Overactivation of notch1 signaling induces ectopic hair cells in the mouse inner ear in an age-dependent manner

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Liu, Zhiyong ^a,b   Owen, Thomas ^a,c   Fang, Jie ^a   Zuo, Jian ^a  

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

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

^c UNIVERSITY OF BATH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH1 RECEPTOR; TAMOXIFEN; TRANSCRIPTION FACTOR SOX10; GT(ROSA)26SOR PROTEIN, MOUSE; NOTCH RECEPTOR; PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COCHLEA; CONTROLLED STUDY; CORTI ORGAN; DEVELOPMENTAL STAGE; ECTOPIC ORGAN; ENZYME ACTIVATION; EPITHELIUM CELL; FEMALE; HAIR CELL; IN VIVO STUDY; INNER EAR; MOUSE; NONHUMAN; ORGANOGENESIS; POSTNATAL GROWTH; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SACCULUS; SIGNAL TRANSDUCTION; UTRICLE; WILD TYPE; AGE; ANIMAL; CELL COMMUNICATION; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; MALE; METABOLISM; MOUSE MUTANT; NEWBORN; PATHOLOGY; PHYSIOLOGY; PRENATAL DEVELOPMENT; REGENERATION; TRANSGENIC MOUSE;

MUS;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CELL COMMUNICATION; COCHLEA; EAR, INNER; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HAIR CELLS, AUDITORY; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PROTEINS; RECEPTORS, NOTCH; REGENERATION; SIGNAL TRANSDUCTION;

EID: 84863376392     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034123     Document Type: Article

References (72)

1. Fekete DM, Wu DK, (2002) Revisiting cell fate specification in the inner ear. Curr Opin Neurobiol 12: 35-42.
2. Kelley MW, (2006) Regulation of cell fate in the sensory epithelia of the inner ear. Nat Rev Neurosci 7: 837-849.
3. Brigande JV, Heller S, (2009) Quo vadis, hair cell regeneration? Nat Neurosci 12: 679-685.
4. Kelly MC, Chen P, (2009) Development of form and function in the mammalian cochlea. Curr Opin Neurobiol 19: 395-401.
5. Groves AK, Bronner-Fraser M, (2000) Competence, specification and commitment in otic placode induction. Development 127: 3489-3499.
6. Ohyama T, Groves AK, Martin K, (2007) The first steps towards hearing: mechanisms of otic placode induction. Int J Dev Biol 51: 463-472.
7. Morsli H, Choo D, Ryan A, Johnson R, Wu DK, (1998) Development of the mouse inner ear and origin of its sensory organs. J Neurosci 18: 3327-3335.
8. 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.
9. Takebayashi S, Yamamoto N, Yabe D, Fukuda H, Kojima K, et al. (2007) Multiple roles of Notch signaling in cochlear development. Dev Biol 307: 165-178.
10. Hayashi T, Kokubo H, Hartman BH, Ray CA, Reh TA, et al. (2008) Hesr1 and Hesr2 may act as early effectors of Notch signaling in the developing cochlea. Dev Biol 316: 87-99.
11. Hayashi T, Ray CA, Bermingham-McDonogh O, (2008) Fgf20 is required for sensory epithelial specification in the developing cochlea. J Neurosci 28: 5991-5999.
12. Eddison M, Le Roux I, Lewis J, (2000) Notch signaling in the development of the inner ear: lessons from Drosophila. Proc Natl Acad Sci U S A 97: 11692-11699.
13. Daudet N, Lewis J, (2005) Two contrasting roles for Notch activity in chick inner ear development: specification of prosensory patches and lateral inhibition of hair-cell differentiation. Development 132: 541-551.
14. Kiernan AE, Ahituv N, Fuchs H, Balling R, Avraham KB, et al. (2001) The Notch ligand Jagged1 is required for inner ear sensory development. Proc Natl Acad Sci U S A 98: 3873-3878.
15. Tsai H, Hardisty RE, Rhodes C, Kiernan AE, Roby P, et al. (2001) The mouse slalom mutant demonstrates a role for Jagged1 in neuroepithelial patterning in the organ of Corti. Hum Mol Genet 10: 507-512.
16. Brooker R, Hozumi K, Lewis J, (2006) Notch ligands with contrasting functions: Jagged1 and Delta1 in the mouse inner ear. Development 133: 1277-1286.
17. 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.
18. Daudet N, Ariza-McNaughton L, Lewis J, (2007) Notch signalling is needed to maintain, but not to initiate, the formation of prosensory patches in the chick inner ear. Development 134: 2369-2378.
19. Jayasena CS, Ohyama T, Segil N, Groves AK, (2008) Notch signaling augments the canonical Wnt pathway to specify the size of the otic placode. Development 135: 2251-2261.
20. Basch ML, Ohyama T, Segil N, Groves AK, (2011) Canonical Notch signaling is not necessary for prosensory induction in the mouse cochlea: insights from a conditional mutant of RBPjkappa. J Neurosci 31: 8046-8058.
21. Yamamoto N, Chang W, Kelley MW, (2011) Rbpj regulates development of prosensory cells in the mammalian inner ear. Dev Biol 353: 367-379.
22. 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.
23. 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.
24. Woods C, Montcouquiol M, Kelley MW, (2004) Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat Neurosci 7: 1310-1318.
25. 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.
26. Chen P, Johnson JE, Zoghbi HY, Segil N, (2002) The role of Math1 in inner ear development: Uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 129: 2495-2505.
27. Millimaki BB, Sweet EM, Dhason MS, Riley BB, (2007) Zebrafish atoh1 genes: classic proneural activity in the inner ear and regulation by Fgf and Notch. Development 134: 295-305.
28. Kiernan AE, Cordes R, Kopan R, Gossler A, Gridley T, (2005) The Notch ligands DLL1 and JAG2 act synergistically to regulate hair cell development in the mammalian inner ear. Development 132: 4353-4362.
29. Doetzlhofer A, Basch ML, Ohyama T, Gessler M, Groves AK, et al. (2009) Hey2 regulation by FGF provides a Notch-independent mechanism for maintaining pillar cell fate in the organ of Corti. Dev Cell 16: 58-69.
30. Yamamoto N, Tanigaki K, Tsuji M, Yabe D, Ito J, et al. (2006) Inhibition of Notch/RBP-J signaling induces hair cell formation in neonate mouse cochleas. J Mol Med 84: 37-45.
31. Pan W, Jin Y, Stanger B, Kiernan AE, (2010) Notch signaling is required for the generation of hair cells and supporting cells in the mammalian inner ear. Proc Natl Acad Sci U S A 107: 15798-15803.
32. Hartman BH, Reh TA, Bermingham-McDonogh O, (2010) Notch signaling specifies prosensory domains via lateral induction in the developing mammalian inner ear. Proc Natl Acad Sci U S A 107: 15792-15797.
33. Eminli S, Foudi A, Stadtfeld M, Maherali N, Ahfeldt T, et al. (2009) Differentiation stage determines potential of hematopoietic cells for reprogramming into induced pluripotent stem cells. Nat Genet 41: 968-976.
34. Breuskin I, Bodson M, Thelen N, Thiry M, Borgs L, et al. (2009) Sox10 promotes the survival of cochlear progenitors during the establishment of the organ of Corti. Dev Biol 335: 327-339.
35. Lanford PJ, Lan Y, Jiang R, Lindsell C, Weinmaster G, et al. (1999) Notch signalling pathway mediates hair cell development in mammalian cochlea. Nat Genet 21: 289-292.
36. Neves J, Parada C, Chamizo M, Giraldez F, (2011) Jagged 1 regulates the restriction of Sox2 expression in the developing chicken inner ear: a mechanism for sensory organ specification. Development 138: 735-744.
37. Mustapha M, Fang Q, Gong TW, Dolan DF, Raphael Y, et al. (2009) Deafness and permanently reduced potassium channel gene expression and function in hypothyroid Pit1dw mutants. J Neurosci 29: 1212-1223.
38. Hackney CM, Mahendrasingam S, Penn A, Fettiplace R, (2005) The concentrations of calcium buffering proteins in mammalian cochlear hair cells. J Neurosci 25: 7867-7875.
39. Kiernan AE, Pelling AL, Leung KK, Tang AS, Bell DM, et al. (2005) Sox2 is required for sensory organ development in the mammalian inner ear. Nature 434: 1031-1035.
40. Jadhav AP, Cho SH, Cepko CL, (2006) Notch activity permits retinal cells to progress through multiple progenitor states and acquire a stem cell property. Proc Natl Acad Sci U S A 103: 18998-19003.
41. Murtaugh LC, Stanger BZ, Kwan KM, Melton DA, (2003) Notch signaling controls multiple steps of pancreatic differentiation. Proc Natl Acad Sci U S A 100: 14920-14925.
42. Murata J, Tokunaga A, Okano H, Kubo T, (2006) Mapping of notch activation during cochlear development in mice: implications for determination of prosensory domain and cell fate diversification. J Comp Neurol 497: 502-518.
43. Raft S, Koundakjian EJ, Quinones H, Jayasena CS, Goodrich LV, et al. (2007) Cross-regulation of Ngn1 and Math1 coordinates the production of neurons and sensory hair cells during inner ear development. Development 134: 4405-4415.
44. Jahan I, Pan N, Kersigo J, Fritzsch B, (2011) Neurod1 suppresses hair cell differentiation in ear ganglia and regulates hair cell subtype development in the cochlea. PLoS One 5: e11661.
45. Morrison A, Hodgetts C, Gossler A, Hrabe de Angelis M, Lewis J, (1999) Expression of Delta1 and Serrate1 (Jagged1) in the mouse inner ear. Mech Dev 84: 169-172.
46. Jeon SJ, Fujioka M, Kim SC, Edge AS, (2011) Notch signaling alters sensory or neuronal cell fate specification of inner ear stem cells. J Neurosci 31: 8351-8358.
47. Stone JS, Cotanche DA, (2007) Hair cell regeneration in the avian auditory epithelium. Int J Dev Biol 51: 633-647.
48. Kwan T, White PM, Segil N, (2009) Development and regeneration of the inner ear. Ann N Y Acad Sci 1170: 28-33.
49. Burns J, Christophel JJ, Collado MS, Magnus C, Carfrae M, et al. (2008) Reinforcement of cell junctions correlates with the absence of hair cell regeneration in mammals and its occurrence in birds. J Comp Neurol 511: 396-414.
50. Collado MS, Burns JC, Hu Z, Corwin JT, (2008) Recent advances in hair cell regeneration research. Curr Opin Otolaryngol Head Neck Surg 16: 465-471.
51. Sweet EM, Vemaraju S, Riley BB, (2011) Sox2 and Fgf interact with Atoh1 to promote sensory competence throughout the zebrafish inner ear. Dev Biol 358: 113-121.
52. Pirvola U, Ylikoski J, Trokovic R, Hebert JM, McConnell SK, et al. (2002) FGFR1 is required for the development of the auditory sensory epithelium. Neuron 35: 671-680.
53. Hatch EP, Noyes CA, Wang X, Wright TJ, Mansour SL, (2007) Fgf3 is required for dorsal patterning and morphogenesis of the inner ear epithelium. Development 134: 3615-3625.
54. Urness LD, Paxton CN, Wang X, Schoenwolf GC, Mansour SL, (2010) FGF signaling regulates otic placode induction and refinement by controlling both ectodermal target genes and hindbrain Wnt8a. Dev Biol 340: 595-604.
55. Wright TJ, Mansour SL, (2003) FGF signaling in ear development and innervation. Curr Top Dev Biol 57: 225-259.
56. Huh S, Jones J, Warchol M, Ornitz D, (2012) Differentiation of the Lateral Compartment of the Cochlea Requires a Temporally Restricted FGF20 Signal PLoS Biol 10: e1001231.
57. Ohyama T, Mohamed OA, Taketo MM, Dufort D, Groves AK, (2006) Wnt signals mediate a fate decision between otic placode and epidermis. Development 133: 865-875.
58. Freyer L, Morrow BE, (2010) Canonical Wnt signaling modulates Tbx1, Eya1, and Six1 expression, restricting neurogenesis in the otic vesicle. Dev Dyn 239: 1708-1722.
59. Riccomagno MM, Takada S, Epstein DJ, (2005) Wnt-dependent regulation of inner ear morphogenesis is balanced by the opposing and supporting roles of Shh. Genes Dev 19: 1612-1623.
60. Li H, Corrales CE, Wang Z, Zhao Y, Wang Y, et al. (2005) BMP4 signaling is involved in the generation of inner ear sensory epithelia. BMC Dev Biol 5: 16.
61. Puligilla C, Feng F, Ishikawa K, Bertuzzi S, Dabdoub A, et al. (2007) Disruption of fibroblast growth factor receptor 3 signaling results in defects in cellular differentiation, neuronal patterning, and hearing impairment. Dev Dyn 236: 1905-1917.
62. Hwang CH, Guo D, Harris MA, Howard O, Mishina Y, et al. (2010) Role of bone morphogenetic proteins on cochlear hair cell formation: analyses of Noggin and Bmp2 mutant mice. Dev Dyn 239: 505-513.
63. Ohyama T, Basch ML, Mishina Y, Lyons KM, Segil N, et al. (2010) BMP signaling is necessary for patterning the sensory and nonsensory regions of the developing mammalian cochlea. J Neurosci 30: 15044-15051.
64. Bok J, Dolson DK, Hill P, Ruther U, Epstein DJ, et al. (2007) Opposing gradients of Gli repressor and activators mediate Shh signaling along the dorsoventral axis of the inner ear. Development 134: 1713-1722.
65. Riccomagno MM, Martinu L, Mulheisen M, Wu DK, Epstein DJ, (2002) Specification of the mammalian cochlea is dependent on Sonic hedgehog. Genes Dev 16: 2365-2378.
66. Driver EC, Pryor SP, Hill P, Turner J, Ruther U, et al. (2008) Hedgehog signaling regulates sensory cell formation and auditory function in mice and humans. J Neurosci 28: 7350-7358.
67. Rawlins EL, Clark CP, Xue Y, Hogan BL, (2009) The Id2+ distal tip lung epithelium contains individual multipotent embryonic progenitor cells. Development 136: 3741-3745.
68. Hayashi S, McMahon AP, (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305-318.
69. Nyabi O, Naessens M, Haigh K, Gembarska A, Goossens S, et al. (2009) Efficient mouse transgenesis using Gateway-compatible ROSA26 locus targeting vectors and F1 hybrid ES cells. Nucleic Acids Res 37: e55.
70. Chen CM, Krohn J, Bhattacharya S, Davies B, (2011) A comparison of exogenous promoter activity at the ROSA26 locus using a PhiC31 integrase mediated cassette exchange approach in mouse ES cells. PLoS One 6: e23376.
71. 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.
72. 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.