Zic-associated holoprosencephaly: Zebrafish Zic1 controls midline formation and forebrain patterning by regulating Nodal, Hedgehog, and retinoic acid signaling

Genes and Development

Volumn 23, Issue 12, 2009, Pages 1461-1473

  Maurus, Daniel ^a   Harris, William A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cyclops; Cyp26a1; Midline interhemispheric holoprosencephaly; Retina; Sonic hedgehog; Zic2

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CYTOCHROME P450 26A1; PROTEIN NODAL; RETINOIC ACID; SONIC HEDGEHOG PROTEIN; CYTOCHROME P450; NDR2 PROTEIN, ZEBRAFISH; NODAL SIGNALING PROTEIN; RETINOIC ACID 4 HYDROXYLASE; RETINOIC ACID 4-HYDROXYLASE; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR; ZEBRAFISH PROTEIN; ZIC1 PROTEIN, ZEBRAFISH;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYCLOPIA; DIENCEPHALON; EMBRYO; GENE CONTROL; GENE EXPRESSION; GENETIC ASSOCIATION; HOLOPROSENCEPHALY; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; ZEBRA FISH; ZIC GENE; ZIC1 GENE; ZIC2 GENE; ANIMAL; FOREBRAIN; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; MORPHOGENESIS; PHYSIOLOGY; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION; UPREGULATION;

DANIO RERIO; ERINACEIDAE;

ANIMALS; BODY PATTERNING; CYTOCHROME P-450 ENZYME SYSTEM; DIENCEPHALON; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; HEDGEHOG PROTEINS; HOLOPROSENCEPHALY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NODAL SIGNALING LIGANDS; PROSENCEPHALON; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRETINOIN; UP-REGULATION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 67149139838     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.517009     Document Type: Article

References (67)

1. Abu-Abed S, Dollé P, Metzger D, Beckett B, Chambon P, Petkovich M. 2001. The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes & Dev 15: 226-240. (Pubitemid 32107667)
2. Aruga J, Inoue T, Hoshino J, Mikoshiba K. 2002a. Zic2 controls cerebellar development in cooperation with Zic1. J Neurosci 22: 218-225. (Pubitemid 34033499)
3. Aruga J, Tohmonda T, Homma S, Mikoshiba K. 2002b. Zic1 promotes the expansion of dorsal neural progenitors in spinal cord by inhibiting neuronal differentiation. Dev Biol 244: 329-341. (Pubitemid 34450647)
4. Barresi MJ, Stickney HL, Devoto SH. 2000. The zebrafish slow-muscle-omitted gene product is required for Hedgehog signal transduction and the development of slow muscle identity. Development 127: 2189-2199. (Pubitemid 30386682)
5. Begemann G, Ingham PW. 2000. Developmental regulation of Tbx5 in zebrafish embryogenesis. Mech Dev 90: 299-304. (Pubitemid 30042938)
6. 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. (Pubitemid 44636221)
7. Blumberg B, Bolado J Jr, Moreno TA, Kintner C, Evans RM, Papalopulu N. 1997. An essential role for retinoid signalling in anteroposterior neural patterning. Development 124: 373-379. (Pubitemid 27101671)
8. 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.
9. 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. (Pubitemid 28455452)
10. Brown LY, Odent S, David V, Blayau M, Dubourg C, Apacik C, Delgado MA, Hall BD, Reynolds JF, Sommer A, et al. 2001. Holoprosencephaly due to mutations in ZIC2: Alanine tract expansion mutations may be caused by parental somatic recombination. Hum Mol Genet 10: 791-796. (Pubitemid 32331589)
11. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383: 407-413. (Pubitemid 26330823)
12. Cohen MM Jr. 2006. Holoprosencephaly: Clinical, anatomic, and molecular dimensions. Birth Defects Res A Clin Mol Teratol 76: 658-673. (Pubitemid 44521971)
13. Concordet JP, Lewis KE, Moore JW, Goodrich LV, Johnson RL, Scott MP, Ingham PW. 1996. Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 122: 2835-2846. (Pubitemid 26326515)
14. Ekker SC, Ungar AR, Greenstein P, von Kessler DP, Porter JA, Moon RT, Beachy PA. 1995. Patterning activities of vertebrate hedgehog proteins in the developing eye and brain. Curr Biol 5: 944-955.
15. Elsen GE, Choi LY, Millen KJ, Grinblat Y, Prince VE. 2008. Zic1 and Zic4 regulate zebrafish roof plate specification and hindbrain ventricle morphogenesis. Dev Biol 314: 376-392.
16. Emoto Y, Wada H, Okamoto H, Kudo A, Imai Y. 2005. Retinoic acid-metabolizing enzyme Cyp26a1 is essential for determining territories of hindbrain and spinal cord in zebrafish. Dev Biol 278: 415-427. (Pubitemid 40175039)
17. Fernandes M, Hébert JM. 2008. The ups and downs of holoprosencephaly: Dorsal versus ventral patterning forces. Clin Genet 73: 413-423.
18. Fernandes M, Gutin G, Alcorn H, McConnell SK, Hébert JM. 2007. Mutations in the BMP pathway in mice support the existence of two molecular classes of holoprosencephaly. Development 134: 3789-3794. (Pubitemid 350187338)
19. Franco PG, Paganelli AR, López SL, Carrasco AE. 1999. Functional association of retinoic acid and hedgehog signalling in Xenopus primary neurogenesis. Development 126: 4257-4265. (Pubitemid 29509341)
20. Gongal PA, Waskiewicz AJ. 2008. Zebrafish model of holoprosencephaly demonstrates a key role for TGIF in regulating retinoic acid metabolism. Human Mol Gen 17: 525-538. (Pubitemid 351209294)
21. Grinblat Y, Sive H. 2001. zic gene expression marks anteroposterior pattern in the presumptive neurectoderm of the zebrafish gastrula. Dev Dyn 222: 688-693. (Pubitemid 33136339)
22. Grinblat Y, Gamse J, Patel M, Sive H. 1998. Determination of the zebrafish forebrain: Induction and patterning. Development 125: 4403-4416. (Pubitemid 28564285)
23. Hamade A, Deries M, Begemann G, Bally-Cuif L, Genêt C, Sabatier F, Bonnieu A, Cousin X. 2006. Retinoic acid activates myogenesis in vivo through Fgf8 signalling. Dev Biol 289: 127-140. (Pubitemid 41804093)
24. Hernandez RE, Putzke AP, Myers JP, Margaretha L, Moens CB. 2007. Cyp26 enzymes generate the retinoic acid response pattern necessary for hindbrain development. Development 134: 177-187. (Pubitemid 46152718)
25. Houston DW, Wylie C. 2005. Maternal Xenopus Zic2 negatively regulates Nodal-related gene expression during anteroposterior patterning. Development 132: 4845-4855. (Pubitemid 41685293)
26. Hyatt GA, Schmitt EA, Marsh-Armstrong NR, Dowling JE. 1992. Retinoic acid-induced duplication of the zebrafish retina. Proc Natl Acad Sci 89: 8293-8297.
27. Hyatt GA, Schmitt EA, Marsh-Armstrong N, McCaffery P, Dräger UC, Dowling JE. 1996. Retinoic acid establishes ventral retinal characteristics. Development 122: 195-204. (Pubitemid 26038431)
28. Inoue T, Ota M, Ogawa M, Mikoshiba K, Aruga J. 2007a. Zic1 and Zic3 regulate medial forebrain development through expansion of neuronal progenitors. J Neurosci 27: 5461-5473. (Pubitemid 46790167)
29. Inoue T, Ota M, Mikoshiba K, Aruga J. 2007b. Zic2 and Zic3 synergistically control neurulation and segmentation of paraxial mesoderm in mouse embryo. Dev Biol 306: 669-684. (Pubitemid 46873543)
30. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. 1995. Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
31. Krauss S, Johansen T, Korzh V, Moens U, Ericson JU, Fjose A. 1991a. Zebrafish pax[zf-a]: A paired box-containing gene expressed in the neural tube. EMBO J 10: 3609-3619. (Pubitemid 21905386)
32. Krauss S, Johansen T, Korzh V, Fjose A. 1991b. Expression of the zebrafish paired box gene pax[zf-b] during early neurogenesis. Development 113: 1193-1206.
33. Krauss S, Concordet JP, Ingham PW. 1993. A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75: 1431-1444. (Pubitemid 24021916)
34. Kudoh T, Wilson SW, Dawid IB. 2002. Distinct roles for Fgf, Wnt and retinoic acid in posteriorizing the neural ectoderm. Development 129: 4335-4346.
35. Langenau DM, Jette C, Berghmans S, Palomero T, Kanki JP, Kutok JL, Look AT. 2005. Suppression of apoptosis by bcl-2 overexpression in lymphoid cells of transgenic zebrafish. Blood 105: 3278-3285. (Pubitemid 40504350)
36. Lewis KE, Concordet JP, Ingham PW. 1999. Characterisation of a second patched gene in the zebrafish Danio rerio and the differential response of patched genes to Hedgehog signalling. Dev Biol 208: 14-29. (Pubitemid 29149444)
37. Lowe LA, Yamada S, Kuehn MR. 2001. Genetic dissection of nodal function in patterning the mouse embryo. Development 128: 1831-1843. (Pubitemid 32514862)
38. Lupo G, Liu Y, Qiu R, Chandraratna RA, Barsacchi G, He RQ, Harris WA. 2005. Dorsoventral patterning of the Xenopus eye: A collaboration of Retinoid, Hedgehog and FGF receptor signalling. Development 132: 1737-1748. (Pubitemid 40575872)
39. Lupo G, Harris WA, Lewis KE. 2006. Mechanisms of ventral patterning in the vertebrate nervous system. Nat Rev Neurosci 7: 103-114. (Pubitemid 43151597)
40. Macdonald R, Barth KA, Xu Q, Holder N, Mikkola I, Wilson SW. 1995. Midline signalling is required for Pax gene regulation and patterning of the eyes. Development 121: 3267-3278.
41. Maden M, Blentic A, Reijntjes S, Seguin S, Gale E, Graham A. 2007. Retinoic acid is required for specification of the ventral eye field and for Rathke's pouch in the avian embryo. Int J Dev Biol 51: 191-200. (Pubitemid 46910348)
42. Mathieu J, Barth A, Rosa FM, Wilson SW, Peyriéras N. 2002. Distinct and cooperative roles for Nodal and Hedgehog signals during hypothalamic development. Development 129: 3055-3065. (Pubitemid 34874281)
43. Mathieu J, Griffin K, Herbomel P, Dickmeis T, Strähle U, Kimelman D, Rosa FM, Peyriéras N. 2004. Nodal and Fgf pathways interact through a positive regulatory loop and synergize to maintain mesodermal cell populations. Development 131: 629-641. (Pubitemid 38240005)
44. Matsunaga E, Shiota K. 1977. Holoprosencephaly in human embryos: Epidemiologic studies of 150 cases. Teratology 16: 261-272. (Pubitemid 8236371)
45. Maves L, Jackman W, Kimmel CB. 2002. FGF3 and FGF8 mediate a rhombomere 4 signaling activity in the zebrafish hindbrain. Development 129: 3825-3837. (Pubitemid 34994013)
46. Mui SH, Kim JW, Lemke G, Bertuzzi S. 2005. Vax genes ventralize the embryonic eye. Genes & Dev 19: 1249-1259. (Pubitemid 40696190)
47. Müller F, Albert S, Blader P, Fischer N, Hallonet M, Strähle U. 2000. Direct action of the nodal-related signal cyclops in induction of sonic hedgehog in the ventral midline of the CNS. Development 127: 3889-3897. (Pubitemid 30793768)
48. 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 97: 1618-1623. (Pubitemid 30118491)
49. Negron JF, Lockshin RA. 2004. Activation of apoptosis and caspase-3 in zebrafish early gastrulae. Dev Dyn 231: 161-170. (Pubitemid 39095206)
50. Perz-Edwards A, Hardison NL, Linney E. 2001. Retinoic acid-mediated gene expression in transgenic reporter zebrafish. Dev Biol 229: 89-101. (Pubitemid 32061716)
51. Rebagliati MR, Toyama R, Haffter P, Dawid IB. 1998a. cyclops encodes a nodal-related factor involved in midline signalling. Proc Natl Acad Sci 95: 9932-9937. (Pubitemid 28415272)
52. Rebagliati MR, Toyama R, Fricke C, Haffter P, Dawid IB. 1998b. Zebrafish nodal-related genes are implicated in axial patterning and establishing left-right asymmetry. Dev Biol 199: 261-272. (Pubitemid 28364207)
53. Rissi M, Wittbrodt J, Délot E, Naegeli M, Rosa FM. 1995. Zebrafish Radar: A new member of the TGF-β superfamily defines dorsal regions of the neural plate and the embryonic retina. Mech Dev 49: 223-234.
54. 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. (Pubitemid 29343758)
55. Rohr KB, Barth KA, Varga ZM, Wilson SW. 2001. The nodal pathway acts upstream of hedgehog signalling to specify ventral telencephalic identity. Neuron 29: 341-351. (Pubitemid 32206475)
56. Saijoh Y, Adachi H, Sakuma R, Yeo CY, Yashiro K, Watanabe M, Hashiguchi H, Mochida K, Ohishi S, Kawabata M, et al. 2000. Left-right asymmetric expression of lefty2 and nodal is induced by a signalling pathway that includes the transcription factor FAST2. Mol Cell 5: 35-47. (Pubitemid 30105434)
57. Sampath K, Rubinstein AL, Cheng AM, Liang JO, Fekany K, Solnica-Krezel L, Korzh V, Halpern ME, Wright CV. 1998. Induction of the zebrafish ventral brain and floorplate requires cyclops/nodal signalling. Nature 395: 185-189. (Pubitemid 28425659)
58. Sanek NA, Grinblat Y. 2008. A novel role for zebrafish zic2a during forebrain development. Dev Biol 317: 325-335.
59. Schier AF, Neuhauss SC, Helde KA, Talbot WS, Driever W. 1997. The one-eyed pinhead gene functions in mesoderm and endoderm formation in zebrafish and interacts with no tail. Development 124: 327-342. (Pubitemid 27101667)
60. Schneider RA, Hu D, Rubenstein JL, Maden M, Helms JA. 2001. Local retinoid signaling coordinates forebrain and facial morphogenesis by maintaining FGF8 and SHH. Development 128: 2755-2767. (Pubitemid 32701004)
61. Shanmugalingam S, Houart C, Picker A, Reifers F, Macdonald R, Barth A, Griffin K, Brand M, Wilson SW. 2000. Ace/Fgf8 is required for forebrain commissure formation and patterning of the telencephalon. Development 127: 2549-2561. (Pubitemid 30426803)
62. Takamiya M, Campos-Ortega JA. 2006. Hedgehog signalling controls zebrafish neural keel morphogenesis via its level-dependent effects on neurogenesis. Dev Dyn 235: 978-997.
63. Take-uchi M, Clarke JD, Wilson SW. 2003. Hedgehog signalling maintains the optic stalk-retinal interface through the regulation of Vax gene activity. Development 130: 955-968. (Pubitemid 36367513)
64. Varga ZM, Wegner J, Westerfield M. 1999. Anterior movement of ventral diencephalic precursors separates the primordial eye field in the neural plate and requires cyclops. Development 126: 5533-5546. (Pubitemid 30035003)
65. Walshe J, Mason I. 2003. Unique and combinatorial functions of Fgf3 and Fgf8 during zebrafish forebrain development. Development 130: 4337-4349. (Pubitemid 37185322)
66. Warr N, Powles-Glover N, Chappell A, Robson J, Norris D, Arkell RM. 2008. Zic2-associated holoprosencephaly is caused by a transient defect in the organizer region during gastrulation. Hum Mol Genet 17: 2986-2996.
67. White RJ, Nie Q, Lander AD, Schilling TF. 2007. Complex regulation of cyp26a1 creates a robust retinoic acid gradient in the zebrafish embryo. PLoS Biol 5: e304. doi: 10.1371/journal.pbio.0050304. (Pubitemid 350276928)