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Journal of Neuroscience, Vol 13, 820-833, Copyright © 1993 by Society for Neuroscience
Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse
T Takahashi, RS Nowakowski and VS Caviness Jr
Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston 02114.
Cytogenesis is the critical determinant of the total number of neurons that
contribute to the formation of the cerebral cortex and the rate at which
the cells are produced. Two distinct cell populations constitute the
proliferative population, a pseudostratified ventricular epithelium (PVE)
lying within the ventricular zone (VZ) at the margin of the ventricle, and
a secondary proliferative population that is intermixed with the PVE within
the VZ but also is distributed through the overlying subventricular and
intermediate zones of the cerebral wall. The present analysis, based upon
cumulative S-phase labeling of the proliferative cells with
5-bromo-2'-deoxyuridine, is principally concerned with the PVE of the
gestational-day-14 (E14) murine cerebral wall. It has immediate but also
more far reaching general objectives. The most immediate objective,
essential to the design and interpretation of later experiments, is to
provide estimates of critical parameters of cytogenesis for the PVE. The
growth fraction is virtually 100%. The lengths of the overall cell cycle,
S-, G2+M-m, and G1-phases are 15.1 hr, 3.8 hr, 2 hr, and 9.3 hr,
respectively. The PVE is homogeneous with respect to cell cycle length. For
methodological considerations, these estimates are more accurate than
estimates of the same parameters obtained in earlier analyses based upon
S-phase labeling with tritiated thymidine. It is particularly with respect
to a shorter length of S-phase determined here that the present values are
different from those obtained with thymidine. At a more innovative level,
the temporal and spatial resolution of nuclear movement made possible by
the methods developed here will allow, in a way not previously attempted, a
fine-grained tracking of nuclear movement as cells execute the successive
stages of the cell cycle or exit the cycle subsequent to mitosis. Such
observations are pertinent to our understanding of the regulatory
mechanisms of neocortical histogenesis and the cell biological mechanisms
that govern the proliferative cycle of the ventricular epithelium itself.
It is known that the velocity of nuclear movement in the PVE is maximum in
G2 (fourfold increase from S- phase) and minimum in M and early
G1.(ABSTRACT TRUNCATED AT 400 WORDS)
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|
|
|
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|
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|
|
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|
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|
|
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[Full Text]
[PDF]
|
|
|
|
|
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[Abstract]
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[PDF]
|
|
|
|
|
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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March 1, 1999;
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188 - 195.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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January 5, 1999;
126(10):
2141 - 2147.
[Abstract]
[PDF]
|
|
|
|
|
|
|
D. R. Kornack and P. Rakic
Changes in cell-cycle kinetics during the development and evolution of primate neocortex
PNAS,
February 3, 1998;
95(3):
1242 - 1246.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Alvarez-Buylla, J. M. Garcia-Verdugo, A. S. Mateo, and H. Merchant-Larios
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J. Neurosci.,
February 1, 1998;
18(3):
1020 - 1037.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Bittman, D. F. Owens, A. R. Kriegstein, and J. J. LoTurco
Cell Coupling and Uncoupling in the Ventricular Zone of Developing Neocortex
J. Neurosci.,
September 15, 1997;
17(18):
7037 - 7044.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Conti, C. De Fraja, M. Gulisano, E. Migliaccio, S. Govoni, and E. Cattaneo
Expression and activation of SH2/PTB-containing ShcA adaptor protein reflects the pattern of neurogenesis in the mammalian brain
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July 22, 1997;
94(15):
8185 - 8190.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Cai, N. L. Hayes, and R. S. Nowakowski
Local Homogeneity of Cell Cycle Length in Developing Mouse Cortex
J. Neurosci.,
March 15, 1997;
17(6):
2079 - 2087.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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J. Neurosci.,
March 15, 1997;
17(6):
2088 - 2100.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Thomaidou, M. C. Mione, J. F. R. Cavanagh, and J. G. Parnavelas
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J. Neurosci.,
February 1, 1997;
17(3):
1075 - 1085.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G Diez-Roux and R. Lang
Macrophages induce apoptosis in normal cells in vivo
Development,
January 9, 1997;
124(18):
3633 - 3638.
[Abstract]
[PDF]
|
|
|
|
|
|
|
C. Reid, S. Tavazoie, and C. Walsh
Clonal dispersion and evidence for asymmetric cell division in ferret cortex
Development,
January 6, 1997;
124(12):
2441 - 2450.
[Abstract]
[PDF]
|
|
|
|
|
|
|
N Warren and D. Price
Roles of Pax-6 in murine diencephalic development
Development,
January 4, 1997;
124(8):
1573 - 1582.
[Abstract]
[PDF]
|
|
|
|
|
|
|
T. Takahashi, R. S. Nowakowski, and V. S. Caviness Jr.
The Leaving or Q Fraction of the Murine Cerebral Proliferative Epithelium: A General Model of Neocortical Neuronogenesis
J. Neurosci.,
October 1, 1996;
16(19):
6183 - 6196.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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J. Neurosci.,
September 15, 1996;
16(18):
5762 - 5776.
[Abstract]
[Full Text]
[PDF]
|
|
|
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|
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A. Blaschke, K Staley, and J Chun
Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex
Development,
January 4, 1996;
122(4):
1165 - 1174.
[Abstract]
[PDF]
|
|
|
|
|
|
|
L. H. Tsai, T. Takahashi, V. S. Caviness, and E. Harlow
Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system
Development,
December 1, 1993;
119(4):
1029 - 1040.
[Abstract]
[PDF]
|
|
|
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