Her9 represses neurogenic fate downstream of Tbx1 and retinoic acid signaling in the inner ear

Development

Volumn 138, Issue 3, 2011, Pages 397-408

  Radosevic, Marija ^a   Robert Moreno, Àlex ^a   Coolen, Marion ^b   Bally Cuif, Laure ^b   Alsina, Berta ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b CNRS   (France)

Author keywords

HES; Inner ear; Neurogenesis; Proneural; Retinoic acid (RA) signaling; Sensory organs; Tbx1; Zebrafish

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; RETINOIC ACID; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HER9; TRANSCRIPTION FACTOR TBX1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; EMBRYO; GENE; GENE FUNCTION; GENETICS; HER9 GENE; INNER EAR; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL PROLIFERATION; EAR, INNER; EMBRYO, NONMAMMALIAN; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; T-BOX DOMAIN PROTEINS; TRETINOIN; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; ERINACEIDAE;

EID: 78751526821     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.056093     Document Type: Article

References (95)

1. Abello, G., Khatri, S., Giraldez, F. and Alsina, B. (2007). Early regionalization of the otic placode and its regulation by the Notch signaling pathway. Mech. Dev. 124, 631-645.
2. Abello, G., Khatri, S., Radosevic, M., Scotting, P. J., Giraldez, F. and Alsina, B. (2010). Independent regulation of Sox3 and Lmx1b by FGF and BMP signaling influences the neurogenic and non-neurogenic domains in the chick otic placode. Dev. Biol. 339, 166-178.
3. Adam, J., Myat, A., Le Roux, I., Eddison, M., Henrique, D., Ish-Horowicz, D. and Lewis, J. (1998). Cell fate choices and the expression of Notch, Delta and Serrate homologues in the chick inner ear: parallels with Drosophila sense-organ development. Development 125, 4645-4654.
4. Alsina, B., Abello, G., Ulloa, E., Henrique, D., Pujades, C. and Giraldez, F. (2004). FGF signaling is required for determination of otic neuroblasts in the chick embryo. Dev. Biol. 267, 119-134.
5. Amoyel, M., Cheng, Y. C., Jiang, Y. J. and Wilkinson, D. G. (2005). Wnt1 regulates neurogenesis and mediates lateral inhibition of boundary cell specification in the zebrafish hindbrain. Development 132, 775-785.
6. Andermann, P., Ungos, J. and Raible, D. W. (2002). Neurogenin1 defines zebrafish cranial sensory ganglia precursors. Dev. Biol. 251, 45-58.
7. Artavanis-Tsakonas, S., Rand, M. D. and Lake, R. J. (1999). Notch signaling: cell fate control and signal integration in development. Science 5415, 770-776.
8. Bae, Y. K., Shimizu, T. and Hibi, M. (2005). Patterning of proneuronal and inter-proneuronal domains by hairy-and enhancer of split-related genes in zebrafish neuroectoderm. Development 132, 1375-1385.
9. Baek, J. H., Hatakeyama, J., Sakamoto, S., Ohtsuka, T. and Kageyama, R. (2006). Persistent and high levels of Hes1 expression regulate boundary formation in the developing central nervous system. Development 133, 2467-2476.
10. Begemann, G., Schilling, T. F., Rauch, G. J., Geisler, R. and Ingham, P. W. (2001). The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 128, 3081-3094.
11. 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.
12. Bok, J., Bronner-Fraser, M. and Wu, D. K. (2005). Role of the hindbrain in dorsoventral but not anteroposterior axial specification of the inner ear. Development 132, 2115-2124.
13. Brend, T. and Holley, S. A. (2009). Expression of the oscillating gene her1 is directly regulated by Hairy/Enhancer of Split, T-box, and Suppressor of Hairless proteins in the zebrafish segmentation clock. Dev. Dyn. 238, 2745-2759.
14. Campos-Ortega, J. A. (1993). Mechanisms of early neurogenesis in Drosophila melanogaster. J. Neurobiol. 24, 1305-1327.
15. Campos-Ortega, J. A. and Jan, Y. N. (1991). Genetic and molecular bases of neurogenesis in Drosophila melanogaster. Annu. Rev. Neurosci. 14, 399-420.
16. Curry, C. L., Reed, L. L., Nickoloff, B. J., Miele, L. and Foreman, K. E. (2006). Notch-independent regulation of Hes-1 expression by c-Jun N-terminal kinase signaling in human endothelial cells. Lab. Invest. 86, 842-852.
17. Diez del Corral, R., Olivera-Martinez, I., Goriely, A., Gale, E., Maden, M. and Storey, K. (2003). Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40, 65-79.
18. Dupe, V., Ghyselinck, N. B., Wendling, O., Chambon, P. and Mark, M. (1999). Key roles of retinoic acid receptors alpha and beta in the patterning of the caudal hindbrain, pharyngeal arches and otocyst in the mouse. Development 126, 5051-5059.
19. Fischer, A. and Gessler, M. (2007). Delta-Notch-and then? Protein interactions and proposed modes of repression by Hes and Hey bHLH factors. Nucleic Acids Res. 35, 4583-4596.
20. Gale, E., Zile, M. and Maden, M. (1999). Hindbrain respecification in the retinoid-deficient quail. Mech. Dev. 89, 43-54.
21. Gavalas, A. and Krumlauf, R. (2000). Retinoid signalling and hindbrain patterning. Curr. Opin. Genet. Dev. 10, 380-386.
22. Geling, A., Steiner, H., Willem, M., Bally-Cuif, L. and Haass, C. (2002). A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep. 3, 688-694.
23. Gonzalez-Quevedo, R., Lee, Y., Poss, K. D. and Wilkinson, D. G. (2010). Neuronal regulation of the spatial patterning of neurogenesis. Dev. Cell 18, 136-147.
24. Haddon, C., Mowbray, C., Whitfield, T., Jones, D., Gschmeissner, S. and Lewis, J. (1999). Hair cells without supporting cells: further studies in the ear of the zebrafish mind bomb mutant. J. Neurocytol. 28, 837-850.
25. Hammond, K. L., Loynes, H. E., Folarin, A. A., Smith, J. and Whitfield, T. T. (2003). Hedgehog signalling is required for correct anteroposterior patterning of the zebrafish otic vesicle. Development 130, 1403-1417.
26. Hammond, K. L., van Eeden, F. J. and Whitfield, T. T. (2010). Repression of Hedgehog signalling is required for the acquisition of dorsolateral cell fates in the zebrafish otic vesicle. Development 137, 1361-1371.
27. Hans, S. and Westerfield, M. (2007). Changes in retinoic acid signaling alter otic patterning. Development 134, 2449-2458.
28. Hans, S., Scheer, N., Riedl, I., v. Weizsacker, E., Blader, P. and Campos-Ortega, J. A. (2004). her3, a zebrafish member of the hairy-E(spl) family, is repressed by Notch signalling. Development 131, 2957-2969.
29. Imayoshi, I., Shimogori, T., Ohtsuka, T. and Kageyama, R. (2008). Hes genes and neurogenin regulate non-neural versus neural fate specification in the dorsal telencephalic midline. Development 135, 2531-2541.
30. Imayoshi, I., Sakamoto, M., Yamaguchi, M., Mori, K. and Kageyama, R. (2010). Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J. Neurosci. 30, 3489-3498.
31. Ingram, W. J., McCue, K. I., Tran, T. H., Hallahan, A. R. and Wainwright, B. J. (2008). Sonic Hedgehog regulates Hes1 through a novel mechanism that is independent of canonical Notch pathway signalling. Oncogene 27, 1489-1500.
32. Ishibashi, M., Moriyoshi, K., Sasai, Y., Shiota, K., Nakanishi, S. and Kageyama, R. (1994). Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J. 13, 1799-1805.
33. Ishiko, E., Matsumura, I., Ezoe, S., Gale, K., Ishiko, J., Satoh, Y., Tanaka, H., Shibayama, H., Mizuki, M., Era, T. et al. (2005). Notch signals inhibit the development of erythroid/megakaryocytic cells by suppressing GATA-1 activity through the induction of HES1. J. Biol. Chem. 280, 4929-4939.
34. Itoh, M. and Chitnis, A. B. (2001). Expression of proneural and neurogenic genes in the zebrafish lateral line primordium correlates with selection of hair cell fate in neuromasts. Mech. Dev. 102, 263-266.
35. Kageyama, R., Ohtsuka, T., Hatakeyama, J. and Ohsawa, R. (2005). Roles of bHLH genes in neural stem cell differentiation. Exp. Cell Res. 306, 343-348.
36. Kageyama, R., Ohtsuka, T. and Kobayashi, T. (2007). The Hes gene family: repressors and oscillators that orchestrate embryogenesis. Development 134, 1243-1251.
37. Kageyama, R., Ohtsuka, T. and Kobayashi, T. (2008). Roles of Hes genes in neural development. Dev. Growth Differ. 50, S97-S103.
38. Kiernan, A. E., Ahituv, N., Fuchs, H., Balling, R., Avraham, K. B., Steel, K. P. and Hrabe de Angelis, M. (2001). The Notch ligand Jagged1 is required for inner ear sensory development. Proc. Natl. Acad. Sci. USA 98, 3873-3878.
39. 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.
40. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
41. Kubo, F. and Nakagawa, S. (2009). Hairy1 acts as a node downstream of Wnt signaling to maintain retinal stem cell-like progenitor cells in the chick ciliary marginal zone. Development 136, 1823-1833.
42. Kwak, S. J., Phillips, B. T., Heck, R. and Riley, B. B. (2002). An expanded domain of fgf3 expression in the hindbrain of zebrafish valentino mutants results in mis-patterning of the otic vesicle. Development 129, 5279-5287.
43. Lanford, P. J., Lan, Y., Jiang, R., Lindsell, C., Weinmaster, G., Gridley, T. and Kelley, M. W. (1999). Notch signalling pathway mediates hair cell development in mammalian cochlea. Nat. Genet. 21, 289-292.
44. Lanford, P. J., Shailam, R., Norton, C. R., Gridley, T. and Kelley, M. W. (2000). Expression of Math1 and HES5 in the cochleae of wildtype and Jag2 mutant mice. J. Assoc. Res. Otolaryngol. 1, 161-171.
45. Latimer, A. J., Shin, J. and Appel, B. (2005). Her9 promotes floor plate development in zebrafish. Dev. Dyn. 232, 1098-1104.
46. Leger, S. and Brand, M. (2002). Fgf8 and Fgf3 are required for zebrafish ear placode induction, maintenance and inner ear patterning. Mech. Dev. 119, 91-108.
47. Leve, C., Gajewski, M., Rohr, K. B. and Tautz, D. (2001). Homologues of chairy1 (her9) and lunatic fringe in zebrafish are expressed in the developing central nervous system, but not in the presomitic mesoderm. Dev. Genes Evol. 211, 493-500.
48. Linville, A., Gumusaneli, E., Chandraratna, R. A. and Schilling, T. F. (2004). Independent roles for retinoic acid in segmentation and neuronal differentiation in the zebrafish hindbrain. Dev. Biol. 270, 186-199.
49. Linville, A., Radtke, K., Waxman, J. S., Yelon, D. and Schilling, T. F. (2009). Combinatorial roles for zebrafish retinoic acid receptors in the hindbrain, limbs and pharyngeal arches. Dev. Biol. 325, 60-70.
50. Ma, Q., Anderson, D. J. and Fritzsch, B. (2000). Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. J. Assoc. Res. Otolaryngol. 1, 129-143.
51. Maden, M. (2007). Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat. Rev. Neurosci. 8, 755-765.
52. Martin, K. and Groves, A. (2006). Competence of cranial ectoderm to respond to Fgf signaling suggests a two-step model of otic placode induction. Development 133, 877-887.
53. Millimaki, B. B., Sweet, E. M., Dhason, M. S. and Riley, B. B. (2007). Zebrafish atoh1 genes: classic proneural activity in the inner ear and regulation by Fgf and Notch. Development 134, 295-305.
54. Moens, C. B., Yan, Y. L., Appel, B., Force, A. G. and Kimmel, C. B. (1996). Valentino: a zebrafish gene required for normal hindbrain segmentation. Development 122, 3981-3990.
55. Moraes, F., Novoa, A., Jerome-Majewska, L. A., Papaioannou, V. E. and Mallo, M. (2005). Tbx1 is required for proper neural crest migration and to stabilize spatial patterns during middle and inner ear development. Mech. Dev. 126, 199-212.
56. Murata, J., Ohtsuka, T., Tokunaga, A., Nishiike, S., Inohara, H., Okano, H. and Kageyama, R. (2009). Notch-Hes1 pathway contributes to the cochlear prosensory formation potentially through the transcriptional down-regulation of p27Kip1. J. Neurosci. Res. 87, 3521-3534.
57. Niederreither, K., Subbarayan, V., Dolle, P. and Chambon, P. (1999). Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet. 21, 444-448.
58. Niederreither, K., Vermot, J., Schuhbaur, B., Chambon, P. and Dolle, P. (2000). Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development 127, 75-85.
59. Ninkovic, J., Tallafuss, A., Leucht, C., Topczewski, J., Tannhauser, B., Solnica-Krezel, L. and Bally-Cuif, L. (2005). Inhibition of neurogenesis at the zebrafish midbrain-hindbrain boundary by the combined and dose-dependent activity of a new hairy/E(spl) gene pair. Development 132, 75-88.
60. Oxtoby, E. and Jowett, T. (1993). Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acids Res. 21, 1087-1095.
61. Phillips, B. T., Bolding, K. and Riley, B. B. (2001). Zebrafish fgf3 and fgf8 encode redundant functions required for otic placode induction. Dev. Biol. 235, 351-365.
62. Piotrowski, T., Ahn, D. G., Schilling, T. F., Nair, S., Ruvinsky, I., Geisler, R., Rauch, G. J., Haffter, P., Zon, L. I., Zhou, Y. et al. (2003). The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans. Development 130, 5043-5052.
63. Pittman, A. J., Law, M. Y. and Chien, C. B. (2008). Pathfinding in a large vertebrate axon tract: isotypic interactions guide retinotectal axons at multiple choice points. Development 135, 2865-2871.
64. Raft, S., Nowotschin, S., Liao, J. and Morrow, B. E. (2004). Suppression of neural fate and control of inner ear morphogenesis by Tbx1. Development 131, 1801-1812.
65. Riccomagno, M. M., Martinu, L., Mulheisen, M., Wu, D. K. and Epstein, D. J. (2002). Specification of the mammalian cochlea is dependent on Sonic hedgehog. Genes Dev. 16, 2365-2378.
66. Riddle, R. D., Johnson, R. L., Laufer, E. and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416.
67. Romand, R. (2003). The roles of retinoic acid during inner ear development. Curr. Top. Dev. Biol. 57, 261-291.
68. Ross, S. E., Greenberg, M. E. and Stiles, C. D. (2003). Basic helix-loop-helix factors in cortical development. Neuron 39, 13-25.
69. Sang, L., Coller, H. A. and Roberts, J. M. (2008). Control of the reversibility of cellular quiescence by the transcriptional repressor HES1. Science 321, 1095-1100.
70. Sang, L., Roberts, J. M. and Coller, H. A. (2010). Hijacking HES1: how tumors co-opt the anti-differentiation strategies of quiescent cells. Trends Mol. Med. 16, 17-26.
71. Sapede, D. and Pujades, C. (2010). Hedgehog signaling governs the development of otic sensory epithelium and its associated innervation in zebrafish. J. Neurosci. 30, 3612-3623.
72. Sasai, Y., Kageyama, R., Tagawa, Y., Shigemoto, R. and Nakanishi, S. (1992). Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev. 6, 2620-2634.
73. Schneider, R. A., Hu, D., Rubenstein, J. L., Maden, M. and Helms, J. A. (2001). Local retinoid signaling coordinates forebrain and facial morphogenesis by maintaining FGF8 and SHH. Development 128, 2755-2767.
74. Schneider-Maunoury, S. and Pujades, C. (2007). Hindbrain signals in otic regionalization: walk on the wild side. Int. J. Dev. Biol. 51, 495-506.
75. Shiotsugu, J., Katsuyama, Y., Arima, K., Baxter, A., Koide, T., Song, J., Chandraratna, R. A. and Blumberg, B. (2004). Multiple points of interaction between retinoic acid and FGF signaling during embryonic axis formation. Development 131, 2653-2667.
76. Stigloher, C., Chapouton, P., Adolf, B. and Bally-Cuif, L. (2008). Identification of neural progenitor pools by E(Spl) factors in the embryonic and adult brain. Brain Res. Bull. 75, 266-273.
77. Stockhausen, M. T., Sjolund, J. and Axelson, H. (2005). Regulation of the Notch target gene Hes-1 by TGFalpha induced Ras/MAPK signaling in human neuroblastoma cells. Exp. Cell Res. 310, 218-228.
78. Takke, C., Dornseifer, P., v. Weizsacker, E. and Campos-Ortega, J. A. (1999). her4, a zebrafish homologue of the Drosophila neurogenic gene E(spl), is a target of NOTCH signalling. Development 126, 1811-1821.
79. Thisse, B., Heyer, V., Lux, A., Alunni, V., Degrave, A., Seiliez, I., Kirchner, J., Parkhill, J. P. and Thisse, C. (2004). Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. Methods Cell Biol. 77, 505-519.
80. Vermot, J., Niederreither, K., Garnier, J. M., Chambon, P. and Dolle, P. (2003). Decreased embryonic retinoic acid synthesis results in a DiGeorge syndrome phenotype in newborn mice. Proc. Natl. Acad. Sci. USA 100, 1763-1768.
81. Vitelli, F., Viola, A., Morishima, M., Pramparo, T., Baldini, A. and Lindsay, E. (2003). TBX1 is required for inner ear morphogenesis. Hum. Mol. Genet. 12, 2041-2048.
82. Wang, X., Emelyanov, A., Korzh, V. and Gong, Z. (2003). Zebrafish atonal homologue zath3 is expressed during neurogenesis in embryonic development. Dev. Dyn. 227, 587-592.
83. Waxman, J. S., Keegan, B. R., Roberts, R. W., Poss, K. D. and Yelon, D. (2008). Hoxb5b acts downstream of retinoic acid signaling in the forelimb field to restrict heart field potential in zebrafish. Dev. Cell 15, 923-934.
84. White, J. C., Shankar, V. N., Highland, M., Epstein, M. L., DeLuca, H. F. and Clagett-Dame, M. (1998). Defects in embryonic hindbrain development and fetal resorption resulting from vitamin A deficiency in the rat are prevented by feeding pharmacological levels of all-trans-retinoic acid. Proc. Natl. Acad. Sci. USA 95, 13459-13464.
85. White, J. C., Highland, M., Kaiser, M. and Clagett-Dame, M. (2000). Vitamin A deficiency results in the dose-dependent acquisition of anterior character and shortening of the caudal hindbrain of the rat embryo. Dev. Biol. 220, 263-284.
86. White, R. J., Nie, Q., Lander, A. D. and Schilling, T. F. (2007). Complex regulation of cyp26a1 creates a robust retinoic acid gradient in the zebrafish embryo. PLoS Biol. 5, e304.
87. Whitfield, T. T. and Hammond, K. L. (2007). Axial patterning in the developing vertebrate inner ear. Int. J. Dev. Biol. 51, 507-520.
88. Woods, C., Montcouquiol, M. and Kelley, M. W. (2004). Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat. Neurosci. 7, 1310-1318.
89. Xiao, T., Roeser, T., Staub, W. and Baier, H. (2005). A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection. Development 132, 2955-2967.
90. Xu, H., Viola, A., Zhang, Z., Gerken, C. P., Lindsay-Illingworth, E. A. and Baldini, A. (2007). Tbx1 regulates population, proliferation and cell fate determination of otic epithelial cells. Dev. Biol. 302, 670-682.
91. Yamagishi, H., Maeda, J., Hu, T., McAnally, J., Conway, S. J., Kume, T., Meyers, E. N., Yamagishi, C. and Srivastava, D. (2003). Tbx1 is regulated by tissue-specific forkhead proteins through a common Sonic hedgehog-responsive enhancer. Genes Dev. 17, 269-281.
92. Yoon, K. and Gaiano, N. (2005). Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat. Neurosci. 8, 709-715.
93. Zheng, J. L., Shou, J., Guillemot, F., Kageyama, R. and Gao, W. Q. (2000). Hes1 is a negative regulator of inner ear hair cell differentiation. Development 127, 4551-4560.
94. Zine, A., Van De Water, T. R. and de Ribaupierre, F. (2000). Notch signaling regulates the pattern of auditory hair cell differentiation in mammals. Development 127, 3373-3383.
95. Zine, A., Aubert, A., Qiu, J., Therianos, S., Guillemot, F., Kageyama, R. and de Ribaupierre, F. (2001). Hes1 and Hes5 activities are required for the normal development of the hair cells in the mammalian inner ear. J. Neurosci. 21, 4712-4720.