Lunatic fringe promotes the lateral inhibition of neurogenesis

Development

Volumn 136, Issue 15, 2009, Pages 2523-2533

  Nikolaou, Nikolas ^a   Watanabe Asaka, Tomomi ^a   Gerety, Sebastian ^a   Distel, Martin ^b   Köster, Reinhard W ^b   Wilkinson, David G ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Fringe; Lateral inhibition; Neural progenitors; Neurogenesis; Notch; Zebrafish

Indexed keywords

DROSOPHILA PROTEIN; LUNATIC FRINGE PROTEIN; NOTCH RECEPTOR; PROTEIN LFNG; UNCLASSIFIED DRUG; ZEBRAFISH PROTEIN;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO SEGMENTATION; EXON; FEEDBACK SYSTEM; INTRON; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OOCYTE CLEAVAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UPREGULATION; ZEBRA FISH;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; GLYCOSYLTRANSFERASES; MODELS, BIOLOGICAL; MOSAICISM; NEUROGENESIS; NEURONS; PHENOTYPE; RECEPTORS, NOTCH; RHOMBENCEPHALON; STEM CELLS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; VERTEBRATA;

EID: 69049118162     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.034736     Document Type: Article

References (100)

1. Ahn, D. G., Ruvinsky, I., Oates, A. C., Silver, L. M. and Ho, R. K. (2000). tbx20, a new vertebrate T-box gene expressed in the cranial motor neurons and developing cardiovascular structures in zebrafish. Mech. Dev. 95, 253-258.
2. Allende, M. L. and Weinberg, E. S. (1994). The expression pattern of two zebrafish achaete-scute homolog (ash) genes is altered in the embryonic brain of the cyclops mutant. Dev. Biol. 166, 509-530.
3. 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.
4. Ando, H., Kobayashi, M., Tsubokawa, T., Uyemura, K., Furuta, T. and Okamoto, H. (2005). Lhx2 mediates the activity of Six3 in zebrafish forebrain growth. Dev. Biol. 287, 456-468.
5. Bae, S., Bessho, Y., Hojo, M. and Kageyama, R. (2000). The bHLH gene Hes6, an inhibitor of Hes1, promotes neuronal differentiation. Development 127, 2933-2943.
6. Bae, Y. K., Shimizu, T. and Hibi, M. (2005). Patterning of proneuronal and interproneuronal domains by hairy- and enhancer of split-related genes in zebrafish neuroectoderm. Development 132, 1375-1385.
7. Bai, G., Sheng, N., Xie, Z., Bian, W., Yokota, Y., Benezra, R., Kageyama, R., Guillemot, F. and Jing, N. (2007). Id sustains Hes1 expression to inhibit precocious neurogenesis by releasing negative autoregulation of Hes1. Dev. Cell 13, 283-297.
8. Balciunas, D., Wangensteen, K. J., Wilber, A., Bell, J., Geurts, A., Sivasubbu, S., Wang, X., Hackett, P. B., Largaespada, D. A., McIvor, R. S. et al. (2006). Harnessing a high cargo-capacity transposon for genetic applications in vertebrates. PLoS Genet. 2, e169.
9. Bally-Cuif, L., Dubois, L. and Vincent, A. (1998). Molecular cloning of Zcoe2, the zebrafish homolog of Xenopus Xcoe2 and mouse EBF-2, and its expression during primary neurogenesis. Mech. Dev. 77, 85-90.
10. Batista, M. F., Jacobstein, J. and Lewis, K. E. (2008). Zebrafish V2 cells develop into excitatory CiD and Notch signalling dependent inhibitory VeLD interneurons. Dev. Biol. 322, 263-275.
11. Bierkamp, C. and Campos-Ortega, J. A. (1993). A zebrafish homologue of the Drosophila neurogenic gene Notch and its pattern of transcription during early embryogenesis. Mech. Dev. 43, 87-100.
12. Bingham, S., Chaudhari, S., Vanderlaan, G., Itoh, M., Chitnis, A. and Chandrasekhar, A. (2003). Neurogenic phenotype of mind bomb mutants leads to severe patterning defects in the zebrafish hindbrain. Dev. Dyn. 228, 451-463.
13. Blader, P., Fischer, N., Gradwohl, G., Guillemot, F. and Strahle, U. (1997). The activity of neurogenin1 is controlled by local cues in the zebrafish embryo. Development 124, 4557-4569.
14. Castro, B., Barolo, S., Bailey, A. M. and Posakony, J. W. (2005). Lateral inhibition in proneural clusters: cis-regulatory logic and default repression by Suppressor of Hairless. Development 132, 3333-3344.
15. Castro, D. S., Skowronska-Krawczyk, D., Armant, O., Donaldson, I. J., Parras, C., Hunt, C., Critchley, J. A., Nguyen, L., Gossler, A., Gottgens, B. et al. (2006). Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. Dev. Cell 11, 831-844.
16. Chan, J., Mably, J. D., Serluca, F. C., Chen, J. N., Goldstein, N. B., Thomas, M. C., Cleary, J. A., Brennan, C., Fishman, M. C. and Roberts, T. M. (2001). Morphogenesis of prechordal plate and notochord requires intact Eph/ephrin B signaling. Dev. Biol. 234, 470-482.
17. Chandrasekhar, A., Moens, C. B., Warren, J. T., Jr, Kimmel, C. B. and Kuwada, J. Y. (1997). Development of branchiomotor neurons in zebrafish. Development 124, 2633-2644.
18. Cheng, Y. C., Amoyel, M., Qiu, X., Jiang, Y. J., Xu, Q. and Wilkinson, D. G. (2004). Notch activation regulates the segregation and differentiation of rhombomere boundary cells in the zebrafish hindbrain. Dev. Cell 6, 539-550.
19. Culi, J. and Modolell, J. (1998). Proneural gene self-stimulation in neural precursors: an essential mechanism for sense organ development that is regulated by Notch signaling. Genes Dev. 12, 2036-2047.
20. de Bellard, M., Barembaum, M., Arman, O. and Bronner-Fraser, M. (2007). Lunatic fringe causes expansion and increased neurogenesis of trunk neural tube and neural crest populations. Neuron Glia Biol. 3, 93-103.
21. de Celis, J. F., Garcia-Bellido, A. and Bray, S. J. (1996). Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc. Development 122, 359-369.
22. Del Barrio, M. G., Taveira-Marques, R., Muroyama, Y., Yuk, D. I., Li, S., Wines-Samuelson, M., Shen, J., Smith, H. K., Xiang, M., Rowitch, D. et al. (2007). A regulatory network involving Foxn4, Mash1 and delta-like 4/Notch1 generates V2a and V2b spinal interneurons from a common progenitor pool. Development 134, 3427-3436.
23. Dominguez, M. and de Celis, J. F. (1998). A dorsal/ventral boundary established by Notch controls growth and polarity in the Drosophila eye. Nature 396, 276-278.
24. Dubois, L., Bally-Cuif, L., Crozatier, M., Moreau, J., Paquereau, L. and Vincent, A. (1998). XCoe2, a transcription factor of the Col/ Olf-1/EBF family involved in the specification of primary neurons in Xenopus. Curr. Biol. 8, 199-209.
25. Fryer, C. J., Lamar, E., Turbachova, I., Kintner, C. and Jones, K. A. (2002). Mastermind mediates chromatin-specific transcription and turnover of the Notch enhancer complex. Genes Dev. 16, 1397-1411.
26. Gaiano, N., Nye, J. S. and Fishell, G. (2000). Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26, 395-404.
27. 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.
28. Glittenberg, M., Pitsouli, C., Garvey, C., Delidakis, C. and Bray, S. (2006). Role of conserved intracellular motifs in Serrate signalling, cis-inhibition and endocytosis. EMBO J. 25, 4697-4706.
29. Gray, M., Moens, C. B., Amacher, S. L., Eisen, J. S. and Beattie, C. E. (2001). Zebrafish deadly seven functions in neurogenesis. Dev. Biol. 237, 306-323.
30. Haddon, C., Smithers, L., Schneider-Maunoury, S., Coche, T., Henrique, D. and Lewis, J. (1998). Multiple delta genes and lateral inhibition in zebrafish primary neurogenesis. Development 125, 359-370.
31. Hanneman, E., Trevarrow, B., Metcalfe, W. K., Kimmel, C. B. and Westerfield, M. (1988). Segmental pattern of development of the hindbrain and spinal cord of the zebrafish embryo. Development 103, 49-58.
32. Heitzler, P., Bourouis, M., Ruel, L., Carteret, C. and Simpson, P. (1996). Genes of the Enhancer of split and achaete-scute complexes are required for a regulatory loop between Notch and Delta during lateral signalling in Drosophila. Development 122, 161-171.
33. Holley, S. A., Julich, D., Rauch, G. J., Geisler, R. and Nusslein-Volhard, C. (2002). her1 and the notch pathway function within the oscillator mechanism that regulates zebrafish somitogenesis. Development 129, 1175-1183.
34. Irving, C., Nieto, M. A., DasGupta, R., Charnay, P. and Wilkinson, D. G. (1996). Progressive spatial restriction of Sek-1 and Krox-20 gene expression during hindbrain segmentation. Dev. Biol. 173, 26-38.
35. Ishii, Y., Nakamura, S. and Osumi, N. (2000). Demarcation of early mammalian cortical development by differential expression of fringe genes. Brain Res. Dev. Brain Res. 119, 307-320.
36. Itoh, M., Kim, C. H., Palardy, G., Oda, T., Jiang, Y. J., Maust, D., Yeo, S. Y., Lorick, K., Wright, G. J., Ariza-McNaughton, L. et al. (2003). Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev. Cell 4, 67-82.
37. Jacobsen, T. L., Brennan, K., Arias, A. M. and Muskavitch, M. A. (1998). Cis-interactions between Delta and Notch modulate neurogenic signalling in Drosophila. Development 125, 4531-4540.
38. Jiang, Y. J., Brand, M., Heisenberg, C. P., Beuchle, D., Furutani-Seiki, M., Kelsh, R. N., Warga, R. M., Granato, M., Haffter, P., Hammerschmidt, M. et al. (1996). Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio. Development 123, 205-216.
39. Johnston, S. H., Rauskolb, C., Wilson, R., Prabhakaran, B., Irvine, K. D. and Vogt, T. F. (1997). A family of mammalian Fringe genes implicated in boundary determination and the Notch pathway. Development 124, 2245-2254.
40. Julich, D., Hwee Lim, C., Round, J., Nicolaije, C., Schroeder, J., Davies, A., Geisler, R., Lewis, J., Jiang, Y. J. and Holley, S. A. (2005). beamter/deltaC and the role of Notch ligands in the zebrafish somite segmentation, hindbrain neurogenesis and hypochord differentiation. Dev. Biol. 286, 391-404.
41. Kageyama, R., Ohtsuka, T. and Kobayashi, T. (2007). The Hes gene family: repressors and oscillators that orchestrate embryogenesis. Development 134, 1243-1251.
42. Kageyama, R., Ohtsuka, T., Shimojo, H. and Imayoshi, I. (2008). Dynamic Notch signaling in neural progenitor cells and a revised view of lateral inhibition. Nat. Neurosci. 11, 1247-1251.
43. Kawakami, K., Shima, A. and Kawakami, N. (2000). Identification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineage. Proc. Natl. Acad. Sci. USA 97, 11403-11408.
44. Kim, C. H., Bae, Y. K., Yamanaka, Y., Yamashita, S., Shimizu, T., Fujii, R., Park, H. C., Yeo, S. Y., Huh, T. L., Hibi, M. et al. (1997). Overexpression of neurogenin induces ectopic expression of HuC in zebrafish. Neurosci. Lett. 239, 113-116.
45. Kim, J., Irvine, K. D. and Carroll, S. B. (1995). Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing Drosophila wing. Cell 82, 795-802.
46. 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.
47. Korzh, V., Sleptsova, I., Liao, J., He, J. and Gong, Z. (1998). Expression of zebrafish bHLH genes ngn1 and nrd defines distinct stages of neural differentiation. Dev. Dyn. 213, 92-104.
48. Koyano-Nakagawa, N., Kim, J., Anderson, D. and Kintner, C. (2000). Hes6 acts in a positive feedback loop with the neurogenins to promote neuronal differentiation. Development 127, 4203-4216.
49. Kunisch, M., Haenlin, M. and Campos-Ortega, J. A. (1994). Lateral inhibition mediated by the Drosophila neurogenic gene delta is enhanced by proneural proteins. Proc. Natl. Acad. Sci. USA 91, 10139-10143.
50. Laufer, E., Dahn, R., Orozco, O. E., Yeo, C. Y., Pisenti, J., Henrique, D., Abbott, U. K., Fallon, J. F. and Tabin, C. (1997). Expression of Radical fringe in limb-bud ectoderm regulates apical ectodermal ridge formation. Nature 386, 366-373.
51. 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.
52. Lewis, J. (1998). Notch signalling and the control of cell fate choices in vertebrates. Semin. Cell Dev. Biol. 9, 583-589.
53. Liu, Q., Babb, S. G., Novince, Z. M., Doedens, A. L., Marrs, J. and Raymond, P. A. (2001). Differential expression of cadherin-2 and cadherin-4 in the developing and adult zebrafish visual system. Vis. Neurosci. 18, 923-933.
54. Louvi, A. and Artavanis-Tsakonas, S. (2006). Notch signalling in vertebrate neural development. Nat. Rev. Neurosci. 7, 93-102.
55. Malatesta, P., Hartfuss, E. and Gotz, M. (2000). Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127, 5253-5263.
56. Malatesta, P., Hack, M. A., Hartfuss, E., Kettenmann, H., Klinkert, W., Kirchhoff, F. and Gotz, M. (2003). Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37, 751-764.
57. Martin, S. C., Heinrich, G. and Sandell, J. H. (1998). Sequence and expression of glutamic acid decarboxylase isoforms in the developing zebrafish. J. Comp. Neurol. 396, 253-266.
58. Matsuda, M. and Chitnis, A. B. (2009). Interaction with Notch determines endocytosis of specific Delta ligands in zebrafish neural tissue. Development 136, 197-206.
59. Maves, L., Jackman, W. and Kimmel, C. B. (2002). FGF3 and FGF8 mediate a rhombomere 4 signaling activity in the zebrafish hindbrain. Development 129, 3825-3837.
60. Mendelson, B. (1986). Development of reticulospinal neurons of the zebrafish. I. Time of origin. J. Comp. Neurol. 251, 160-171.
61. Micchelli, C. A. and Blair, S. S. (1999). Dorsoventral lineage restriction in wing imaginal discs requires Notch. Nature 401, 473-476.
62. Micchelli, C. A., Rulifson, E. J. and Blair, S. S. (1997). The function and regulation of cut expression on the wing margin of Drosophila: Notch, Wingless and a dominant negative role for Delta and Serrate. Development 124, 1485-1495.
63. Mikkola, I., Fjose, A., Kuwada, J. Y., Wilson, S., Guddal, P. H. and Krauss, S. (1992). The paired domain-containing nuclear factor pax[b] is expressed in specific commissural interneurons in zebrafish embryos. J. Neurobiol. 23, 933-946.
64. 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.
65. Moloney, D. J., Panin, V. M., Johnston, S. H., Chen, J., Shao, L., Wilson, R., Wang, Y., Stanley, P., Irvine, K. D., Haltiwanger, R. S. et al. (2000). Fringe is a glycosyltransferase that modifies Notch. Nature 406, 369-375.
66. Mumm, J. S., Schroeter, E. H., Saxena, M. T., Griesemer, A., Tian, X., Pan, D. J., Ray, W. J. and Kopan, R. (2000). A ligand-induced extracellular cleavage regulates gamma-secretase-like proteolytic activation of Notch1. Mol. Cell 5, 197-206.
67. Neave, B., Rodaway, A., Wilson, S. W., Patient, R. and Holder, N. (1995). Expression of zebrafish GATA 3 (gta3) during gastrulation and neurulation suggests a role in the specification of cell fate. Mech. Dev. 51, 169-182.
68. Ohtsuka, T., Ishibashi, M., Gradwohl, G., Nakanishi, S., Guillemot, F. and Kageyama, R. (1999). Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J. 18, 2196-2207.
69. Okuda, Y., Yoda, H., Uchikawa, M., Furutani-Seiki, M., Takeda, H., Kondoh, H. and Kamachi, Y. (2006). Comparative genomic and expression analysis of group B1 sox genes in zebrafish indicates their diversification during vertebrate evolution. Dev. Dyn. 235, 811-825.
70. 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.
71. Panin, V. M., Papayannopoulos, V., Wilson, R. and Irvine, K. D. (1997). Fringe modulates Notch-ligand interactions. Nature 387, 908-912.
72. Papayannopoulos, V., Tomlinson, A., Panin, V. M., Rauskolb, C. and Irvine, K. D. (1998). Dorsal-ventral signaling in the Drosophila eye. Science 281, 2031-2034.
73. Park, H. C., Hong, S. K., Kim, H. S., Kim, S. H., Yoon, E. J., Kim, C. H., Miki, N. and Huh, T. L. (2000). Structural comparison of zebrafish Elav/Hu and their differential expressions during neurogenesis. Neurosci. Lett. 279, 81-84.
74. Park, S. H., Yeo, S. Y., Yoo, K. W., Hong, S. K., Lee, S., Rhee, M., Chitnis, A. B. and Kim, C. H. (2003). Zath3, a neural basic helix-loop-helix gene, regulates early neurogenesis in the zebrafish. Biochem. Biophys. Res. Commun. 308, 184-190.
75. Passini, M. A., Kurtzman, A. L., Canger, A. K., Asch, W. S., Wray, G. A., Raymond, P. A. and Schechter, N. (1998). Cloning of zebrafish vsx1: expression of a paired-like homeobox gene during CNS development. Dev. Genet. 23, 128-141.
76. Peng, C. Y., Yajima, H., Burns, C. E., Zon, L. I., Sisodia, S. S., Pfaff, S. L. and Sharma, K. (2007). Notch and MAML signaling drives Scl-dependent interneuron diversity in the spinal cord. Neuron 53, 813-827.
77. Postlethwait, J., Amores, A., Cresko, W., Singer, A. and Yan, Y. L. (2004). Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends Genet. 20, 481-490.
78. Prince, V. E., Holley, S. A., Bally-Cuif, L., Prabhakaran, B., Oates, A. C., Ho, R. K. and Vogt, T. F. (2001). Zebrafish lunatic fringe demarcates segmental boundaries. Mech. Dev. 105, 175-180.
79. Qiu, X., Xu, H., Haddon, C., Lewis, J. and Jiang, Y. J. (2004). Sequence and embryonic expression of three zebrafish fringe genes: lunatic fringe, radical fringe, and manic fringe. Dev. Dyn. 231, 621-630.
80. Rauskolb, C., Correia, T. and Irvine, K. D. (1999). Fringe-dependent separation of dorsal and ventral cells in the Drosophila wing. Nature 401, 476-480.
81. Robu, M. E., Larson, J. D., Nasevicius, A., Beiraghi, S., Brenner, C., Farber, S. A. and Ekker, S. C. (2007). p53 activation by knockdown technologies. PLoS Genet. 3, e78.
82. Rodriguez-Esteban, C., Schwabe, J. W., De La Pena, J., Foys, B., Eshelman, B. and Belmonte, J. C. (1997). Radical fringe positions the apical ectodermal ridge at the dorsoventral boundary of the vertebrate limb. Nature 386, 360-366.
83. Sakamoto, K., Ohara, O., Takagi, M., Takeda, S. and Katsube, K. (2002). Intracellular cell-autonomous association of Notch and its ligands: a novel mechanism of Notch signal modification. Dev. Biol. 241, 313-326.
84. Schier, A. F., Neuhauss, S. C., Harvey, M., Malicki, J., Solnica-Krezel, L., Stainier, D. Y., Zwartkruis, F., Abdelilah, S., Stemple, D. L., Rangini, Z. et al. (1996). Mutations affecting the development of the embryonic zebrafish brain. Development 123, 165-178.
85. Seth, A., Culverwell, J., Walkowicz, M., Toro, S., Rick, J. M., Neuhauss, S. C., Varga, Z. M. and Karlstrom, R. O. (2006). belladonna/(Ihx2) is required for neural patterning and midline axon guidance in the zebrafish forebrain. Development 133, 725-735.
86. Shih, J. and Fraser, S. E. (1995). Distribution of tissue progenitors within the shield region of the zebrafish gastrula. Development 121, 2755-2765.
87. Shimojo, H., Ohtsuka, T. and Kageyama, R. (2008). Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58, 52-64.
88. Sieger, D., Tautz, D. and Gajewski, M. (2004). her11 is involved in the somitogenesis clock in zebrafish. Dev. Genes Evol. 214, 393-406.
89. 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.
90. Thaeron, C., Avaron, F., Casane, D., Borday, V., Thisse, B., Thisse, C., Boulekbache, H. and Laurenti, P. (2000). Zebrafish evx1 is dynamically expressed during embryogenesis in subsets of interneurones, posterior gut and urogenital system. Mech. Dev. 99, 167-172.
91. Thisse, C., Thisse, B., Schilling, T. F. and Postlethwait, J. H. (1993). Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119, 1203-1215.
92. Thomas, G. B. and van Meyel, D. J. (2007). The glycosyltransferase Fringe promotes Delta-Notch signaling between neurons and glia, and is required for subtype-specific glial gene expression. Development 134, 591-600.
93. Trevarrow, B., Marks, D. L. and Kimmel, C. B. (1990). Organization of hindbrain segments in the zebrafish embryo. Neuron 4, 669-679.
94. van Eeden, F. J., Granato, M., Schach, U., Brand, M., Furutani-Seiki, M., Haffter, P., Hammerschmidt, M., Heisenberg, C. P., Jiang, Y. J., Kane, D. A. et al. (1996). Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 123, 153-164.
95. Visan, I., Tan, J. B., Yuan, J. S., Harper, J. A., Koch, U. and Guidos, C. J. (2006). Regulation of T lymphopoiesis by Notch1 and Lunatic fringe-mediated competition for intrathymic niches. Nat. Immunol. 7, 634-643.
96. 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.
97. Westin, L. and Lardelli, M. (1997). Three novel Notch genes in zebrafish: implications for vertebrate Notch gene evolution and function. Dev. Genes Evol. 207, 51-63.
98. Wettstein, D. A., Turner, D. L. and Kintner, C. (1997). The Xenopus homolog of Drosophila Suppressor of Hairless mediates Notch signaling during primary neurogenesis. Development 124, 693-702.
99. Yeo, S. Y., Kim, M., Kim, H. S., Huh, T. L. and Chitnis, A. B. (2007). Fluorescent protein expression driven by her4 regulatory elements reveals the spatiotemporal pattern of Notch signaling in the nervous system of zebrafish embryos. Dev. Biol. 301, 555-567.
100. Zeltser, L. M., Larsen, C. W. and Lumsden, A. (2001). A new developmental compartment in the forebrain regulated by Lunatic fringe. Nat. Neurosci. 4, 683-684.