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Development ePress online publication date 2 Jun 2004
doi: 10.1242/dev.01173
Research article
Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells
Takaki Miyata*,
Ayano Kawaguchi,
Kanako Saito,
Masako Kawano,
Tetsuji Muto,
and
Masaharu Ogawa
* Author for correspondence (e-mail: tmiyata{at}med.nagoya-u.ac.jp)
Mature neocortical layers all derive from the cortical plate (CP), a transient zone in the dorsal telencephalon into which young neurons are continuously delivered. To understand cytogenetic and histogenetic events that trigger the emergence of the CP, we have used a slice culture technique. Most divisions at the ventricular surface generated paired cycling daughters (P/P divisions) and the majority of the P/P divisions were asymmetric in daughter cell behavior; they frequently sent one daughter cell to a non-surface (NS) position, the subventricular zone (SVZ), within a single cell-cycle length while keeping the other mitotic daughter for division at the surface. The NS-dividing cells were mostly Hu+ and their daughters were also Hu+, suggesting their commitment to the neuronal lineage and supply of early neurons at a position much closer to their destiny than from the ventricular surface. The release of a cycling daughter cell to SVZ was achieved by collapse of the ventricular process of the cell, followed by its NS division. Neurogenin2 (Ngn2) was immunohistochemically detected in a certain cycling population during G1 phase and was further restricted during G2-M phases to the SVZ-directed population. Its retroviral introduction converted surface divisions to NS divisions. The asymmetric P/P division may therefore contribute to efficient neuron/progenitor segregation required for CP initiation through cell cycle-dependent and lineage-restricted expression of Ngn2.
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|
|
|
|
|
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|
|
|
|
|
|
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|
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|
|
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|
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|
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|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
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|
|
|
|
|
|
|
J. L. Fish, Y. Kosodo, W. Enard, S. Paabo, and W. B. Huttner
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|
|
|
|
|
|
|
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May 1, 2006;
133(9):
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[Full Text]
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|
|
|
|
|
|
|
S.-X. Wu, S. Goebbels, K. Nakamura, K. Nakamura, K. Kometani, N. Minato, T. Kaneko, K.-A. Nave, and N. Tamamaki
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17172 - 17177.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Yamamoto, I. Yoshino, T. Shimazaki, M. Murohashi, R. F. Hevner, I. Lax, H. Okano, M. Shibuya, J. Schlessinger, and N. Gotoh
Essential role of Shp2-binding sites on FRS2{alpha} for corticogenesis and for FGF2-dependent proliferation of neural progenitor cells
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102(44):
15983 - 15988.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Arai, N. Funatsu, K. Numayama-Tsuruta, T. Nomura, S. Nakamura, and N. Osumi
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9752 - 9761.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. A. Siegenthaler and M. W. Miller
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25(38):
8627 - 8636.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Gotz and L. Sommer
Cortical development: the art of generating cell diversity
Development,
August 1, 2005;
132(15):
3327 - 3332.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Calegari, W. Haubensak, C. Haffner, and W. B. Huttner
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J. Neurosci.,
July 13, 2005;
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6533 - 6538.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A.-M. Marzesco, P. Janich, M. Wilsch-Brauninger, V. Dubreuil, K. Langenfeld, D. Corbeil, and W. B. Huttner
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July 1, 2005;
118(13):
2849 - 2858.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Kanatani, H. Tabata, and K. Nakajima
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J Child Neurol,
April 1, 2005;
20(4):
274 - 279.
[Abstract]
[PDF]
|
|
|
|
|
|
|
C. Gregg and S. Weiss
CNTF/LIF/gp130 receptor complex signaling maintains a VZ precursor differentiation gradient in the developing ventral forebrain
Development,
February 1, 2005;
132(3):
565 - 578.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Englund, A. Fink, C. Lau, D. Pham, R. A. M. Daza, A. Bulfone, T. Kowalczyk, and R. F. Hevner
Pax6, Tbr2, and Tbr1 Are Expressed Sequentially by Radial Glia, Intermediate Progenitor Cells, and Postmitotic Neurons in Developing Neocortex
J. Neurosci.,
January 5, 2005;
25(1):
247 - 251.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Haubst, J. Berger, V. Radjendirane, J. Graw, J. Favor, G. F. Saunders, A. Stoykova, and M. Gotz
Molecular dissection of Pax6 function: the specific roles of the paired domain and homeodomain in brain development
Development,
December 15, 2004;
131(24):
6131 - 6140.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Kanatani, H. Tabata, and K. Nakajima
Topical Review: Neuronal Migration in Cortical Development
J Child Neurol,
March 1, 2004;
19(3):
274 - 279.
[Abstract]
[PDF]
|
|
|
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