A Fox stops the Wnt: Implications for forebrain development and diseases

Current Opinion in Genetics and Development

Volumn 22, Issue 4, 2012, Pages 323-330

  Danesin, Catherine ^a   Houart, Corinne ^b  

^a UNIVERSITÉ PAUL SABATIER   (France)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; PROTEIN FOXG1; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WNT PROTEIN;

BRAIN DEVELOPMENT; FOREBRAIN; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MENTAL DISEASE; MORPHOGENESIS; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TELENCEPHALON; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINEAGE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; PROSENCEPHALON; SIGNAL TRANSDUCTION; WNT PROTEINS;

DANIO RERIO;

EID: 84865605055     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2012.05.001     Document Type: Review

References (93)

1. Monuki E.S., Walsh C.A. Proto-mapping the areas of cerebral cortex: transcription factors make the grade. Nat Neurosci 2000, 3:640-641.
2. Ragsdale C.W., Grove E.A. Patterning the mammalian cerebral cortex. Curr Opin Neurobiol 2001, 11:50-58.
3. Rubenstein J.L. Development of the cerebral cortex: V. Transcription factors and brain development. J Am Acad Child Adolesc Psychiatry 1998, 37:561-562.
4. Tao W., Lai E. Telencephalon-restricted expression of BF-1, a new member of the HNF-3/fork head gene family, in the developing rat brain. Neuron 1992, 8:957-966.
5. Shen Q., Wang Y., Dimos J.T., Fasano C.A., Phoenix T.N., Lemischka I.R., Ivanova N.B., Stifani S., Morrisey E.E., Temple S. The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 2006, 9:743-751.
6. Obendorf M., Meyer R., Henning K., Mitev Y.A., Schröder J., Patchev V.K., Wolf S.S. FoxG1, a member of the forkhead family, is a corepressor of the androgen receptor. J Steroid Biochem Mol Biol 2007, 104:195-207.
7. Bahi-Buisson N., Nectoux J., Girard B., Van Esch H., De Ravel T., Boddaert N., Plouin P., Rio M., Fichou Y., Chelly J., et al. Revisiting the phenotype associated with FOXG1 mutations: two novel cases of congenital Rett variant. Neurogenetics 2010, 11:241-249.
8. Jacob F.D., Ramaswamy V., Andersen J., Bolduc F.V. Atypical Rett syndrome with selective FOXG1 deletion detected by comparative genomic hybridization: case report and review of literature. Eur J Hum Genet 2009, 17:1577-1581.
9. Mencarelli M.A., Spanhol-Rosseto A., Artuso R., Rondinella D., De Filippis R., Bahi-Buisson N., Nectoux J., Rubinsztajn R., Bienvenu T., Moncla A., et al. Novel FOXG1 mutations associated with the congenital variant of Rett syndrome. J Med Genet 2010, 47:49-53.
10. Philippe C., Amsallem D., Francannet C., Lambert L., Saunier A., Verneau F., Jonveaux P. Phenotypic variability in Rett syndrome associated with FOXG1 mutations in females. J Med Genet 2010, 47:59-65.
11. Danesin C., Peres J.N., Johansson M., Snowden V., Cording A., Papalopulu N., Houart C. Integration of telencephalic Wnt and hedgehog signaling center activities by Foxg1. Dev Cell 2009, 16:576-587.
12. Shimamura K., Rubenstein J.L. Inductive interactions direct early regionalization of the mouse forebrain. Development 1997, 124:2709-2718.
13. Shimamura K., Hartigan D.J., Martinez S., Puelles L., Rubenstein J.L. Longitudinal organization of the anterior neural plate and neural tube. Development 1995, 121:3923-3933.
14. Houart C., Westerfield M., Wilson S.W. A small population of anterior cells patterns the forebrain during zebrafish gastrulation. Nature 1998, 391:788-792.
15. Houart C., Caneparo L., Heisenberg C., Barth K., Take-Uchi M., Wilson S. Establishment of the telencephalon during gastrulation by local antagonism of Wnt signaling. Neuron 2002, 35:255-265.
16. Lagutin O.V., Zhu C.C., Kobayashi D., Topczewski J., Shimamura K., Puelles L., Russell H.R., McKinnon P.J., Solnica-Krezel L., Oliver G. Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev 2003, 17:368-379.
17. Masai I., Heisenberg C.P., Barth K.A., Macdonald R., Adamek S., Wilson S.W. Floating head and masterblind regulate neuronal patterning in the roof of the forebrain. Neuron 1997, 18:43-57.
18. Wilson S.W., Houart C. Early steps in the development of the forebrain. Dev Cell 2004, 6:167-181.
19. Paek H., Gutin G., Hébert J.M. FGF signaling is strictly required to maintain early telencephalic precursor cell survival. Development 2009, 136:2457-2465.
20. Storm E.E., Garel S., Borello U., Hebert J.M., Martinez S., McConnell S.K., Martin G.R., Rubenstein J.L. Dose-dependent functions of Fgf8 in regulating telencephalic patterning centers. Development 2006, 133:1831-1844.
21. Ye W., Shimamura K., Rubenstein J.L., Hynes M.A., Rosenthal A. FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 1998, 93:755-766.
22. Storm E.E., Rubenstein J.L., Martin G.R. Dosage of Fgf8 determines whether cell survival is positively or negatively regulated in the developing forebrain. Proc Natl Acad Sci USA 2003, 100:1757-1762.
23. Meyers E.N., Lewandoski M., Martin G.R. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat Genet 1998, 18:136-141.
24. Hanashima C., Fernandes M., Hebert J.M., Fishell G. The role of Foxg1 and dorsal midline signaling in the generation of Cajal-Retzius subtypes. J Neurosci 2007, 27:11103-11111.
25. Stigloher C., Ninkovic J., Laplante M., Geling A., Tannhäuser B., Topp S., Kikuta H., Becker T.S., Houart C., Bally-Cuif L. Segregation of telencephalic and eye-field identities inside the zebrafish forebrain territory is controlled by Rx3. Development 2006, 133:2925-2935.
26. Beccari L., Conte I., Cisneros E., Bovolenta P. Sox2-mediated differential activation of Six3.2 contributes to forebrain patterning. Development 2012, 139:151-164.
27. Furuta Y., Piston D.W., Hogan B.L. Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 1997, 124:2203-2212.
28. Grove E.A., Tole S., Limon J., Yip L., Ragsdale C.W. The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 1998, 125:2315-2325.
29. Lee S.M., Tole S., Grove E., McMahon A.P. A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 2000, 127:457-467.
30. Bourguignon C., Li J., Papalopulu N. XBF-1, a winged helix transcription factor with dual activity, has a role in positioning neurogenesis in Xenopus competent ectoderm. Development 1998, 125:4889-4900.
31. Dou C., Lee J., Liu B., Liu F., Massague J., Xuan S., Lai E. BF-1 interferes with transforming growth factor beta signaling by associating with Smad partners. Mol Cell Biol 2000, 20:6201-6211.
32. Seoane J., Le H.V., Shen L., Anderson S.A., Massague J. Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 2004, 117:211-223.
33. Yao J., Lai E., Stifani S. The winged-helix protein brain factor 1 interacts with groucho and hes proteins to repress transcription. Mol Cell Biol 2001, 21:1962-1972.
34. Ahlgren S., Vogt P., Bronner-Fraser M. Excess FoxG1 causes overgrowth of the neural tube. J Neurobiol 2003, 57:337-349.
35. Sonderegger C.K., Vogt P.K. Binding of the corepressor TLE1 to Qin enhances Qin-mediated transformation of chicken embryo fibroblasts. Oncogene 2003, 22:1749-1757.
36. Tan K., Shaw A.L., Madsen B., Jensen K., Taylor-Papadimitriou J., Freemont P.S. Human PLU-1 Has transcriptional repression properties and interacts with the developmental transcription factors BF-1 and PAX9. J Biol Chem 2003, 278:20507-20513.
37. Martynoga B., Morrison H., Price D.J., Mason J.O. Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis. Dev Biol 2005, 283:113-127.
38. Xuan S., Baptista C.A., Balas G., Tao W., Soares V.C., Lai E. Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 1995, 14:1141-1152.
39. Manuel M., Martynoga B., Yu T., West J.D., Mason J.O., Price D.J. The transcription factor Foxg1 regulates the competence of telencephalic cells to adopt subpallial fates in mice. Development 2010, 137:487-497.
40. Shanmugalingam S., Houart C., Picker A., Reifers F., Macdonald R., Barth A., Griffin K., Brand M., Wilson S.W. Ace/Fgf8 is required for forebrain commissure formation and patterning of the telencephalon. Development 2000, 127:2549-2561.
41. Shinya M., Koshida S., Sawada A., Kuroiwa A., Takeda H. Fgf signalling through MAPK cascade is required for development of the subpallial telencephalon in zebrafish embryos. Development 2001, 128:4153-4164.
42. Walshe J., Mason I. Unique and combinatorial functions of Fgf3 and Fgf8 during zebrafish forebrain development. Development 2003, 130:4337-4349.
43. Gutin G., Fernandes M., Palazzolo L., Paek H., Yu K., Ornitz D.M., McConnell S.K., Hebert J.M. FGF signalling generates ventral telencephalic cells independently of SHH. Development 2006, 133:2937-2946.
44. Kohtz J.D., Baker D.P., Corte G., Fishell G. Regionalization within the mammalian telencephalon is mediated by changes in responsiveness to Sonic Hedgehog. Development 1998, 125:5079-5089.
45. Ohkubo Y., Chiang C., Rubenstein J.L. Coordinate regulation and synergistic actions of BMP4, SHH and FGF8 in the rostral prosencephalon regulate morphogenesis of the telencephalic and optic vesicles. Neuroscience 2002, 111:1-17.
46. Rallu M., Machold R., Gaiano N., Corbin J.G., McMahon A.P., Fishell G. Dorsoventral patterning is established in the telencephalon of mutants lacking both Gli3 and Hedgehog signaling. Development 2002, 129:4963-4974.
47. Kuschel S., Ruther U., Theil T. A disrupted balance between Bmp/Wnt and Fgf signaling underlies the ventralization of the Gli3 mutant telencephalon. Dev Biol 2003, 260:484-495.
48. Chiang C., Litingtung Y., Lee E., Young K.E., Corden J.L., Westphal H., Beachy P.A. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 1996, 383:407-413.
49. Ericson J., Muhr J., Placzek M., Lints T., Jessell T.M., Edlund T. Sonic hedgehog induces the differentiation of ventral forebrain neurons: a common signal for ventral patterning within the neural tube. Cell 1995, 81:747-756.
50. Crossley P.H., Martinez S., Ohkubo Y., Rubenstein J.L. Coordinate expression of Fgf8, Otx2, Bmp4, and Shh in the rostral prosencephalon during development of the telencephalic and optic vesicles. Neuroscience 2001, 108:183-206.
51. Aoto K., Nishimura T., Eto K., Motoyama J. Mouse GLI3 regulates Fgf8 expression and apoptosis in the developing neural tube, face, and limb bud. Dev Biol 2002, 251:320-332.
52. Huh S., Hatini V., Marcus R.C., Li S.C., Lai E. Dorsal-ventral patterning defects in the eye of BF-1-deficient mice associated with a restricted loss of shh expression. Dev Biol 1999, 211:53-63.
53. Hardcastle Z., Papalopulu N. Distinct effects of XBF-1 in regulating the cell cycle inhibitor p27(XIC1) and imparting a neural fate. Development 2000, 127:1303-1314.
54. Dou C.L., Li S., Lai E. Dual role of brain factor-1 in regulating growth and patterning of the cerebral hemispheres. Cereb Cortex 1999, 9:543-550.
55. Hanashima C., Shen L., Li S.C., Lai E. Brain factor-1 controls the proliferation and differentiation of neocortical progenitor cells through independent mechanisms. J Neurosci 2002, 22:6526-6536.
56. Muzio L., Mallamaci A. Foxg1 confines Cajal-Retzius neuronogenesis and hippocampal morphogenesis to the dorsomedial pallium. J Neurosci 2005, 25:4435-4441.
57. Hebert J.M., Mishina Y., McConnell S.K. BMP signaling is required locally to pattern the dorsal telencephalic midline. Neuron 2002, 35:1029-1041.
58. Panchision D.M., Pickel J.M., Studer L., Lee S.H., Turner P.A., Hazel T.G., McKay R.D. Sequential actions of BMP receptors control neural precursor cell production and fate. Genes Dev 2001, 15:2094-2110.
59. Fernandes M., Gutin G., Alcorn H., McConnell S.K., Hébert J.M. Mutations in the BMP pathway in mice support the existence of two molecular classes of holoprosencephaly. Development 2007, 134:3789-3794.
60. Galceran J., Miyashita-Lin E.M., Devaney E., Rubenstein J.L., Grosschedl R. Hippocampus development and generation of dentate gyrus granule cells is regulated by LEF1. Development 2000, 127:469-482.
61. Bhide P.G. Cell cycle kinetics in the embryonic mouse corpus striatum. J Comp Neurol 1996, 374:506-522.
62. Caviness V.S., Takahashi T. Proliferative events in the cerebral ventricular zone. Brain Dev 1995, 17:159-163.
63. Sheth A.N., Bhide P.G. Concurrent cellular output from two proliferative populations in the early embryonic mouse corpus striatum. J Comp Neurol 1997, 383:220-230.
64. Takahashi T., Nowakowski R.S., Caviness V.S. Interkinetic and migratory behavior of a cohort of neocortical neurons arising in the early embryonic murine cerebral wall. J Neurosci 1996, 16:5762-5776.
65. Hanashima C., Li S.C., Shen L., Lai E., Fishell G. Foxg1 suppresses early cortical cell fate. Science 2004, 303:56-59.
66. Machon O., Backman M., Machonova O., Kozmik Z., Vacik T., Andersen L., Krauss S. A dynamic gradient of Wnt signaling controls initiation of neurogenesis in the mammalian cortex and cellular specification in the hippocampus. Dev Biol 2007, 311:223-237.
67. Machon O., van den Bout C.J., Backman M., Kemler R., Krauss S. Role of beta-catenin in the developing cortical and hippocampal neuroepithelium. Neuroscience 2003, 122:129-143.
68. Hirabayashi Y., Itoh Y., Tabata H., Nakajima K., Akiyama T., Masuyama N., Gotoh Y. The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 2004, 131:2791-2801.
69. Karalay O., Doberauer K., Vadodaria K.C., Knobloch M., Berti L., Miquelajauregui A., Schwark M., Jagasia R., Taketo M.M., Tarabykin V., et al. Prospero-related homeobox 1 gene (Prox1) is regulated by canonical Wnt signaling and has a stage-specific role in adult hippocampal neurogenesis. Proc Natl Acad Sci USA 2011, 108:5807-5812.
70. Lyu J., Yamamoto V., Lu W. Cleavage of the Wnt receptor Ryk regulates neuronal differentiation during cortical neurogenesis. Dev Cell 2008, 15:773-780.
71. Munji R.N., Choe Y., Li G., Siegenthaler J.A., Pleasure S.J. Wnt signaling regulates neuronal differentiation of cortical intermediate progenitors. J Neurosci 2011, 31:1676-1687.
72. Dahmane N., Sánchez P., Gitton Y., Palma V., Sun T., Beyna M., Weiner H., Ruiz i Altaba A. The Sonic Hedgehog-Gli pathway regulates dorsal brain growth and tumorigenesis. Development 2001, 128:5201-5212.
73. Xu Q., Wonders C.P., Anderson S.A. Sonic hedgehog maintains the identity of cortical interneuron progenitors in the ventral telencephalon. Development 2005, 132:4987-4998.
74. Pozniak C.D., Pleasure S.J. A tale of two signals: Wnt and Hedgehog in dentate neurogenesis. Sci STKE 2006, 2006:pe5.
75. Takahashi S., Matsumoto N., Okayama A., Suzuki N., Araki A., Okajima K., Tanaka H., Miyamoto A. FOXG1 mutations in Japanese patients with the congenital variant of Rett syndrome. Clin Genet 2011, 10.1111/j.1399-0004.2011.01819.
76. De Filippis R., Pancrazi L., Bjørgo K., Rosseto A., Kleefstra T., Grillo E., Panighini A., Cardarelli F., Meloni I., Ariani F., et al. Expanding the phenotype associated with FOXG1 mutations and in vivo FoxG1 chromatin-binding dynamics. Clin Genet 2011, 10.1111/j.1399-0004.2011.01810.
77. Kortüm F., Das S., Flindt M., Morris-Rosendahl D.J., Stefanova I., Goldstein A., Horn D., Klopocki E., Kluger G., Martin P., et al. The core FOXG1 syndrome phenotype consists of postnatal microcephaly, severe mental retardation, absent language, dyskinesia, and corpus callosum hypogenesis. J Med Genet 2011, 48:396-406.
78. Le Guen T., Fichou Y., Nectoux J., Bahi-Buisson N., Rivier F., Boddaert N., Diebold B., Héron D., Chelly J., Bienvenu T. A missense mutation within the fork-head domain of the forkhead box G1 Gene (FOXG1) affects its nuclear localization. Hum Mutat 2011, 32:E2026-E2035.
79. Brunetti-Pierri N., Paciorkowski A.R., Ciccone R., Mina E.D., Bonaglia M.C., Borgatti R., Schaaf C.P., Sutton V.R., Xia Z., Jelluma N., et al. Duplications of FOXG1 in 14q12 are associated with developmental epilepsy, mental retardation, and severe speech impairment. Eur J Hum Genet 2011, 19:102-107.
80. Ariani F., Hayek G., Rondinella D., Artuso R., Mencarelli M.A., Spanhol-Rosseto A., Pollazzon M., Buoni S., Spiga O., Ricciardi S., et al. FOXG1 is responsible for the congenital variant of Rett syndrome. Am J Hum Genet 2008, 83:89-93.
81. Yoshioka S., King M.L., Ran S., Okuda H., Maclean J.A., McAsey M.E., Sugino N., Brard L., Watabe K., Hayashi K. WNT7A regulates tumor growth and progression in ovarian cancer through the WNT/β-catenin pathway. Mol Cancer Res 2012, 10:469-482.
82. Bitler B.G., Nicodemus J.P., Li H., Cai Q., Wu H., Hua X., Li T., Birrer M.J., Godwin A.K., Cairns P., et al. Wnt5a suppresses epithelial ovarian cancer by promoting cellular senescence. Cancer Res 2011, 71:6184-6194.
83. Chan D.W., Liu V.W., To R.M., Chiu P.M., Lee W.Y., Yao K.M., Cheung A.N., Ngan H.Y. Overexpression of FOXG1 contributes to TGF-beta resistance through inhibition of p21WAF1/CIP1 expression in ovarian cancer. Br J Cancer 2009, 101:1433-1443.
84. Okerlund N.D., Cheyette B.N. Synaptic Wnt signaling-a contributor to major psychiatric disorders?. J Neurodev Disord 2011, 3:162-174.
85. Ahmad-Annuar A., Ciani L., Simeonidis I., Herreros J., Fredj N.B., Rosso S.B., Hall A., Brickley S., Salinas P.C. Signaling across the synapse: a role for Wnt and Dishevelled in presynaptic assembly and neurotransmitter release. J Cell Biol 2006, 174:127-139.
86. Lucas F.R., Salinas P.C. WNT-7a induces axonal remodeling and increases synapsin I levels in cerebellar neurons. Dev Biol 1997, 192:31-44.
87. Hall A.C., Lucas F.R., Salinas P.C. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 2000, 100:525-535.
88. Sahores M., Gibb A., Salinas P.C. Frizzled-5, a receptor for the synaptic organizer Wnt7a, regulates activity-mediated synaptogenesis. Development 2010, 137:2215-2225.
89. Farías G.G., Godoy J.A., Cerpa W., Varela-Nallar L., Inestrosa N.C. Wnt signaling modulates pre- and postsynaptic maturation: therapeutic considerations. Dev Dyn 2010, 239:94-101.
90. Bamji S.X., Shimazu K., Kimes N., Huelsken J., Birchmeier W., Lu B., Reichardt L.F. Role of beta-catenin in synaptic vesicle localization and presynaptic assembly. Neuron 2003, 40:719-731.
91. Salinas P.C., Zou Y. Wnt signaling in neural circuit assembly. Annu Rev Neurosci 2008, 31:339-358.
92. Regad T., Roth M., Bredenkamp N., Illing N., Papalopulu N. The neural progenitor-specifying activity of FoxG1 is antagonistically regulated by CKI and FGF. Nat Cell Biol 2007, 9:531-540.
93. Rash B.G., Grove E.A. Patterning the dorsal telencephalon: a role for sonic hedgehog?. J Neurosci 2007, 27:11595-11603.