 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
Volume 16, Number 19, Issue of October 1, 1996 pp. 6183-6196
Copyright ©1996 Society for NeuroscienceThe Leaving or Q Fraction of the Murine Cerebral Proliferative Epithelium: A General Model of Neocortical Neuronogenesis
Received April 4, 1996; revised June 5, 1996; accepted July 12, 1996.
Takao Takahashi1, 2, Richard S. Nowakowski3, and Verne S. Caviness Jr.1 1 Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts 02114, 2 Department of Pediatrics, Keio University School of Medicine, Tokyo 160, Japan, and 3 Department of Neuroscience and Cell Biology, University of Medicine and Dentistry of New Jersey-Robert Wood Johnson Medical School, Piscataway, New Jersey 08854
Neurons of neocortical layers II-VI in the dorsomedial cortex of the mouse arise in the pseudostratified ventricular epithelium (PVE) through 11 cell cycles over the six embryonic days 11-17 (E11-E17). The present experiments measure the proportion of daughter cells that leave the cycle (quiescent or Q fraction or Q) during a single cell cycle and the complementary proportion that continues to proliferate (proliferative or P fraction or P; P = 1
Q). Q and P for the PVE become 0.5 in the course of the eighth cycle, occurring on E14, and Q rises to ~0.8 (and P falls to ~0.2) in the course of the 10th cycle occurring on E16. This indicates that early in neuronogenesis, neurons are produced relatively slowly and the PVE expands rapidly but that the reverse happens in the final phase of neuronogenesis. The present analysis completes a cycle of analyses that have determined the four fundamental parameters of cell proliferation: growth fraction, lengths of cell cycle, and phases Q and P. These parameters are the basis of a coherent neuronogenetic model that characterizes patterns of growth of the PVE and mathematically relates the size of the initial proliferative population to the neuronal population of the adult neocortex.
Key words: neocortical neuronogenesis; cell cycle; proliferation; mouse; ventricular zone
This article has been cited by other articles:
R. Qiu, X. Wang, A. Davy, C. Wu, K. Murai, H. Zhang, J. G. Flanagan, P. Soriano, and Q. Lu
Regulation of neural progenitor cell state by ephrin-B
J. Cell Biol., October 21, 2008; 181(6): 973 - 983.
[Abstract] [Full Text] [PDF]
A. E. Schwob, L. J. Nguyen, and K. F. Meiri
Immortalization of Neural Precursors When Telomerase Is Overexpressed in Embryonal Carcinomas and Stem Cells
Mol. Biol. Cell, April 1, 2008; 19(4): 1548 - 1560.
[Abstract] [Full Text] [PDF]
W. Li, G. Sun, S. Yang, Q. Qu, K. Nakashima, and Y. Shi
Nuclear Receptor TLX Regulates Cell Cycle Progression in Neural Stem Cells of the Developing Brain
Mol. Endocrinol., January 1, 2008; 22(1): 56 - 64.
[Abstract] [Full Text] [PDF]
B. Suter, R. S. Nowakowski, P. G. Bhide, and V. S. Caviness
Navigating Neocortical Neurogenesis and Neuronal Specification: A Positional Information System Encoded by Neurogenetic Gradients
J. Neurosci., October 3, 2007; 27(40): 10777 - 10784.
[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. Fukumitsu, M. Ohtsuka, R. Murai, H. Nakamura, K. Itoh, and S. Furukawa
Brain-Derived Neurotrophic Factor Participates in Determination of Neuronal Laminar Fate in the Developing Mouse Cerebral Cortex
J. Neurosci., December 20, 2006; 26(51): 13218 - 13230.
[Abstract] [Full Text] [PDF]
G. J. Woodhead, C. A. Mutch, E. C. Olson, and A. Chenn
Cell-Autonomous beta-Catenin Signaling Regulates Cortical Precursor Proliferation
J. Neurosci., November 29, 2006; 26(48): 12620 - 12630.
[Abstract] [Full Text] [PDF]
P. Coti Bertrand, J. R. O'Kusky, and S. M. Innis
Maternal Dietary (n-3) Fatty Acid Deficiency Alters Neurogenesis in the Embryonic Rat Brain
J. Nutr., June 1, 2006; 136(6): 1570 - 1575.
[Abstract] [Full Text] [PDF]
J. S. Gal, Y. M. Morozov, A. E. Ayoub, M. Chatterjee, P. Rakic, and T. F. Haydar
Molecular and Morphological Heterogeneity of Neural Precursors in the Mouse Neocortical Proliferative Zones
J. Neurosci., January 18, 2006; 26(3): 1045 - 1056.
[Abstract] [Full Text] [PDF]
H. A. Mason, S. M. Rakowiecki, M. Raftopoulou, S. Nery, Y. Huang, T. Gridley, and G. Fishell
Notch signaling coordinates the patterning of striatal compartments
Development, October 1, 2005; 132(19): 4247 - 4258.
[Abstract] [Full Text] [PDF]
T. Tarui, T. Takahashi, R.S. Nowakowski, N.L. Hayes, P.G. Bhide, and V.S. Caviness
Overexpression of p27Kip1, Probability of Cell Cycle Exit, and Laminar Destination of Neocortical Neurons
Cereb Cortex, September 1, 2005; 15(9): 1343 - 1355.
[Abstract] [Full Text] [PDF]
S. N. Sansom, J. M. Hebert, U. Thammongkol, J. Smith, G. Nisbet, M. A. Surani, S. K. McConnell, and F. J. Livesey
Genomic characterisation of a Fgf-regulated gradient-based neocortical protomap
Development, September 1, 2005; 132(17): 3947 - 3961.
[Abstract] [Full Text] [PDF]
J. M. Gohlke, W. C. Griffith, and E. M. Faustman
A Systems-Based Computational Model for Dose-Response Comparisons of Two Mode of Action Hypotheses for Ethanol-Induced Neurodevelopmental Toxicity
Toxicol. Sci., August 1, 2005; 86(2): 470 - 484.
[Abstract] [Full Text] [PDF]
W. J. Moody and M. M. Bosma
Ion Channel Development, Spontaneous Activity, and Activity-Dependent Development in Nerve and Muscle Cells
Physiol Rev, July 1, 2005; 85(3): 883 - 941.
[Abstract] [Full Text] [PDF]
A. Dori, J. Cohen, W. F. Silverman, Y. Pollack, and H. Soreq
Functional Manipulations of Acetylcholinesterase Splice Variants Highlight Alternative Splicing Contributions to Murine Neocortical Development
Cereb Cortex, April 1, 2005; 15(4): 419 - 430.
[Abstract] [Full Text] [PDF]
W. Akamatsu, H. Fujihara, T. Mitsuhashi, M. Yano, S. Shibata, Y. Hayakawa, H. J. Okano, S.-i. Sakakibara, H. Takano, T. Takano, et al.
The RNA-binding protein HuD regulates neuronal cell identity and maturation
PNAS, March 22, 2005; 102(12): 4625 - 4630.
[Abstract] [Full Text] [PDF]
K.-i. Mizutani and T. Saito
Progenitors resume generating neurons after temporary inhibition of neurogenesis by Notch activation in the mammalian cerebral cortex
Development, March 15, 2005; 132(6): 1295 - 1304.
[Abstract] [Full Text] [PDF]
R. D. Hodge, A. J. D'Ercole, and J. R. O'Kusky
Insulin-Like Growth Factor-I Accelerates the Cell Cycle by Decreasing G1 Phase Length and Increases Cell Cycle Reentry in the Embryonic Cerebral Cortex
J. Neurosci., November 10, 2004; 24(45): 10201 - 10210.
[Abstract] [Full Text] [PDF]
K. Roy, K. Kuznicki, Q. Wu, Z. Sun, D. Bock, G. Schutz, N. Vranich, and A. P. Monaghan
The Tlx Gene Regulates the Timing of Neurogenesis in the Cortex
J. Neurosci., September 22, 2004; 24(38): 8333 - 8345.
[Abstract] [Full Text] [PDF]
T. Miyata, A. Kawaguchi, K. Saito, M. Kawano, T. Muto, and M. Ogawa
Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells
Development, July 1, 2004; 131(13): 3133 - 3145.
[Abstract] [Full Text] [PDF]
M. Albrieux, J.-C. Platel, A. Dupuis, M. Villaz, and W. J. Moody
Early Expression of Sodium Channel Transcripts and Sodium Current by Cajal-Retzius Cells in the Preplate of the Embryonic Mouse Neocortex
J. Neurosci., February 18, 2004; 24(7): 1719 - 1725.
[Abstract] [Full Text] [PDF]
C. Gregg and S. Weiss
Generation of Functional Radial Glial Cells by Embryonic and Adult Forebrain Neural Stem Cells
J. Neurosci., December 17, 2003; 23(37): 11587 - 11601.
[Abstract] [Full Text] [PDF]
F. Calegari and W. B. Huttner
An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis
J. Cell Sci., December 15, 2003; 116(24): 4947 - 4955.
[Abstract] [Full Text] [PDF]
D. A. Lyons, A. T. Guy, and J. D. W. Clarke
Monitoring neural progenitor fate through multiple rounds of division in an intact vertebrate brain
Development, August 1, 2003; 130(15): 3427 - 3436.
[Abstract] [Full Text] [PDF]
H. Valcanis and S.-S. Tan
Layer Specification of Transplanted Interneurons in Developing Mouse Neocortex
J. Neurosci., June 15, 2003; 23(12): 5113 - 5122.
[Abstract] [Full Text] [PDF]
T. Weissman, S. C. Noctor, B. K. Clinton, L. S. Honig, and A. R. Kriegstein
Neurogenic Radial Glial Cells in Reptile, Rodent and Human: from Mitosis to Migration
Cereb Cortex, June 1, 2003; 13(6): 550 - 559.
[Abstract] [Full Text] [PDF]
Q. Shen, W. Zhong, Y. N. Jan, and S. Temple
Asymmetric Numb distribution is critical for asymmetric cell division of mouse cerebral cortical stem cells and neuroblasts
Development, March 12, 2003; 129(20): 4843 - 4853.
[Abstract] [Full Text] [PDF]
T. F. Haydar, E. Ang Jr., and P. Rakic
Mitotic spindle rotation and mode of cell division in the developing telencephalon
PNAS, March 4, 2003; 100(5): 2890 - 2895.
[Abstract] [Full Text] [PDF]
H. L. P. Bahrey and W. J. Moody
Voltage-gated Currents, Dye and Electrical Coupling in the Embryonic Mouse Neocortex
Cereb Cortex, March 1, 2003; 13(3): 239 - 251.
[Abstract] [Full Text] [PDF]
D. Koketsu, A. Mikami, Y. Miyamoto, and T. Hisatsune
Nonrenewal of Neurons in the Cerebral Neocortex of Adult Macaque Monkeys
J. Neurosci., February 1, 2003; 23(3): 937 - 942.
[Abstract] [Full Text] [PDF]
C. Hanashima, L. Shen, S. C. Li, and E. Lai
Brain Factor-1 Controls the Proliferation and Differentiation of Neocortical Progenitor Cells through Independent Mechanisms
J. Neurosci., August 1, 2002; 22(15): 6526 - 6536.
[Abstract] [Full Text] [PDF]
A. Chenn and C. A. Walsh
Regulation of Cerebral Cortical Size by Control of Cell Cycle Exit in Neural Precursors
Science, July 19, 2002; 297(5580): 365 - 369.
[Abstract] [Full Text] [PDF]
T. Hatta, K. Moriyama, K. Nakashima, T. Taga, and H. Otani
The Role of gp130 in Cerebral Cortical Development: In Vivo Functional Analysis in a Mouse Exo Utero System
J. Neurosci., July 1, 2002; 22(13): 5516 - 5524.
[Abstract] [Full Text] [PDF]
R. A. Rachel, G. Dolen, N. L. Hayes, A. Lu, L. Erskine, R. S. Nowakowski, and C. A. Mason
Spatiotemporal Features of Early Neuronogenesis Differ in Wild-Type and Albino Mouse Retina
J. Neurosci., June 1, 2002; 22(11): 4249 - 4263.
[Abstract] [Full Text] [PDF]
T. Mitsuhashi, Y. Aoki, Y. Z. Eksioglu, T. Takahashi, P. G. Bhide, S. A. Reeves, and V. S. Caviness Jr.
Overexpression of p27Kip1 lengthens the G1 phase in a mouse model that targets inducible gene expression to central nervous system progenitor cells
PNAS, May 22, 2001; 98(11): 6435 - 6440.
[Abstract] [Full Text] [PDF]
A. Cahana, T. Escamez, R. S. Nowakowski, N. L. Hayes, M. Giacobini, A. von Holst, O. Shmueli, T. Sapir, S. K. McConnell, W. Wurst, et al.
Targeted mutagenesis of Lis1 disrupts cortical development and LIS1 homodimerization
PNAS, May 3, 2001; (2001) 101122598.
[Abstract] [Full Text]
A. L. S. Dowling, E. A. Iannacone, and R. T. Zoeller
Maternal Hypothyroidism Selectively Affects the Expression of Neuroendocrine-Specific Protein A Messenger Ribonucleic Acid in the Proliferative Zone of the Fetal Rat Brain Cortex
Endocrinology, January 1, 2001; 142(1): 390 - 399.
[Abstract] [Full Text] [PDF]
C. Dou, J. Lee, B. Liu, F. Liu, J. Massague, S. Xuan, and E. Lai
BF-1 Interferes with Transforming Growth Factor beta Signaling by Associating with Smad Partners
Mol. Cell. Biol., September 1, 2000; 20(17): 6201 - 6211.
[Abstract] [Full Text]
T. F. Haydar, F. Wang, M. L. Schwartz, and P. Rakic
Differential Modulation of Proliferation in the Neocortical Ventricular and Subventricular Zones
J. Neurosci., August 1, 2000; 20(15): 5764 - 5774.
[Abstract] [Full Text] [PDF]
R. Raballo, J. Rhee, R. Lyn-Cook, J. F. Leckman, M. L. Schwartz, and F. M. Vaccarino
Basic Fibroblast Growth Factor (Fgf2) Is Necessary for Cell Proliferation and Neurogenesis in the Developing Cerebral Cortex
J. Neurosci., July 1, 2000; 20(13): 5012 - 5023.
[Abstract] [Full Text] [PDF]
T. F. Haydar, R. S. Nowakowski, P. J. Yarowsky, and B. K. Krueger
Role of Founder Cell Deficit and Delayed Neuronogenesis in Microencephaly of the Trisomy 16 Mouse
J. Neurosci., June 1, 2000; 20(11): 4156 - 4164.
[Abstract] [Full Text] [PDF]
P. J. Horner, A. E. Power, G. Kempermann, H. G. Kuhn, T. D. Palmer, J. Winkler, L. J. Thal, and F. H. Gage
Proliferation and Differentiation of Progenitor Cells Throughout the Intact Adult Rat Spinal Cord
J. Neurosci., March 15, 2000; 20(6): 2218 - 2228.
[Abstract] [Full Text] [PDF]
I. Delalle, T. Takahashi, R.S. Nowakowski, L.-H. Tsai, and V.S. Caviness Jr
Cyclin E-p27 Opposition and Regulation of the G1 Phase of the Cell Cycle in the Murine Neocortical PVE: A Quantitative Analysis of mRNA In Situ Hybridization
Cereb Cortex, December 1, 1999; 9(8): 824 - 832.
[Abstract] [Full Text] [PDF]
T. Takahashi, T. Goto, S. Miyama, R. S. Nowakowski, and V. S. Caviness Jr
Sequence of Neuron Origin and Neocortical Laminar Fate: Relation to Cell Cycle of Origin in the Developing Murine Cerebral Wall
J. Neurosci., December 1, 1999; 19(23): 10357 - 10371.
[Abstract] [Full Text] [PDF]
P. C. Mabie, M. F. Mehler, and J. A. Kessler
Multiple Roles of Bone Morphogenetic Protein Signaling in the Regulation of Cortical Cell Number and Phenotype
J. Neurosci., August 15, 1999; 19(16): 7077 - 7088.
[Abstract] [Full Text] [PDF]
T. Takahashi, R.S. Nowakowski, and V.S. Caviness Jr
Review : Cell Cycle as Operational Unit of Neocortical Neuronogenesis
Neuroscientist, May 1, 1999; 5(3): 155 - 163.
[Abstract] [PDF]
P. Iacopetti, M. Michelini, I. Stuckmann, B. Oback, E. Aaku-Saraste, and W. B. Huttner
Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division
PNAS, April 13, 1999; 96(8): 4639 - 4644.
[Abstract] [Full Text] [PDF]
K. S. Bittman and J. J. LoTurco
Differential Regulation of Connexin 26 and 43 in Murine Neocortical Precursors
Cereb Cortex, March 1, 1999; 9(2): 188 - 195.
[Abstract] [Full Text] [PDF]
F. Polleux, C. Dehay, and H. Kennedy
Neurogenesis and Commitment of Corticospinal Neurons in reeler
J. Neurosci., December 1, 1998; 18(23): 9910 - 9923.
[Abstract] [Full Text] [PDF]
W. Li, C. A. Cogswell, and J. J. LoTurco
Neuronal Differentiation of Precursors in the Neocortical Ventricular Zone Is Triggered by BMP
J. Neurosci., November 1, 1998; 18(21): 8853 - 8862.
[Abstract] [Full Text] [PDF]
Z. Zhang and D. S. Galileo
Retroviral Transfer of Antisense Integrin alpha 6 or alpha 8 Sequences Results in Laminar Redistribution or Clonal Cell Death in Developing Brain
J. Neurosci., September 1, 1998; 18(17): 6928 - 6938.
[Abstract] [Full Text] [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
Primary Neural Precursors and Intermitotic Nuclear Migration in the Ventricular Zone of Adult Canaries
J. Neurosci., February 1, 1998; 18(3): 1020 - 1037.
[Abstract] [Full Text] [PDF]
F. Polleux, C. Dehay, B. Moraillon, and H. Kennedy
Regulation of Neuroblast Cell-Cycle Kinetics Plays a Crucial Role in the Generation of Unique Features of Neocortical Areas
J. Neurosci., October 15, 1997; 17(20): 7763 - 7783.
[Abstract] [Full Text] [PDF]
V. Tropepe, C. G. Craig, C. M. Morshead, and D. van der Kooy
Transforming Growth Factor-alpha Null and Senescent Mice Show Decreased Neural Progenitor Cell Proliferation in the Forebrain Subependyma
J. Neurosci., October 15, 1997; 17(20): 7850 - 7859.
[Abstract] [Full Text] [PDF]
A. Cahana, T. Escamez, R. S. Nowakowski, N. L. Hayes, M. Giacobini, A. von Holst, O. Shmueli, T. Sapir, S. K. McConnell, W. Wurst, et al.
Targeted mutagenesis of Lis1 disrupts cortical development and LIS1 homodimerization
PNAS, May 22, 2001; 98(11): 6429 - 6434.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|