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The Journal of Neuroscience, March 3, 2004, 24(9):2286-2295; doi:10.1523/JNEUROSCI.4671-03.2004
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Development/Plasticity/Repair
Generation of Reelin-Positive Marginal Zone Cells from the Caudomedial Wall of Telencephalic Vesicles
Keiko Takiguchi-Hayashi,1
Mariko Sekiguchi,1
Shizuko Ashigaki,1,3
Masako Takamatsu,3
Hiroshi Hasegawa,3
Rika Suzuki-Migishima,2
Minesuke Yokoyama,2
Shigetada Nakanishi,4,5 and
Yasuto Tanabe1,3
1Translational Research Department, Molecular Bio-Medicine Unit, 2Mouse Genome Technology Center, and Precursory Research for Embryonic Science and Technology, Japan Science and Technology, Mitsubishi Kagaku Institute of Life Sciences, Machida, Tokyo, 194-8511, 4Department of Biological Sciences, Faculty of Medicine, and 5Department of Molecular and System Biology, Graduate School of Biostudies, Kyoto University, Kyoto 606-8501, Japan
An early and fundamental step of the laminar organization of developing neocortex is controlled by the developmental programs that critically depend on the activities of reelin-positive cells in the marginal zone. However, the ontogeny of reelin-positive cells remained elusive. To gain insights into the spatial and temporal regulation of reelin-positive marginal zone cell development, we used a transgenic mouse line in which we defined the green fluorescent protein (GFP) transgene as a novel reliable molecular marker of reelin-positive marginal zone cells from the early stages of their development. We further used exo utero electroporation-mediated gene transfer that allows us to mark progenitor cells and monitor the descendants in the telencephalon in vivo. We show here the generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles, including the cortical hem, where the prominent expression of GFP is initially detected. These neurons tangentially migrate at the cortical marginal zone and are distributed throughout the entire neocortex in a caudomedial-high to rostrolateral-low gradient during the dynamic developmental period of corticogenesis. Therefore, our findings on reelin-positive marginal zone cells, in addition to the cortical interneurons, add to the emerging view that the neocortex consists of neuronal subtypes that originate from a focal source extrinsic to the neocortex, migrate tangentially into the neocortex, and thereby underlie neural organization of the neocortex.
Key words: Cajal-Retzius cells; neocortex; cerebral cortex; laminar organization; tangential cell migration; caudomedial-rostrolateral axis
Received Oct 16, 2003;
revised December 28, 2003;
accepted January 6, 2004.
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|
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|
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