Zic1 and Zic4 regulate zebrafish roof plate specification and hindbrain ventricle morphogenesis

Developmental Biology

Volumn 314, Issue 2, 2008, Pages 376-392

  Elsen, Gina E ^a   Choi, Louis Y ^a   Millen, Kathleen J ^a   Grinblat, Yevgenya ^b   Prince, Victoria E ^a,c  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

Dorsal signaling center; Hindbrain; Morphogenesis; Proliferation; Rhombomere boundaries; Roof plate; Ventricle; Zebrafish; Zic genes

Indexed keywords

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN FOURTH VENTRICLE; BRAIN SIZE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL GENE; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE SEQUENCE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOLECULAR CLONING; MORPHOGENESIS; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; STEM CELL; ZEBRA FISH; ZIC1 GENE; ZIC4 GENE;

DANIO RERIO;

EID: 38949193475     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.12.006     Document Type: Article

References (82)

1. Adolf B., Bellipanni G., Huber V., and Bally-Cuif L. atoh1.2 and beta3.1 are two new bHLH-encoding genes expressed in selective precursor cells of the zebrafish anterior hindbrain. Gene Expr. Patterns 5 (2004) 35-41
2. Akimenko M.A., Ekker M., Wegner J., Lin W., and Westerfield M. Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J. Neurosci. 14 (1994) 3475-3486
3. Amoyel M., Cheng Y.C., Jiang Y.J., and Wilkinson D.G. Wnt1 regulates neurogenesis and mediates lateral inhibition of boundary cell specification in the zebrafish hindbrain. Development 132 (2005) 775-785
4. Aruga J. The role of Zic genes in neural development. Mol. Cell. Neurosci. 26 (2004) 205-221
5. Aruga J., Minowa O., Yaginuma H., Kuno J., Nagai T., Noda T., and Mikoshiba K. Mouse Zic1 is involved in cerebellar development. J. Neurosci. 18 (1998) 284-293
6. Aruga J., Inoue T., Hoshino J., and Mikoshiba K. Zic2 controls cerebellar development in cooperation with Zic1. J. Neurosci. 22 (2002) 218-225
7. Aruga J., Tohmonda T., Homma S., and Mikoshiba K. Zic1 promotes the expansion of dorsal neural progenitors in spinal cord by inhibiting neuronal differentiation. Dev. Biol. 244 (2002) 329-341
8. Bae Y.K., Shimizu T., and Hibi M. Patterning of proneuronal and inter-proneuronal domains by hairy- and enhancer of split-related genes in zebrafish neuroectoderm. Development 132 (2005) 1375-1385
9. Benedyk M.J., Mullen J.R., and DiNardo S. odd-paired: a zinc finger pair-rule protein required for the timely activation of engrailed and wingless in Drosophila embryos. Genes Dev. 8 (1994) 105-117
10. Bergsneider M., Egnor M.R., Johnston M., Kranz D., Madsen J.R., McAllister II J.P., Stewart C., Walker M.L., and Williams M.A. What we don't (but should) know about hydrocephalus. J. Neurosurg. 104 (2006) 157-159
11. Bingham S., Chaudhari S., Vanderlaan G., Itoh M., Chitnis A., and Chandrasekhar A. Neurogenic phenotype of mind bomb mutants leads to severe patterning defects in the zebrafish hindbrain. Dev. Dyn. 228 (2003) 451-463
12. Brewster R., Lee J., and Ruiz i Altaba A. Gli/Zic factors pattern the neural plate by defining domains of cell differentiation. Nature 393 (1998) 579-583
13. Brown L.Y., Odent S., David V., Blayau M., Dubourg C., Apacik C., Delgado M.A., Hall B.D., Reynolds J.F., Sommer A., Wieczorek D., Brown S.A., and Muenke M. Holoprosencephaly due to mutations in ZIC2: alanine tract expansion mutations may be caused by parental somatic recombination. Hum. Mol. Genet. 10 (2001) 791-796
14. Cheng Y.C., Amoyel M., Qiu X., Jiang Y.J., Xu Q., and Wilkinson D.G. Notch activation regulates the segregation and differentiation of rhombomere boundary cells in the zebrafish hindbrain. Dev. Cell 6 (2004) 539-550
15. Cheng X., Hsu C.M., Currle D.S., Hu J.S., Barkovich A.J., and Monuki E.S. Central roles of the roof plate in telencephalic development and holoprosencephaly. J. Neurosci. 26 (2006) 7640-7649
16. Chizhikov V.V., and Millen K.J. Mechanisms of roof plate formation in the vertebrate CNS. Nat. Rev., Neurosci. 5 (2004) 808-812
17. Chizhikov V.V., and Millen K.J. Control of roof plate development and signaling by Lmx1b in the caudal vertebrate CNS. J. Neurosci. 24 (2004) 5694-5703
18. Chizhikov V.V., and Millen K.J. Control of roof plate formation by Lmx1a in the developing spinal cord. Development 131 (2004) 2693-2705
19. Chizhikov V.V., and Millen K.J. Roof plate-dependent patterning of the vertebrate dorsal central nervous system. Dev. Biol. 277 (2005) 287-295
20. Ciruna B., Jenny A., Lee D., Mlodzik M., and Schier A.F. Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature 439 (2006) 220-224
21. Concha M.L., and Adams R.J. Oriented cell divisions and cellular morphogenesis in the zebrafish gastrula and neurula: a time-lapse analysis. Development 125 (1998) 983-994
22. Davidson A.J., Postlethwait J.H., Yan Y.L., Beier D.R., van Doren C., Foernzler D., Celeste A.J., Crosier K.E., and Crosier P.S. Isolation of zebrafish gdf7 and comparative genetic mapping of genes belonging to the growth/differentiation factor 5, 6, 7 subgroup of the TGF-beta superfamily. Genome Res. 9 (1999) 121-129
23. Ding Y.Q., Yin J., Kania A., Zhao Z.Q., Johnson R.L., and Chen Z.F. Lmx1b controls the differentiation and migration of the superficial dorsal horn neurons of the spinal cord. Development 131 (2004) 3693-3703
24. Dorsky R.I., Itoh M., Moon R.T., and Chitnis A. Two tcf3 genes cooperate to pattern the zebrafish brain. Development 130 (2003) 1937-1947
25. Fujimi T.J., Mikoshiba K., and Aruga J. Xenopus Zic4: conservation and diversification of expression profiles and protein function among the Xenopus Zic family. Dev. Dyn. 235 (2006) 3379-3386
26. Geldmacher-Voss B., Reugels A.M., Pauls S., and Campos-Ortega J.A. A 90-degree rotation of the mitotic spindle changes the orientation of mitoses of zebrafish neuroepithelial cells. Development 130 (2003) 3767-3780
27. Grinberg I., and Millen K.J. The ZIC gene family in development and disease. Clin. Genet. 67 (2005) 290-296
28. Grinberg I., Northrup H., Ardinger H., Prasad C., Dobyns W.B., and Millen K.J. Heterozygous deletion of the linked genes ZIC1 and ZIC4 is involved in Dandy-Walker malformation. Nat. Genet. 36 (2004) 1053-1055
29. Grinblat Y., and Sive H. zic gene expression marks anteroposterior pattern in the presumptive neurectoderm of the zebrafish gastrula. Dev. Dyn. 222 (2001) 688-693
30. Grinblat Y., Gamse J., Patel M., and Sive H. Determination of the zebrafish forebrain: induction and patterning. Development 125 (1998) 4403-4416
31. Guo C., Qiu H.Y., Huang Y., Chen H., Yang R.Q., Chen S.D., Johnson R.L., Chen Z.F., and Ding Y.Q. Lmx1b is essential for Fgf8 and Wnt1 expression in the isthmic organizer during tectum and cerebellum development in mice. Development 134 (2007) 317-325
32. Hong E., and Brewster R. N-cadherin is required for the polarized cell behaviors that drive neurulation in the zebrafish. Development 133 (2006) 3895-3905
33. Irving C., Flenniken A., Alldus G., and Wilkinson D.G. Cell-cell interactions and segmentation in the developing vertebrate hindbrain. Biochem. Soc. Symp. 62 (1996) 85-95
34. 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., Kane D.A., Mullins M.C., Odenthal J., van Eeden F.J., and Nusslein-Volhard C. Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio. Development 123 (1996) 205-216
35. Kahane N., and Kalcheim C. Identification of early postmitotic cells in distinct embryonic sites and their possible roles in morphogenesis. Cell Tissue Res. 294 (1998) 297-307
36. Keller M.J., and Chitnis A.B. Insights into the evolutionary history of the vertebrate zic3 locus from a teleost-specific zic6 gene in the zebrafish, Danio rerio. Dev. Genes Evol. 217 (2007) 541-547
37. Kimmel C.B., Warga R.M., and Kane D.A. Cell cycles and clonal strings during formation of the zebrafish central nervous system. Development 120 (1994) 265-276
38. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., and Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (1995) 253-310
39. Koster R.W., and Fraser S.E. Direct imaging of in vivo neuronal migration in the developing cerebellum. Curr. Biol. 11 (2001) 1858-1863
40. Krauss S., Concordet J.P., and Ingham P.W. A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75 (1993) 1431-1444
41. Lele Z., Folchert A., Concha M., Rauch G.J., Geisler R., Rosa F., Wilson S.W., Hammerschmidt M., and Bally-Cuif L. parachute/n-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube. Development 129 (2002) 3281-3294
42. Lowery L.A., and Sive H. Strategies of vertebrate neurulation and a re-evaluation of teleost neural tube formation. Mech. Dev. 121 (2004) 1189-1197
43. Lowery L.A., and Sive H. Initial formation of zebrafish brain ventricles occurs independently of circulation and requires the nagie oko and snakehead/atp1a1a.1 gene products. Development 132 (2005) 2057-2067
44. Lyons D.A., Guy A.T., and Clarke J.D. Monitoring neural progenitor fate through multiple rounds of division in an intact vertebrate brain. Development 130 (2003) 3427-3436
45. Manzanares M., Trainor P.A., Ariza-McNaughton L., Nonchev S., and Krumlauf R. Dorsal patterning defects in the hindbrain, roof plate and skeleton in the dreher (dr(J)) mouse mutant. Mech. Dev. 94 (2000) 147-156
46. Mawdsley D.J., Cooper H.M., Hogan B.M., Cody S.H., Lieschke G.J., and Heath J.K. The Netrin receptor Neogenin is required for neural tube formation and somitogenesis in zebrafish. Dev. Biol. 269 (2004) 302-315
47. McAllister II J.P., and Chovan P. Neonatal hydrocephalus. Mechanisms and consequences. Neurosurg. Clin. N. Am. 9 (1998) 73-93
48. McClintock J.M., Carlson R., Mann D.M., and Prince V.E. Consequences of Hox gene duplication in the vertebrates: an investigation of the zebrafish Hox paralogue group 1 genes. Development 128 (2001) 2471-2484
49. Megason S.G., and McMahon A.P. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129 (2002) 2087-2098
50. Merzdorf C.S. Emerging roles for zic genes in early development. Dev. Dyn. 236 (2007) 922-940
51. Merzdorf C.S., and Sive H.L. The zic1 gene is an activator of Wnt signaling. Int. J. Dev. Biol. 50 (2006) 611-617
52. Millonig J.H., Millen K.J., and Hatten M.E. The mouse Dreher gene Lmx1a controls formation of the roof plate in the vertebrate CNS. Nature 403 (2000) 764-769
53. Miyan J.A., Nabiyouni M., and Zendah M. Development of the brain: a vital role for cerebrospinal fluid. Can. J. Physiol. Pharmacol. 81 (2003) 317-328
54. Moens C.B., and Prince V.E. Constructing the hindbrain: insights from the zebrafish. Dev. Dyn. 224 (2002) 1-17
55. Muroyama Y., Fujihara M., Ikeya M., Kondoh H., and Takada S. Wnt signaling plays an essential role in neuronal specification of the dorsal spinal cord. Genes Dev. 16 (2002) 548-553
56. Nagai T., Aruga J., Minowa O., Sugimoto T., Ohno Y., Noda T., and Mikoshiba K. Zic2 regulates the kinetics of neurulation. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 1618-1623
57. Nakata K., Nagai T., Aruga J., and Mikoshiba K. Xenopus Zic family and its role in neural and neural crest development. Mech. Dev. 75 (1998) 43-51
58. Nakata K., Koyabu Y., Aruga J., and Mikoshiba K. A novel member of the Xenopus Zic family, Zic5, mediates neural crest development. Mech. Dev. 99 (2000) 83-91
59. Nasevicius A., and Ekker S.C. Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26 (2000) 216-220
60. Novak Z., Krupa P., Zlatos J., and Nadvornik P. The function of the cerebrospinal fluid space and its expansion. Bratisl. Lek. L. 101 (2000) 594-597
61. Nyholm M.K., Wu S.F., Dorsky R.I., and Grinblat Y. The zebrafish zic2a-zic5 gene pair acts downstream of canonical Wnt signaling to control cell proliferation in the developing tectum. Development 134 (2007) 735-746
62. O'Hara F.P., Beck E., Barr L.K., Wong L.L., Kessler D.S., and Riddle R.D. Zebrafish Lmx1b.1 and Lmx1b.2 are required for maintenance of the isthmic organizer. Development 132 (2005) 3163-3173
63. Oxtoby E., and Jowett T. Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acids Res. 21 (1993) 1087-1095
64. Papan C., and Campos-Ortega J.A. On the formation of the neural keel and neural tube in the zebrafish Danio (braquydanio) rerio. Roux's Arch. Dev. Biol. 203 (1994) 178-198
65. Phillips B.T., Kwon H.J., Melton C., Houghtaling P., Fritz A., and Riley B.B. Zebrafish msxB, msxC and msxE function together to refine the neural-nonneural border and regulate cranial placodes and neural crest development. Dev. Biol. 294 (2006) 376-390
66. Prince V.E., Moens C.B., Kimmel C.B., and Ho R.K. Zebrafish hox genes: expression in the hindbrain region of wild-type and mutants of the segmentation gene, valentino. Development 125 (1998) 393-406
67. Riley B.B., Chiang M.Y., Storch E.M., Heck R., Buckles G.R., and Lekven A.C. Rhombomere boundaries are Wnt signaling centers that regulate metameric patterning in the zebrafish hindbrain. Dev. Dyn. 231 (2004) 278-291
68. Rohr K.B., Schulte-Merker S., and Tautz D. Zebrafish zic1 expression in brain and somites is affected by BMP and hedgehog signalling. Mech. Dev. 85 (1999) 147-159
69. 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., Yang H., and Driever W. Mutations affecting the development of the embryonic zebrafish brain. Development 123 (1996) 165-178
70. Schmitz B., Papan C., and Campos-Ortega J.A. Neurulation in the anterior trunk region of the zebrafish Bracydanio rerio. Roux's Arch. Dev. Biol. 202 (1993) 250-259
71. Seo H.C., Saetre B.O., Havik B., Ellingsen S., and Fjose A. The zebrafish Pax3 and Pax7 homologues are highly conserved, encode multiple isoforms and show dynamic segment-like expression in the developing brain. Mech. Dev. 70 (1998) 49-63
72. Shepard J.L., Stern H.M., Pfaff K.L., and Amatruda J.F. Analysis of the cell cycle in zebrafish embryos. Methods Cell Biol. 76 (2004) 109-125
73. Song M.H., Brown N.L., and Kuwada J.Y. The cfy mutation disrupts cell divisions in a stage-dependent manner in zebrafish embryos. Dev. Biol. 276 (2004) 194-206
74. Stewart R.A., Arduini B.L., Berghmans S., George R.E., Kanki J.P., Henion P.D., and Look A.T. Zebrafish foxd3 is selectively required for neural crest specification, migration and survival. Dev. Biol. 292 (2006) 174-188
75. Tawk M., Araya C., Lyons D.A., Reugels A.M., Girdler G.C., Bayley P.R., Hyde D.R., Tada M., and Clarke J.D. A mirror-symmetric cell division that orchestrates neuroepithelial morphogenesis. Nature 446 (2007) 797-800
76. Thisse B., Pflumio S., Fürthauer M., Loppin B., Heyer V., Degrave A., Woehl R., Lux A., Steffan T., Charbonnier X.Q., and Thisse C. Expression of the zebrafish genome during embryogenesis (NIH R01 RR15402). ZFIN Direct Data Submission (2001)
77. Trevarrow B., Marks D.L., and Kimmel C.B. Organization of hindbrain segments in the zebrafish embryo. Neuron 4 (1990) 669-679
78. Wiellette E., Grinblat Y., Austen M., Hirsinger E., Amsterdam A., Walker C., Westerfield M., and Sive H. Combined haploid and insertional mutation screen in the zebrafish. Genesis 40 (2004) 231-240
79. Wurst W., and Bally-Cuif L. Neural plate patterning: upstream and downstream of the isthmic organizer. Nat. Rev., Neurosci. 2 (2001) 99-108
80. Zechner D., Fujita Y., Hulsken J., Muller T., Walther I., Taketo M.M., Crenshaw III E.B., Birchmeier W., and Birchmeier C. beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev. Biol. 258 (2003) 406-418
81. Zechner D., Muller T., Wende H., Walther I., Taketo M.M., Crenshaw III EB., Treier M., Birchmeier W., and Birchmeier C. Bmp and Wnt/beta-catenin signals control expression of the transcription factor Olig3 and the specification of spinal cord neurons. Dev. Biol. 303 (2007) 181-190
82. Zhao Z.Q., Scott M., Chiechio S., Wang J.S., Renner K.J., Gereau R.W.t., Johnson R.L., Deneris E.S., and Chen Z.F. Lmx1b is required for maintenance of central serotonergic neurons and mice lacking central serotonergic system exhibit normal locomotor activity. J. Neurosci. 26 (2006) 12781-12788