taylor, R.R.; Forge, A.; Fyffe, R.; Goldenberg, R.; Cowper-Sallari, R.; Tomlinson, C.R. MicroRNAs and regeneration: Let-7 members as potential regulators of dedifferentiation in lens and inner ear hair cell regeneration of the adult newt. Biochem. Biophys. Res. Comm. 2007, 362, 940–945, doi:10.1016/j.bbrc.2007.08.077.
[87]  Elkan-Miller, T.; Ulitsky, I.; Hertzano, R.; Rudnicki, A.; Dror, A.; Lenz, D.; Elkon, R.; Irmler, M.; Beckers, J.; Shamir, R.; et al. Integration of transcriptomics, proteomics, and microRNA analyses reveals novel microRNA regulation of targets in the mammalian inner ear. PLoS One 2011, 6, e18195, doi:10.1371/journal.pone.0018195.
[88]  Weston, M.; Pierce, M.; Jensen-Smith, H.; Fritzsch, B.; Rocha-Sanchez, S.; Beisel, K.; Soukup, G. MicroRNA-183 family expression in hair cell development and requirement of microRNAs for hair cell maintenance and survival. Dev. Dynam. 2011, 240, 808–819, doi:10.1002/dvdy.22591.
[89]  Mencia, A.; Modamio-Hoybjor, S.; Reshaw, N.; Morin, M.; Mayo-Merino, F.; Olavarrieta, L.; Aguirre, L.A.; del Castillo, I.; Steel, K.P.; Dalmay, T.; et al. Mutations in the seed region of human miR-96 are responsible for nonsyndromic progressive hearing loss. Nat. Genet. 2009, 41, 609–613, doi:10.1038/ng.355.
[90]  Reinhart, B.J.; Slack, F.J.; Basson, M.; Pasquinelli, A.E.; Bettinger, J.C.; Rougvie, A.E.; Horvitz, H.R.; Ruvkun, G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403, 901–906, doi:10.1038/35002607.
[91]  Solda, G.; Robusto, M.; Primignani, P.; Castorina, P.; Benzoni, E.; Cesarani, A.; Ambrosetti, U.; Asselta, R.; Duga, S. A novel mutation within the MIR96 gene causes non-syndromic inherited hearing loss in an Italian family by altering pre-miRNA processing. Hum. Mol. Genet. 2012, doi:10.1093/hmg/ddr493.
[92]  Kiernan, A.; Pelling, A.; Leung, K.; Tang, A.; Bell, D.; Tease, C.; Lovell-Badge, R.; Steel, K.P.; Cheah, K.S.E. Sox2 is required for sensory organ development in the mammalian inner ear. Nature 2005, 434, 1031–1035, doi:10.1038/nature03487.
[93]  Schwanhausser, B.; Busse, D.; Li, N.; Dittmar, G.; Schuchhardt, J.; Wolf, J.; Chen, W.; Selbach, M. Global quantification of mammalian gene expression control. Nature 2011, 473, 337–342, doi:10.1038/nature10098.
[94]  Uthaiah, R.; Hudspeth, A. Molecular anatomy of the hair cell’s ribbon synapse. J. Neurosci. 2010, 30, 12387–12399, doi:10.1523/JNEUROSCI.1014-10.2010.
[95]  Lee, K.Y.; Nakagawa, T.; Okano, T.; Hori, R.; Ono, K.; Tabata, Y.; Lee, S.H.; Ito, J. Novel therapy for hearing loss: Delivery of insulin-like growth factor 1 to the cochlea using gelatin hydrogel. Otol. Neurotol. 2007, 28, 976–981, doi:10.1097/MAO.0b013e31811f40db.
[96]  Nakagawa, T.; Sakamoto, T.; Hiraumi, H.; Kikkawa, Y.S.; Yamamoto, N.; Hamaguchi, K.; Ono, K.; Yamamoto, M.; Tabata, Y.; Teramukai, S.; et al. Topical insulin-like growth factor 1 treatment using gelatin hydrogels for glucocorticoid-resistant sudden sensorineural hearing loss: A prospective clinical trial. BMC Med. 2010, 8, 76, doi:10.1186/1741-7015-8-76.
[97]  Hayashi, Y.; Yamamoto, N.; Nakagawa, T.; Ito, J. Insulin-like growth factor 1 inhibits hair cell apoptosis and promotes the cell cycle of supporting cells by activating different downstream cascades after pharmacological hair cell injury. Mol. Cell Neurosci. 2013, 56, 29–38, doi:10.1016/j.mcn.2013.03.003.

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