The fully linked HTML version of this article has now been published.
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.
This article has been cited by other articles:
|
|
|
|
 
A. Alvarez-Buylla, M. Kohwi, T.M. Nguyen, and F.T. Merkle
The Heterogeneity of Adult Neural Stem Cells and the Emerging Complexity of Their Niche
Cold Spring Harb Symp Quant Biol,
November 6, 2008;
(2008)
sqb.2008.73.019v1.
[Abstract]
[PDF]
|
|
|
|
|
|
|
A. Kawaguchi, T. Ikawa, T. Kasukawa, H. R. Ueda, K. Kurimoto, M. Saitou, and F. Matsuzaki
Single-cell gene profiling defines differential progenitor subclasses in mammalian neurogenesis
Development,
September 15, 2008;
135(18):
3113 - 3124.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. L. Fish, C. Dehay, H. Kennedy, and W. B. Huttner
Making bigger brains-the evolution of neural-progenitor-cell division
J. Cell Sci.,
September 1, 2008;
121(17):
2783 - 2793.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Cubelos, A. Sebastian-Serrano, S. Kim, C. Moreno-Ortiz, J. M. Redondo, C. A. Walsh, and M. Nieto
Cux-2 Controls the Proliferation of Neuronal Intermediate Precursors of the Cortical Subventricular Zone
Cereb Cortex,
August 1, 2008;
18(8):
1758 - 1770.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. A. Siegenthaler, B. A. Tremper-Wells, and M. W. Miller
Foxg1 Haploinsufficiency Reduces the Population of Cortical Intermediate Progenitor Cells: Effect of Increased p21 Expression
Cereb Cortex,
August 1, 2008;
18(8):
1865 - 1875.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Bayatti, J. A. Moss, L. Sun, P. Ambrose, J. F. H. Ward, S. Lindsay, and G. J. Clowry
A Molecular Neuroanatomical Study of the Developing Human Neocortex from 8 to 17 Postconceptional Weeks Revealing the Early Differentiation of the Subplate and Subventricular Zone
Cereb Cortex,
July 1, 2008;
18(7):
1536 - 1548.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Osumi, H. Shinohara, K. Numayama-Tsuruta, and M. Maekawa
Concise Review: Pax6 Transcription Factor Contributes to both Embryonic and Adult Neurogenesis as a Multifunctional Regulator
Stem Cells,
July 1, 2008;
26(7):
1663 - 1672.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Q. Doe
Neural stem cells: balancing self-renewal with differentiation
Development,
May 1, 2008;
135(9):
1575 - 1587.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Sunabori, A. Tokunaga, T. Nagai, K. Sawamoto, M. Okabe, A. Miyawaki, Y. Matsuzaki, T. Miyata, and H. Okano
Cell-cycle-specific nestin expression coordinates with morphological changes in embryonic cortical neural progenitors
J. Cell Sci.,
April 15, 2008;
121(8):
1204 - 1212.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. D. Hodge, T. D. Kowalczyk, S. A. Wolf, J. M. Encinas, C. Rippey, G. Enikolopov, G. Kempermann, and R. F. Hevner
Intermediate Progenitors in Adult Hippocampal Neurogenesis: Tbr2 Expression and Coordinate Regulation of Neuronal Output
J. Neurosci.,
April 2, 2008;
28(14):
3707 - 3717.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Estivill-Torrus, P. Llebrez-Zayas, E. Matas-Rico, L. Santin, C. Pedraza, I. De Diego, I. Del Arco, P. Fernandez-Llebrez, J. Chun, and F. R. De Fonseca
Absence of LPA1 Signaling Results in Defective Cortical Development
Cereb Cortex,
April 1, 2008;
18(4):
938 - 950.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. E. Russo, C. Reali, M. Radmilovich, A. Fernandez, and O. Trujillo-Cenoz
Connexin 43 Delimits Functional Domains of Neurogenic Precursors in the Spinal Cord
J. Neurosci.,
March 26, 2008;
28(13):
3298 - 3309.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. R. Costa, G. Wen, A. Lepier, T. Schroeder, and M. Gotz
Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex
Development,
January 1, 2008;
135(1):
11 - 22.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Guillemot
Spatial and temporal specification of neural fates by transcription factor codes
Development,
November 1, 2007;
134(21):
3771 - 3780.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. R. Costa, N. Kessaris, W. D. Richardson, M. Gotz, and C. Hedin-Pereira
The Marginal Zone/Layer I as a Novel Niche for Neurogenesis and Gliogenesis in Developing Cerebral Cortex
J. Neurosci.,
October 17, 2007;
27(42):
11376 - 11388.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. M. Gohlke, W. C. Griffith, and E. M. Faustman
Computational Models of Neocortical Neuronogenesis and Programmed Cell Death in the Developing Mouse, Monkey, and Human
Cereb Cortex,
October 1, 2007;
17(10):
2433 - 2442.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Tamai, H. Shinohara, T. Miyata, K. Saito, Y. Nishizawa, T. Nomura, and N. Osumi
Pax6 transcription factor is required for the interkinetic nuclear movement of neuroepithelial cells
Genes Cells,
September 1, 2007;
12(9):
983 - 996.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Sirko, A. von Holst, A. Wizenmann, M. Gotz, and A. Faissner
Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells
Development,
August 1, 2007;
134(15):
2727 - 2738.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. J. Gilbertson and D. H. Gutmann
Tumorigenesis in the Brain: Location, Location, Location
Cancer Res.,
June 15, 2007;
67(12):
5579 - 5582.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. C. Wilcock, J. R. Swedlow, and K. G. Storey
Mitotic spindle orientation distinguishes stem cell and terminal modes of neuron production in the early spinal cord
Development,
May 15, 2007;
134(10):
1943 - 1954.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Battiste, A. W. Helms, E. J. Kim, T. K. Savage, D. C. Lagace, C. D. Mandyam, A. J. Eisch, G. Miyoshi, and J. E. Johnson
Ascl1 defines sequentially generated lineage-restricted neuronal and oligodendrocyte precursor cells in the spinal cord
Development,
January 15, 2007;
134(2):
285 - 293.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M.-C. Tiveron, M. Rossel, B. Moepps, Y. L. Zhang, R. Seidenfaden, J. Favor, N. Konig, and H. Cremer
Molecular Interaction between Projection Neuron Precursors and Invading Interneurons via Stromal-Derived Factor 1 (CXCL12)/CXCR4 Signaling in the Cortical Subventricular Zone/Intermediate Zone
J. Neurosci.,
December 20, 2006;
26(51):
13273 - 13278.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Borrell, B. K. Kaspar, F. H. Gage, and E. M. Callaway
In vivo Evidence for Radial Migration of Neurons by Long-Distance Somal Translocation in the Developing Ferret Visual Cortex
Cereb Cortex,
November 1, 2006;
16(11):
1571 - 1583.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Haubst, E. Georges-Labouesse, A. De Arcangelis, U. Mayer, and M. Gotz
Basement membrane attachment is dispensable for radial glial cell fate and for proliferation, but affects positioning of neuronal subtypes
Development,
August 15, 2006;
133(16):
3245 - 3254.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. L. Fish, Y. Kosodo, W. Enard, S. Paabo, and W. B. Huttner
Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells
PNAS,
July 5, 2006;
103(27):
10438 - 10443.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Imai, S.-i. Hirai, K. Akimoto, H. Koyama, T. Miyata, M. Ogawa, S. Noguchi, T. Sasaoka, T. Noda, and S. Ohno
Inactivation of aPKC{lambda} results in the loss of adherens junctions in neuroepithelial cells without affecting neurogenesis in mouse neocortex
Development,
May 1, 2006;
133(9):
1735 - 1744.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S.-X. Wu, S. Goebbels, K. Nakamura, K. Nakamura, K. Kometani, N. Minato, T. Kaneko, K.-A. Nave, and N. Tamamaki
Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone
PNAS,
November 22, 2005;
102(47):
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
PNAS,
November 1, 2005;
102(44):
15983 - 15988.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Arai, N. Funatsu, K. Numayama-Tsuruta, T. Nomura, S. Nakamura, and N. Osumi
Role of Fabp7, a Downstream Gene of Pax6, in the Maintenance of Neuroepithelial Cells during Early Embryonic Development of the Rat Cortex
J. Neurosci.,
October 19, 2005;
25(42):
9752 - 9761.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. A. Siegenthaler and M. W. Miller
Transforming Growth Factor {beta}1 Promotes Cell Cycle Exit through the Cyclin-Dependent Kinase Inhibitor p21 in the Developing Cerebral Cortex
J. Neurosci.,
September 21, 2005;
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
Selective Lengthening of the Cell Cycle in the Neurogenic Subpopulation of Neural Progenitor Cells during Mouse Brain Development
J. Neurosci.,
July 13, 2005;
25(28):
6533 - 6538.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A.-M. Marzesco, P. Janich, M. Wilsch-Brauninger, V. Dubreuil, K. Langenfeld, D. Corbeil, and W. B. Huttner
Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells
J. Cell Sci.,
July 1, 2005;
118(13):
2849 - 2858.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Kanatani, H. Tabata, and K. Nakajima
Topical Review: Neuronal Migration in Cortical Development
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]
|
|
|
© The Company of Biologists Ltd 2004
