Continued Expression of GATA3 Is Necessary for Cochlear Neurosensory Development

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Duncan, Jeremy S ^a   Fritzsch, Bernd ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; RECOMBINANT PROTEIN; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR PAX2; TRANSCRIPTION FACTOR SOX2;

ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATOH1 GENE; CELL DIFFERENTIATION; COCHLEA DUCT; COCHLEAR NERVE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EYA1 GENE; FOXG1 GENE; GATA 3 GENE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; HAIR CELL; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROEPITHELIUM; NONHUMAN; PAIRED BOX GENE 2; POU4F3 GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOX2 GENE;

ANIMALS; COCHLEAR DUCT; GATA3 TRANSCRIPTION FACTOR; HAIR CELLS, AUDITORY; MICE;

MAMMALIA; MUS;

EID: 84876166958     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062046     Document Type: Article

References (91)

1. Grocott T, Tambalo M, Streit A, (2012) The peripheral sensory nervous system in the vertebrate head: a gene regulatory perspective. Dev Biol 370: 3-23.
2. Fritzsch B, Beisel KW, Hansen LA, (2006) The molecular basis of neurosensory cell formation in ear development: a blueprint for hair cell and sensory neuron regeneration? Bioessays 28: 1181-1193.
3. Fekete DM, Wu DK, (2002) Revisiting cell fate specification in the inner ear. Curr Opin Neurobiol 12: 35-42.
4. Brigande JV, Kiernan AE, Gao X, Iten LE, Fekete DM, (2000) Molecular genetics of pattern formation in the inner ear: do compartment boundaries play a role? Proc Natl Acad Sci U S A 97: 11700-11706.
5. Fritzsch B, Beisel KW, Bermingham NA, (2000) Developmental evolutionary biology of the vertebrate ear: conserving mechanoelectric transduction and developmental pathways in diverging morphologies. Neuroreport 11: R35-44.
6. Nichols DH, Pauley S, Jahan I, Beisel KW, Millen KJ, et al. (2008) Lmx1a is required for segregation of sensory epithelia and normal ear histogenesis and morphogenesis. Cell Tissue Res 334: 339-358.
7. 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.
8. Cole LK, Le Roux I, Nunes F, Laufer E, Lewis J, et al. (2000) Sensory organ generation in the chicken inner ear: Contributions of bone morphogenetic protein 4, serrate1, and lunatic fringe. Journal of Comparative Neurology 424: 509-520.
9. Oh SH, Johnson R, Wu DK, (1996) Differential expression of bone morphogenetic proteins in the developing vestibular and auditory sensory organs. Journal of Neuroscience 16: 6463-6475.
10. 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.
11. Pauley S, Wright TJ, Pirvola U, Ornitz D, Beisel K, et al. (2003) Expression and function of FGF10 in mammalian inner ear development. Developmental Dynamics 227: 203-215.
12. Bouchard M, de Caprona D, Busslinger M, Xu P, Fritzsch B, (2010) Pax2 and Pax8 cooperate in mouse inner ear morphogenesis and innervation. BMC Dev Biol 10: 89.
13. Ladher RK, Wright TJ, Moon AM, Mansour SL, Schoenwolf GC, (2005) FGF8 initiates inner ear induction in chick and mouse. Genes Dev 19: 603-613.
14. Huh SH, Jones J, Warchol ME, Ornitz DM, (2012) Differentiation of the lateral compartment of the cochlea requires a temporally restricted FGF20 signal. PLoS Biol 10: e1001231.
15. Pirvola U, Spencer-Dene B, Xing-Qun L, Kettunen P, Thesleff I, et al. (2000) FGF/FGFR-2(IIIb) signaling is essential for inner ear morphogenesis. J Neurosci 20: 6125-6134.
16. 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.
17. Pan N, Jahan I, Kersigo J, Kopecky B, Santi P, et al. (2011) Conditional deletion of Atoh1 using Pax2-Cre results in viable mice without differentiated cochlear hair cells that have lost most of the organ of Corti. Hearing Research 275: 66-80.
18. 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.
19. 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. Development129: 2495-2505.
20. Fritzsch B, Matei VA, Nichols DH, Bermingham N, Jones K, et al. (2005) Atoh1 null mice show directed afferent fiber growth to undifferentiated ear sensory epithelia followed by incomplete fiber retention. Developmental dynamics: an official publication of the American Association of Anatomists 233: 570-583.
21. 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. Developmental Dynamics 234: 633-650.
22. Jahan I, Pan N, Kersigo J, Fritzsch B, (2013) Beyond generalized hair cells: Molecular cues for hair cell types. Hearing Research 297: 30-41.
23. 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. Journal of Neuroscience 32: 6699-6710.
24. 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. Journal of Neuroscience 32: 6600-6610.
25. 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. Journal of Neuroscience 32: 3712-3725.
26. Zhao LD, Guo WW, Lin C, Li LX, Sun JH, et al. (2011) Effects of DAPT and Atoh1 overexpression on hair cell production and hair bundle orientation in cultured Organ of Corti from neonatal rats. PLoS One 6: e23729.
27. Ahmed M, Xu J, Xu PX, (2012) EYA1 and SIX1 drive the neuronal developmental program in cooperation with the SWI/SNF chromatin-remodeling complex and SOX2 in the mammalian inner ear. Development139: 1965-1977.
28. 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. Developmental Cell 22: 377-390.
29. George KM, Leonard MW, Roth ME, Lieuw KH, Kioussis D, et al. (1994) Embryonic expression and cloning of the murine GATA-3 gene. Development120: 2673-2686.
30. Karis A, Pata I, van Doorninck JH, Grosveld F, de Zeeuw CI, et al. (2001) Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. Journal of Comparative Neurology 429: 615-630.
31. Lawoko-Kerali G, Rivolta MN, Holley M, (2002) Expression of the transcription factors GATA3 and Pax2 during development of the mammalian inner ear. Journal of Comparative Neurology 442: 378-391.
32. Gross J, Stute K, Moller R, Fuchs J, Amarjargal N, et al. (2010) Expression of prestin and Gata-3,-2,-1 mRNA in the rat organ of Corti during the postnatal period and in culture. Hearing Research 261: 9-21.
33. Lu CC, Appler JM, Houseman EA, Goodrich LV, (2011) Developmental profiling of spiral ganglion neurons reveals insights into auditory circuit assembly. Journal of Neuroscience 31: 10903-10918.
34. van der Wees J, van Looij MA, de Ruiter MM, Elias H, van der Burg H, et al. (2004) Hearing loss following Gata3 haploinsufficiency is caused by cochlear disorder. Neurobiol Dis 16: 169-178.
35. Rivolta MN, Holley MC, (1998) GATA3 is downregulated during hair cell differentiation in the mouse cochlea. Journal of Neurocytology 27: 637-647.
36. Van Esch H, Groenen P, Nesbit MA, Schuffenhauer S, Lichtner P, et al. (2000) GATA3 haplo-insufficiency causes human HDR syndrome. Nature 406: 419-422.
37. Ali A, Christie PT, Grigorieva IV, Harding B, Van Esch H, et al. (2007) Functional characterization of GATA3 mutations causing the hypoparathyroidism-deafness-renal (HDR) dysplasia syndrome: insight into mechanisms of DNA binding by the GATA3 transcription factor. Hum Mol Genet 16: 265-275.
38. Duncan JS, Lim KC, Engel JD, Fritzsch B (2011) Gata3 is necessary for cochlear neurosensory developement. International Journal of Developmental Biology.
39. Haugas M, Lillevali K, Salminen M, (2012) Defects in sensory organ morphogenesis and generation of cochlear hair cells in Gata3-deficient mouse embryos. Hearing Research 283: 151-161.
40. Hebert JM, McConnell SK, (2000) Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Developmental Biology 222: 296-306.
41. Hatini V, Ye X, Balas G, Lai E, (1999) Dynamics of placodal lineage development revealed by targeted transgene expression. Dev Dyn 215: 332-343.
42. Pauley S, Lai E, Fritzsch B, (2006) Foxg1 is required for morphogenesis and histogenesis of the mammalian inner ear. Developmental Dynamics 235: 2470-2482.
43. Ohyama T, Groves AK, (2004) Generation of Pax2-Cre mice by modification of a Pax2 bacterial artificial chromosome. Genesis 38: 195-199.
44. Grote D, Boualia SK, Souabni A, Merkel C, Chi X, et al. (2008) Gata3 Acts Downstream of beta-Catenin Signaling to Prevent Ectopic Metanephric Kidney Induction. Plos Genetics 4.
45. Pandolfi PP, Roth ME, Karis A, Leonard MW, Dzierzak E, et al. (1995) Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nature Genetics 11: 40-44.
46. Duncan J, Kersigo J, Gray B, Fritzsch B (2011) Combining Lipophilic dye, in situ Hybridization, Immunohistochemistry, and Histology. J Vis Exp: e2451.
47. Fritzsch B, Muirhead KA, Feng F, Gray BD, Ohlsson-Wilhelm BM, (2005) Diffusion and imaging properties of three new lipophilic tracers, NeuroVue Maroon, NeuroVue Red and NeuroVue Green and their use for double and triple labeling of neuronal profile. Brain Research Bulletin 66: 249-258.
48. Maklad A, Kamel S, Wong E, Fritzsch B, (2010) Developmentand organization of polarity-specific segregation of primary vestibular afferent fibers in mice. Cell and Tissue Research 340: 303-321.
49. Simmons D, Duncan J, Caprona DC, Fritzsch B (2011) Developmentof the Inner Ear Efferent System. Auditory and Vestibular Efferents.New York:Springer pp. 187-216.
50. Bustin SA, Beaulieu JF, Huggett J, Jaggi R, Kibenge FS, et al. (2010) MIQE precis: Practical implementation of minimum standard guidelines for fluorescence-based quantitative real-time PCR experiments. BMC Mol Biol 11: 74.
51. Kopecky BJ, Duncan JS, Elliott KL, Fritzsch B, (2012) Three-dimensional reconstructions from optical sections of thick mouse inner ears using confocal microscopy. J Microsc 248: 292-298.
52. Kopecky B, Johnson S, Schmitz H, Santi P, Fritzsch B, (2012) Scanning thin-sheet laser imaging microscopy elucidates details on mouse ear development. Dev Dyn 241: 465-480.
53. Grote D, Souabni A, Busslinger M, Bouchard M, (2006) Pax 2/8-regulated Gata-3 expression is necessary for morphogenesis and guidance of the nephric duct in the developing kidney. DevelopmentCambridge, England. 133: 53-61.
54. Yang T, Kersigo J, Jahan I, Pan N, Fritzsch B, (2011) The molecular basis of making spiral ganglion neurons and connecting them to hair cells of the organ of Corti. Hear Res 278: 21-33.
55. Ma Q, Anderson DJ, Fritzsch B, (2000) Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. Journal of the Association for Research in Otolaryngology: JARO 1: 129-143.
56. 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.
57. 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. Development138: 735-744.
58. 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. Development134: 2369-2378.
59. Chang W, Lin Z, Kulessa H, Hebert J, Hogan BL, et al. (2008) Bmp4 is essential for the formation of the vestibular apparatus that detects angular head movements. PLoS Genet 4: e1000050.
60. 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. Journal of Neuroscience 30: 15044-15051.
61. Groves AK, Fekete DM, (2012) Shaping sound in space: the regulation of inner ear patterning. Development139: 245-257.
62. Lillevali K, Haugas M, Matilainen T, Pussinen C, Karis A, et al. (2006) Gata3 is required for early morphogenesis and Fgf10 expression during otic development. Mechanisms of Development123: 415-429.
63. Fischer M, Kaech S, Wagner U, Brinkhaus H, Matus A, (2000) Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat Neurosci 3: 887-894.
64. Zou D, Erickson C, Kim EH, Jin D, Fritzsch B, et al. (2008) Eya1 gene dosage critically affects the development of sensory epithelia in the mammalian inner ear. Human Molecular Genetics 17: 3340-3356.
65. Burton Q, Cole LK, Mulheisen M, Chang W, Wu DK, (2004) The role of Pax2 in mouse inner ear development. Developmental Biology 272: 161-175.
66. Moreno-Pelayo MA, Goodyear RJ, Mencia A, Modamio-Hoybjor S, Legan PK, et al. (2008) Characterization of a spontaneous, recessive, missense mutation arising in the Tecta gene. J Assoc Res Otolaryngol 9: 202-214.
67. Chai R, Xia A, Wang T, Jan TA, Hayashi T, et al. (2011) Dynamic expression of Lgr5, a Wnt target gene, in the developing and mature mouse cochlea. J Assoc Res Otolaryngol 12: 455-469.
68. Kersigo J, D'Angelo A, Gray BD, Soukup GA, Fritzsch B, (2011) The role of sensory organs and the forebrain for the development of the craniofacial shape as revealed by Foxg1-cre-mediated microRNA loss. Genesis 49: 326-341.
69. Soukup GA, Fritzsch B, Pierce ML, Weston MD, Jahan I, et al. (2009) Residual microRNA expression dictates the extent of inner ear development in conditional Dicer knockout mice. Developmental Biology 328: 328-341.
70. Karis A, Pata I, van Doorninck JH, Grosveld F, de Zeeuw CI, et al. (2001) Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. J Comp Neurol 429: 615-630.
71. Jahan I, Kersigo J, Pan N, Fritzsch B, (2010) Neurod1 regulates survival and formation of connections in mouse ear and brain. Cell Tissue Res 341: 95-110.
72. Lanford PJ, Shailam R, Norton CR, Gridley T, Kelley MW, (2000) Expression of Math1 and HES5 in the cochleae of wildtype and Jag2 mutant mice. J Assoc Res Otolaryngol 1: 161-171.
73. 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.
74. Ramain P, Khechumian R, Khechumian K, Arbogast N, Ackermann C, et al. (2000) Interactions between chip and the achaete/scute-daughterless heterodimers are required for pannier-driven proneural patterning. Mol Cell 6: 781-790.
75. Home P, Ray S, Dutta D, Bronshteyn I, Larson M, et al. (2009) GATA3 is selectively expressed in the trophectoderm of peri-implantation embryo and directly regulates Cdx2 gene expression. J Biol Chem 284: 28729-28737.
76. Yamashita M, Ukai-Tadenuma M, Kimura M, Omori M, Inami M, et al. (2002) Identification of a conserved GATA3 response element upstream proximal from the interleukin-13 gene locus. J Biol Chem 277: 42399-42408.
77. Alvarado DM, Veile R, Speck J, Warchol M, Lovett M, (2009) Downstream targets of GATA3 in the vestibular sensory organs of the inner ear. Dev Dyn 238: 3093-3102.
78. Milo M, Cacciabue-Rivolta D, Kneebone A, Van Doorninck H, Johnson C, et al. (2009) Genomic analysis of the function of the transcription factor gata3 during development of the mammalian inner ear. PLoS One 4: e7144.
79. Camarero G, Villar MA, Contreras J, Fernandez-Moreno C, Pichel JG, et al. (2002) Cochlear abnormalities in insulin-like growth factor-1 mouse mutants. Hear Res 170: 2-11.
80. Camarero G, Leon Y, Gorospe I, De Pablo F, Alsina B, et al. (2003) Insulin-like growth factor 1 is required for survival of transit-amplifying neuroblasts and differentiation of otic neurons. Dev Biol 262: 242-253.
81. Ruben RJ (1967) Developmentof the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Oto-Laryngologica: Suppl 220:221-244.
82. Kopecky B, Santi P, Johnson S, Schmitz H, Fritzsch B, (2011) Conditional deletion of N-Myc disrupts neurosensory and non-sensory development of the ear. Developmental Dynamics 240: 1373-1390.
83. 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.
84. 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. Developmental Biology 372: 68-80.
85. Richardson GP, Lukashkin AN, Russell IJ, (2008) The tectorial membrane: one slice of a complex cochlear sandwich. Curr Opin Otolaryngol Head Neck Surg 16: 458-464.
86. Chang W, Brigande JV, Fekete DM, Wu DK, (2004) The development of semicircular canals in the inner ear: role of FGFs in sensory cristae. Development131: 4201-4211.
87. Pirvola U, Zhang X, Mantela J, Ornitz DM, Ylikoski J, (2004) Fgf9 signaling regulates inner ear morphogenesis through epithelial-mesenchymal interactions. Developmental Biology 273: 350-360.
88. Bok J, Chang W, Wu DK, (2007) Patterning and morphogenesis of the vertebrate inner ear. International Journal of Developmental Biology 51: 521-533.
89. Fritzsch B, Signore M, Simeone A, (2001) Otx1 null mutant mice show partial segregation of sensory epithelia comparable to lamprey ears. Dev Genes Evol 211: 388-396.
90. Fritzsch B, Pan N, Jahan I, Duncan JS, Kopecky BJ, et al. (2013) Evolution and development of the tetrapod auditory system: an organ of Corti-centric perspective. Evolution & Development15: 63-79.
91. Appler JM, Lu CC, Druckenbrod NR, Yu WM, Koundakjian EJ, et al. (2013) Gata3 is a critical regulator of cochlear wiring. J Neurosci 33: 3679-3691.