A disrupted balance between Bmp/Wnt and Fgf signaling underlies the ventralization of the Gli3 mutant telencephalon

Developmental Biology

Volumn 260, Issue 2, 2003, Pages 484-495

  Kuschel, Stefanie ^a   Rüther, Ulrich ^a   Theil, Thomas ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Bmp; Dorsal ventral patterning; Fgf8; Forebrain; Gli3; Mouse; Shh; Wnt

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR; MUTANT PROTEIN; TRANSCRIPTION FACTOR GLI3; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; GENE LOCUS; GENETIC TRANSCRIPTION; HOMOZYGOSITY; NONHUMAN; PRIORITY JOURNAL; RETROPOSON; SIGNAL TRANSDUCTION; TELENCEPHALON;

ANIMALIA;

EID: 0042061387     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0012-1606(03)00252-5     Document Type: Article

References (67)

1. 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. 251:2002;320-332.
2. Berman D.M., Karhadkar S.S., Hallahan A.R., Pritchard J.I., Eberhart C.G., Watkins D.N., Chen J.K., Cooper M.K., Taipale J., Olson J.M., Beachy P.A. Medulloblastoma growth inhibition by hedgehog pathway blockade. Science. 297:2002;1559-1561.
3. Bulfone A., Puelles L., Porteus M.H., Frohman M.A., Martin G.R., Rubenstein J.L. Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J. Neurosci. 13:1993;3155-3172.
4. Büscher D., Bosse B., Heymer J., Rüther U. Evidence for genetic control of Sonic hedgehog by Gli3 in mouse limb development. Development. 124:1997;1313-1322.
5. Büscher D., Grotewold L., Rüther U. The Xt-J allele generates a Gli3 fusion transcript. Mamm. Genome. 9:1998;676-678.
6. Casarosa S., Fode C., Guillemot F. Mash1 regulates neurogenesis in the ventral telencephalon. Development. 126:1999;525-534.
7. 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. 383:1996;407-413.
8. Couly G.F., Le Douarin N.M. Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev. Biol. 110:1985;422-439.
9. Couly G.F., Le Douarin N.M. Mapping of the early neural primordium in quail-chick chimeras. II. The prosencephalic neural plate and neural folds implications for the genesis of cephalic human congenital abnormalities . Dev. Biol. 120:1987;198-214.
10. Crossley P.H., Martin G.R. The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development. 121:1995;439-451.
11. 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. 108:2001;183-206.
12. Ding Q., Motoyama J., Gasca S., Mo R., Sasaki H., Rossant J., Hui C.C. Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development. 125:1998;2533-2543.
13. Dou C.L., Li S., Lai E. Dual role of brain factor-1 in regulating growth and patterning of the cerebral hemispheres. Cereb. Cortex. 9:1999;543-550.
14. Eagleson G., Ferreiro B., Harris W.A. Fate of the anterior neural ridge and the morphogenesis of the Xenopus forebrain. J. Neurobiol. 28:1995;146-158.
15. Eagleson G.W., Harris W.A. Mapping of the presumptive brain regions in the neural plate of Xenopus laevis. J. Neurobiol. 21:1990;427-440.
16. 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. 81:1995;747-756.
17. Fode C., Ma Q., Casarosa S., Ang S.L., Anderson D.J., Guillemot F. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 14:2000;67-80.
18. Franz T. Extra-toes (Xt) homozygous mutant mice demonstrate a role for the Gli-3 gene in the development of the forebrain. Acta Anat. 150:1994;38-44.
19. Fukuchi-Shimogori T., Grove E.A. Neocortex patterning by the secreted signaling molecule FGF8. Science. 294:2001;1071-1074.
20. Furuta Y., Piston D.W., Hogan B.L. Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development. 124:1997;2203-2212.
21. 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. 127:2000;469-482.
22. Garel S., Huffman K.J., Rubenstein J.L. Molecular regionalization of the neocortex is disrupted in Fgf8 hypomorphic mutants. Development. 130:2003;1903-1914.
23. Golden J.A., Bracilovic A., McFadden K.A., Beesley J.S., R Rubenstein J.L., Grinspan J.B. Ectopic bone morphogenetic proteins 5 and 4 in the chicken forebrain lead to cyclopia and holoprosencephaly. Proc. Natl. Acad. Sci. USA. 96:1999;2439-2444.
24. Gradwohl G., Fode C., Guillemot F. Restricted expression of a novel murine atonal-related bHLH protein in undifferentiated neural precursors. Dev. Biol. 180:1996;227-241.
25. 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. 125:1998;2533-2543.
26. Guillemot F., Joyner A.L. Dynamic expression of the murine Achaete-Scute homologue Mash-1 in the developing nervous system. Mech. Dev. 42:1993;171-185.
27. Hebert J.M., Mishina Y., McConnell S.K. BMP signaling is required locally to pattern the dorsal telencephalic midline. Neuron. 35:2002;1029-1041.
28. Houart C., Westerfield M., Wilson S.W. A small population of anterior cells patterns the forebrain during zebrafish gastrulation. Nature. 391:1998;788-792.
29. Hui C.C., Joyner A.L. A mouse model of greig cephalopolysyndactyly syndrome the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene . Ciba Found. Symp. 181:1993;118-134. discussion 134-143.
30. Jessell T.M. Neuronal specification in the spinal cord inductive signals and transcriptional codes . Nat. Rev. Genet. 1:2000;20-29.
31. Johnson D.R. Extra-toes a new mutant gene causing multiple abnormalities in the mouse . J. Embryol. Exp. Morphol. 17:1967;543-581.
32. Jones C.M., Lyons K.M., Hogan B.L. Involvement of Bone Morphogenetic Protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development. 111:1991;531-542.
33. 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. 125:1998;5079-5089.
34. Lazzaro D., Price M., de Felice M., Di Lauro R. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development. 113:1991;1093-1104.
35. Lee S.M., Tole S., Grove E., McMahon A.P. A local Wnt-3a signal is required for development of the mammalian hippocampus. Development. 127:2000;457-467.
36. Litingtung Y., Chiang C. Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat. Neurosci. 3:2000;979-985.
37. Marin O., Rubenstein J.L.R. Patterning, regionalization and cell differentiation in the forebrain. Rossant J., Tam P. Mouse Development. 2002;75-106 Academic Press, San Diego.
38. Masuya H., Sagai T., Moriwaki K., Shiroishi T. Multigenic control of the localization of the zone of polarizing activity in limb morphogenesis in the mouse. Nat. Genet. 15:1997;266-268.
39. Matise M.P., Epstein D.J., Park H.L., Platt K.A., Joyner A.L. Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development. 125:1998;2759-2770.
40. Maynard T.M., Jain M.D., Balmer C.W., LaMantia A.S. High-resolution mapping of the Gli3 mutation extra-toes reveals a 51.5-kb deletion. Mamm. Genome. 13:2002;58-61.
41. Meyers E.N., Lewandoski M., Martin G.R. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 18:1998;136-141.
42. Minowada G., Jarvis L.A., Chi C.L., Neubuser A., Sun X., Hacohen N., Krasnow M.A., Martin G.R. Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development. 126:1999;4465-4475.
43. 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. 111:2002;1-17.
44. Parras C.M., Schuurmans C., Scardigli R., Kim J., Anderson D.J., Guillemot F. Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes Dev. 16:2002;324-338.
45. Puelles L., Kuwana E., Puelles E., Rubenstein J.L. Comparison of the mammalian and avian telencephalon from the perspective of gene expression data. Eur. J. Morphol. 37:1999;139-150.
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. 129:2002;4963-4974.
47. Rubenstein J.L., Shimamura K., Martinez S., Puelles L. Regionalization of the prosencephalic neural plate. Annu. Rev. Neurosci. 21:1998;445-477.
48. Schimmang T., Oda S.I., Rüther U. The mouse mutant Polydactyly Nagoya (Pdn) defines a novel allele of the zinc finger gene Gli3. Hum. Mol. Genet. 3:1994;1405-1408.
49. 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. 127:2000;2549-2561.
50. Shimamura K., Rubenstein J.L. Inductive interactions direct early regionalization of the mouse forebrain. Development. 124:1997;2709-2718.
51. 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. 128:2001;4153-4164.
52. Simeone A., Gulisano M., Acampora D., Stornaiuolo A., Rambaldi M., Boncinelli E. Two vertebrate homeobox genes related to the Drosophila empty spiracles gene are expressed in the embryonic cerebral cortex. EMBO J. 11:1992;2541-2550.
53. Simeone A., Acampora D., Pannese M., D'Esposito M., Stornaiuolo A., Gulisano M., Mallamaci A., Kastury K., Druck T., Huebner K., et al. Cloning and characterization of two members of the vertebrate Dlx gene family. Proc. Natl. Acad. Sci. USA. 91:1994;2250-2254.
54. 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. 100:2003;1757-1762.
55. Stoykova A., Treichel D., Hallonet M., Gruss P. Pax6 modulates the dorsoventral patterning of the mammalian telencephalon. J. Neurosci. 20:2000;8042-8050.
56. Theil T., Alvarez-Bolado G., Walter A., Rüther U. Gli3 is required for Emx gene expression during dorsal telencephalon development. Development. 126:1999;3561-3571.
57. Theil T., Ariza-McNaughton L., Manzanares M., Brodie J., Krumlauf R., Wilkinson D.G. Requirement for downregulation of kreisler during late patterning of the hindbrain. Development. 129:2002;1477-1485.
58. Theil T., Aydin S., Koch S., Grotewold L., Rüther U. Wnt and Bmp signalling cooperatively regulate graded Emx2 expression in the dorsal telencephalon. Development. 129:2002;3045-3054.
59. Thein H., Rüther U. The mouse mutation Pdn (Polydactyly Nagoya) is caused by the integration of a retrotransposon into the Gli3 gene. Mamm. Genome. 10:1999;205-209.
60. Tole S., Ragsdale C.W., Grove E.A. Dorsoventral patterning of the telencephalon is disrupted in the mouse mutant extra-toes(J). Dev. Biol. 217:2000;254-265.
61. Toresson H., Potter S.S., Campbell K. Genetic control of dorsal-ventral identity in the telencephalon opposing roles for Pax6 and Gsh2 . Development. 127:2000;4361-4371.
62. Tsuchida T., Ensini M., Morton S.B., Baldassare M., Edlund T., Jessell T.M., Pfaff S.L. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell. 79:1994;957-970.
63. Walther C., Gruss P. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development. 113:1991;1435-1449.
64. Wilson S.W., Rubenstein J.L. Induction and dorsoventral patterning of the telencephalon. Neuron. 28:2000;641-651.
65. 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. 93:1998;755-766.
66. Yun K., Potter S., Rubenstein J.L. Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development. 128:2001;193-205.
67. Yun K., Fischman S., Johnson J., De Angelis M.H., Weinmaster G., Rubenstein J.L. Modulation of the notch signaling by Mash1 and Dlx1/2 regulates sequential specification and differentiation of progenitor cell types in the subcortical telencephalon. Development. 129:2002;5029-5040.