In vivo generation of immature inner hair cells in neonatal mouse cochleae by ectopic Atoh1 expression

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Liu, Zhiyong ^a,b   Fang, Jie ^a   Dearman, Jennifer ^a   Zhang, Lingli ^a   Zuo, Jian ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 8; GLUTAMATE RECEPTOR 2; MEMBRANE PROTEIN; OTOFERLIN; PROTEIN ATOH1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 3; AMINO ACID TRANSPORTER; ATOH1 PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; FGF8 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; OTOFERLIN PROTEIN, MOUSE; POU4F3 PROTEIN, MOUSE; TRANSCRIPTION FACTOR POU4F3; VESICULAR GLUTAMATE TRANSPORTER 3, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL MATURATION; CELL REGENERATION; CELL TYPE; COCHLEA; CONTROLLED STUDY; DEVELOPMENTAL STAGE; HAIR CELL; IN VIVO STUDY; MOUSE; NEWBORN; NONHUMAN; PERINATAL DEVELOPMENT; PHALANX; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PROTEIN EXPRESSION; STEREOCILIUM; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; ELECTROPHYSIOLOGY; FLUORESCENCE IN SITU HYBRIDIZATION; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; INNER HAIR CELL; METABOLISM; PHYSIOLOGY; REGENERATION; TRANSGENIC MOUSE;

AMINO ACID TRANSPORT SYSTEMS, ACIDIC; ANIMALS; ANIMALS, NEWBORN; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; COCHLEA; ELECTROPHYSIOLOGY; FIBROBLAST GROWTH FACTOR 8; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAIR CELLS, AUDITORY, INNER; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; IN SITU HYBRIDIZATION, FLUORESCENCE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; REGENERATION; TRANSCRIPTION FACTOR BRN-3C;

EID: 84895899350     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089377     Document Type: Article

References (75)

1. Walters BJ, Zuo J (2013) Postnatal development, maturation and aging in the mouse cochlea and their effects on hair cell regeneration. Hear Res 297: 68-83.
2. Brigande JV, Heller S (2009) Quo vadis, hair cell regeneration? Nat Neurosci 12: 679-685.
3. Lewis RM, Hume CR, Stone JS (2012) Atoh1 expression and function during auditory hair cell regeneration in post-hatch chickens. Hear Res 289: 74-85.
4. Fekete DM, Muthukumar S, Karagogeos D (1998) Hair cells and supporting cells share a common progenitor in the avian inner ear. J Neurosci 18: 7811-7821. (Pubitemid 28441021)
5. 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: 1837-1841.
6. Zheng JL, Gao WQ (2000) Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat Neurosci 3: 580-586. (Pubitemid 30332077)
7. Cafaro J, Lee GS, Stone JS (2007) Atoh1 expression defines activated progenitors and differentiating hair cells during avian hair cell regeneration. Dev Dyn 236: 156-170. (Pubitemid 46095088)
8. Liu Z, Dearman JA, Cox BC, Walters BJ, Zhang L, et al. (2012) Age-dependent in vivo conversion of mouse cochlear pillar and Deiters' cells to immature hair cells by Atoh1 ectopic expression. J Neurosci 32: 6600-6610.
9. 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: 6699-6710.
10. Gubbels SP, Woessner DW, Mitchell JC, Ricci AJ, Brigande JV (2008) Functional auditory hair cells produced in the mammalian cochlea by in utero gene transfer. Nature 455: 537-541.
11. Appler JM, Goodrich LV (2011) Connecting the ear to the brain: Molecular mechanisms of auditory circuit assembly. Prog Neurobiol 93: 488-508.
12. Gomez-Casati ME, Murtie J, Taylor B, Corfas G (2010) Cell-specific inducible gene recombination in postnatal inner ear supporting cells and glia. J Assoc Res Otolaryngol 11: 19-26.
13. Avraham KB, Hasson T, Steel KP, Kingsley DM, Russell LB, et al. (1995) The mouse Snell's waltzer deafness gene encodes an unconventional myosin required for structural integrity of inner ear hair cells. Nat Genet 11: 369-375.
14. Ma Q, Chen Z, del Barco Barrantes I, de la Pompa JL, Anderson DJ (1998) neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 20: 469-482. (Pubitemid 28153078)
15. Reim G, Brand M (2002) Spiel-ohne-grenzen/pou2 mediates regional competence to respond to Fgf8 during zebrafish early neural development. Development 129: 917-933. (Pubitemid 34874116)
16. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676. (Pubitemid 44233629)
17. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, et al. (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38: 431-440.
18. Jahan I, Pan N, Kersigo J, Fritzsch B (2010) Neurod1 suppresses hair cell differentiation in ear ganglia and regulates hair cell subtype development in the cochlea. PLoS One 5: e11661.
19. Xiang M, Gan L, Li D, Chen ZY, Zhou L, et al. (1997) Essential role of POU-domain factor Brn-3c in auditory and vestibular hair cell development. Proc Natl Acad Sci U S A 94: 9445-9450. (Pubitemid 27357849)
20. Liu Z, Walters BJ, Owen T, Brimble MA, Steigelman KA, et al. (2012) Regulation of p27Kip1 by Sox2 maintains quiescence of inner pillar cells in the murine auditory sensory epithelium. J Neurosci 32: 10530-10540.
21. Neves J, Vachkov I, Giraldez F (2013) Sox2 regulation of hair cell development: incoherence makes sense. Hear Res 297: 20-29.
22. Sweet EM, Vemaraju S, Riley BB (2011) Sox2 and Fgf interact with Atoh1 to promote sensory competence throughout the zebrafish inner ear. Dev Biol.
23. Glowatzki E, Cheng N, Hiel H, Yi E, Tanaka K, et al. (2006) The glutamate-aspartate transporter GLAST mediates glutamate uptake at inner hair cell afferent synapses in the mammalian cochlea. J Neurosci 26: 7659-7664. (Pubitemid 44315185)
24. Jin ZH, Kikuchi T, Tanaka K, Kobayashi T (2003) Expression of glutamate transporter GLAST in the developing mouse cochlea. Tohoku J Exp Med 200: 137-144. (Pubitemid 37258811)
25. Nakamura T, Colbert MC, Robbins J (2006) Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system. Circ Res 98: 1547-1554. (Pubitemid 44297078)
26. Zheng L, Sekerkova G, Vranich K, Tilney LG, Mugnaini E, et al. (2000) The deaf jerker mouse has a mutation in the gene encoding the espin actin-bundling proteins of hair cell stereocilia and lacks espins. Cell 102: 377-385.
27. Jacques BE, Montcouquiol ME, Layman EM, Lewandoski M, Kelley MW (2007) Fgf8 induces pillar cell fate and regulates cellular patterning in the mammalian cochlea. Development 134: 3021-3029. (Pubitemid 47386913)
28. Jahan I, Pan N, Kersigo J, Fritzsch B (2013) Beyond generalized hair cells: Molecular cues for hair cell types. Hear Res 297: 30-41.
29. Macatee TL, Hammond BP, Arenkiel BR, Francis L, Frank DU, et al. (2003) Ablation of specific expression domains reveals discrete functions of ectodermand endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 130: 6361-6374. (Pubitemid 38008833)
30. Liberman MC, Gao J, He DZ, Wu X, Jia S, et al. (2002) Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419: 300-304.
31. Zheng J, Shen W, He DZ, Long KB, Madison LD, et al. (2000) Prestin is the motor protein of cochlear outer hair cells. Nature 405: 149-155. (Pubitemid 30313525)
32. Corey DP, Hudspeth AJ (1983) Kinetics of the receptor current in bullfrog saccular hair cells. J Neurosci 3: 962-976. (Pubitemid 13135421)
33. Nagiel A, Andor-Ardo D, Hudspeth AJ (2008) Specificity of afferent synapses onto plane-polarized hair cells in the posterior lateral line of the zebrafish. J Neurosci 28: 8442-8453.
34. Roux I, Wersinger E, McIntosh JM, Fuchs PA, Glowatzki E (2011) Onset of cholinergic efferent synaptic function in sensory hair cells of the rat cochlea. J Neurosci 31: 15092-15101.
35. Gale JE, Marcotti W, Kennedy HJ, Kros CJ, Richardson GP (2001) FM1-43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J Neurosci 21: 7013-7025. (Pubitemid 32846949)
36. Meyers JR, MacDonald RB, Duggan A, Lenzi D, Standaert DG, et al. (2003) Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. J Neurosci 23: 4054-4065. (Pubitemid 36958424)
37. Marcotti W, Kros CJ (1999) Developmental expression of the potassium current IK,n contributes to maturation of mouse outer hair cells. J Physiol 520 Pt 3: 653-660. (Pubitemid 29533025)
38. Marcotti W, Johnson SL, Holley MC, Kros CJ (2003) Developmental changes in the expression of potassium currents of embryonic, neonatal and mature mouse inner hair cells. J Physiol 548: 383-400. (Pubitemid 36527462)
39. Zuo J, Treadaway J, Buckner TW, Fritzsch B (1999) Visualization of alpha9 acetylcholine receptor expression in hair cells of transgenic mice containing a modified bacterial artificial chromosome. Proc Natl Acad Sci U S A 96: 14100-14105.
40. Seal RP, Akil O, Yi E, Weber CM, Grant L, et al. (2008) Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3. Neuron 57: 263-275.
41. Roux I, Safieddine S, Nouvian R, Grati M, Simmler MC, et al. (2006) Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 127: 277-289. (Pubitemid 44572372)
42. Akil O, Seal RP, Burke K, Wang C, Alemi A, et al. (2012) Restoration of hearing in the VGLUT3 knockout mouse using virally mediated gene therapy. Neuron 75: 283-293.
43. Ruel J, Emery S, Nouvian R, Bersot T, Amilhon B, et al. (2008) Impairment of SLC17A8 encoding vesicular glutamate transporter-3, VGLUT3, underlies nonsyndromic deafness DFNA25 and inner hair cell dysfunction in null mice. Am J Hum Genet 83: 278-292.
44. Heidrych P, Zimmermann U, Kuhn S, Franz C, Engel J, et al. (2009) Otoferlin interacts with myosin VI: implications for maintenance of the basolateral synaptic structure of the inner hair cell. Hum Mol Genet 18: 2779-2790.
45. Uthaiah RC, Hudspeth AJ (2010) Molecular anatomy of the hair cell's ribbon synapse. J Neurosci 30: 12387-12399.
46. Khimich D, Nouvian R, Pujol R, Tom Dieck S, Egner A, et al. (2005) Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434: 889-894. (Pubitemid 40559000)
47. Liberman LD, Wang H, Liberman MC (2011) Opposing gradients of ribbon size and AMPA receptor expression underlie sensitivity differences among cochlearnerve/hair-cell synapses. J Neurosci 31: 801-808.
48. Obholzer N, Wolfson S, Trapani JG, Mo W, Nechiporuk A, et al. (2008) Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells. J Neurosci 28: 2110-2118. (Pubitemid 351317615)
49. Vahava O, Morell R, Lynch ED, Weiss S, Kagan ME, et al. (1998) Mutation in transcription factor POU4F3 associated with inherited progressive hearing loss in humans. Science 279: 1950-1954. (Pubitemid 28168652)
50. Ahmed M, Wong EY, Sun J, Xu J, Wang F, et al. (2012) Eya1-Six1 interaction is sufficient to induce hair cell fate in the cochlea by activating Atoh1 expression in cooperation with Sox2. Dev Cell 22: 377-390.
51. Masuda M, Pak K, Chavez E, Ryan AF (2012) TFE2 and GATA3 enhance induction of POU4F3 and myosin VIIa positive cells in nonsensory cochlear epithelium by ATOH1. Dev Biol 372: 68-80.
52. Oshima K, Shin K, Diensthuber M, Peng AW, Ricci AJ, et al. (2010) Mechanosensitive hair cell-like cells from embryonic and induced pluripotent stem cells. Cell 141: 704-716.
53. Yang H, Xie X, Deng M, Chen X, Gan L (2010) Generation and characterization of Atoh1-Cre knock-in mouse line. Genesis 48: 407-413.
54. Matei V, Pauley S, Kaing S, Rowitch D, Beisel KW, et al. (2005) Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Dev Dyn 234: 633-650. (Pubitemid 41532984)
55. Li S, Price SM, Cahill H, Ryugo DK, Shen MM, et al. (2002) Hearing loss caused by progressive degeneration of cochlear hair cells in mice deficient for the Barhl1 homeobox gene. Development 129: 3523-3532.
56. Yang H, Gan J, Xie X, Deng M, Feng L, et al. (2010) Gfi1-Cre knock-in mouse line: A tool for inner ear hair cell-specific gene deletion. Genesis 48: 400-406.
57. Wallis D, Hamblen M, Zhou Y, Venken KJ, Schumacher A, et al. (2003) The zinc finger transcription factor Gfi1, implicated in lymphomagenesis, is required for inner ear hair cell differentiation and survival. Development 130: 221-232. (Pubitemid 36113957)
58. Yang J, Bouvron S, Lv P, Chi F, Yamoah EN (2012) Functional features of trans-differentiated hair cells mediated by Atoh1 reveals a primordial mechanism. J Neurosci 32: 3712-3725.
59. Brooker R, Hozumi K, Lewis J (2006) Notch ligands with contrasting functions: Jagged1 and Delta1 in the mouse inner ear. Development 133: 1277-1286.
60. Kiernan AE, Xu J, Gridley T (2006) The Notch ligand JAG1 is required for sensory progenitor development in the mammalian inner ear. PLoS Genet 2: e4.
61. Kelley MW (2007) Cellular commitment and differentiation in the organ of Corti. Int J Dev Biol 51: 571-583.
62. Simonneau L, Gallego M, Pujol R (2003) Comparative expression patterns of T-, N-, E-cadherins, beta-catenin, and polysialic acid neural cell adhesion molecule in rat cochlea during development: implications for the nature of Kolliker's organ. J Comp Neurol 459: 113-126. (Pubitemid 36384314)
63. Pauley S, Wright TJ, Pirvola U, Ornitz D, Beisel K, et al. (2003) Expression and function of FGF10 in mammalian inner ear development. Dev Dyn 227: 203-215. (Pubitemid 36666749)
64. Shi F, Cheng YF, Wang XL, Edge AS (2010) Beta-catenin up-regulates Atoh1 expression in neural progenitor cells by interaction with an Atoh1 3′ enhancer. J Biol Chem 285: 392-400.
65. Chai R, Kuo B, Wang T, Liaw EJ, Xia A, et al. (2012) Wnt signaling induces proliferation of sensory precursors in the postnatal mouse cochlea. Proc Natl Acad Sci U S A 109: 8167-8172.
66. Liu Z, Walters BJ, Owen T, Kopan R, Zuo J (2013) In vivo visualization of notch1 proteolysis reveals the heterogeneity of notch1 signaling activity in the mouse cochlea. PLoS One 8: e64903.
67. Cohen DE, Melton D (2011) Turning straw into gold: directing cell fate for regenerative medicine. Nat Rev Genet 12: 243-252.
68. Song K, Nam YJ, Luo X, Qi X, Tan W, et al. (2012) Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 485: 599-604.
69. Qian L, Huang Y, Spencer CI, Foley A, Vedantham V, et al. (2012) In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 485: 593-598.
70. Collombat P, Xu X, Ravassard P, Sosa-Pineda B, Dussaud S, et al. (2009) The ectopic expression of Pax4 in the mouse pancreas converts progenitor cells into alpha and subsequently beta cells. Cell 138: 449-462.
71. Golub JS, Tong L, Ngyuen TB, Hume CR, Palmiter RD, et al. (2012) Hair cell replacement in adult mouse utricles after targeted ablation of hair cells with diphtheria toxin. J Neurosci 32: 15093-15105.
72. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13: 133-140.
73. Liu Z, Owen T, Zhang L, Zuo J (2010) Dynamic expression pattern of Sonic hedgehog in developing cochlear spiral ganglion neurons. Dev Dyn 239: 1674-1683.
74. Yu Y, Weber T, Yamashita T, Liu Z, Valentine MB, et al. (2010) In vivo proliferation of postmitotic cochlear supporting cells by acute ablation of the retinoblastoma protein in neonatal mice. J Neurosci 30: 5927-5936.
75. Pan N, Jahan I, Kersigo J, Duncan JS, Kopecky B, et al. (2012) A novel atoh1 "self-terminating" mouse model reveals the necessity of proper atoh1 level and duration for hair cell differentiation and viability. PLoS One 7: e30358.