Emerging roles for zic genes in early development

Developmental Dynamics

Volumn 236, Issue 4, 2007, Pages 922-940

  Merzdorf, Christa S ^a  

^a MONTANA STATE UNIVERSITY   (United States)

Author keywords

Cell proliferation; Neural crest; Neural tube; Somite; Zic; zic1; zic2; zic3; zic4; zic5

Indexed keywords

PROTEIN ZIC; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

BRAIN DEVELOPMENT; CELL PROLIFERATION; CELL SPECIFICITY; CEREBELLUM; DEVELOPMENTAL GENE; DEVELOPMENTAL GENETICS; GENE EXPRESSION; HUMAN; MULTIGENE FAMILY; NERVOUS TISSUE; NEURAL CREST; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; RETINA GANGLION CELL; REVIEW; SIGNAL TRANSDUCTION; SOMITE; ZIC GENE;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYONIC DEVELOPMENT; EVOLUTION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MESODERM; MODELS, BIOLOGICAL; MULTIGENE FAMILY; NEURAL CREST; PROTEIN BINDING; TRANSCRIPTION FACTORS;

EID: 34247332335     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21098     Document Type: Review

References (149)

1. Alper S, Kenyon C. 2002. The zinc finger protein REF-2 functions with the Hox genes to inhibit cell fusion in the ventral epidermis of C. elegans. Development 129:3335-3348.
2. Andreazzoli M, Gestri G, Cremisi F, Casarosa S, Dawid IB, Barsacchi G. 2003. Xrx1 controls proliferation and neurogenesis in Xenopus anterior neural plate. Development 130:5143-5154.
3. Aruga J. 2004. The role of Zic genes in neural development. Mol Cell Neurosci 26:205-221.
4. Aruga J, Yokota N, Hashimoto M, Furuichi T, Fukuda M, Mikoshiba K. 1994. A novel zinc finger protein, zic, is involved in neurogenesis, especially in the cell lineage of cerebellar granule cells. J Neurochem 63:1880-1890.
5. Aruga J, Nagai T, Tokuyama T, Hayashizaki Y, Okazaki Y, Chapman VM, Mikoshiba K. 1996. The mouse zic gene family. Homologues of the Drosophila pair-rule gene odd-paired. J Biol Chem 271:1043-1047.
6. Aruga J, Minowa O, Yaginuma H, Kuno J, Nagai T, Noda T, Mikoshiba K. 1998. Mouse Zic1 is involved in cerebellar development. J Neurosci 18:284-293.
7. Aruga J, Mizugishi K, Koseki H, Imai K, Balling R, Noda T, Mikoshiba K. 1999. Zic1 regulates the patterning of vertebral arches in cooperation with Gli3. Mech Dev 89:141-150.
8. Aruga J, Shimoda K, Mikoshiba K. 2000. A 5′ segment of the mouse Zic1 gene contains a region specific enhancer for dorsal hindbrain and spinal cord. Brain Res Mol Brain Res 78:15-25.
9. Aruga J, Tohmonda T, Homma S, Mikoshiba K. 2002. Zic1 promotes the expansion of dorsal neural progenitors in spinal cord by inhibiting neuronal differentiation. Dev Biol 244:329-341.
10. Aruga J, Kamiya A, Takahashi H, Fujimi TJ, Shimizu Y, Ohkawa K, Yazawa S, Umesono Y, Noguchi H, Shimizu T, Saitou N, Mikoshiba K, Sakaki Y, Agata K, Toyoda A. 2006. A wide-range phylogenetic analysis of Zic proteins: implications for correlations between protein structure conservation and body plan complexity. Genomics 87:783-792.
11. Bagutti C, Forro G, Ferralli J, Rubin B, Chiquet-Ehrismann R. 2003. The intracellular domain of teneurin-2 has a nuclear function and represses zic-1-mediated transcription. J Cell Sci 116:2957-2966.
12. Bang AG, Papalopulu N, Kintner C, Goulding MD. 1997. Expression of Pax-3 is initiated in the early neural plate by posteriorizing signals produced by the organizer and by posterior non-axial mesoderm. Development 124:2075-2085.
13. Barembaum M, Bronner-Fraser M. 2005. Early steps in neural crest specification. Semin Cell Dev Biol 16:642-646.
14. Basch ML, Garcia-Castro MI, Bronner-Fraser M. 2004. Molecular mechanisms of neural crest induction. Birth Defects Res C Embryo Today 72:109-123.
15. Baumgartner S, Martin D, Hagios C, Chiquet-Ehrismann R. 1994. Tenm, a Drosophila gene related to tenascin, is a new pair-rule gene. Embo J 13:3728-3740.
16. Bedard JE, Purnell JD, Ware SM. 2007. Nuclear import and export signals are essential for proper cellular trafficking and function of ZIC3. Hum Mol Genet 16:187-198.
17. Belmont JW, Mohapatra B, Towbin JA, Ware SM. 2004. Molecular genetics of heterotaxy syndromes. Curr Opin Cardiol 19:216-220.
18. Benedyk MJ, Mullen JR, DiNardo S. 1994. odd-paired: a zinc finger pair-rule protein required for the timely activation of engrailed and wingless in Drosophila embryos. Genes Dev 8:105-117.
19. Berger MF, Bulyk ML. 2006. Protein binding microarrays (PBMs) for rapid, high-throughput characterization of the sequence specificities of DNA binding proteins. Methods Mol Biol 338:245-260.
20. Bertrand N, Dahmane N. 2006. Sonic hedgehog signaling in forebrain development and its interactions with pathways that modify its effects. Trends Cell Biol 16:597-605.
21. Borghesani PR, Peyrin JM, Klein R, Rubin J, Carter AR, Schwartz PM, Luster A, Corfas G, Segal RA. 2002. BDNF stimulates migration of cerebellar granule cells. Development 129:1435-1442.
22. Brewster R, Lee J, Ruiz i Altaba A. 1998. Gli/Zic factors pattern the neural plate by defining domains of cell differentiation. Nature 393:579-583.
23. Brown L, Paraso M, Arkell R, Brown S. 2005. In vitro analysis of partial loss-of-function ZIC2 mutations in holoprosencephaly: alanine tract expansion modulates DNA binding and transactivation. Hum Mol Genet 14:411-420.
24. Brown SA, Warburton D, Brown LY, Yu CY, Roeder ER, Stengel-Rutkowski S, Hennekam RC, Muenke M. 1998. Holoprosencephaly due to mutations in ZIC2, a homologue of Drosophila odd-paired. Nat Genet 20:180-183.
25. Brugmann SA, Pandur PD, Kenyon KL, Pignoni F, Moody SA. 2004. Six1 promotes a placodal fate within the lateral neurogenic ectoderm by functioning as both a transcriptional activator and repressor. Development 131:5871-5881.
26. Bulyk ML. 2006. Analysis of sequence specificities of DNA-binding proteins with protein binding microarrays. Methods Enzymol 410:279-299.
27. Carrel T, Purandare SM, Harrison W, Elder F, Fox T, Casey B, Herman GE. 2000. The X-linked mouse mutation Bent tail is associated with a deletion of the Zic3 locus. Hum Mol Genet 9:1937-1942.
28. Chen CM, Kraut N, Groudine M, Weintraub H. 1996. I-mf, a novel myogenic repressor, interacts with members of the MyoD family. Cell 86:731-741.
29. Cimbora DM, Sakonju S. 1995. Drosophila midgut morphogenesis requires the function of the segmentation gene odd-paired. Dev Biol 169:580-595.
30. Cohen MM Jr. 2006. Holoprosencephaly: clinical, anatomic, and molecular dimensions. Birth Defects Res A Clin Mol Teratol 76:658-673.
31. Cornell RA, Eisen JS. 2005. Notch in the pathway: the roles of Notch signaling in neural crest development. Semin Cell Dev Biol 16:663-672.
32. Cui Y, Brown JD, Moon RT, Christian JL. 1995. Xwnt-8b: a maternally expressed Xenopus Wnt gene with a potential role in establishing the dorsoventral axis. Development 121:2177-2186.
33. Dahmane N, Ruiz I Altaba A. 1999. Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126:3089-3100.
34. Denetclaw WF, Jr., Christ B, Ordahl CP. 1997. Location and growth of epaxial myotome precursor cells. Development 124:1601-1610.
35. Ding YQ, Yin J, Kania A, Zhao ZQ, Johnson RL, Chen ZF. 2004. Lmx1b controls the differentiation and migration of the superficial dorsal horn neurons of the spinal cord. Development 131:3693-3703.
36. Dubourg C, Lazaro L, Pasquier L, Bendavid C, Blayau M, Le Duff F, Durou MR, Odent S, David V. 2004. Molecular screening of SHH, ZIC2, SIX3, and TGIF genes in patients with features of holoprosencephaly spectrum: Mutation review and genotype-phenotype correlations. Hum Mutat 24:43-51.
37. Ebert PJ, Timmer JR, Nakada Y, Helms AW, Parab PB, Liu Y, Hunsaker TL, Johnson JE. 2003. Zic1 represses Math1 expression via interactions with the Math1 enhancer and modulation of Math1 autoregulation. Development 130:1949-1959.
38. Elms P, Siggers P, Napper D, Greenfield A, Arkell R. 2003. Zic2 is required for neural crest formation and hindbrain patterning during mouse development. Dev Biol 264:391-406.
39. Elms P, Scurry A, Davies J, Willoughby C, Hacker T, Bogani D, Arkell R. 2004. Overlapping and distinct expression domains of Zic2 and Zic3 during mouse gastrulation. Gene Expr Patterns 4:505-511.
40. Feledy JA, Beanan MJ, Sandoval JJ, Goodrich JS, Lim JH, Matsuo-Takasaki M, Sato SM, Sargent TD. 1999. Inhibitory patterning of the anterior neural plate in Xenopus by homeodomain factors Dlx3 and Msx1. Dev Biol 212:455-464.
41. Fox AH, Liew C, Holmes M, Kowalski K, Mackay J, Crossley M. 1999. Transcriptional cofactors of the FOG family interact with GATA proteins by means of multiple zinc fingers. Embo J 18:2812-2822.
42. Franco PG, Paganelli AR, Lopez SL, Carrasco AE. 1999. Functional association of retinoic acid and hedgehog signaling in Xenopus primary neurogenesis. Development 126:4257-4265.
43. Fujimi TJ, Mikoshiba K, Aruga J. 2006. Xenopus Zic4: Conservation and diversification of expression profiles and protein function among the Xenopus Zic family. Dev Dyn 235:3379-3386.
44. Furushima K, Murata T, Matsuo I, Aizawa S. 2000. A new murine zinc finger gene, Opr. Mech Dev 98:161-164.
45. Furushima K, Murata T, Kiyonari H, Aizawa S. 2005. Characterization of Opr deficiency in mouse brain: subtle defects in dorsomedial telencephalon and medioventral forebrain. Dev Dyn 232:1056-1061.
46. Gamse JT, Sive H. 2001. Early anteroposterior division of the presumptive neurectoderm in Xenopus. Mech Dev 104:21-36.
47. Gaston-Massuet C, Henderson DJ, Greene ND, Copp AJ. 2005. Zic4, a zinc-finger transcription factor, is expressed in the developing mouse nervous system. Dev Dyn 233:1110-1115.
48. Gebbia M, Ferrero GB, Pilia G, Bassi MT, Aylsworth A, Penman-Splitt M, Bird LM, Bamforth JS, Burn J, Schlessinger D, Nelson DL, Casey B. 1997. X-linked situs abnormalities result from mutations in ZIC3. Nat Genet 17:305-308.
49. Gestri G, Carl M, Appolloni I, Wilson SW, Barsacchi G, Andreazzoli M. 2005. Six3 functions in anterior neural plate specification by promoting cell proliferation and inhibiting Bmp4 expression. Development 132:2401-2413.
50. Glavic A, Gomez-Skarmeta JL, Mayor R. 2002. The homeoprotein Xiro1 is required for midbrain-hindbrain boundary formation. Development 129:1609-1621.
51. Grinberg I, Millen KJ. 2005. The ZIC gene family in development and disease. Clin Genet 67:290-296.
52. Grinberg I, Northrup H, Ardinger H, Prasad C, Dobyns WB, Millen KJ. 2004. Heterozygous deletion of the linked genes ZIC1 and ZIC4 is involved in Dandy-Walker malformation. Nat Genet 36:1053-1055.
53. Grinblat Y, Sive H. 2001. zic Gene expression marks anteroposterior pattern in the presumptive neurectoderm of the zebrafish gastrula. Dev Dyn 222:688-693.
54. Grinblat Y, Gamse J, Patel M, Sive H. 1998. Determination of the zebrafish forebrain: induction and patterning. Development 125:4403-4416.
55. Herman GE, El-Hodiri HM. 2002. The role of ZIC3 in vertebrate development. Cytogenet Genome Res 99:229-235.
56. Herrera E, Brown L, Aruga J, Rachel RA, Dolen G, Mikoshiba K, Brown S, Mason CA. 2003. Zic2 patterns binocular vision by specifying the uncrossed retinal projection. Cell 114:545-557.
57. Herrera E, Marcus R, Li S, Williams SE, Erskine L, Lai E, Mason C. 2004. Foxd1 is required for proper formation of the optic chiasm. Development 131:5727-5739.
58. Hoshino J, Aruga J, Ishiguro A, Mikoshiba K. 2003. Dorz1, a novel gene expressed in differentiating cerebellar granule neurons, is down-regulated in Zic1-deficient mouse. Brain Res Mol Brain Res 120:57-64.
59. Houston DW, Wylie C. 2005. Maternal Xenopus Zic2 negatively regulates Nodal-related gene expression during anteroposterior patterning. Development 132:4845-4855.
60. Huang H, Rastegar M, Bodner C, Goh SL, Rambaldi I, Featherstone M. 2005. MEIS C termini harbor transcriptional activation domains that respond to cell signaling. J Biol Chem 280:10119-10127.
61. Huang X, Saint-Jeannet JP. 2004. Induction of the neural crest and the opportunities of life on the edge. Dev Biol 275:1-11.
62. Imai KS, Satou Y, Satoh N. 2002. Multiple functions of a Zic-like gene in the differentiation of notochord, central nervous system and muscle in Ciona savignyi embryos. Development 129:2723-2732.
63. Inoue T, Hatayama M, Tohmonda T, Itohara S, Aruga J, Mikoshiba K. 2004. Mouse Zic5 deficiency results in neural tube defects and hypoplasia of cephalic neural crest derivatives. Dev Biol 270:146-162.
64. Ishibashi M. 2004. Molecular mechanisms for morphogenesis of the central nervous system in mammals. Anat Sci Int 79:226-234.
65. Ishiguro A, Inoue T, Mikoshiba K, Aruga J. 2004. Molecular properties of Zic4 and Zic5 proteins: functional diversity within Zic family. Biochem Biophys Res Commun 324:302-307.
66. Jacobs Y, Schnabel CA, Cleary ML. 1999. Trimeric association of Hox and TALE homeodomain proteins mediates Hoxb2 hindbrain enhancer activity. Mol Cell Biol 19:5134-5142.
67. Kasper M, Regl G, Frischauf AM, Aberger F. 2006. GLI transcription factors: mediators of oncogenic Hedgehog signalling. Eur J Cancer 42:437-445.
68. Kawasaki H, Crowley JC, Livesey FJ, Katz LC. 2004. Molecular organization of the ferret visual thalamus. J Neurosci 24:9962-9970.
69. Kelly LE, Carrel TL, Herman GE, El-Hodiri HM. 2006. Pbx1 and Meis1 regulate activity of the Xenopus laevis Zic3 promoter through a highly conserved region. Biochem Biophys Res Commun 344:1031-1037.
70. Kim TH, Ren B. 2006. Genome-wide analysis of protein-DNA interactions. Annu Rev Genomics Hum Genet 7:81-102.
71. Kitaguchi T, Nagai T, Nakata K, Aruga J, Mikoshiba K. 2000. Zic3 is involved in the left-right specification of the Xenopus embryo. Development 127:4787-4795.
72. Kitaguchi T, Mizugishi K, Hatayama M, Aruga J, Mikoshiba K. 2002. Xenopus Brachyury regulates mesodermal expression of Zic3, a gene controlling left-right asymmetry. Dev Growth Differ 44:55-61.
73. Klootwijk R, Franke B, van der Zee CE, de Boer RT, Wilms W, Hol FA, Mariman EC. 2000. A deletion encompassing Zic3 in bent tail, a mouse model for X-linked neural tube defects. Hum Mol Genet 9:1615-1622.
74. Klootwijk R, Schijvenaars MM, Mariman EC, Franke B. 2004. Further characterization of the genetic defect of the Bent tail mouse, a mouse model for human neural tube defects. Birth Defects Res A Clin Mol Teratol 70:880-884.
75. Koyabu Y, Nakata K, Mizugishi K, Aruga J, Mikoshiba K. 2001. Physical and functional interactions between Zic and Gli proteins. J Biol Chem 276:6889-6892.
76. Kraut N, Snider L, Chen CM, Tapscott SJ, Groudine M. 1998. Requirement of the mouse I-mfa gene for placental development and skeletal patterning. Embo J 17:6276-6288.
77. Kuo JS, Patel M, Gamse J, Merzdorf C, Liu X, Apekin V, Sive H. 1998. Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus. Development 125:2867-2882.
78. Kurata T, Ueno N. 2003. Xenopus Nbx, a novel NK-1 related gene essential for neural crest formation. Dev Biol 257:30-40.
79. Lagutin OV, Zhu CC, Kobayashi D, Topczewski J, Shimamura K, Puelles L, Russell HR, McKinnon PJ, Solnica-Krezel L, Oliver G. 2003. Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev 17:368-379.
80. Lee SY, Lee HS, Moon JS, Kim JI, Park JB, Lee JY, Park MJ, Kim J. 2004. Transcriptional regulation of Zic3 by heterodimeric AP-1(c-Jun/c-Fos) during Xenopus development. Exp Mol Med 36:468-475.
81. Li S, Shin Y, Cho KW, Merzdorf CS. 2006. The Xfeb gene is directly upregulated by Zic1 during early neural development. Dev Dyn 235:2817-2827.
82. Lindgens D, Holstein TW, Technau U. 2004. Hyzic, the Hydra homolog of the zic/odd-paired gene, is involved in the early specification of the sensory nematocytes. Development 131:191-201.
83. Liu Y, Helms AW, Johnson JE. 2004. Distinct activities of Msx1 and Msx3 in dorsal neural tube development. Development 131:1017-1028.
84. Maeda R, Mood K, Jones TL, Aruga J, Buchberg AM, Daar IO. 2001. Xmeis1, a protooncogene involved in specifying neural crest cell fate in Xenopus embryos. Oncogene 20:1329-1342.
85. Maeda R, Ishimura A, Mood K, Park EK, Buchberg AM, Daar IO. 2002. Xpbx1b and Xmeis1b play a collaborative role in hindbrain and neural crest gene expression in Xenopus embryos. Proc Natl Acad Sci USA 99:5448-5453.
86. Marcelle C, Stark MR, Bronner-Fraser M. 1997. Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 124:3955-3963.
87. McCarty AS, Kleiger G, Eisenberg D, Smale ST. 2003. Selective dimerization of a C2H2 zinc finger subfamily. Mol Cell 11:459-470.
88. McGrew LL, Otte AP, Moon RT. 1992. Analysis of Xwnt-4 in embryos of Xenopus laevis: a Wnt family member expressed in the brain and floor plate. Development 115:463-473.
89. Melton KR, Iulianella A, Trainor PA. 2004. Gene expression and regulation of hindbrain and spinal cord development. Front Biosci 9:117-138.
90. Merzdorf CS, Sive HL. 2006. The zic1 gene is an activator of Wnt signaling. Int J Dev Biol 50:611-617.
91. Mizugishi K, Aruga J, Nakata K, Mikoshiba K. 2001. Molecular properties of Zic proteins as transcriptional regulators and their relationship to GLI proteins. J Biol Chem 276:2180-2188.
92. Mizugishi K, Hatayama M, Tohmonda T, Ogawa M, Inoue T, Mikoshiba K, Aruga J. 2004. Myogenic repressor I-mfa interferes with the function of Zic family proteins. Biochem Biophys Res Commun 320:233-240.
93. Mizuseki K, Kishi M, Matsui M, Nakanishi S, Sasai Y. 1998. Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. Development 125:579-587.
94. Monsoro-Burq AH, Fletcher RB, Harland RM. 2003. Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. Development 130:3111-3124.
95. Monsoro-Burq AH, Wang E, Harland R. 2005. Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction. Dev Cell 8:167-178.
96. Motoyama J. 2006. Essential roles of Gli3 and sonic hedgehog in pattern formation and developmental anomalies caused by their dysfunction. Congenit Anom (Kyoto) 46:123-128.
97. Muenke M, Beachy PA. 2000. Genetics of ventral forebrain development and holoprosencephaly. Curr Opin Genet Dev 10:262-269.
98. Nagai T, Aruga J, Takada S, Gunther T, Sporle R, Schughart K, Mikoshiba K. 1997. The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. Dev Biol 182:299-313.
99. Nagai T, Aruga J, Minowa O, Sugimoto T, Ohno Y, Noda T, Mikoshiba K. 2000. Zic2 regulates the kinetics of neurulation. Proc Natl Acad Sci USA 97:1618-1623.
100. Nakata K, Nagai T, Aruga J, Mikoshiba K. 1997. Xenopus Zic3, a primary regulator both in neural and neural crest development. Proc Natl Acad Sci USA 94:11980-11985.
101. Nakata K, Nagai T, Aruga J, Mikoshiba K. 1998. Xenopus Zic family and its role in neural and neural crest development. Mech Dev 75:43-51.
102. Nakata K, Koyabu Y, Aruga J, Mikoshiba K. 2000. A novel member of the Xenopus Zic family, Zic5, mediates neural crest development. Mech Dev 99:83-91.
103. Negre N, Lavrov S, Hennetin J, Bellis M, Cavalli G. 2006. Mapping the distribution of chromatin proteins by ChIP on chip. Methods Enzymol 410:316-341.
104. Nishida H, Sawada K. 2001. macho-1 encodes a localized mRNA in ascidian eggs that specifies muscle fate during embryogenesis. Nature 409:724-729.
105. Nyholm MK, Wu SF, Dorsky RI, Grinblat Y. 2007. The zebrafish zic2a-zic5 gene pair acts downstream of canonical Wnt signaling to control cell proliferation in the developing tectum. Development 134:735-746.
106. Ohtsuka M, Kikuchi N, Yokoi H, Kinoshita M, Wakamatsu Y, Ozato K, Takeda H, Inoko H, Kimura M. 2004. Possible roles of zic1 and zic4, identified within the medaka Double anal fin (Da) locus, in dorsoventral patterning of the trunk-tail region (related to phenotypes of the Da mutant). Mech Dev 121:873-882.
107. Ordahl CP, Berdougo E, Venters SJ, Denetclaw WF Jr. 2001. The dermomyotome dorsomedial lip drives growth and morphogenesis of both the primary myotome and dermomyotome epithelium. Development 128:1731-1744.
108. Pabo CO, Peisach E, Grant RA. 2001. Design and selection of novel Cys2His2 zinc finger proteins. Annu Rev Biochem 70:313-340.
109. Pan W, Jia Y, Wang J, Tao D, Gan X, Tsiokas L, Jing N, Wu D, Li L. 2005. Beta-catenin regulates myogenesis by relieving I-mfa-mediated suppression of myogenic regulatory factors in P19 cells. Proc Natl Acad Sci USA 102:17378-17383.
110. Pandur PD, Moody SA. 2000. Xenopus Six1 gene is expressed in neurogenic cranial placodes and maintained in the differentiating lateral lines. Mech Dev 96:253-257.
111. Park GT, Morasso MI. 2002. Bone morphogenetic protein-2 (BMP-2) transactivates Dlx3 through Smad1 and Smad4: alternative mode for Dlx3 induction in mouse keratinocytes. Nucleic Acids Res 30:515-522.
112. Pavletich NP, Pabo CO. 1993. Crystal structure of a five-finger GLI-DNA complex: new perspectives on zinc fingers. Science 261:1701-1707.
113. Pennisi E. 2004. Searching for the genome's second code. Science 306:632-635.
114. Purandare SM, Ware SM, Kwan KM, Gebbia M, Bassi MT, Deng JM, Vogel H, Behringer RR, Belmont JW, Casey B. 2002. A complex syndrome of left-right axis, central nervous system and axial skeleton defects in Zic3 mutant mice. Development 129:2293-2302.
115. Qin L, Wine-Lee L, Ahn KJ, Crenshaw EB, 3rd. 2006. Genetic analyses demonstrate that bone morphogenetic protein signaling is required for embryonic cerebellar development. J Neurosci 26:1896-1905.
116. Rallu M, Machold R, Gaiano N, Corbin JG, McMahon AP, Fishell G. 2002. Dorsoventral patterning is established in the telencephalon of mutants lacking both Gli3 and Hedgehog signaling. Development 129:4963-4974.
117. Ramos C, Robert B. 2005. msh/Msx gene family in neural development. Trends Genet 21:624-632.
118. Rhinn M, Brand M. 2001. The midbrain - hindbrain boundary organizer. Curr Opin Neurobiol 11:34-42.
119. Rohr KB, Schulte-Merker S, Tautz D. 1999. Zebrafish zic1 expression in brain and somites is affected by BMP and hedgehog signalling. Mech Dev 85:147-159.
120. Sakurada T, Mima K, Kurisaki A, Sugino H, Yamauchi T. 2005. Neuronal cell type-specific promoter of the alpha CaM kinase II gene is activated by Zic2, a Zic family zinc finger protein. Neurosci Res 53:323-330.
121. Salero E, Perez-Sen R, Aruga J, Gimenez C, Zafra F. 2001. Transcription factors Zic1 and Zic2 bind and transactivate the apolipoprotein E gene promoter. J Biol Chem 276:1881-1888.
122. Sato T, Sasai N, Sasai Y. 2005. Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development 132:2355-2363.
123. Selleck MA, Bronner-Fraser M. 1995. Origins of the avian neural crest: the role of neural plate-epidermal interactions. Development 121:525-538.
124. Shimeld SM, Holland PW. 2000. Vertebrate innovations. Proc Natl Acad Sci USA 97:4449-4452.
125. Steventon B, Carmona-Fontaine C, Mayor R. 2005. Genetic network during neural crest induction: from cell specification to cell survival. Semin Cell Dev Biol 16:647-654.
126. Stewart D, Tomita A, Shi YB, Wong J. 2006. Chromatin immunoprecipitation for studying transcriptional regulation in Xenopus oocytes and tadpoles. Methods Mol Biol 322:165-181.
127. Su HL, Muguruma K, Matsuo-Takasaki M, Kengaku M, Watanabe K, Sasai Y. 2006. Generation of cerebellar neuron precursors from embryonic stem cells. Dev Biol 290:287-296.
128. Sugimoto K, Okabayashi K, Sedohara A, Hayata T, Asashima M. 2007. The role of XBtg2 in Xenopus neural development. Dev Neurosci (in press).
129. Sun Rhodes LS, Merzdorf CS. 2006. The zic1 gene is expressed in chick somites but not in migratory neural crest. Gene Expr Patterns 6:539-545.
130. Toyama R, Gomez DM, Mana MD, Dawid IB. 2004. Sequence relationships and expression patterns of zebrafish zic2 and zic5 genes. Gene Expr Patterns 4:345-350.
131. Tribulo C, Aybar MJ, Nguyen VH, Mullins MC, Mayor R. 2003. Regulation of Msx genes by a Bmp gradient is essential for neural crest specification. Development 130:6441-6452.
132. Tropepe V, Li S, Dickinson A, Gamse JT, Sive HL. 2006. Identification of a BMP inhibitor-responsive promoter module required for expression of the early neural gene zic1. Dev Biol 289:517-529.
133. Tucker RP, Chiquet-Ehrismann R. 2006. Teneurins: a conserved family of transmembrane proteins involved in intercellular signaling during development. Dev Biol 290:237-245.
134. Venkatesh B. 2003. Evolution and diversity of fish genomes. Curr Opin Genet Dev 13:588-592.
135. Venters SJ, Ordahl CP. 2002. Persistent myogenic capacity of the dermomyotome dorsomedial lip and restriction of myogenic competence. Development 129:3873-3885.
136. Volff JN. 2005. Genome evolution and biodiversity in teleost fish. Heredity 94:280-294.
137. Wada S, Saiga H. 2002. HrzicN, a new Zic family gene of ascidians, plays essential roles in the neural tube and notochord development. Development 129:5597-5608.
138. Wang B, Fallon JF, Beachy PA. 2000. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100:423-434.
139. Ware SM, Peng J, Zhu L, Fernbach S, Colicos S, Casey B, Towbin J, Belmont JW. 2004. Identification and functional analysis of ZIC3 mutations in heterotaxy and related congenital heart defects. Am J Hum Genet 74:93-105.
140. Ware SM, Harutyunyan KG, Belmont JW. 2006. Heart defects in X-linked heterotaxy: evidence for a genetic interaction of Zic3 with the nodal signaling pathway. Dev Dyn 235:1631-1637.
141. Warner SJ, Hutson MR, Oh SH, Gerlach-Bank LM, Lomax MI, Barald KF. 2003. Expression of ZIC genes in the development of the chick inner ear and nervous system. Dev Dyn 226:702-712.
142. Weber JR, Sokol SY. 2003. Identification of a phylogenetically conserved activin-responsive enhancer in the Zic3 gene. Mech Dev 120:955-964.
143. Wolda SL, Moody CJ, Moon RT. 1993. Overlapping expression of Xwnt-3A and Xwnt-1 in neural tissue of Xenopus laevis embryos. Dev Biol 155:46-57.
144. Yabe S, Tanegashima K, Haramoto Y, Takahashi S, Fujii T, Kozuma S, Taketani Y, Asashima M. 2003. FRL-1, a member of the EGF-CFC family, is essential for neural differentiation in Xenopus early development. Development 130:2071-2081.
145. Yagi K, Takatori N, Satou Y, Satoh N. 2005. Ci-Tbx6b and Ci-Tbx6c are key mediators of the maternal effect gene Ci-macho1 in muscle cell differentiation in Ciona intestinalis embryos. Dev Biol 282:535-549.
146. Yamamoto TS, Takagi C, Ueno N. 2000. Requirement of Xmsx-1 in the BMP-triggered ventralization of Xenopus embryos. Mech Dev 91:131-141.
147. Yang Y, Hwang CK, Junn E, Lee G, Mouradian MM. 2000. ZIC2 and Sp3 repress Sp1-induced activation of the human D1A dopamine receptor gene. J Biol Chem 275:38863-38869.
148. Yokota N, Aruga J, Takai S, Yamada K, Hamazaki M, Iwase T, Sugimura H, Mikoshiba K. 1996. Predominant expression of human zic in cerebellar granule cell lineage and medulloblastoma. Cancer Res 56:377-383.
149. Zhou X, Hollemann T, Pieler T, Gruss P. 2000. Cloning and expression of xSix3, the Xenopus homologue of murine Six3. Mech Dev 91:327-330.