GATA3 controls the specification of prosensory domain and neuronal survival in the mouse cochlea

Human Molecular Genetics

Volumn 22, Issue 18, 2013, Pages 3609-3623

  Luo, Xiong jian ^a,b   Deng, Min ^b   Xie, Xiaoling ^b   Huang, Liang ^c,d,e   Wang, Hui ^f   Jiang, Lichun ^f   Liang, Guoqing ^a   Hu, Fang ^c   Tieu, Roger ^b   Chen, Rui ^f   Gan, Lin ^a,b  

^a HANGZHOU NORMAL UNIVERSITY   (China)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c NANCHANG UNIVERSITY   (China)

^d Jiangxi Provincial People's Hospital   (China)

^e GANNAN MEDICAL UNIVERSITY   (China)

^f BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR GATA 3;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL SURVIVAL; COCHLEA; COCHLEA DUCT; DEVELOPMENTAL DISORDER; GANGLION; HAIR CELL; HDR SYNDROME; HYPOPARATHYROIDISM; KIDNEY DISEASE; MORPHOGENESIS; MOUSE; NERVE CELL; NEURONAL SURVIVAL; NONHUMAN; PERCEPTION DEAFNESS; PRIORITY JOURNAL; SENSE ORGAN;

ANIMALS; APOPTOSIS; COCHLEAR DUCT; DISEASE MODELS, ANIMAL; EAR, INNER; GATA3 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAIR CELLS, AUDITORY; HEARING LOSS, SENSORINEURAL; HUMANS; HYPOPARATHYROIDISM; MICE; MICE, KNOCKOUT; NEPHROSIS; SENSORY RECEPTOR CELLS; SPIRAL GANGLION;

EID: 84882971210     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt212     Document Type: Article

References (55)

1. Anagnostopoulos, A.V. (2002) A compendium of mouse knockouts with inner ear defects. Trends Genet., 18, 499.
2. Bermingham, N.A., Hassan, B.A., Price, S.D., Vollrath, M.A., Ben-Arie, N., Eatock, R.A., Bellen, H.J., Lysakowski, A. and Zoghbi, H.Y. (1999) Math1: an essential gene for the generation of inner ear hair cells. Science, 284, 1837-1841.
3. Kiernan, A.E., Pelling, A.L., Leung, K.K., Tang, A.S., Bell, D.M., Tease, C., Lovell-Badge, R., Steel, K.P. and Cheah, K.S. (2005) Sox2 is required for sensory organ development in the mammalian inner ear. Nature, 434, 1031-1035.
4. Torres, M., Gomez-Pardo, E. and Gruss, P. (1996) Pax2 contributes to inner ear patterning and optic nerve trajectory. Development, 122, 3381-3391.
5. Xiang, M., Gan, L., Li, D., Chen, Z.Y., Zhou, L., O'Malley, B.W. Jr, Klein, W. and Nathans, J. (1997) Essential role of POU-domain factor Brn-3c in auditory and vestibular hair cell development. Proc. Natl Acad. Sci. USA, 94, 9445-9450.
6. Xiang, M., Maklad, A., Pirvola, U. and Fritzsch, B. (2003) Brn3c null mutant mice show long-term, incomplete retention of some afferent inner ear innervation. BMC Neurosci., 4, 2.
7. Chen, P., Johnson, J.E., Zoghbi, H.Y. and 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.
8. Kim, W.Y., Fritzsch, B., Serls, A., Bakel, L.A., Huang, E.J., Reichardt, L.F., Barth, D.S. and Lee, J.E. (2001) NeuroD-null mice are deaf due to a severe loss of the inner ear sensory neurons during development. Development, 128, 417-426.
9. Puligilla, C., Dabdoub, A., Brenowitz, S.D. and Kelley, M.W. (2010) Sox2 induces neuronal formation in the developing mammalian cochlea. J. Neurosci., 30, 714-722.
10. Patient, R.K. and McGhee, J.D. (2002) The GATA family (vertebrates and invertebrates). Curr. Opin. Genet. Dev., 12, 416-422.
11. Van Esch, H., Groenen, P., Nesbit, M.A., Schuffenhauer, S., Lichtner, P., Vanderlinden, G., Harding, B., Beetz, R., Bilous, R.W., Holdaway, I. et al. (2000) GATA3 haplo-insufficiency causes human HDR syndrome. Nature, 406, 419-422.
12. Van Esch, H. and Devriendt, K. (2001) Transcription factor GATA3 and the human HDR syndrome. Cell. Mol. Life Sci., 58, 1296-1300.
13. Grote, D., Souabni, A., Busslinger, M. and Bouchard, M. (2006) Pax 2/8-regulated Gata 3 expression is necessary for morphogenesis and guidance of the nephric duct in the developing kidney. Development, 133, 53-61.
14. Grigorieva, I.V., Mirczuk, S., Gaynor, K.U., Nesbit, M.A., Grigorieva, E.F., Wei, Q., Ali, A., Fairclough, R.J., Stacey, J.M., Stechman, M.J. et al. (2010) Gata3-deficient mice develop parathyroid abnormalities due to dysregulation of the parathyroid-specific transcription factor Gcm2. J. Clin. Invest., 120, 2144-2155.
15. Rivolta, M.N. and Holley, M.C.(1998)GATA3is downregulated during hair cell differentiation in the mouse cochlea. J. Neurocytol., 27, 637-647.
16. Karis, A., Pata, I., van Doorninck, J.H., Grosveld, F., de Zeeuw, C.I., de Caprona, D. and Fritzsch, B. (2001) Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. J. Comp. Neurol., 429, 615-630.
17. Lawoko-Kerali, G., Rivolta, M.N. and Holley, M. (2002) Expression of the transcription factors GATA3 and Pax2 during development of the mammalian inner ear. J. Comp. Neurol., 442, 378-391.
18. Rivolta, M.N., Halsall, A., Johnson, C.M., Tones, M.A. and Holley, M.C. (2002) Transcript profiling of functionally related groups of genes during conditional differentiation of a mammalian cochlear hair cell line. Genome Res., 12, 1091-1099.
19. Hawkins, R.D., Bashiardes, S., Helms, C.A., Hu, L., Saccone, N.L., Warchol, M.E. and Lovett, M. (2003) Gene expression differences in quiescent versus regenerating hair cells of avian sensory epithelia: implications forhumanhearing and balance disorders. Hum. Mol. Genet., 12, 1261-1272.
20. Lawoko-Kerali, G., Rivolta, M.N., Lawlor, P., Cacciabue-Rivolta, D.I., Langton-Hewer, C., van Doorninck, J.H. and Holley, M.C. (2004) GATA3 andNeuroDdistinguish auditory and vestibular neurons during development of the mammalian inner ear. Mech. Dev., 121, 287-299.
21. van der Wees, J., van Looij, M.A., de Ruiter, M.M., Elias, H., van der Burg, H., Liem, S.S., Kurek, D., Engel, J.D., Karis, A., van Zanten, B.G. et al. (2004) Hearing loss following Gata3 haploinsufficiency is caused by cochlear disorder. Neurobiol. Dis., 16, 169-178.
22. Lillevali, K., Matilainen, T., Karis, A. and Salminen, M. (2004) Partially overlapping expression of Gata2 and Gata3 during inner ear development. Dev. Dyn., 231, 775-781.
23. van Looij, M.A., van der Burg, H., van der Giessen, R.S., de Ruiter, M.M., van der Wees, J., van Doorninck, J.H., De Zeeuw, C.I. and van Zanten, G.A. (2005) GATA3 haploinsufficiency causes a rapid deterioration of distortion product otoacoustic emissions(DPOAEs) in mice. Neurobiol. Dis., 20, 890-897.
24. Lillevali, K., Haugas, M., Matilainen, T., Pussinen, C., Karis, A. and Salminen, M. (2006) Gata3 is required for early morphogenesis and Fgf10 expression during otic development. Mech. Dev., 123, 415-429.
25. Lu, C.C., Appler, J.M., Houseman, E.A. and Goodrich, L.V. (2011) Developmental profiling of spiral ganglion neurons reveals insights into auditory circuit assembly. J. Neurosci., 31, 10903-10918.
26. Pandolfi, P.P., Roth, M.E., Karis, A., Leonard, M.W., Dzierzak, E., Grosveld, F.G., Engel, J.D. and Lindenbaum, M.H. (1995) Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat. Genet., 11, 40-44.
27. Haugas, M., Lillevali, K. and Salminen, M. (2012) Defects in sensory organ morphogenesis and generation of cochlear hair cells in Gata3-deficient mouse embryos. Hear. Res., 283, 151-161.
28. Kelley, M.W. (2006) Regulation of cell fate in the sensory epithelia of the inner ear. Nat. Rev. Neurosci., 7, 837-849.
29. Morsli, H., Choo, D., Ryan, A., Johnson, R. and Wu, D.K. (1998) Development of the mouse inner ear and origin of its sensory organs. J. Neurosci., 18, 3327-3335.
30. Radde-Gallwitz, K., Pan, L., Gan, L., Lin, X., Segil, N. and Chen, P. (2004) Expression of Islet1 marks the sensory and neuronal lineages in the mammalian inner ear. J. Comp. Neurol., 477, 412-421.
31. Ohyama, T. and Groves, A.K. (2004) Generation of Pax2-Cre mice by modification of a Pax2 bacterial artificial chromosome. Genesis, 38, 195-199.
32. Ohyama, T., Basch, M.L., Mishina, Y., Lyons, K.M., Segil, N. and Groves, A.K. (2010) BMP signaling is necessary for patterning the sensory and nonsensory regions of the developing mammalian cochlea. J. Neurosci., 30, 15044-15051.
33. Dabdoub, A., Puligilla, C., Jones, J.M., Fritzsch, B., Cheah, K.S., Pevny, L.H. and Kelley, M.W. (2008) Sox2 signaling in prosensory domain specification and subsequent hair cell differentiation in the developing cochlea. Proc. Natl Acad. Sci. USA, 105, 18396-18401.
34. Smith, R.J., Bale, J.F. Jr and White, K.R. (2005) Sensorineural hearing loss in children. Lancet, 365, 879-890.
35. Muroya, K., Hasegawa, T., Ito, Y., Nagai, T., Isotani, H., Iwata, Y., Yamamoto, K., Fujimoto, S., Seishu, S., Fukushima, Y. et al. (2001)GATA3 abnormalities and the phenotypic spectrum of HDR syndrome. J. Med. Genet., 38, 374-380.
36. Fukami, M., Muroya, K., Miyake, T., Iso, M., Kato, F., Yokoi, H., Suzuki, Y., Tsubouchi, K., Nakagomi, Y., Kikuchi, N. et al. (2011) GATA3 abnormalities in six patients with HDR syndrome. Endocr. J., 58, 117-121.
37. Ralston, A., Cox, B.J., Nishioka, N., Sasaki, H., Chea, E., Rugg-Gunn, P., Guo, G., Robson, P., Draper, J.S. and Rossant, J. (2010) Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development, 137, 395-403.
38. Economou, A., Datta, P., Georgiadis, V., Cadot, S., Frenz, D. and Maconochie, M.(2013) Gata3 directly regulates early inner ear expression of Fgf10. Dev. Biol., 374, 210-222.
39. Pirvola, U., Ylikoski, J., Trokovic, R., Hebert, J.M., McConnell, S.K. and Partanen, J. (2002) FGFR1 is required for the development of the auditory sensory epithelium. Neuron, 35, 671-680.
40. Jacques, B.E., Montcouquiol, M.E., Layman, E.M., Lewandoski, M. and Kelley, M.W. (2007) Fgf8 induces pillar cell fate and regulates cellular patterning in the mammalian cochlea. Development, 134, 3021-3029.
41. Hatch, E.P., Noyes, C.A., Wang, X., Wright, T.J. and Mansour, S.L. (2007) Fgf3 is required for dorsal patterning and morphogenesis of the inner ear epithelium. Development, 134, 3615-3625.
42. Zelarayan, L.C., Vendrell, V., Alvarez, Y., Dominguez-Frutos, E., Theil, T., Alonso, M.T., Maconochie, M. and Schimmang, T. (2007) Differential requirements for FGF3, FGF8 and FGF10 during inner ear development. Dev. Biol., 308, 379-391.
43. Ladher, R.K., Wright, T.J., Moon, A.M., Mansour, S.L. and Schoenwolf, G.C. (2005) FGF8 initiates inner ear induction in chick and mouse. Genes Dev., 19, 603-613.
44. Alvarez, Y., Alonso, M.T., Vendrell, V., Zelarayan, L.C., Chamero, P., Theil, T., Bosl, M.R., Kato, S., Maconochie, M., Riethmacher, D. et al. (2003) Requirements for FGF3 and FGF10 during inner ear formation. Development, 130, 6329-6338.
45. Wright, T.J. and Mansour, S.L. (2003) Fgf3 and Fgf10 are required formouse otic placode induction. Development, 130, 3379-3390.
46. Pauley, S., Wright, T.J., Pirvola, U., Ornitz, D., Beisel, K. and Fritzsch, B. (2003) Expression and function of FGF10 in mammalian inner ear development. Dev. Dyn., 227, 203-215.
47. Rusznak, Z. and Szucs, G. (2009) Spiral ganglion neurones: an overview of morphology, firing behaviour, ionic channels and function. Pflugers Arch., 457, 1303-1325.
48. Zilberstein, Y., Liberman, M.C. and Corfas, G. (2012) Inner hair cells are not required for survival of spiral ganglion neurons in the adult cochlea. J. Neurosci., 32, 405-410.
49. Tsarovina, K., Reiff, T., Stubbusch, J., Kurek, D., Grosveld, F.G., Parlato, R., Schutz, G. and Rohrer, H. (2010) The Gata3 transcription factor is required for the survival of embryonic and adult sympathetic neurons. J. Neurosci., 30, 10833-10843.
50. Martin, S.J., Lennon, S.V., Bonham, A.M. and Cotter, T.G. (1990) Induction of apoptosis (programmed cell death) in human leukemic HL-60 cells by inhibition of RNA or protein synthesis. J. Immunol., 145, 1859-1867.
51. George, S.H., Gertsenstein, M., Vintersten, K., Korets-Smith, E.,Murphy, J., Stevens, M.E., Haigh, J.J. and Nagy, A. (2007) Developmental and adult phenotyping directly from mutant embryonic stem cells. Proc. Natl Acad. Sci. USA, 104, 4455-4460.
52. Ding, Q., Chen, H., Xie, X., Libby, R.T., Tian, N. and Gan, L. (2009) BARHL2 differentially regulates the development of retinal amacrine and ganglion neurons. J. Neurosci., 29, 3992-4003.
53. Deng, M., Pan, L., Xie, X. and Gan, L. (2010) Requirement for Lmo4 in the vestibular morphogenesis of mouse inner ear. Dev. Biol., 338, 38-49.
54. Luo, X.J., Li, M., Huang, L., Nho, K., Deng, M., Chen, Q., Weinberger, D.R., Vasquez, A.A., Rijpkema, M., Mattay, V.S. et al.. (2012) The interleukin 3 gene (IL3) contributes to human brain volume variation by regulating proliferation and survival of neural progenitors. PLoS ONE, 7, e50375.
55. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol., 3, RESEARCH0034.