Lamination of the cerebral cortex is disturbed in Gli3 mutant mice

Developmental Biology

Volumn 318, Issue 1, 2008, Pages 203-214

  Friedrichs, Melanie ^a   Larralde, Osmany ^c   Skutella, Thomas ^b   Theil, Thomas ^a,b,c  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b Anatomical Institute   (Germany)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cerebral cortex; Gli3; Lamination; Reelin

Indexed keywords

CALRETININ; REELIN; TRANSCRIPTION FACTOR GLI3;

ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CELL DIFFERENTIATION; COILED BODY; CONTROLLED STUDY; EMBRYO; GLIA CELL; IMMUNOHISTOCHEMISTRY; MOUSE; MOUSE MUTANT; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN SECRETION; STEM CELL; TELENCEPHALON;

ANIMALIA; MUS;

EID: 43449127484     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.03.032     Document Type: Article

References (72)

1. S. Alcantara E. Pozas C.F. Ibanez E. Soriano BDNF-modulated spatial organization of Cajal-Retzius and GABAergic neurons in the marginal zone plays a role in the development of cortical organization Cereb. Cortex 16 2006 487 499
2. S. Alcantara M. Ruiz G. D'Arcangelo F. Ezan L. de Lecea T. Curran C. Sotelo E. Soriano Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse J. Neurosci. 18 1998 7779 7799
3. S.A. Anderson O. Marin C. Horn K. Jennings J.L. Rubenstein Distinct cortical migrations from the medial and lateral ganglionic eminences Development 128 2001 353 363
4. E.S. Ang Jr. T.F. Haydar V. Gluncic P. Rakic Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex J. Neurosci. 23 2003 5805 5815
5. S. Assimacopoulos E.A. Grove C.W. Ragsdale Identification of a Pax6-dependent epidermal growth factor family signaling source at the lateral edge of the embryonic cerebral cortex J. Neurosci. 23 2003 6399 6403
6. C.B. Bai D. Stephen A.L. Joyner All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3 Dev. Cell 6 2004 103 115
7. F. Bielle A. Griveau N. Narboux-Neme S. Vigneau M. Sigrist S. Arber M. Wassef A. Pierani Multiple origins of Cajal-Retzius cells at the borders of the developing pallium Nat. Neurosci. 8 2005 1002 1012
8. V. Borrell O. Marin Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling Nat. Neurosci. 9 2006 1284 1293
9. A. Bulfone L. Puelles M.H. Porteus M.A. Frohman G.R. Martin J.L. Rubenstein 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
10. D. Büscher L. Grotewold U. Rüther The Xt-J allele generates a Gli3 fusion transcript Mamm. Genome 9 1998 676 678
11. T. Curran G. D'Arcangelo Role of reelin in the control of brain development Brain Res. Brain Res. Rev. 26 1998 285 294
12. G. D'Arcangelo G.G. Miao S.C. Chen H.D. Soares J.I. Morgan T. Curran A protein related to extracellular matrix proteins deleted in the mouse mutant reeler Nature 374 1995 719 723
13. J.A. del Rio A. Martinez M. Fonseca C. Auladell E. Soriano Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretinin antibody Cereb. Cortex 5 1995 13 21
14. W. Duan T. Cole G. Schreiber Cloning and nucleotide sequencing of transthyretin (prealbumin) cDNA from rat choroid plexus and liver Nucleic Acids Res. 17 1989 3979
15. Y. Echelard D.J. Epstein B. St-Jacques L. Shen J. Mohler J.A. McMahon A.P. McMahon Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity Cell 75 1993 1417 1430
16. C. Englund A. Fink C. Lau D. Pham R.A. Daza A. Bulfone T. Kowalczyk R.F. Hevner 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
17. V. Fotaki T. Yu P.A. Zaki J.O. Mason D.J. Price Abnormal positioning of diencephalic cell types in neocortical tissue in the dorsal telencephalon of mice lacking functional Gli3 J. Neurosci. 26 2006 9282 9292
18. G. Gradwohl C. Fode F. Guillemot Restricted expression of a novel murine atonal-related bHLH protein in undifferentiated neural precursors Dev. Biol. 180 1996 227 241
19. E.A. Grove S. Tole J. Limon L. Yip C.W. Ragsdale 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
20. C. Hanashima L. Shen S.C. Li E. Lai Brain factor-1 controls the proliferation and differentiation of neocortical progenitor cells through independent mechanisms J. Neurosci. 22 2002 6526 6536
21. J.M. Hebert Y. Mishina S.K. McConnell BMP signaling is required locally to pattern the dorsal telencephalic midline Neuron 35 2002 1029 1041
22. R.F. Hevner R.A. Daza J.L. Rubenstein H. Stunnenberg J.F. Olavarria C. Englund Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons Dev. Neurosci. 25 2003 139 151
23. R.F. Hevner T. Neogi C. Englund R.A. Daza A. Fink Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdays suggest a pallial origin Brain Res. Dev. Brain Res. 141 2003 39 53
24. R.F. Hevner L. Shi N. Justice Y. Hsueh M. Sheng S. Smiga A. Bulfone A.M. Goffinet A.T. Campagnoni J.L. Rubenstein Tbr1 regulates differentiation of the preplate and layer 6 Neuron 29 2001 353 366
25. R.E. Hill P.F. Jones A.R. Rees C.M. Sime M.J. Justice N.G. Copeland N.A. Jenkins E. Graham D.R. Davidson A new family of mouse homeo box-containing genes: molecular structure, chromosomal location, and developmental expression of Hox-7.1 Genes Dev. 3 1989 26 37
26. S.E. Hong Y.Y. Shugart D.T. Huang S.A. Shahwan P.E. Grant J.O. Hourihane N.D. Martin C.A. Walsh Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations Nat. Genet. 26 2000 93 96
27. B.W. Howell R. Hawkes P. Soriano J.A. Cooper Neuronal position in the developing brain is regulated by mouse disabled-1 Nature 389 1997 733 737
28. C.M. Jones K.M. Lyons B.L. Hogan Involvement of Bone Morphogenetic Protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse Development 111 1991 531 542
29. A.S. Kim S.A. Anderson J.L.R. Rubenstein D.H. Lowenstein S.J. Pleasure Pax-6 regulates expression of SFRP-2 and Wnt-7b in the developing CNS J. Neurosci. 21 2001 132RC-
30. S. Kuschel U. Rüther T. Theil A disrupted balance between Bmp/Wnt and Fgf signaling underlies the ventralization of the Gli3 mutant telencephalon Dev. Biol. 260 2003 484 495
31. V. Lefebvre P. Li B. de Crombrugghe A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene EMBO J. 17 1998 5718 5733
32. Q. Lei A.K. Zelman E. Kuang S. Li M.P. Matise Transduction of graded Hedgehog signaling by a combination of Gli2 and Gli3 activator functions in the developing spinal cord Development 131 2004 3593 3604
33. J.H. Lin T. Saito D.J. Anderson C. Lance-Jones T.M. Jessell S. Arber Functionally related motor neuron pool and muscle sensory afferent subtypes defined by coordinate ETS gene expression Cell 95 1998 393 407
34. B. Lustig B. Jerchow M. Sachs S. Weiler T. Pietsch U. Karsten M. van de Wetering H. Clevers P.M. Schlag W. Birchmeier J. Behrens Negative feedback loop of Wnt signaling through upregulation of Conductin/Axin2 in colorectal and liver tumors Mol. Cell. Biol. 22 2002 1184 1193
35. V.S. Mangale K.E. Hirokawa P.R. Satyaki N. Gokulchandran S. Chikbire L. Subramanian A.S. Shetty B. Martynoga J. Paul M.V. Mai Y. Li L.A. Flanagan S. Tole E.S. Monuki Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate Science 319 2008 304 309
36. L. Medina I. Legaz G. Gonzalez F. De Castro J.L. Rubenstein L. Puelles Expression of Dbx1, Neurogenin 2, Semaphorin 5A, Cadherin 8, and Emx1 distinguish ventral and lateral pallial histogenetic divisions in the developing mouse claustroamygdaloid complex J. Comp. Neurol. 474 2004 504 523
37. G. Meyer P. Wahle The paleocortical ventricle is the origin of reelin-expressing neurons in the marginal zone of the foetal human neocortex Eur. J. Neurosci. 11 1999 3937 3944
38. G. Meyer A.M. Goffinet A. Fairen What is a Cajal-Retzius cell? A reassessment of a classical cell type based on recent observations in the developing neocortex Cereb. Cortex 9 1999 765 775
39. G. Meyer C.G. Perez-Garcia H. Abraham D. Caput Expression of p73 and Reelin in the developing human cortex J. Neurosci. 22 2002 4973 4986
40. G. Meyer A. Cabrera Socorro C.G. Perez Garcia L. Martinez Millan N. Walker D. Caput Developmental roles of p73 in Cajal-Retzius cells and cortical patterning J. Neurosci. 24 2004 9878 9887
41. L. Muzio A. Mallamaci Foxg1 confines Cajal-Retzius neuronogenesis and hippocampal morphogenesis to the dorsomedial pallium J. Neurosci. 25 2005 4435 4441
42. S. Nery G. Fishell J.G. Corbin The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations Nat. Neurosci. 5 2002 1279 1287
43. S. Nishikawa S. Goto T. Hamasaki K. Yamada Y. Ushio Involvement of reelin and Cajal-Retzius cells in the developmental formation of vertical columnar structures in the cerebral cortex: evidence from the study of mouse presubicular cortex Cereb. Cortex 12 2002 1024 1030
44. M. Ogawa T. Miyata K. Nakajima K. Yagyu M. Seike K. Ikenaka H. Yamamoto K. Mikoshiba The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons Neuron 14 1995 899 912
45. M.F. Paredes G. Li O. Berger S.C. Baraban S.J. Pleasure Stromal-derived factor-1 (CXCL12) regulates laminar position of Cajal-Retzius cells in normal and dysplastic brains J. Neurosci. 26 2006 9404 9412
46. M. Persson D. Stamataki P. te Welscher E. Andersson J. Bose U. Ruther J. Ericson J. Briscoe Dorsal–ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity Genes Dev. 16 2002 2865 2878
47. L. Puelles E. Kuwana E. Puelles A. Bulfone K. Shimamura J. Keleher S. Smiga J.L. Rubenstein Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1 J. Comp. Neurol. 424 2000 409 438
48. P. Rakic Elusive radial glial cells: historical and evolutionary perspective Glia 43 2003 19 32
49. D.S. Rice T. Curran Role of the reelin signaling pathway in central nervous system development Annu. Rev. Neurosci. 24 2001 1005 1039
50. M. Richardson D. Redmond C.J. Watson J.O. Mason Mouse Wnt8B is expressed in the developing forebrain and maps to chromosome 19 Mamm. Genome 10 1999 923 925
51. T. Ringstedt S. Linnarsson J. Wagner U. Lendahl Z. Kokaia E. Arenas P. Ernfors C.F. Ibanez BDNF regulates reelin expression and Cajal-Retzius cell development in the cerebral cortex Neuron 21 1998 305 315
52. H. Roelink R. Nusse Expression of two members of the Wnt family during mouse development–restricted temporal and spatial patterns in the developing neural tube Genes Dev. 5 1991 381 388
53. T. Schimmang S.I. Oda U. Ruther The mouse mutant Polydactyly Nagoya (Pdn) defines a novel allele of the zinc finger gene Gli3 Mamm. Genome 5 1994 384 386
54. T. Seki Y. Arai Expression of highly polysialylated NCAM in the neocortex and piriform cortex of the developing and the adult rat Anat. Embryol. (Berl) 184 1991 395 401
55. M. Sheldon D.S. Rice G. D'Arcangelo H. Yoneshima K. Nakajima K. Mikoshiba B.W. Howell J.A. Cooper D. Goldowitz T. Curran Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice Nature 389 1997 730 733
56. T. Soda R. Nakashima D. Watanabe K. Nakajima I. Pastan S. Nakanishi Segregation and coactivation of developing neocortical layer 1 neurons J. Neurosci. 23 2003 6272 6279
57. H. Super E. Soriano H.B. Uylings The functions of the preplate in development and evolution of the neocortex and hippocampus Brain Res. Brain Res. Rev. 27 1998 40 64
58. H. Super J.A. Del Rio A. Martinez P. Perez-Sust E. Soriano Disruption of neuronal migration and radial glia in the developing cerebral cortex following ablation of Cajal-Retzius cells Cereb. Cortex 10 2000 602 613
59. K. Takiguchi-Hayashi M. Sekiguchi S. Ashigaki M. Takamatsu H. Hasegawa R. Suzuki-Migishima M. Yokoyama S. Nakanishi Y. Tanabe Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles J. Neurosci. 24 2004 2286 2295
60. W. Tao E. Lai 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
61. T. Theil Gli3 is required for the specification and differentiation of preplate neurons Dev. Biol. 286 2005 559 571
62. T. Theil G. Alvarez-Bolado A. Walter U. Rüther Gli3 is required for Emx gene expression during dorsal telencephalon development Development 126 1999 3561 3571
63. H. Thien U. Rüther The mouse mutation Pdn (Polydactyly Nagoya) is caused by the integration of a retrotransposon into the Gli3 gene Mamm. Genome 10 1999 205 209
64. F. Tissir A.M. Goffinet Reelin and brain development Nat. Rev. Neurosci. 4 2003 496 505
65. S. Tole G. Goudreau S. Assimacopoulos E.A. Grove Emx2 is required for growth of the hippocampus but not for hippocampal field specification J. Neurosci. 20 2000 2618 2625
66. S. Tole C.W. Ragsdale E.A. Grove Dorsoventral patterning of the telencephalon is disrupted in the mouse mutant extra-toes(J) Dev. Biol. 217 2000 254 265
67. M. Trommsdorff M. Gotthardt T. Hiesberger J. Shelton W. Stockinger J. Nimpf R.E. Hammer J.A. Richardson J. Herz Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2 Cell 97 1999 689 701
68. A. Tsuru M. Mizuguchi K. Uyemura S. Takashima Immunohistochemical expression of cell adhesion molecule L1 during development of the human brain Early Hum. Dev. 45 1996 93 101
69. M. Wijgerde J.A. McMahon M. Rule A.P. McMahon A direct requirement for Hedgehog signaling for normal specification of all ventral progenitor domains in the presumptive mammalian spinal cord 10.1101/gad.1025702 Genes Dev. 16 2002 2849 2864
70. M. Yoshida S. Assimacopoulos K.R. Jones E.A. Grove Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order Development 133 2006 537 545
71. K. Yun S. Potter J.L. Rubenstein Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon Development 128 2001 193 205
72. C. Zimmer M.C. Tiveron R. Bodmer H. Cremer Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons Cereb. Cortex 14 2004 1408 1420