Gli3 is required autonomously for dorsal telencephalic cells to adopt appropriate fates during embryonic forebrain development

Developmental Biology

Volumn 327, Issue 1, 2009, Pages 204-215

  Quinn, Jane C ^a,b   Molinek, Michael ^a   Mason, John O ^a   Price, David J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b CHARLES STURT UNIVERSITY   (Australia)

Author keywords

Chimera; Forebrain; Gli3; Mouse; Telencephalon

Indexed keywords

GLUTAMATE DECARBOXYLASE 67; GLUTATHIONE SYNTHASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DLX2; TRANSCRIPTION FACTOR FOXG1; TRANSCRIPTION FACTOR GLI3; TRANSCRIPTION FACTOR LHX1; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; DIENCEPHALON; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; FOREBRAIN; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TELENCEPHALON;

EID: 59649089100     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.12.008     Document Type: Article

References (51)

1. Aboitiz F., and Montiel J. Co-option of signaling mechanisms from neural induction to telencephalic patterning. Rev. Neurosci. 18 (2007) 311-342
2. Aoto K., Nishimura T., Eto K., and Motoyama J. Mouse GLI3 regulates Fgf8 expression and apoptosis in the developing neural tube, face, and limb bud. Dev. Biol. 251 (2002) 320-332
3. Blaess S., Corrales J.D., and Joyner A.L. Sonic hedgehog regulates Gli activator and repressor functions with spatial and temporal precision in the mid/hindbrain region. Development 133 (2006) 1799-1809
4. Blaess S., Stephen D., and Joyner A.L. Gli3 coordinates three-dimensional patterning and growth of the tectum and cerebellum by integrating Shh and Fgf8 signaling. Development 135 (2008) 2093-2103
5. Brox A., Puelles L., Ferreiro B., and Medina L. Expression of the genes Emx1, Tbr1, and Eomes (Tbr2) in the telencephalon of Xenopus laevis confirms the existence of a ventral pallial division in all tetrapods. J. Comp. Neurol. 474 (2004) 562-577
6. Bulfone A., Puelles L., Porteus M.H., Frohman M.A., Martin G.R., and 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
7. Casarosa S., Fode C., and Guillemot F. Mash1 regulates neurogenesis in the ventral telencephalon. Development 126 (1999) 525-534
8. Copp A.J. Genetic models of mammalian neural tube defects. Ciba Found. Symp. 181 (1994) 118-134 discussion 134-43
9. Englund C., Fink A., Lau C., Pham D., Daza R.A., Bulfone A., Kowalczyk T., and Hevner R.F. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25 (2005) 247-251
10. Fotaki V., Yu T., Zaki P.A., Mason J.O., and Price D.J. Abnormal positioning of diencephalic cell types in neocortical tissue in the dorsal telencephalon of mice lacking functional Gli3. J. Neurosci. 26 (2006) 9282-9292
11. Franz T. Extra-toes (Xt) homozygous mutant mice demonstrate a role for the Gli-3 gene in the development of the forebrain. Acta Anat. (Basel) 150 (1994) 38-44
12. Franz T., and Besecke A. The development of the eye in homozygotes of the mouse mutant Extra-toes. Anat. Embryol. (Berl) 184 (1991) 355-361
13. Grove E.A., Tole S., Limon J., Yip L., and 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) 2315-2325
14. Hebert J.M., and Fishell G. The genetics of early telencephalon patterning: some assembly required. Nat. Rev. Neurosci. 9 (2008) 678-685
15. Hsieh-Li H.M., Witte D.P., Szucsik J.C., Weinstein M., Li H., and Potter S.S. Gsh-2, a murine homeobox gene expressed in the developing brain. Mech. Dev. 50 (1995) 177-186
16. Hui C.C., and Joyner A.L. A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat. Genet. 3 (1993) 241-246
17. Johnson D.R. Extra-toes: anew mutant gene causing multiple abnormalities in the mouse. J. Embryol. Exp. Morphol. 17 (1967) 543-581
18. Kitamura K., Miura H., Yanazawa M., Miyashita T., and Kato K. Expression patterns of Brx1 (Rieg gene), Sonic hedgehog, Nkx2.2, Dlx1 and Arx during zona limitans intrathalamica and embryonic ventral lateral geniculate nuclear formation. Mech. Dev. 67 (1997) 83-96
19. Kuschel S., Ruther U., and Theil T. A disrupted balance between Bmp/Wnt and Fgf signaling underlies the ventralization of the Gli3 mutant telencephalon. Dev. Biol. 260 (2003) 484-495
20. Lo C.W., Coulling M., and Kirby C. Tracking of mouse cell lineage using microinjected DNA sequences: analyses using genomic Southern blotting and tissue-section in situ hybridizations. Differentiation 35 (1987) 37-44
21. López-Bendito G., Sturgess K., Erdélyi F., Szabó G., Molnár Z., and Paulsen O. Preferential origin and layer destination of GAD65-GFP cortical interneurons. Cereb. Cortex 14 (2004) 1122-1133
22. Maynard T.M., Jain M.D., Balmer C.W., and LaMantia A.S. High-resolution mapping of the Gli3 mutation extra-toes reveals a 51.5-kb deletion. Mamm. Genome 13 (2002) 58-61
23. Meyer N.P., and Roelink H. The amino-terminal region of Gli3 antagonizes the Shh response and acts in dorsoventral fate specification in the developing spinal cord. Dev. Biol. 257 (2003) 343-355
24. Price M. Members of the Dlx- and Nkx2-gene families are regionally expressed in the developing forebrain. J. Neurobiol. 24 (1993) 1385-1399
25. Quinn J.C., Molinek M., Martynoga B.S., Zaki P.A., Faedo A., Bulfone A., Hevner R.F., West J.D., and Price D.J. Pax6 controls cerebral cortical cell number by regulating exit from the cell cycle and specifies cortical cell identity by a cell autonomous mechanism. Dev. Biol. 302 (2007) 50-65
26. Rallu M., Machold R., Gaiano N., Corbin J.G., McMahon A.P., and Fishell G. Dorsoventral patterning is established in the telencephalon of mutants lacking both Gli3 and Hedgehog signaling. Development 129 (2002) 4963-4974
27. Rash B.G., and Grove E.A. Patterning the dorsal telencephalon: a role for sonic hedgehog?. J. Neurosci. 27 (2007) 11595-11603
28. Sheng H.Z., Bertuzzi S., Chiang C., Shawlot W., Taira M., Dawid I., and Westphal H. Expression of murine Lhx5 suggests a role in specifying the forebrain. Dev. Dyn. 208 (1997) 266-277
29. Shimogori T., Banuchi V., Ng H.Y., Strauss J.B., and Grove E.A. Embryonic signaling centers expressing BMP, WNT and FGF proteins interact to pattern the cerebral cortex. Development 131 (2004) 5639-5647
30. Stoykova A., Götz M., Gruss P., and Price J. Pax6-dependent regulation of adhesive patterning, R-cadherin expression and boundary formation in developing forebrain. Development 124 (1997) 3765-3777
31. Sussel L., Marin O., Kimura S., and Rubenstein J.L. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126 (1999) 3359-3370
32. Takahashi H., and Liu F.C. Genetic patterning of the mammalian telencephalon by morphogenetic molecules and transcription factors. Birth Defects Res. C Embryo Today 78 (2006) 256-266
33. Tam P.P.L., and Rossant J. Mouse embryonic chimeras: tools for studying mammalian development. Development 130 (2003) 6155-6163
34. Tao W., and 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 8 (1992) 957-966
35. Theil T. Gli3 is required for the specification and differentiation of preplate neurons. Dev. Biol. 286 (2005) 559-571
36. Theil T., Alvarez-Bolado G., Walter A., and Ruther U. Gli3 is required for Emx gene expression during dorsal telencephalon development. Development 126 (1999) 3561-3571
37. Theil T., Aydin S., Koch S., Grotewold L., and Ruther U. Wnt and Bmp signalling cooperatively regulate graded Emx2 expression in the dorsal telencephalon. Development 129 (2002) 3045-3054
38. Tole S., Ragsdale C.W., and Grove E.A. Dorsoventral patterning of the telencephalon is disrupted in the mouse mutant extra-toes(J). Dev. Biol. 217 (2000) 254-265
39. Turksen K. Embryonic Stem Cells, Methods and Protocols (2002), Humana Press, Totowa, New Jersey
40. Ulloa F., and Briscoe J. Morphogens and the control of cell proliferation and patterning in the spinal cord. Cell Cycle 6 (2007) 2640-2649
41. Vortkamp A., Franz T., Gessler M., and Grzeschik K.H. Deletion of GLI3 supports the homology of the human Greig cephalopolysyndactyly syndrome (GCPS) and the mouse mutant extra toes (Xt). Mamm. Genome 3 (1992) 461-463
42. Vue T.Y., Aaker J., Taniguchi A., Kazemzadeh C., Skidmore J.M., Martin D.M., Martin J.F., Treier M., and Nakagawa Y. Characterization of progenitor domains in the developing mouse thalamus. J. Comp. Neurol. 505 (2007) 73-91
43. Vyas A., Saha B., Lai E., and Tole S. Paleocortex is specified in mice in which dorsal telencephalic patterning is severely disrupted. J. Comp. Neurol. 466 (2003) 545-553
44. Walther C., and Gruss P. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113 (1991) 1435-1449
45. West J.D., and Flockhart J.H. Genotypically unbalanced diploid < = = > diploid foetal mouse chimaeras: possible relevance to human confined mosaicism. Genet. Res. 63 (1994) 87-99
46. Winter R.M., and Huson S.M. Greig cephalopolysyndactyly syndrome: a possible mouse homologue (Xt-extra toes). Am. J. Med. Genet. 31 (1988) 793-798
47. Wonders C.P., and Anderson S.A. The origin and specification of cortical interneurons. Nat. Rev., Neurosci. 7 (2006) 687-696
48. Xuan S., Baptista C.A., Balas G., Tao W., Soares V.C., and Lai E. Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 14 (1995) 1141-1152
49. Yamazaki H., Sekiguchi M., Takamatsu M., Tanabe Y., and Nakanishi S. Distinct ontogenic and regional expressions of newly identified Cajal-Retzius cell-specific genes during neocorticogenesis. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 14509-14514
50. Zaki P.A., Martynoga B., Delafield-Butt J.T., Fotaki V., Yu T., and Price D.J. Loss of Gli3 enhances the viability of embryonic telencephalic cells in vitro. Eur. J. Neurosci. 22 (2005) 1547-1551
51. Zaki P.A., Collinson J.M., Toraiwa J., Simpson T.I., Price D.J., and Quinn J.C. Penetrance of eye defects in mice heterozygous for mutation of Gli3 is enhanced by heterozygous mutation of Pax6. BMC Dev. Biol. 6 (2006) 46