Multiple origins of Cajal-Retzius cells at the borders of the developing pallium

Nature Neuroscience

Volumn 8, Issue 8, 2005, Pages 1002-1012

  Bielle, Franck ^a   Griveau, Amélie ^a   Narboux Nême, Nicolas ^a   Vigneau, Sébastien ^a,e   Sigrist, Markus ^b,c   Arber, Silvia ^b,c   Wassef, Marion ^a   Pierani, Alessandra ^a,d  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b UNIVERSITY OF BASEL   (Switzerland)

^c FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^d Och Spine at New York Presbyterian Hospitals   (United States)

^e INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DBX1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MIGRATION; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENETIC TRANSCRIPTION; INTERSTITIAL CELL OF CAJAL; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTOPLASMATIC ASTROCYTE; TELENCEPHALON;

AGING; ANIMALS; ANIMALS, NEWBORN; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL ADHESION MOLECULES, NEURONAL; CELL DIVISION; CELL MOVEMENT; CEREBRAL CORTEX; EMBRYO; EXTRACELLULAR MATRIX PROTEINS; GENETIC TECHNIQUES; HOMEODOMAIN PROTEINS; MICE; MICE, NEUROLOGIC MUTANTS; NERVE TISSUE PROTEINS; NEURONS; RECOMBINANT FUSION PROTEINS; SERINE ENDOPEPTIDASES; TAU PROTEINS; TELENCEPHALON; TISSUE DISTRIBUTION;

EID: 23044491525     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1511     Document Type: Article

References (48)

1. Marin-Padilla, M. Cajal-Retzius cells and the development of the neocortex. Trends Neurosci. 21, 64-71 (1998).
2. Kriegstein, A.R. & Noctor, S.C. Patterns of neuronal migration in the embryonic cortex. Trends Neurosci. 27, 392-399 (2004).
3. Marin, O. & Rubenstein, J.L. Cell migration in the forebrain. Annu. Rev. Neurosci. 26, 441-483 (2003).
4. Meyer, G., Goffinet, A.M. & Fairen, A. 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 (1999).
5. Zecevic, N. & Rakic, P. Development of layer I neurons in the primate cerebral cortex. J. Neurosci. 21, 5607-5619 (2001).
6. D'Arcangelo, G. et al. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374, 719-723 (1995).
7. Ogawa, M. et al. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14, 899-912 (1995).
8. Super, H., Del Rio, J.A., Martinez, A., Perez-Sust, P. & Soriano, E. Disruption of neuronal migration and radial glia in the developing cerebral cortex following ablation of Cajal-Retzius cells. Cereb. Cortex 10, 602-613 (2000).
9. Del Rio, J.A. et al. A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385, 70-74 (1997).
10. Alcantara, S. et al. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J. Neurosci. 18, 7779-7799 (1998).
11. Hevner, R.F., Neogi, T., Englund, C., Daza, R.A. & Fink, A. Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdays suggest a palliai origin. Brain Res. Dev. Brain Res. 141, 39-53 (2003).
12. Gorski, J.A. et al. Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J. Neurosci. 22, 6309-6314 (2002).
13. Shinozaki, K. et al. Absence of Cajal-Retzius cells and subplate neurons associated with defects of tangential cell migration from ganglionic eminence in Emx1/2 double mutant cerebral cortex. Development 129, 3479-3492 (2002).
14. Meyer, G. & Wahle, P. The paleocortical ventricle is the origin of reelin-expressing neurons in the marginal zone of the foetal human neocortex. Eur. J. Neurosci. 11, 3937-3944 (1999).
15. Meyer, G., Perez-Garcia, C.G., Abraham, H. & Caput, D. Expression of p73 and Reelin in the developing human cortex. J. Neurosci. 22, 4973-4986 (2002).
16. Lavdas, A.A., Grigoriou, M., Pachnis, V. & Parnavelas, J.G. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 19, 7881-7888 (1999).
17. Takiguchi-Hayashi, K. et al. Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J. Neurosci. 24, 2286-2295 (2004).
18. Jessell, T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29 (2000).
19. Schuurmans, C. & Guillemot, F. Molecular mechanisms underlying cell fate specification in the developing telencephalon. Curr. Opin. Neurobiol. 12, 26-34 (2002).
20. Campbell, K. Dorsal-ventral patterning in the mammalian telencephalon. Curr. Opin. Neurobiol. 13, 50-56 (2003).
21. Lu, S., Bogarad, L.D., Murtha, M.T. & Ruddle, F.H. Expression pattern of a murine homeobox gene, Dbx, displays extreme spatial restriction in embryonic forebrain and spinal cord. Proc. Natl. Acad. Sci. USA 89, 8053-8057 (1992).
22. Shoji, H. et al. Regionalized expression of the Dbx family homeobox genes in the embryonic CNS of the mouse. Mech. Dev. 56, 25-39 (1996).
23. Pierani, A., Brenner-Morton, S., Chiang, C. & Jessell, T.M. A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97, 903-915 (1999).
24. Pierani, A. et al. Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29, 367-384 (2001).
25. Lanuza, G.M., Gosgnach, S., Pierani, A., Jessell, T.M. & Goulding, M. Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 42, 375-386 (2004).
26. Yun, K., Potter, S. & Rubenstein, J.L. Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128, 193-205 (2001).
27. Medina, L. et al. 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, 504-523 (2004).
28. Zinyk, D.L., Mercer, E.H., Harris, E., Anderson, D.J. & Joyner, A.L. Fate mapping of the mouse midbrain-hindbrain constriction using a site-specific recombination system. Curr. Biol. 8, 665-668 (1998).
29. de Carlos, J.A., Lopez-Mascaraque, L. & Valverde, F. Dynamics of cell migration from the lateral ganglionic eminence in the rat. J. Neurosci. 16, 6146-6156 (1996).
30. Corbin, J.G., Nery, S. & Fishell, G. Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain. Nat. Neurosci. 4, 1177-1182 (2001).
31. Marin, O. & Rubenstein, J.L. A long, remarkable journey: tangential migration in the telencephalon. Nat. Rev. Neurosci. 2, 780-790 (2001).
32. Tronche, F. et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 23, 99-103 (1999).
33. Tamamaki, N., Fujimori, K.E. & Takauji, R. Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J. Neurosci. 17, 8313-8323 (1997).
34. Ang, E.S., Jr., Haydar, T.F., Gluncic, V. & Rakic, P. Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. J. Neurosci. 23, 5805-5815 (2003).
35. Hevner, R.F. et al. Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29, 353-366 (2001).
36. Mallamaci, A. et al. The lack of Emx2 causes impairment of Reelin signaling and defects of neuronal migration in the developing cerebral cortex. J. Neurosci. 20, 1109-1118 (2000).
37. -/- mutant mice. Nat. Neurosci. 3, 679-686 (2000).
38. Borrell, V. et al. Reelin regulates the development and synaptogenesis of the layer-specific entorhino-hippocampal connections. J. Neurosci. 19, 1345-1358 (1999).
39. Meyer, G., Soria, J.M., Martinez-Galan, J.R., Martin-Clemente, B. & Fairen, A. Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J. Comp. Neurol. 397, 493-518 (1998).
40. Meyer, G. et al. Developmental roles of p73 in Cajal-Retzius cells and cortical patterning. J. Neurosci. 24, 9878-9887 (2004).
41. Aboitiz, F., Montiel, J. & Lopez, J. Critical steps in the early evolution of the isocortex: insights from developmental biology. Braz. J. Med. J. Biol. Res. 35, 1455-1472 (2002).
42. Palmiter, R.D. et al. Cell lineage ablation in transgenic mice by cell-specific expression of a toxin gene. Cell 50, 435-443 (1987).
43. Lee, K.J., Dietrich, P. & Jessell, T.M. Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification. Nature 403, 734-740 (2000).
44. Cohen-Tannoudji, M. et al. I-Scel-induced gene replacement at a natural lccus in embryonic stem cells. Mol. Cell. Biol. 18, 1444-1448 (1998).
45. Hippenmeyer, S. et al. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 3, e159 (2005).
46. Schiffmann, S.N., Bernier, B. & Goffinet, A.M. Reelin mRNA expression during mouse brain development. Eur. J. Neurosci. 9, 1055-1071 (1997).
47. Lu, S., Wise, T.L. & Ruddle, F.H. Mouse homeobox gene Dbx: sequence, gene structure and expression pattern during mid-gestation. Mech. Dev. 47, 187-195 (1994).
48. Wilkinson, D.G., Bhatt, S., Ryseck, R.P. & Bravo, R. Tissue-specific expression of c-jun and junB during organogenesis in the mouse. Development 106, 465-471 (1989).