A novel role for Dbx1-derived Cajal-Retzius cells in early regionalization of the cerebral cortical neuroepithelium

PLoS Biology

Volumn 8, Issue 7, 2010, Pages

  Griveau, Amélie ^a   Borello, Ugo ^a   Causeret, Frédéric ^a   Tissir, Fadel ^b   Boggetto, Nicole ^a   Karaz, Sonia ^a   Pierani, Alessandra ^a  

^a INSTITUT JACQUES MONOD   (France)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DBX1 PROTEIN; HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; DBX1 PROTEIN, MOUSE; MESSENGER RNA; WNT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; MITOSIS; MOUSE; NEUROEPITHELIUM; NONHUMAN; PERINATAL PERIOD; PROTEIN EXPRESSION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; STEM CELL; ANIMAL; CYTOLOGY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORPHOGENESIS; NERVOUS SYSTEM DEVELOPMENT; PRENATAL DEVELOPMENT; SEPTUM PELLUCIDUM;

MUS;

ANIMALS; BODY PATTERNING; CELL PROLIFERATION; CEREBRAL CORTEX; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MICE; NEUROEPITHELIAL CELLS; NEUROGENESIS; RNA, MESSENGER; SEPTUM OF BRAIN; WNT PROTEINS;

EID: 77955027897     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000440     Document Type: Article

References (73)

1. Wolpert L (1969) Positional information and the spatial pattern of cellular differentiation. J Theor Biol 25: 1-47.
2. Sur M, Rubenstein JL (2005) Patterning and plasticity of the cerebral cortex. Science 310: 805-810.
3. Rash BG, Grove EA (2006) Area and layer patterning in the developing cerebral cortex. Curr Opin Neurobiol 16: 25-34.
4. Mallamaci A, Stoykova A (2006) Gene networks controlling early cerebral cortex arealization. Eur J Neurosci 23: 847-856.
5. O'Leary DD, Sahara S (2008) Genetic regulation of arealization of the neocortex. Curr Opin Neurobiol 18: 90-100.
6. Gurdon JB, Bourillot PY (2001) Morphogen gradient interpretation. Nature 413: 797-803.
7. Tabata T, Takei Y (2004) Morphogens, their identification and regulation. Development 131: 703-712.
8. Levitt P, Barbe MF, Eagleson KL (1997) Patterning and specification of the cerebral cortex. Annu Rev Neurosci 20: 1-24.
9. Gitton Y, Cohen-Tannoudji M, Wassef M (1999) Specification of somatosensory area identity in cortical explants. J Neurosci 19: 4889-4898.
10. Mallamaci A, Muzio L, Chan CH, Parnavelas J, Boncinelli E (2000) Areaidentityshifts in the early cerebral cortex of Emx22/2 mutant mice. Nat Neurosci 3: 679-686.
11. Marin-Padilla M (1998) Cajal-Retzius cells and the development of the neocortex. Trends Neurosci 21: 64-71.
12. Meyer G, Goffinet AM, Fairen A (1999) What is a Cajal-Retzius cell? A reassessment of a classical cell type based on recent observations in the developing neocortex. Cereb Cortex 9: 765-775.
13. Soriano E, Del Rio JA (2005) The cells of cajal-retzius: still a mystery one century after. Neuron 46: 389-394.
14. D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, et al. (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374: 719-723.
15. Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, et al. (1995) The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14: 899-912.
16. Marin O, Rubenstein JL (2003) Cell migration in the forebrain. Annu Rev Neurosci 26: 441-483.
17. Super H, Del Rio JA, Martinez A, Perez-Sust P, Soriano E (2000) Disruption of neuronal migration and radial glia in the developing cerebral cortex following ablation of Cajal-Retzius cells. Cereb Cortex 10: 602-613.
18. Soriano E, Alvarado-Mallart RM, Dumesnil N, Del Rio JA, Sotelo C (1997) Cajal-Retzius cells regulate the radial glia phenotype in the adult and developing cerebellum and alter granule cell migration. Neuron 18: 563-577.
19. Del Rio JA, Heimrich B, Borrell V, Forster E, Drakew A, et al. (1997) A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385: 70-74.
20. Bielle F, Griveau A, Narboux-Neme N, Vigneau S, Sigrist M, et al. (2005) Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci 8: 1002-1012.
21. Takiguchi-Hayashi K, Sekiguchi M, Ashigaki S, Takamatsu M, Hasegawa H, et al. (2004) Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J Neurosci 24: 2286-2295.
22. Yoshida M, Assimacopoulos S, Jones KR, Grove EA (2006) Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 133: 537-545.
23. Imayoshi I, Shimogori T, Ohtsuka T, Kageyama R (2008) Hes genes and neurogenin regulate non-neural versus neural fate specification in the dorsal telencephalic midline. Development 135: 2531-2541.
24. Tissir F, Ravni A, Achouri Y, Riethmacher D, Meyer G, et al. (2009) DeltaNp73 regulates neuronal survival in vivo. Proc Natl Acad Sci U S A 106: 16871-16876.
25. Abellan A, Menuet A, Dehay C, Medina L, Retaux S (2009) Differential Expression of LIM-Homeodomain Factors in Cajal-Retzius Cells of Primates, Rodents, and Birds. Cereb Cortex. E-pub ahead of print. doi:10.1093/cercor/bhp242.
26. Hanashima C, Fernandes M, Hebert JM, Fishell G (2007) The role of Foxg1 and dorsal midline signaling in the generation of Cajal-Retzius subtypes. J Neurosci 27: 11103-11111.
27. Meyer G, Perez-Garcia CG, Abraham H, Caput D (2002) Expression of p73 and Reelin in the developing human cortex. J Neurosci 22: 4973-4986.
28. Inoue T, Ogawa M, Mikoshiba K, Aruga J (2008) Zic deficiency in the cortical marginal zone and meninges results in cortical lamination defects resembling those in type II lissencephaly. J Neurosci 28: 4712-4725.
29. Zimmer C, Lee J, Griveau A, Arber S, Pierani A, et al. (2010) Role of Fgf8 signalling in the specification of rostral Cajal-Retzius cells. Development 137: 293-302.
30. Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, et al. (2002) Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J Neurosci 22: 6309-6314.
31. Hevner RF, Neogi T, Englund C, Daza RA, Fink A (2003) Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdays suggest a pallial origin. Brain Res Dev Brain Res 141: 39-53.
32. Englund C, Fink A, Lau C, Pham D, Daza RA, et al. (2005) Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25: 247-251.
33. Suzuki SC, Inoue T, Kimura Y, Tanaka T, Takeichi M (1997) Neuronal circuits are subdivided by differential expression of type-II classic cadherins in postnatal mouse brains. Mol Cell Neurosci 9: 433-447.
34. Nakagawa Y, Johnson JE, O'Leary DD (1999) Graded and areal expression patterns of regulatory genes and cadherins in embryonic neocortex independent of thalamocortical input. J Neurosci 19: 10877-10885.
35. Nakagawa Y, O'Leary DD (2003) Dynamic patterned expression of orphan nuclear receptor genes RORalpha and RORbeta in developing mouse forebrain. Dev Neurosci 25: 234-244.
36. Borrell V, Marin O (2006) Meninges control tangential migration of hem- derived Cajal-Retzius cells via CXCL12/CXCR4 signaling. Nat Neurosci 9: 1284-1293.
37. Hebert JM, Fishell G (2008) The genetics of early telencephalon patterning: some assembly required. Nat Rev Neurosci 9: 678-685.
38. Hamasaki T, Leingartner A, Ringstedt T, O'Leary DD (2004) EMX2 regulates sizes and positioning of the primary sensory and motor areas in neocortex by direct specification of cortical progenitors. Neuron 43: 359-372.
39. Storm EE, Garel S, Borello U, Hebert JM, Martinez S, et al. (2006) Dose- dependent functions of Fgf8 in regulating telencephalic patterning centers. Development 133: 1831-1844.
40. Muzio L, DiBenedetto B, Stoykova A, Boncinelli E, Gruss P, et al. (2002) Emx2 and Pax6 control regionalization of the pre-neuronogenic cortical primordium. Cereb Cortex 12: 129-139.
41. Cholfin JA, Rubenstein JL (2008) Frontal cortex subdivision patterning is coordinately regulated by Fgf8, Fgf17, and Emx2. J Comp Neurol 509: 144-155.
42. Fukuchi-Shimogori T, Grove EA (2003) Emx2 patterns the neocortex by regulating FGF positional signaling. Nat Neurosci 6: 825-831.
43. Hasegawa H, Ashigaki S, Takamatsu M, Suzuki-Migishima R, Ohbayashi N, et al. (2004) Laminar patterning in the developing neocortex by temporally coordinated fibroblast growth factor signaling. J Neurosci 24: 8711-8719.
44. Theil T, Aydin S, Koch S, Grotewold L, Ruther U (2002) Wnt and Bmp signalling cooperatively regulate graded Emx2 expression in the dorsal telencephalon. Development 129: 3045-3054.
45. Yun K, Potter S, Rubenstein JL (2001) Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128: 193-205.
46. Mallamaci A, Mercurio S, Muzio L, Cecchi C, Pardini CL, et al. (2000) The lack of Emx2 causes impairment of Reelin signaling and defects of neuronal migration in the developing cerebral cortex. J Neurosci 20: 1109-1118.
47. Stoykova A, Hatano O, Gruss P, Gotz M (2003) Increase in reelin-positive cells in the marginal zone of Pax6 mutant mouse cortex. Cereb Cortex 13: 560-571.
48. Faedo A, Tomassy GS, Ruan Y, Teichmann H, Krauss S, et al. (2008) COUP-TFI coordinates cortical patterning, neurogenesis, and laminar fate and modulates MAPK/ERK, AKT, and beta-catenin signaling. Cereb Cortex 18: 2117-2131.
49. Meyer G, Cabrera Socorro A, Perez Garcia CG, Martinez Millan L, Walker N, et al. (2004) Developmental roles of p73 in Cajal-Retzius cells and cortical patterning. J Neurosci 24: 9878-9887.
50. Borello U, Cobos I, Long JE, McWhirter JR, Murre C, et al. (2008) FGF15 promotes neurogenesis and opposes FGF8 function during neocortical development. Neural Dev 3: 17.
51. Polleux F, Dehay C, Kennedy H (1997) The timetable of laminar neurogenesis contributes to the specification of cortical areas in mouse isocortex. J Comp Neurol 385: 95-116.
52. Takahashi T, Goto T, Miyama S, Nowakowski RS, Caviness VS Jr. (1999) Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci 19: 10357-10371.
53. Kowalczyk T, Pontious A, Englund C, Daza RA, Bedogni F, et al. (2009) Intermediate Neuronal Progenitors (Basal Progenitors) Produce Pyramidal- Projection Neurons for All Layers of Cerebral Cortex. Cereb Cortex 19: 2439-50.
54. Polleux F, Dehay C, Kennedy H (1998) Neurogenesis and commitment of corticospinal neurons in reeler. J Neurosci 18: 9910-9923.
55. Magdaleno S, Keshvara L, Curran T (2002) Rescue of ataxia and preplate splitting by ectopic expression of Reelin in reeler mice. Neuron 33: 573-586.
56. Lander AD (2007) Morpheus unbound: reimagining the morphogen gradient. Cell 128: 245-256.
57. Scholpp S, Brand M (2004) Endocytosis controls spreading and effective signaling range of Fgf8 protein. Curr Biol 14: 1834-1841.
58. Gritli-Linde A, Lewis P, McMahon AP, Linde A (2001) The whereabouts of a morphogen: direct evidence for short- and graded long-range activity of hedgehog signaling peptides. Dev Biol 236: 364-386.
59. Nguyen-Ba-Charvet KT, Picard-Riera N, Tessier-Lavigne M, Baron-Van Evercooren A, Sotelo C, et al. (2004) Multiple roles for slits in the control of cell migration in the rostral migratory stream. J Neurosci 24: 1497-1506.
60. Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin JA, Yamada M, et al. (2006) New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311: 629-632.
61. Etchevers HC, Couly G, Vincent C, Le Douarin NM (1999) Anterior cephalic neural crest is required for forebrain viability. Development 126: 3533-3543.
62. Creuzet S, Schuler B, Couly G, Le Douarin NM (2004) Reciprocal relationships between Fgf8 and neural crest cells in facial and forebrain development. Proc Natl Acad Sci USA 101: 4843-4847.
63. 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.
64. Dehay C, Savatier P, Cortay V, Kennedy H (2001) Cell-cycle kinetics of neocortical precursors are influenced by embryonic thalamic axons. J Neurosci 21: 201-214.
65. Pierani A, Moran-Rivard L, Sunshine MJ, Littman DR, Goulding M, et al. (2001) Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29: 367-384.
66. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, et al. (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1: 4.
67. Hubbell E, Liu WM, Mei R (2002) Robust estimators for expression analysis. Bioinformatics 18: 1585-1592.
68. Liu WM, Mei R, Di X, Ryder TB, Hubbell E, et al. (2002) Analysis of high density expression microarrays with signed-rank call algorithms. Bioinformatics 18: 1593-1599.
69. Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: a free, open- source system for microarray data management and analysis. Biotechniques 34: 374-378.
70. Spandidos A, Wang X, Wang H, Seed B PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 38: D792-799.
71. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
72. Sansom SN, Hebert JM, Thammongkol U, Smith J, Nisbet G, et al. (2005) Genomic characterisation of a Fgf-regulated gradient-based neocortical proto- map. Development 132: 3947-3961.
73. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.