1932

Abstract

Deafness or hearing deficits are debilitating conditions. They are often caused by loss of sensory hair cells or defects in their function. In contrast to mammals, nonmammalian vertebrates robustly regenerate hair cells after injury. Studying the molecular and cellular basis of nonmammalian vertebrate hair cell regeneration provides valuable insights into developing cures for human deafness. In this review, we discuss the current literature on hair cell regeneration in the context of other models for sensory cell regeneration, such as the retina and the olfactory epithelium. This comparison reveals commonalities with, as well as differences between, the different regenerating systems, which begin to define a cellular and molecular blueprint of regeneration. In addition, we propose how new technical advances can address outstanding questions in the field.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100818-125503
2019-10-06
2024-06-24
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/35/1/annurev-cellbio-100818-125503.html?itemId=/content/journals/10.1146/annurev-cellbio-100818-125503&mimeType=html&fmt=ahah

Literature Cited

  1. Abdolazimi Y, Stojanova Z, Segil N 2016. Selection of cell fate in the organ of Corti involves the integration of Hes/Hey signaling at the Atoh1 promoter. Development 143:841–50
    [Google Scholar]
  2. Ahlgren U, Pfaff SL, Jessell TM, Edlund T, Edlund H 1997. Independent requirement for ISL1 in formation of pancreatic mesenchyme and islet cells. Nature 385:257–60
    [Google Scholar]
  3. Alunni A, Krecsmarik M, Bosco A, Galant S, Pan L et al. 2013. Notch3 signaling gates cell cycle entry and limits neural stem cell amplification in the adult pallium. Development 140:3335–47
    [Google Scholar]
  4. Alvarado DM, Hawkins RD, Bashiardes S, Veile RA, Ku YC et al. 2011. An RNA interference–based screen of transcription factor genes identifies pathways necessary for sensory regeneration in the avian inner ear. J. Neurosci. 31:4535–43
    [Google Scholar]
  5. Andrawes MB, Xu X, Liu H, Ficarro SB, Marto JA et al. 2013. Intrinsic selectivity of Notch 1 for Delta-like 4 over Delta-like 1. J. Biol. Chem. 288:25477–89
    [Google Scholar]
  6. Bermingham NA, Hassan BA, Price SD, Vollrath MA, Ben-Arie N et al. 1999. Math1: an essential gene for the generation of inner ear hair cells. Science 284:1837–41
    [Google Scholar]
  7. Bhave SA, Oesterle EC, Coltrera MD 1998. Macrophage and microglia-like cells in the avian inner ear. J. Comp. Neurol. 398:241–56
    [Google Scholar]
  8. Brann JH, Firestein SJ. 2014. A lifetime of neurogenesis in the olfactory system. Front. Neurosci. 8:182
    [Google Scholar]
  9. Briegel K, Lim KC, Plank C, Beug H, Engel JD, Zenke M 1993. Ectopic expression of a conditional GATA-2/estrogen receptor chimera arrests erythroid differentiation in a hormone-dependent manner. Genes Dev 7:1097–109
    [Google Scholar]
  10. Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ 2013. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10:1213
    [Google Scholar]
  11. Burns JC, Cox BC, Thiede BR, Zuo J, Corwin JT 2012. In vivo proliferative regeneration of balance hair cells in newborn mice. J. Neurosci. 32:6570–77
    [Google Scholar]
  12. Caggiano M, Kauer JS, Hunter DD 1994. Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using a replication-incompetent retrovirus. Neuron 13:339–52
    [Google Scholar]
  13. Cai C-L, Liang X, Shi Y, Chu P-H, Pfaff SL et al. 2003. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell 5:877–89
    [Google Scholar]
  14. Carrillo SA, Anguita-Salinas C, Peña OA, Morales RA, Muñoz-Sánchez S et al. 2016. Macrophage recruitment contributes to regeneration of mechanosensory hair cells in the zebrafish lateral line. J. Cell. Biochem. 117:1880–89
    [Google Scholar]
  15. Carson C, Murdoch B, Roskams AJ 2006. Notch 2 and Notch 1/3 segregate to neuronal and glial lineages of the developing olfactory epithelium. Dev. Dyn. 235:1678–88
    [Google Scholar]
  16. Cau E, Casarosa S, Guillemot F 2002. Mash1 and Ngn1 control distinct steps of determination and differentiation in the olfactory sensory neuron lineage. Development 129:1871–80
    [Google Scholar]
  17. Chakrabarti R, Celià-Terrassa T, Kumar S, Hang X, Wei Y et al. 2018. Notch ligand Dll1 mediates cross-talk between mammary stem cells and the macrophageal niche. Science 360:eaan4153
    [Google Scholar]
  18. Clerici WJ, Hensley K, DiMartino DL, Butterfield DA 1996. Direct detection of ototoxicant-induced reactive oxygen species generation in cochlear explants. Hearing Res 98:116–24
    [Google Scholar]
  19. Conner C, Ackerman KM, Lahne M, Hobgood JS, Hyde DR 2014. Repressing notch signaling and expressing TNFα are sufficient to mimic retinal regeneration by inducing Müller glial proliferation to generate committed progenitor cells. J. Neurosci. 34:14403–19
    [Google Scholar]
  20. Corwin JT. 1981. Postembryonic production and aging of inner ear hair cells in sharks. J. Comp. Neurol. 201:541–53
    [Google Scholar]
  21. Corwin JT, Cotanche DA. 1988. Regeneration of sensory hair cells after acoustic trauma. Science 240:1772–74
    [Google Scholar]
  22. Corwin JT, Warchol ME. 1991. Auditory hair cells: structure, function, development, and regeneration. Annu. Rev. Neurosci. 14:301–33
    [Google Scholar]
  23. Costa A, Sanchez-Guardado L, Juniat S, Gale JE, Daudet N, Henrique D 2015. Generation of sensory hair cells by genetic programming with a combination of transcription factors. Development 142:1948–59
    [Google Scholar]
  24. Cox BC, Chai R, Lenoir A, Liu Z, Zhang L et al. 2014. Spontaneous hair cell regeneration in the neonatal mouse cochlea in vivo. Development 141:816–29
    [Google Scholar]
  25. Cruz IA, Kappedal R, Mackenzie SM, Hailey DW, Hoffman TL et al. 2015. Robust regeneration of adult zebrafish lateral line hair cells reflects continued precursor pool maintenance. Dev. Biol. 402:229–38
    [Google Scholar]
  26. Dorfman DM, Wilson DB, Bruns GA, Orkin SH 1992. Human transcription factor GATA-2: evidence for regulation of preproendothelin-1 gene expression in endothelial cells. J. Biol. Chem. 267:1279–85
    [Google Scholar]
  27. Elsaeidi F, Macpherson P, Mills EA, Jui J, Flannery JG, Goldman D 2018. Notch suppression collaborates with Ascl1 and Lin28 to unleash a regenerative response in fish retina, but not in mice. J. Neurosci. 38:2246–61
    [Google Scholar]
  28. Eming SA, Wynn TA, Martin P 2017. Inflammation and metabolism in tissue repair and regeneration. Science 356:1026–30
    [Google Scholar]
  29. Escobedo N, Oliver G. 2016. Lymphangiogenesis: origin, specification, and cell fate determination. Annu. Rev. Cell Dev. Biol. 32:677–91
    [Google Scholar]
  30. Fausett BV, Goldman D. 2006. A role for α1 tubulin–expressing Müller glia in regeneration of the injured zebrafish retina. J. Neurosci. 26:6303–13
    [Google Scholar]
  31. Fischer AJ, Reh TA. 2000. Identification of a proliferating marginal zone of retinal progenitors in postnatal chickens. Dev. Biol. 220:197–210
    [Google Scholar]
  32. Fletcher RB, Das D, Gadye L, Street KN, Baudhuin A et al. 2017. Deconstructing olfactory stem cell trajectories at single-cell resolution. Cell Stem Cell 20:817–30.e8
    [Google Scholar]
  33. Fogarty CE, Diwanji N, Lindblad JL, Tare M, Amcheslavsky A et al. 2016. Extracellular reactive oxygen species drive apoptosis-induced proliferation via Drosophila macrophages. Curr. Biol. 26:575–84
    [Google Scholar]
  34. Forge A, Li L, Corwin J, Nevill G 1993. Ultrastructural evidence for hair cell regeneration in the mammalian inner ear. Science 259:1616–19
    [Google Scholar]
  35. Fryer CJ, White JB, Jones KA 2004. Mastermind recruits CycC:CDK8 to phosphorylate the Notch ICD and coordinate activation with turnover. Mol. Cell 16:509–20
    [Google Scholar]
  36. Gadye L, Das D, Sanchez MA, Street K, Baudhuin A et al. 2017. Injury activates transient olfactory stem cell states with diverse lineage capacities. Cell Stem Cell 21:775–90.e9
    [Google Scholar]
  37. Gemberling M, Bailey TJ, Hyde DR, Poss KD 2013. The zebrafish as a model for complex tissue regeneration. Trends Genet 29:611–20
    [Google Scholar]
  38. Geng R, Noda T, Mulvaney JF, Lin VYW, Edge ASB, Dabdoub A 2016. Comprehensive expression of Wnt signaling pathway genes during development and maturation of the mouse cochlea. PLOS ONE 11:e0148339
    [Google Scholar]
  39. Godwin JW, Pinto AR, Rosenthal NA 2013. Macrophages are required for adult salamander limb regeneration. PNAS 110:9415–20
    [Google Scholar]
  40. Gokoffski KK, Wu HH, Beites CL, Kim J, Kim EJ et al. 2011. Activin and GDF11 collaborate in feedback control of neuroepithelial stem cell proliferation and fate. Development 138:4131–42
    [Google Scholar]
  41. Graziadei PPC, Graziadei GAM. 1979. Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J. Neurocytol. 8:1–18
    [Google Scholar]
  42. Harris RE, Setiawan L, Saul J, Hariharan IK 2016. Localized epigenetic silencing of a damage-activated WNT enhancer limits regeneration in mature Drosophila imaginal discs. eLife 5:e11588
    [Google Scholar]
  43. Hatakeyama J, Kageyama R. 2004. Retinal cell fate determination and bHLH factors. Semin. Cell Dev. Biol. 15:83–89
    [Google Scholar]
  44. Heinz S, Romanoski CE, Benner C, Glass CK 2015. The selection and function of cell type–specific enhancers. Nat. Rev. Mol. Cell Biol. 16:144–54
    [Google Scholar]
  45. Henderson D, McFadden SL, Liu CC, Hight N, Zheng XY 1999. The role of antioxidants in protection from impulse noise. Ann. N. Y. Acad. Sci. 884:368–80
    [Google Scholar]
  46. Hollyfield JG. 1968. Differential addition of cells to the retina in Rana pipiens tadpoles. Dev. Biol. 18:163–79
    [Google Scholar]
  47. Housden BE, Fu AQ, Krejci A, Bernard F, Fischer B et al. 2013. Transcriptional dynamics elicited by a short pulse of Notch activation involves feed-forward regulation by E(spl)/Hes genes. PLOS Genet 9:e1003162
    [Google Scholar]
  48. Huang WC, Yang CC, Chen IH, Liu YM, Chang SJ, Chuang YJ 2013. Treatment of glucocorticoids inhibited early immune responses and impaired cardiac repair in adult zebrafish. PLOS ONE 8:e66613
    [Google Scholar]
  49. Hunt MT. 1901. Regeneration New York/London: Macmillan
    [Google Scholar]
  50. Ikeda R, Pak K, Chavez E, Ryan AF 2015. Transcription factors with conserved binding sites near ATOH1 on the POU4F3 gene enhance the induction of cochlear hair cells. Mol. Neurobiol. 51:672–84
    [Google Scholar]
  51. Ilagan MXG, Lim S, Fulbright M, Piwnica-Worms D, Kopan R 2011. Real-time imaging of Notch activation with a luciferase complementation-based reporter. Sci. Signal. 4:rs7
    [Google Scholar]
  52. Ishibashi M, Ang SL, Shiota K, Nakanishi S, Kageyama R, Guillemot F 1995. Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev 9:3136–48
    [Google Scholar]
  53. Iwai N, Zhou Z, Roop DR, Behringer RR 2008. Horizontal basal cells are multipotent progenitors in normal and injured adult olfactory epithelium. Stem Cells 26:1298–306
    [Google Scholar]
  54. Izumikawa M, Minoda R, Kawamoto K, Abrashkin KA, Swiderski DL et al. 2005. Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat. Med. 11:271–76
    [Google Scholar]
  55. Jacobo A, Dasgupta A, Erzberger A, Siletti K, Hudspeth AJ 2018. Notch-mediated polarity decisions in mechanosensory hair cells. bioRxiv 480798. https://doi.org/10.1101/480798
    [Crossref]
  56. Jacques BE, Montgomery WH IV, Uribe PM, Yatteau A, Asuncion JD et al. 2014. The role of Wnt/β-catenin signaling in proliferation and regeneration of the developing basilar papilla and lateral line. Dev. Neurobiol. 74:438–56
    [Google Scholar]
  57. Jang W, Youngentob SL, Schwob JE 2003. Globose basal cells are required for reconstitution of olfactory epithelium after methyl bromide lesion. J. Comp. Neurol. 460:123–40
    [Google Scholar]
  58. Jarman AP, Groves AK. 2013. The role of Atonal transcription factors in the development of mechanosensitive cells. Semin. Cell Dev. Biol. 24:438–47
    [Google Scholar]
  59. Jasoni CL, Reh TA. 1996. Temporal and spatial pattern of MASH-1 expression in the developing rat retina demonstrates progenitor cell heterogeneity. J. Comp. Neurol. 369:319–27
    [Google Scholar]
  60. Jiang L, Romero-Carvajal A, Haug JS, Seidel CW, Piotrowski T 2014. Gene-expression analysis of hair cell regeneration in the zebrafish lateral line. PNAS 111:E1383–92
    [Google Scholar]
  61. Jiang T, Kindt K, Wu DK 2017. Transcription factor Emx2 controls stereociliary bundle orientation of sensory hair cells. eLife 6:e23661
    [Google Scholar]
  62. Jones JE, Corwin JT. 1993. Replacement of lateral line sensory organs during tail regeneration in salamanders—identification of progenitor cells and analysis of leukocyte activity. J. Neurosci. 13:1022–34
    [Google Scholar]
  63. Jung JY, Avenarius MR, Adamsky S, Alpert E, Feinstein E, Raphael Y 2013. siRNA targeting Hes5 augments hair cell regeneration in aminoglycoside-damaged mouse utricle. Mol. Ther. 21:834–41
    [Google Scholar]
  64. Kang J, Hu J, Karra R, Dickson AL, Tornini VA et al. 2016. Modulation of tissue repair by regeneration enhancer elements. Nature 532:201–6
    [Google Scholar]
  65. Karlsson O, Thor S, Norberg T, Ohlsson H, Edlund T 1990. Insulin gene enhancer binding protein Isl-1 is a member of a novel class of proteins containing both a homeo- and a Cys–His domain. Nature 344:879–82
    [Google Scholar]
  66. Kelley C, Yee K, Harland R, Zon LI 1994. Ventral expression of GATA-1 and GATA-2 in the Xenopus embryo defines induction of hematopoietic mesoderm. Dev. Biol. 165:193–205
    [Google Scholar]
  67. Kelly MC, Chang Q, Pan A, Lin X, Chen P 2012. Atoh1 directs the formation of sensory mosaics and induces cell proliferation in the postnatal mammalian cochlea in vivo. J. Neurosci. 32:6699–710
    [Google Scholar]
  68. Kniss JS, Jiang L, Piotrowski T 2016. Insights into sensory hair cell regeneration from the zebrafish lateral line. Curr. Opin. Genet. Dev. 40:32–40
    [Google Scholar]
  69. Kopke RD, Liu W, Gabaizadeh R, Jacono A, Feghali J et al. 1997. Use of organotypic cultures of Corti's organ to study the protective effects of antioxidant molecules on cisplatin-induced damage of auditory hair cells. Am. J. Otol. 18:559–71
    [Google Scholar]
  70. Korrapati S, Roux I, Glowatzki E, Doetzlhofer A 2013. Notch signaling limits supporting cell plasticity in the hair cell–damaged early postnatal murine cochlea. PLOS ONE 8:e73276
    [Google Scholar]
  71. Ku YC, Renaud NA, Veile RA, Helms C, Voelker CC et al. 2014. The transcriptome of utricle hair cell regeneration in the avian inner ear. J. Neurosci. 34:3523–35
    [Google Scholar]
  72. Kuo BR, Baldwin EM, Layman WS, Taketo MM, Zuo J 2015. In vivo cochlear hair cell generation and survival by coactivation of β-catenin and Atoh1. J. Neurosci. 35:10786–98
    [Google Scholar]
  73. Kyritsis N, Kizil C, Zocher S, Kroehne V, Kaslin J et al. 2012. Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 338:1353–56
    [Google Scholar]
  74. Laugwitz K-L, Moretti A, Caron L, Nakano A, Chien KR 2008. Islet1 cardiovascular progenitors: a single source for heart lineages?. Development 135:193–205
    [Google Scholar]
  75. Ledent V. 2002. Postembryonic development of the posterior lateral line in zebrafish. Development 129:597–604
    [Google Scholar]
  76. Lee Y, Grill S, Sanchez A, Murphy-Ryan M, Poss KD 2005. Fgf signaling instructs position-dependent growth rate during zebrafish fin regeneration. Development 132:5173–83
    [Google Scholar]
  77. Lenhoff HM, Lenhoff SG. 1991. Abraham Trembley and the origins of research on regeneration in animals. A History of Regeneration Research: Milestones in the Evolution of a Science CE Dinsmore 47–66 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  78. Leung CT, Coulombe PA, Reed RR 2007. Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat. Neurosci. 10:720–26
    [Google Scholar]
  79. Li W, Wu J, Yang J, Sun S, Chai R et al. 2015. Notch inhibition induces mitotically generated hair cells in mammalian cochleae via activating the Wnt pathway. PNAS 112:166–71
    [Google Scholar]
  80. Liang J, Wang D, Renaud G, Wolfsberg TG, Wilson AF, Burgess SM 2012. The stat3/socs3a pathway is a key regulator of hair cell regeneration in zebrafish stat3/socs3a pathway: regulator of hair cell regeneration. J. Neurosci. 32:10662–73
    [Google Scholar]
  81. Lin V, Golub JS, Nguyen TB, Hume CR, Oesterle EC, Stone JS 2011. Inhibition of Notch activity promotes nonmitotic regeneration of hair cells in the adult mouse utricles. J. Neurosci. 31:15329–39
    [Google Scholar]
  82. Llorens-Bobadilla E, Zhao S, Baser A, Saiz-Castro G, Zwadlo K, Martin-Villalba A 2015. Single-cell transcriptomics reveals a population of dormant neural stem cells that become activated upon brain injury. Cell Stem Cell 17:329–40
    [Google Scholar]
  83. López-Schier H, Starr CJ, Kappler JA, Kollmar R, Hudspeth AJ 2004. Directional cell migration establishes the axes of planar polarity in the posterior lateral-line organ of the zebrafish. Dev. Cell 7:401–12
    [Google Scholar]
  84. Lush ME, Diaz DC, Koenecke N, Baek S, Boldt H et al. 2019. scRNA-Seq reveals distinct stem cell populations that drive hair cell regeneration after loss of Fgf and Notch signaling. eLife 8:e44431
    [Google Scholar]
  85. Lush ME, Piotrowski T. 2014. Sensory hair cell regeneration in the zebrafish lateral line. Dev. Dyn. 243:1187–202
    [Google Scholar]
  86. Ma EY, Rubel EW, Raible DW 2008. Notch signaling regulates the extent of hair cell regeneration in the zebrafish lateral line. J. Neurosci. 28:2261–73
    [Google Scholar]
  87. Maass JC, Gu R, Basch ML, Waldhaus J, Lopez EM et al. 2015. Changes in the regulation of the Notch signaling pathway are temporally correlated with regenerative failure in the mouse cochlea. Front. Cell. Neurosci. 9:110
    [Google Scholar]
  88. Maier W, Wolburg H. 1979. Regeneration of the goldfish retina after exposure to different doses of ouabain. Cell Tissue Res 202:99–118
    [Google Scholar]
  89. Manglapus GL, Youngentob SL, Schwob JE 2004. Expression patterns of basic helix-loop-helix transcription factors define subsets of olfactory progenitor cells. J. Comp. Neurol. 479:216–33
    [Google Scholar]
  90. Mariotto A, Pavlova O, Park HS, Huber M, Hohl D 2016. HOPX: the unusual homeodomain-containing protein. J. Investig. Dermatol. 136:905–11
    [Google Scholar]
  91. McLean WJ, Yin X, Lu L, Lenz DR, McLean D et al. 2017. Clonal expansion of Lgr5-positive cells from mammalian cochlea and high-purity generation of sensory hair cells. Cell Rep 18:1917–29
    [Google Scholar]
  92. Mizeracka K, DeMaso CR, Cepko CL 2013. Notch1 is required in newly postmitotic cells to inhibit the rod photoreceptor fate. Development 140:3188–97
    [Google Scholar]
  93. Mizutari K, Fujioka M, Hosoya M, Bramhall N, Okano HJ et al. 2013. Notch inhibition induces cochlear hair cell regeneration and recovery of hearing after acoustic trauma. Neuron 77:58–69
    [Google Scholar]
  94. Monje ML, Toda H, Palmer TD 2003. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760–65
    [Google Scholar]
  95. Moshiri A, Close J, Reh TA 2004. Retinal stem cells and regeneration. Int. J. Dev. Biol. 48:1003–14
    [Google Scholar]
  96. Nacu E, Tanaka EM. 2011. Limb regeneration: a new development. Annu. Rev. Cell Dev. Biol. 27:409–40
    [Google Scholar]
  97. Nagashima M, Barthel LK, Raymond PA 2013. A self-renewing division of zebrafish Müller glial cells generates neuronal progenitors that require N-cadherin to regenerate retinal neurons. Development 140:4510–21
    [Google Scholar]
  98. Naik S, Larsen SB, Cowley CJ, Fuchs E 2018. Two to tango: dialog between immunity and stem cells in health and disease. Cell 175:908–20
    [Google Scholar]
  99. Nandagopal N, Santat LA, LeBon L, Sprinzak D, Bronner ME, Elowitz MB 2018. Dynamic ligand discrimination in the Notch signaling pathway. Cell 172:869–80.e19
    [Google Scholar]
  100. Navajas Acedo J, Voas MG, Alexander RL, Woolley T, Unruh J et al. 2019. Parallel control of mechanosensory hair cell orientation by the PCP and Wnt pathways. bioRxiv 527937. https://doi.org/10.1101/527937
    [Crossref]
  101. Nelson CM, Ackerman KM, O'Hayer P, Bailey TJ, Gorsuch RA, Hyde DR 2013. Tumor necrosis factor-α is produced by dying retinal neurons and is required for Müller glia proliferation during zebrafish retinal regeneration. J. Neurosci. 33:6524–39
    [Google Scholar]
  102. Nguyen-Chi M, Laplace-Builhe B, Travnickova J, Luz-Crawford P, Tejedor G et al. 2015. Identification of polarized macrophage subsets in zebrafish. eLife 4:e07288
    [Google Scholar]
  103. Nunez VA, Sarrazin AF, Cubedo N, Allende ML, Dambly-Chaudiere C, Ghysen A 2009. Postembryonic development of the posterior lateral line in the zebrafish. Evol. Dev. 11:391–404
    [Google Scholar]
  104. Oliver G, Sosa-Pineda B, Geisendorf S, Spana EP, Doe CQ, Gruss P 1993. Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech. Dev. 44:3–16
    [Google Scholar]
  105. Osakada F, Ooto S, Akagi T, Mandai M, Akaike A, Takahashi M 2007. Wnt signaling promotes regeneration in the retina of adult mammals. J. Neurosci. 27:4210–19
    [Google Scholar]
  106. Petrie TA, Strand NS, Yang CT, Rabinowitz JS, Moon RT 2014. Macrophages modulate adult zebrafish tail fin regeneration. Development 141:2581–91
    [Google Scholar]
  107. Pfaff SL, Mendelsohn M, Stewart CL, Edlund T, Jessell TM 1996. Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron–dependent step in interneuron differentiation. Cell 84:309–20
    [Google Scholar]
  108. Pinto-Teixeira F, Viader-Llargues O, Torres-Mejia E, Turan M, Gonzalez-Gualda E et al. 2015. Inexhaustible hair-cell regeneration in young and aged zebrafish. Biol. Open 4:903–9
    [Google Scholar]
  109. Piotrowski T, Baker CV. 2014. The development of lateral line placodes: taking a broader view. Dev. Biol. 389:68–81
    [Google Scholar]
  110. Platt C. 1977. Hair cell distribution and orientation in goldfish otolith organs. J. Comp. Neurol. 172:283–97
    [Google Scholar]
  111. Porrello ER, Mahmoud AI, Simpson E, Hill JA, Richardson JA et al. 2011. Transient regenerative potential of the neonatal mouse heart. Science 331:1078–80
    [Google Scholar]
  112. Poss KD, Shen J, Nechiporuk A, McMahon G, Thisse B et al. 2000. Roles for Fgf signaling during zebrafish fin regeneration. Dev. Biol. 222:347–58
    [Google Scholar]
  113. Powell C, Grant AR, Cornblath E, Goldman D 2013. Analysis of DNA methylation reveals a partial reprogramming of the Müller glia genome during retina regeneration. PNAS 110:19814–19
    [Google Scholar]
  114. Ramachandran R, Fausett BV, Goldman D 2010. Ascl1a regulates Müller glia dedifferentiation and retinal regeneration through a Lin-28-dependent, let-7 microRNA signalling pathway. Nat. Cell Biol. 12:1101–7
    [Google Scholar]
  115. Ramachandran R, Zhao XF, Goldman D 2011. Ascl1a/Dkk/β-catenin signaling pathway is necessary and glycogen synthase kinase-3β inhibition is sufficient for zebrafish retina regeneration. PNAS 108:15858–63
    [Google Scholar]
  116. Rochais F, Sturny R, Chao C-M, Mesbah K, Bennett M et al. 2014. FGF10 promotes regional foetal cardiomyocyte proliferation and adult cardiomyocyte cell-cycle re-entry. Cardiovasc. Res. 104:432–42
    [Google Scholar]
  117. Romero-Carvajal A, Navajas Acedo J, Jiang L, Kozlovskaja-Gumbriene A, Alexander R et al. 2015. Regeneration of sensory hair cells requires localized interactions between the Notch and Wnt pathways. Dev. Cell 34:267–82
    [Google Scholar]
  118. Rouse GW, Pickles JO. 1991. Paired development of hair cells in neuromasts of the teleost lateral line. Proc. R. Soc. B Biol. Sci. 246:123–28
    [Google Scholar]
  119. Ryals BM, Rubel EW. 1988. Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240:1774–76
    [Google Scholar]
  120. Sage C, Huang M, Karimi K, Gutierrez G, Vollrath MA et al. 2005. Proliferation of functional hair cells in vivo in the absence of the retinoblastoma protein. Science 307:1114–18
    [Google Scholar]
  121. Samarajeewa A, Lenz DR, Xie L, Chiang H, Kirchner R et al. 2018. Transcriptional response to Wnt activation regulates the regenerative capacity of the mammalian cochlea. Development 145:dev166579
    [Google Scholar]
  122. Seifert AW, Muneoka K. 2018. The blastema and epimorphic regeneration in mammals. Dev. Biol. 433:190–99
    [Google Scholar]
  123. Seleit A, Kramer I, Riebesehl BF, Ambrosio EM, Stolper JS et al. 2017. Neural stem cells induce the formation of their physical niche during organogenesis. eLife 6:e29173
    [Google Scholar]
  124. Shi F, Cheng YF, Wang XL, Edge AS 2010. β-Catenin up-regulates Atoh1 expression in neural progenitor cells by interaction with an Atoh1 3′ enhancer. J. Biol. Chem. 285:392–400
    [Google Scholar]
  125. Shi F, Hu L, Edge AS 2013. Generation of hair cells in neonatal mice by β-catenin overexpression in Lgr5-positive cochlear progenitors. PNAS 110:13851–56
    [Google Scholar]
  126. Shin J, Berg DA, Zhu Y, Shin JY, Song J et al. 2015. Single-cell RNA-seq with waterfall reveals molecular cascades underlying adult neurogenesis. Cell Stem Cell 17:360–72
    [Google Scholar]
  127. Simkin J, Gawriluk TR, Gensel JC, Seifert AW 2017. Macrophages are necessary for epimorphic regeneration in African spiny mice. eLife 6:e24623
    [Google Scholar]
  128. Simkin J, Han M, Yu L, Yan M, Muneoka K 2013. The mouse digit tip: from wound healing to regeneration. Wound Regeneration and Repair: Methods and Protocols RG Gourdie, TA Myers 419–35 Totowa, NJ: Humana Press
    [Google Scholar]
  129. Slowik AD, Bermingham-McDonogh O. 2013. Hair cell generation by notch inhibition in the adult mammalian cristae. J. Assoc. Res. Otolaryngol. 14:813–28
    [Google Scholar]
  130. So H, Kim H, Lee JH, Park C, Kim Y et al. 2007. Cisplatin cytotoxicity of auditory cells requires secretions of proinflammatory cytokines via activation of ERK and NF-κB. J. Assoc. Res. Otolaryngol. 8:338–55
    [Google Scholar]
  131. Stojanova ZP, Kwan T, Segil N 2016. Epigenetic regulation of Atoh1 guides hair cell development in the mammalian cochlea. Development 143:1632
    [Google Scholar]
  132. Stone LS. 1933. The development of lateral-line sense organs in amphibians observed in living and vital-stained preparations. J. Comp. Neurol. 57:507–40
    [Google Scholar]
  133. Stone LS. 1937. Further experimental studies of the development of lateral-line sense organs in amphibians observed in living preparations. J. Comp. Neurol. 68:83–115
    [Google Scholar]
  134. Taylor RR, Filia A, Paredes U, Asai Y, Holt JR et al. 2018. Regenerating hair cells in vestibular sensory epithelia from humans. eLife 7:e34817
    [Google Scholar]
  135. Thomas ED, Raible D. 2019. Distinct progenitor populations mediate regeneration in the zebrafish lateral line. eLife 8:e43736
    [Google Scholar]
  136. Thor S, Ericson J, Brännström T, Edlund T 1991. The homeodomain LIM protein Isl-1 is expressed in subsets of neurons and endocrine cells in the adult rat. Neuron 7:881–89
    [Google Scholar]
  137. Tremblay M, Sanchez-Ferras O, Bouchard M 2018. GATA transcription factors in development and disease. Development 145:dev164384
    [Google Scholar]
  138. Trimarchi JM, Stadler MB, Cepko CL 2008. Individual retinal progenitor cells display extensive heterogeneity of gene expression. PLOS ONE 3:e1588
    [Google Scholar]
  139. Tsai F-Y, Keller G, Kuo FC, Weiss M, Chen J et al. 1994. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 371:221–26
    [Google Scholar]
  140. Viader-Llargues O, Lupperger V, Pola-Morell L, Marr C, Lopez-Schier H 2018. Live cell-lineage tracing and machine learning reveal patterns of organ regeneration. eLife 7:e30823
    [Google Scholar]
  141. Walters BJ, Coak E, Dearman J, Bailey G, Yamashita T et al. 2017. In vivo interplay between p27Kip1, GATA3, ATOH1, and POU4F3 converts non-sensory cells to hair cells in adult mice. Cell Rep 19:307–20
    [Google Scholar]
  142. Walters BJ, Liu Z, Crabtree M, Coak E, Cox BC, Zuo J 2014. Auditory hair cell–specific deletion of p27Kip1 in postnatal mice promotes cell-autonomous generation of new hair cells and normal hearing. J. Neurosci. 34:15751–63
    [Google Scholar]
  143. Wan J, Goldman D. 2016. Retina regeneration in zebrafish. Curr. Opin. Genet. Dev. 40:41–47
    [Google Scholar]
  144. Wan J, Goldman D. 2017. Opposing actions of Fgf8a on Notch signaling distinguish two Müller glial cell populations that contribute to retina growth and regeneration. Cell Rep 19:849–62
    [Google Scholar]
  145. Wan J, Ramachandran R, Goldman D 2012. HB-EGF is necessary and sufficient for Müller glia dedifferentiation and retina regeneration. Dev. Cell 22:334–47
    [Google Scholar]
  146. Warchol ME. 1997. Macrophage activity in organ cultures of the avian cochlea: demonstration of a resident population and recruitment to sites of hair cell lesions. J. Neurobiol. 33:724–34
    [Google Scholar]
  147. Warchol ME. 1999. Immune cytokines and dexamethasone influence sensory regeneration in the avian vestibular periphery. J. Neurocytol. 28:889–900
    [Google Scholar]
  148. Warchol ME, Lambert P, Goldstein B, Forge A, Corwin J 1993. Regenerative proliferation in inner ear sensory epithelia from adult guinea pigs and humans. Science 259:1619–22
    [Google Scholar]
  149. White DT, Sengupta S, Saxena MT, Xu Q, Hanes J et al. 2017. Immunomodulation-accelerated neuronal regeneration following selective rod photoreceptor cell ablation in the zebrafish retina. PNAS 114:E3719–28
    [Google Scholar]
  150. Wibowo I, Pinto-Teixeira F, Satou C, Higashijima S, Lopez-Schier H 2011. Compartmentalized Notch signaling sustains epithelial mirror symmetry. Development 138:1143–52
    [Google Scholar]
  151. Wigle JT, Oliver G. 1999. Prox1 function is required for the development of the murine lymphatic system. Cell 98:769–78
    [Google Scholar]
  152. Wu H-H, Ivkovic S, Murray RC, Jaramillo S, Lyons KM et al. 2003. Autoregulation of neurogenesis by GDF11. Neuron 37:197–207
    [Google Scholar]
  153. Wynn TA, Vannella KM. 2016. Macrophages in tissue repair, regeneration, and fibrosis. Immunity 44:450–62
    [Google Scholar]
  154. Yamamoto M, Ko LJ, Leonard MW, Beug H, Orkin SH, Engel JD 1990. Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev 4:1650–62
    [Google Scholar]
  155. Yu CR, Wu Y. 2017. Regeneration and rewiring of rodent olfactory sensory neurons. Exp. Neurol. 287:395–408
    [Google Scholar]
  156. Yu F-X, Zhao B, Guan K-L 2015. Hippo pathway in organ size control, tissue homeostasis, and cancer. Cell 163:811–28
    [Google Scholar]
  157. Zheng JL, Gao W-Q. 2000. Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat. Neurosci. 3:580–86
    [Google Scholar]
  158. Zhou P, Gu F, Zhang L, Akerberg BN, Ma Q et al. 2017. Mapping cell type–specific transcriptional enhancers using high affinity, lineage-specific Ep300 bioChIP-seq. eLife 6:e22039
    [Google Scholar]
  159. Zine A, Aubert A, Qiu J, Therianos S, Guillemot F et al. 2001. Hes1 and Hes5 activities are required for the normal development of the hair cells in the mammalian inner ear. J. Neurosci. 21:4712–20
    [Google Scholar]
  160. Zywitza V, Misios A, Bunatyan L, Willnow TE, Rajewsky N 2018. Single-cell transcriptomics characterizes cell types in the subventricular zone and uncovers molecular defects impairing adult neurogenesis. Cell Rep 25:2457–69.e8
    [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100818-125503
Loading
/content/journals/10.1146/annurev-cellbio-100818-125503
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error