Cell-cycle control and cortical development

Dehay, Colette; Kennedy, Henry

doi:10.1038/nrn2097

Cited by 655Neurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene RegulationCongenital heart defects research

Cell-cycle control and cortical development

Dehay, Colette, Kennedy, Henry·2007·Nature Reviews Neuroscience

DOI 10.1038/nrn2097

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Abstract

The spatio-temporal timing of the last round of mitosis, followed by the migration of neuroblasts to the cortical plate leads to the formation of the six-layered cortex that is subdivided into functionally defined cortical areas. Whereas many of the cellular and molecular mechanisms have been established in rodents, there are a number of unique features that require further elucidation in primates. Recent findings both in rodents and in primates indicate that regulation of the cell cycle, specifically of the G1 phase has a crucial role in controlling area-specific rates of neuron production and the generation of cytoarchitectonic maps.

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oRGs are present in large numbers in gyrencephalic primates and are considered pivotal to the evolutionary increase in human cortex size and complexity.
“oRGs are present in large numbers in gyrencephalic primates22,23,40–44 and are considered pivotal to the evolutionary increase in human cortex size and complexity45,46.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [43]
G1/S transition rates might be associated with cell decisions because symmetric divisions can have shorter G1/S transition times than asymmetric divisions.
“Interestingly, G1/S transition rates might be associated with these cell decisions as symmetric divisions can have shorter G1/S transition times than asymmetric divisions [93, 101].”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [93]

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Evolution of the neocortex: a perspective from developmental biology
Rakic, P. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2719 · Cited by 1,565 · see citing works
“It is counterintuitive that such a large increase in neocortical size is achieved by a substantial prolongation, rather than reduction in duration of the cell cycl”
Cdks, cyclins and CKIs: roles beyond cell cycle regulation
Lim, S., & Kaldis, P. (2013) · Development · doi:10.1242/dev.091744 · Cited by 1,483 · see citing works
“However, it remains unclear how prolonging G1 induces differentiation mechanistically, other than the hypothesis that because G1 is the period of the cell cycle in which cells are exposed to extrinsic differentiating stimuli, spending more time in G1 should arguably lead to an accumulation of cell fate determinants to…”
Background
The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring
Choi, G. B., Yim, Y. S., Wong, H., Kim, S., Kim, H., Kim, S. V., Hoeffer, C. A., Littman, D. R., & Huh, J. R. (2016) · Science · doi:10.1126/science.aad0314 · Cited by 1,214 · see citing works
“1, H and I); (ii) cortical development starts at about E11 (20), which aligns well with the time points of potential fetal exposure to MIA (7); (iii) disorganized cortex and focal patches of abnormal laminar cytoarchitecture have been found in RESEARCH SCIENCE sciencemag.org 26 FEBRUARY 2016 • VOL 351 ISSUE 6276 933 1…”
Background
The origin and specification of cortical interneurons
Wonders, C. P., & Anderson, S. A. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1954 · Cited by 980 · see citing works
“Through various morphogens that induce cell divisions along the apical surface of the ventricular zone, cortical progenitors are born from radial glia and undergo a series of symmetric and asymmetric cell divisions to give rise to the cellular diversity throughout the cortex (Dehay and Kennedy 2007).”
Background
Development of the human cerebral cortex: Boulder Committee revisited
Bystron, I., Blakemore, C., & Rakic, P. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2252 · Cited by 977 · see citing works
“Attempts have been made to integrate more recent observations into the Boulder Commitee's schem”
Anatomy of hierarchy: Feedforward and feedback pathways in macaque visual cortex
Markov, N. T., Vezoli, J., Chameau, P., Falchier, A., Quilodran, R., Huissoud, C., Lamy, C., Misery, P., Giroud, P., Ullman, S., et al. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23458 · Cited by 759 · see citing works
“The SLN model of cortical hierarchy emphasizes the specificity of the supragranular layers, which in mammalian evolution undergo an expansion to reach a maximum in primates (Dehay and Kennedy, 2007; Hill and Walsh, 2005; Rakic, 2009).”
BackgroundSelf-citation
The use of brain organoids to investigate neural development and disease
Di Lullo, E., & Kriegstein, A. R. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.107 · Cited by 788 · see citing works
The Cell Biology of Neurogenesis: Toward an Understanding of the Development and Evolution of the Neocortex
Taverna, E., Götz, M., & Huttner, W. Β. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101011-155801 · Cited by 737 · see citing works
An intrinsic mechanism of corticogenesis from embryonic stem cells
Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., van den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., Schiffmann, S. N., et al. (2008) · Nature · doi:10.1038/nature07287 · Cited by 641 · see citing works
Neural progenitors, neurogenesis and the evolution of the neocortex
Florio, M., & Huttner, W. Β. (2014) · Development · doi:10.1242/dev.090571 · Cited by 624 · see citing works
“This led to the hypothesis that BP proliferation in the SVZ, and in particular the oSVZ, might be more strongly promoted by thalamocortical axon-derived mitogens in gyrencephalic as compared with lissencephalic species (Dehay and Kennedy, 2007).”
BackgroundResult
A Role for Intermediate Radial Glia in the Tangential Expansion of the Mammalian Cerebral Cortex
Reillo, I., Romero, C. D. J., García‐Cabezas, M. Á., & Borrell, V. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq238 · Cited by 631 · see citing works
“Pixel density was then scaled linearly from 0 to 1 and pseudocolored.”
BackgroundMethodResultInfluential
Area Patterning of the Mammalian Cortex
O’Leary, D. D. M., Chou, S., & Sahara, S. (2007) · Neuron · doi:10.1016/j.neuron.2007.10.010 · Cited by 574 · see citing works
“In vitro experiments using mouse tissue suggest that TCAs release a diffusible mitogenic activity that promotes the production of both glia and neurons by explants of the cortical VZ (Dehay and Kennedy, 2007).”
BackgroundInfluential
Cdk4/CyclinD1 Overexpression in Neural Stem Cells Shortens G1, Delays Neurogenesis, and Promotes the Generation and Expansion of Basal Progenitors
Lange, C. M., Huttner, W. Β., & Calegari, F. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.05.026 · Cited by 565 · see citing works
Coordinating cell proliferation and differentiation: Antagonism between cell cycle regulators and cell type-specific gene expression
Ruijtenberg, S., & van den Heuvel, S. (2016) · Cell Cycle · doi:10.1080/15384101.2015.1120925 · Cited by 552 · see citing works
Inhibition of SRGAP2 function by its human-specific paralogs induces neoteny during spine maturation
Charrier, C., Joshi, K., Coutinho-Budd, J., Kim, J.-E., Lambert, N., de Marchena, J., Jin, W.-L., Vanderhaeghen, P., Ghosh, A., Sassa, T., et al. (2012) · Cell · doi:10.1016/j.cell.2012.03.034 · Cited by 454 · see citing works
“This could support the journey of neurons over the total thickness of the cortical wall, which is substantially increased in humans compared to non-human primates or rodents (Dehay and Kennedy, 2007; Rakic, 2009; Sidman and Rakic, 1973).”
Precursor Diversity and Complexity of Lineage Relationships in the Outer Subventricular Zone of the Primate
Betizeau, M., Cortay, V., Patti, D., Pfister, S., Gautier, E., Bellemin-Ménard, A., Afanassieff, M., Huissoud, C., Douglas, R. J., Kennedy, H., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.032 · Cited by 462 · see citing works
“…and Human Cortex Examination of the timing of the macaque GZ suggested that high proliferative rates are required to maintain and amplify the OSVZ progenitor pool over the protracted period of supragranu-lar neuron production in the macaque (Dehay and Kennedy, 2007; Lukaszewicz et al., 2005).”
InfluentialSelf-citation
Spatio-temporal regulation of circular RNA expression during porcine embryonic brain development
Venø, M. T., Hansen, T. B., Venø, S. T., Clausen, B. H., Grebing, M., Finsen, B. R., Holm, I. E., & Kjems, J. (2015) · Genome biology · doi:10.1186/s13059-015-0801-3 · Cited by 475 · see citing works
“Current knowledge of cellular and molecular mechanisms in brain development has so far mainly been obtained from studies on the rodent smooth-surfaced lissencephalic brain [6].”
Background
SUN1/2 and Syne/Nesprin-1/2 Complexes Connect Centrosome to the Nucleus during Neurogenesis and Neuronal Migration in Mice
Zhang, X., Lei, K., Yuan, X., Wu, X., Zhuang, Y., Xu, T., Xu, R., & Han, M. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.018 · Cited by 462 · see citing works
“Defective INM may also lengthen the G1 phase of RGPCs and lead to more differentiative mitotic divisions, which are expected to reduce the number of IPCs and progenitors lining the VZ (Dehay and Kennedy, 2007).”
Background
Oblique Radial Glial Divisions in the Developing Mouse Neocortex Induce Self-Renewing Progenitors outside the Germinal Zone That Resemble Primate Outer Subventricular Zone Progenitors
Shitamukai, A., Konno, D., & Matsuzaki, F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4773-10.2011 · Cited by 450 · see citing works
“Mouse outer VZ progenitors share cell properties with OSVZ progenitors in gyrencephalic mammals OSVZ progenitors are a different type of self-renewing progenitors implicated in cortical development in the primate and other gyrencephalic mammals (Kriegstein et al., 2006; Dehay and Kennedy, 2007).”
Background
GSK-3 is a master regulator of neural progenitor homeostasis
Kim, W.-Y., Wang, X., Wu, Y., Doble, B. W., Patel, S., Woodgett, J. R., & Snider, W. D. (2009) · Nature Neuroscience · doi:10.1038/nn.2408 · Cited by 399 · see citing works
“Shortened cell cycle has previously been implicated in reduced responsiveness to differentiation signals and it has been suggested that cell-cycle regulation is an important control point for mechanisms that account for differences in neuron number between rodents and primate”
Background
Human-Specific NOTCH2NL Genes Expand Cortical Neurogenesis through Delta/Notch Regulation
Suzuki, I. K., Gacquer, D., Van Heurck, R., Kumar, D., Wojno, M., Bilheu, A., Herpoel, A., Lambert, N., Cheron, J., Polleux, F., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.067 · Cited by 471 · see citing works
“This effect is strikingly in line with the expected pattern of human cortical neurogenesis compared with non-human primates: human cortical RG cells are expected to go through an increased number of self-renewing and/or proliferative cycles compared with non-human primates (Dehay and Kennedy, 2007; Geschwind and Rakic…”
BackgroundResult
Neurogenesis during development of the vertebrate central nervous system
Paridaen, J. T. M. L., & Huttner, W. Β. (2014) · EMBO Reports · doi:10.1002/embr.201438447 · Cited by 390 · see citing works
“Changes in cell cycle length have been implicated in cell fate determination during neurogenesis [23].”
Assessment and surgical outcomes for mild type I and severe type II cortical dysplasia: A critical review and the UCLA experience
Lerner, J. T., Salamon, N., Hauptman, J. S., Velasco, T. R., Hemb, M., Wu, J. Y., Sankar, R., Shields, W. D., Engel, J., Fried, I., et al. (2009) · Epilepsia · doi:10.1111/j.1528-1167.2008.01998.x · Cited by 390 · see citing works
“(40% of cases) This histologic feature of the normal developing cerebral cortex is considered a sign of abnormal cortical development if identified in the postnatal brain (Dehay & Kennedy, 2007).”
Background
Neural stem and progenitor cells shorten S-phase on commitment to neuron production
Arai, Y., Pulvers, J. N., Haffner, C., Schilling, B., Nüsslein, I., Calegari, F., & Huttner, W. Β. (2011) · Nature Communications · doi:10.1038/ncomms1155 · Cited by 372 · see citing works
“, and there are intriguing links between NPC cell-cycle length and neuron outpu”
Background
Cerebral cortex expansion and folding: what have we learned?
Fernández, V., Llinares-Benadero, C., & Borrell, V. (2016) · The EMBO Journal · doi:10.15252/embj.201593701 · Cited by 357 · see citing works
“…enlargement of the brain, which has been related to an excessive production of progenitor cells and cortical neurons due to a decreased apoptosis, or a shortening of cell cycle and increased cell cycle re-entry (Dehay & Kennedy, 2007; Hansen et al , 2010; Wang et al , 2011; Barkovich et al , 2012).”
Influential
Mapping the Matrix: The Ways of Neocortex
Douglas, R. J., & Martin, K. A. C. (2007) · Neuron · doi:10.1016/j.neuron.2007.10.017 · Cited by 355 · see citing works
“This latter result begs the other question of how the counts should be interpreted, for at face value it suggests that there are major differences in the way that area 17 is assembled compared to all other cortical areas, but there are not (for review see Dehay and Kennedy, 2007).”
Background
The ASD Living Biology: from cell proliferation to clinical phenotype
Courchesne, E., Pramparo, T., Gazestani, V. H., Lombardo, M. V., Pierce, K., & Lewis, N. E. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0056-y · Cited by 333 · see citing works
“One of the primary mechanisms that regulate neuroprogenitor divisions is the rate of cell cycle progression, particularly G1/S transition time 92, 93 .”
DNA repair deficiency and neurological disease
McKinnon, P. J. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2559 · Cited by 323 · see citing works
The outer subventricular zone and primate-specific cortical complexification
Dehay, C., Kennedy, H., & Kosik, K. S. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.060 · Cited by 314 · see citing works
Self-citation
Decision by division: making cortical maps
RAKIC, P. T., Ayoub, A. E., Breunig, J. J., & Dominguez, M. H. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.01.007 · Cited by 272 · see citing works
Deletion of ERK2 Mitogen-Activated Protein Kinase Identifies Its Key Roles in Cortical Neurogenesis and Cognitive Function
Samuels, I. S., Karlo, J. C., Faruzzi, A. N., Pickering, K., Herrup, K., Sweatt, J. D., Saitta, S. C., & Landreth, G. E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0679-08.2008 · Cited by 278 · see citing works
“Disruption of the dynamics of NPC or IPC proliferation and differentiation result in alterations in cell number, cellular identity, and organization of the cortex (Dehay and Kennedy, 2007).”
Background
Mitochondrial dynamics in postmitotic cells regulate neurogenesis
Iwata, R., Casimir, P., & Vanderhaeghen, P. (2020) · Science · doi:10.1126/science.aba9760 · Cited by 281 · see citing works
Cell cycle control of mammalian neural stem cells: putting a speed limit on G1
Salomoni, P., & Calegari, F. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.01.006 · Cited by 272 · see citing works
Cortical progenitor expansion, self-renewal and neurogenesis—a polarized perspective
Fietz, S. A., & Huttner, W. Β. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.10.002 · Cited by 270 · see citing works
Trnp1 Regulates Expansion and Folding of the Mammalian Cerebral Cortex by Control of Radial Glial Fate
Stahl, R., Walcher, T., Romero, C. D. J., Pilz, G.-A., Cappello, S., Irmler, M., Sanz-Aquela, J. M., Beckers, J., Blum, R., Borrell, V., et al. (2013) · Cell · doi:10.1016/j.cell.2013.03.027 · Cited by 267 · see citing works
“In gyrated mammals, this radial expansion and lateral dispersion of neurons is achieved by a dramatic increase in neurogenic progenitor cells and the massive formation of bRG in the oSVZ, which are critical to lead radially migrating neurons into lateral dispersion (Dehay and Kennedy, 2007; Borrell and Reillo, 2012).”
Background
Programmed Cell Death in Neurodevelopment
Yamaguchi, Y., & Miura, M. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.01.019 · Cited by 258 · see citing works
Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex
Pilaz, L., Patti, D., Marcy, G., Ollier, É., Pfister, S., Douglas, R. J., Betizeau, M., Gautier, E., Cortay, V., Doerflinger, N., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909894106 · Cited by 244 · see citing works
“These observations and others (11, 12) led to the hypothesis that TG1 could be an integral part of a cellular mechanism regulating the mode of division (13, 14).”
BackgroundSelf-citation
Chd8 mediates cortical neurogenesis via transcriptional regulation of cell cycle and Wnt signaling
Durak, O., Gao, F., Kaeser-Woo, Y. J., Rueda, R., Martorell, A. J., Nott, A., Liu, C. Y., Watson, L. A., & Tsai, L.-H. (2016) · Nature Neuroscience · doi:10.1038/nn.4400 · Cited by 243 · see citing works
Deconstructing cortical folding: genetic, cellular and mechanical determinants
Llinares-Benadero, C., & Borrell, V. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0112-2 · Cited by 243 · see citing works
Ciliary transition zone activation of phosphorylated Tctex-1 controls ciliary resorption, S-phase entry and fate of neural progenitors
Li, A., Saito, M., Chuang, J.-Z., Tseng, Y. Y., Dedesma, C., Tomizawa, K., Kaitsuka, T., & Sung, C.-H. (2011) · Nature Cell Biology · doi:10.1038/ncb2218 · Cited by 231 · see citing works
“4a ), and the relationship between the cell cycle regulation and the fate control of radial glia has already been establishe”
Background
Maintaining genome stability in the nervous system
McKinnon, P. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3537 · Cited by 229 · see citing works
The 16p11.2 Deletion Mouse Model of Autism Exhibits Altered Cortical Progenitor Proliferation and Brain Cytoarchitecture Linked to the ERK MAPK Pathway
Pucilowska, J., Vithayathil, J., Tavares, E. J., Kelly, C., Karlo, J. C., & Landreth, G. E. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.4864-13.2015 · Cited by 207 · see citing works
“We and others have previously established that these potent cell cycle regulators are direct targets of ERK signaling and play important roles in progenitor proliferation (Calegari and Huttner, 2003; Dehay and Kennedy, 2007; Lange et al., 2009; Pucilowska et al., 2012).”
Background
Deficiencies in lamin B1 and lamin B2 cause neurodevelopmental defects and distinct nuclear shape abnormalities in neurons
Coffinier, C., Jung, H.-J., Nobumori, C., Chang, S., Tu, Y., Barnes, R. H., Yoshinaga, Y., de Jong, P. J., Vergnes, L., Reue, K., et al. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-06-0504 · Cited by 225 · see citing works
“(B) Immunostaining for TBR2, a marker for intermediate neuronal progenitors, at E14.”
BackgroundMethodInfluential
Genetic regulation of arealization of the neocortex
O’Leary, D. D. M., & Sahara, S. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.05.011 · Cited by 219 · see citing works
“com contributing to arealization [9].”
Role of radial glial cells in cerebral cortex folding
Borrell, V., & Götz, M. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.02.007 · Cited by 221 · see citing works
“A rapid amplification of bRG would be responsible for expanding the primate OSVZ to its outstanding size, and to prepare it for an eventual tsunami of upper-layer neuron production [16,33,52].”
Shaping Our Minds: Stem and Progenitor Cell Diversity in the Mammalian Neocortex
Franco, S. J., & Müller, U. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.022 · Cited by 219 · see citing works
“In addition, the SVZ is preferentially expanded specifically during the time of upper-layer neurogenesis (Takahashi et al., 1999; Lukaszewicz et al., 2006; Martı́nez-Cerdeño et al., 2006; Dehay and Kennedy, 2007).”
Abundant Occurrence of Basal Radial Glia in the Subventricular Zone of Embryonic Neocortex of a Lissencephalic Primate, the Common Marmoset Callithrix jacchus
Kelava, I., Reillo, I., Murayama, A. Y., Kalinka, A. T., Stenzel, D., Tomančák, P., Matsuzaki, F., Lebrand, C., Sasaki, E., Schwamborn, J. C., et al. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr301 · Cited by 212 · see citing works
Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type
Pilz, G.-A., Shitamukai, A., Reillo, I., Pacary, E., Schwausch, J., Stahl, R., Ninkovic, J., Snippert, H. J. G., Clevers, H. C., Godinho, L., et al. (2013) · Nature Communications · doi:10.1038/ncomms3125 · Cited by 212 · see citing works
“These progenitors are accommodated in additional germinal layers, like the inner and outer subventricular zone (i/oSVZ) 1–4 that are located basal to the ventricular zone (VZ), where progenitors are anchored at the ventricular surface (VS).”
Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex
Costa, M. R., Wen, G., Lepier, A., Schroeder, T., & Götz, M. (2007) · Development · doi:10.1242/dev.009951 · Cited by 208 · see citing works
“Indeed, considerably enlarged upper cortical layers characterize the primary visual area of the cortex in primates (for a review, see Dehay and Kennedy, 2007).”
Background
Genetically engineered human cortical spheroid models of tuberous sclerosis
Blair, J. D., Hockemeyer, D. F., & Bateup, H. S. (2018) · Nature Medicine · doi:10.1038/s41591-018-0139-y · Cited by 207 · see citing works
DISC1-dependent switch from progenitor proliferation to migration in the developing cortex
Ishizuka, K., Kamiya, A., Oh, E. C. T., Kanki, H., Seshadri, S., Robinson, J. F., Murdoch, H., Dunlop, A. J., Kubo, K., Furukori, K., et al. (2011) · Nature · doi:10.1038/nature09859 · Cited by 195 · see citing works
Human Models Are Needed for Studying Human Neurodevelopmental Disorders
Zhao, X., & Bhattacharyya, A. (2018) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2018.10.009 · Cited by 192 · see citing works
Cortical and Clonal Contribution of Tbr2 Expressing Progenitors in the Developing Mouse Brain
Vasistha, N. A., García-Moreno, F., Arora, S., Cheung, A. F. P., Arnold, S. J., Robertson, E. J., & Molnár, Z. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhu125 · Cited by 177 · see citing works
“Studies have shown an inherent difference in cell-cycle kinetics between different regions at embryonic ages that lead to differences in cortical numbers (Dehay et al. 1993; Polleux et al. 1997; Dehay and Kennedy 2007).”
Background
Emerging roles of neural stem cells in cerebral cortex development and evolution
Borrell, V., & Reillo, I. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22013 · Cited by 185 · see citing works
“Developmental Neurobiology Moreover, because cortical development in the lissencephalic mouse and rat does not include the formation of an OSVZ, this layer was believed to play a central role in the development of gyrencephaly (Smart et al., 2002; Dehay and Kennedy, 2007).”
BackgroundResultInfluential
Germinal Zones in the Developing Cerebral Cortex of Ferret: Ontogeny, Cell Cycle Kinetics, and Diversity of Progenitors
Reillo, I., & Borrell, V. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr284 · Cited by 177 · see citing works
“The IFL is a cell-poor zone filled with axon fascicles, which is commonly used to delimit ISVZ from OSVZ at late developmental stages (Smart et al. 2002; Dehay and Kennedy 2007).”
BackgroundResultInfluential
Discrete domains of gene expression in germinal layers distinguish the development of gyrencephaly
Romero, C. D. J., Bruder, C. E. G., Tomasello, U., Sanz‐Anquela, J. M., & Borrell, V. (2015) · The EMBO Journal · doi:10.15252/embj.201591176 · Cited by 173 · see citing works
“…the formation of folds and fissures (Welker, 1990), and many of the critical features defining cortical progenitor cells (cell cycle, amplification, neurogenesis) vary significantly across such regions (Dehay et al , 1993; Lukaszewicz et al , 2005; Dehay & Kennedy, 2007; Reillo et al , 2011).”
Influential
Primary Cilia in Brain Development and Diseases
Youn, Y. H., & Han, Y.-G. (2017) · American Journal Of Pathology · doi:10.1016/j.ajpath.2017.08.031 · Cited by 173 · see citing works
Developmental mechanisms underlying the evolution of human cortical circuits
Vanderhaeghen, P., & Polleux, F. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00675-z · Cited by 173 · see citing works
DYRK1A and cognition: A lifelong relationship
Arbonés, M. L., Thomazeau, A., Nakano-Kobayashi, A., Hagiwara, M., & Delabar, J. M. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.09.010 · Cited by 165 · see citing works
Diet controls normal and tumorous germline stem cells via insulin-dependent and -independent mechanisms in Drosophila
Hsu, H., LaFever, L., & Drummond‐Barbosa, D. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.11.006 · Cited by 168 · see citing works
“Given that the length of the G1 phase corresponds to a window of increased sensitivity to differentiation signals (Dehay and Kennedy, 2007), it is conceivable that shortening the G1 phase might contribute to the maintenance of the undifferentiated state of GSCs, as previously proposed for mammalian embryonic stem cell…”
Background
Cortical Folding: When, Where, How, and Why?
Striedter, G. F., Srinivasan, S., & Monuki, E. S. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034128 · Cited by 163 · see citing works
The N-Myc-DLL3 Cascade Is Suppressed by the Ubiquitin Ligase Huwe1 to Inhibit Proliferation and Promote Neurogenesis in the Developing Brain
Zhao, X., Arca, D. D., Lim, W. K., Brahmachary, M., Carro, M. S., Ludwig, T. E., Cardó, C. C., Guillemot, F., Aldape, K. D., Califano, A., et al. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.07.009 · Cited by 162 · see citing works
“Cortical neurogenesis is associated with progressive lengthening of the cell cycle and results in increased fraction of progenitors that exit the cell cycle and differentiate (Dehay and Kennedy, 2007; Gotz and Huttner, 2005).”
Influential
Progenitor Hyperpolarization Regulates the Sequential Generation of Neuronal Subtypes in the Developing Neocortex
Vitali, I., Fièvre, S., Telley, L., Oberst, P., Bariselli, S., Frangeul, L., Baumann, N., McMahon, J. J., Klingler, E., Bocchi, R., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.036 · Cited by 152 · see citing works
Distribution of neurons in functional areas of the mouse cerebral cortex reveals quantitatively different cortical zones
Herculano‐Houzel, S., WATSON, C. R. R., & Paxinos, G. (2013) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2013.00035 · Cited by 159 · see citing works
“Our findings thus support a combination of the “protomap” and “protocortex” models of specification of cortical areas (Dehay and Kennedy, 2007), one in which two zones are specified in the gray matter that differ in how neurons are added to the developing cortex, followed by functional…”
BackgroundResult
Insulinoma-Associated 1 Has a Panneurogenic Role and Promotes the Generation and Expansion of Basal Progenitors in the Developing Mouse Neocortex
Farkas, L. M., Haffner, C., Giger, T., Khaitovich, P., Nowick, K., Birchmeier, C., Pääbo, S., & Huttner, W. Β. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.020 · Cited by 159 · see citing works
“Two principal parameters determine how many of these divisions occur during cortical neurogenesis: (1) how often a given PC undergoes neurogenic divisions and (2) how many PCs capable of undergoing neurogenic division (neuronal PCs) are formed (Caviness et al., 1995; Dehay and Kennedy, 2007; Huttner and Kosodo, 2005;…”
Background
Gliogenesis in the outer subventricular zone promotes enlargement and gyrification of the primate cerebrum
Rash, B. G., Duque, A., Morozov, Y. M., Arellano, J. I., Micali, N., & Rakic, P. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1822169116 · Cited by 156 · see citing works
“The oSVZ compartment becomes very prominent in primates, including humans, and contains detached RGCs (11), recently renamed as outer radial glia (oRG) or basal radial glia (bRG) (5).”
Background
A Stem Cell Niche for Intermediate Progenitor Cells of the Embryonic Cortex
Javaherian, A., & Kriegstein, A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp029 · Cited by 155 · see citing works
“inside-out assembly of the 6-layered cortex (Smart 1973; McConnell 1995; Kriegstein et al. 2006; Rakic 2006; Cheung et al. 2007; Dehay and Kennedy 2007; Pontious et al. 2008).”
Background
Compartmentalization of Cerebral Cortical Germinal Zones in a Lissencephalic Primate and Gyrencephalic Rodent
García‐Moreno, F., Vasistha, N. A., Trévia, N., Bourne, J. A., & Molnár, Z. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr312 · Cited by 154 · see citing works
Regulation of cerebral cortical neurogenesis by the Pax6 transcription factor
Manuel, M. N., Mi, D., Mason, J. O., & Price, D. J. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00070 · Cited by 153 · see citing works
Interneurons in the developing human neocortex
Zečević, N., Hu, F., & Jakovčevski, I. (2010) · Developmental Neurobiology · doi:10.1002/dneu.20812 · Cited by 153 · see citing works
“Prolonged proliferation in the primate-specific outer SVZ (Lukaszewicz et al., 2006; Dehay and Kennedy, 2007), is temporally matched with emergence of enlarged supragranular layers (layers II–IV) in primates (Hill and Walsh, 2005).”
Background
Recapitulating cortical development with organoid culture in vitro and modeling abnormal spindle-like (ASPM related primary) microcephaly disease
Li, R., Sun, L., Fang, A., Li, P., Wu, Q., & Wang, X. (2017) · Protein & Cell · doi:10.1007/s13238-017-0479-2 · Cited by 154 · see citing works
“This article is an open access publication SVZ (OSVZ) by the inner fiber layer (IFL) in primates (Dehay and Kennedy, 2007; Hansen et al., 2010; LaMonica et al., 2012;Garcia-Morenoet al., 2012).”
Background
From genes to folds: a review of cortical gyrification theory
Ronan, L., & Fletcher, P. C. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0961-z · Cited by 145 · see citing works
“At the onset of neurogenesis, these so-called apical progenitor cells (Dehay and Kennedy 2007; Fietz and Huttner 2011) divide asymmetrically producing either a neuron or two other types of progenitor cells, namely basal radial glia (bRG) or intermediate progenitor cells (IPCs).”
Background
Stage-Specific Modulation of Cortical Neuronal Development by Mmu-miR-134
Gaughwin, P. M., Cieśla, M., Yang, H. H., Lim, B., & Brundin, P. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq262 · Cited by 147 · see citing works
“ventricular zone (VZ) and subventricular zone (SVZ) in a temporally regulated manner (Dehay and Kennedy 2007).”
Background
Generation of cortical neurons from mouse embryonic stem cells
Gaspard, N., Bouschet, T., Herpoel, A., Naeije, G., van den Ameele, J., & Vanderhaeghen, P. (2009) · Nature Protocols · doi:10.1038/nprot.2009.157 · Cited by 142 · see citing works
“, suggesting that some in vivo cues required for the generation of a complete repertoire upper layer neurons are missing in vitro”
Background
Liver X Receptors and Oxysterols Promote Ventral Midbrain Neurogenesis In Vivo and in Human Embryonic Stem Cells
Sacchetti, P., Sousa, K. M., Hall, A. C., Liste, I., Steffensen, K. R., Theofilopoulos, S., Parish, C. L., Hazenberg, C. L. E., Richter, L. Ä., Hovatta, O., et al. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.08.019 · Cited by 142 · see citing works
Symmetric vs. Asymmetric Stem Cell Divisions: An Adaptation against Cancer?
Shahriyari, L., & Komarova, N. L. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076195 · Cited by 136 · see citing works
“The fitness parameter defines the relative probability of the given cell-type to be chosen for division.”
Background
Congenital microcephaly
Alcantara, D., & O’Driscoll, M. (2014) · American Journal of Medical Genetics Part C Seminars in Medical Genetics · doi:10.1002/ajmg.c.31397 · Cited by 136 · see citing works
Synaesthesia and cortical connectivity
Bargary, G., & Mitchell, K. J. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.03.007 · Cited by 129 · see citing works
Neurogenesis in the Developing and Adult Brain—Similarities and Key DifferencesPreprint
Götz, M., Nakafuku, M., & Petřík, D. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018853 · Cited by 131 · see citing works
“Although most radial glial cells have a short cell cycle during development ranging between 10 and 18 h (Götz and Huttner 2005; Dehay and Kennedy 2007; Lange and Calegari 2010; Arai et al. 2011), most adult radial glial cells in the SEZ and subgranular zone (SGZ) of the DG have a much longer cell-cycle length ranging…”
Area-specific temporal control of corticospinal motor neuron differentiation by COUP-TFI
Tomassy, G. S., Leonibus, E. D., Jabaudon, D., Lodato, S., Alfano, C., Mele, A., Macklis, J. D., & Studer, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911792107 · Cited by 126 · see citing works
“The fate of neurons and laminar cytoarchitecture in each specific area determines their function: the adult primary motor cortex contains a large number of CSMN and has a thick layer V; the primary somatosensory area is characterized by a thick layer IV, where the neurons that receive relayed sensory inputs are locate…”
Background
Neuronal migration in the CNS during development and disease: insights from in vivo and in vitro models
Buchsbaum, I. Y., & Cappello, S. (2019) · Development · doi:10.1242/dev.163766 · Cited by 128 · see citing works
Cyclin D2 Is Critical for Intermediate Progenitor Cell Proliferation in the Embryonic Cortex
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“Indeed, changes in Ts across the period of cortical neurogenesis have been observed in primates, in which biphasic modulation of Ts has been related to cortical expansion and “laminar elaboration” (Kornack and Rakic, 1998; Dehay and Kennedy, 2007).”
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“Furthermore, given its capacity to influence progenitor cell renewal, Cyclin D2 lends itself for evolutionary selection to increase the number of cell cycles (known to occur in primates) for generating a larger cortex (Finlay and Darlington, 1995; Rakic, 1995; Dehay and Kennedy, 2007), or within a”
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“The timing of neuronal differentiation by stem/progenitor cells in the telencephalon is regulated by the timing of cell cycle exit, such that over-expression of cyclin D prolongs the proliferation of undifferentiated cells and delays the onset of neurogenesis (Dehay and Kennedy, 2007; Lange et al., 2009).”
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Diverse Behaviors of Outer Radial Glia in Developing Ferret and Human Cortex
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“Specifically, the subventricular zone (SVZ) is greatly expanded in gyrencephalic primates and can be subdivided into an inner and outer region, the latter of which is negligible in lissencephalic rodents (Smart et al., 2002; Lukaszewicz et al., 2005; Zecevic et al., 2005; Dehay and Kennedy, 2007; Bayatti et al., 2008;…”
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ICK is essential for cell type‐specific ciliogenesis and the regulation of ciliary transport
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Modulation of the cell cycle contributes to the parcellation of the primate visual cortex
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Self-citation
G1 Phase Regulation, Area-Specific Cell Cycle Control, and Cytoarchitectonics in the Primate Cortex
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Self-citation
Rôle des régulateurs de la phase G1 du cycle cellulaire dans la corticogenèse
Pilaz, L.-J. (2009) · theses.fr (ABES)
Regulation of Neuroblast Cell-Cycle Kinetics Plays a Crucial Role in the Generation of Unique Features of Neocortical Areas
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Self-citation
Role of G1 phase regulators during corticogenesis
Pilaz, L. (2009) · doi:10.70675/9f47e9acz5e06z4d39z83b5za3e00f543c58

Authors: Dehay, C., & Kennedy, H.
Affiliations: Lyon 1 Université (FR)
Corresponding author: Dehay, Colette
ORCID: Dehay, Colette
Kennedy, Henry
Venue: Nature Reviews Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2007-06
Volume: 8
Issue: 6
Pages: 438-450
ISSN: 1471-003X (ISSN-L)
1471-0048
DOI: 10.1038/nrn2097
OpenAlex: W2010852678
Cited by: 655
References: 170
Citations by year: 2026: 9 · 2025: 15 · 2024: 17 · 2023: 28 · 2022: 18 · 2021: 30 · 2020: 39 · 2019: 30 · 2018: 47 · 2017: 36 · 2016: 39 · 2015: 34 · 2014: 61 · 2013: 52 · 2012: 47
FWCI: 3.18
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature reviews. Neuroscience (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
Keywords: cortical development, cell cycle regulation, G1 phase, neuronal proliferation, neuronal differentiation, neuroblast migration, cortical plate, cortical lamination, cortical regions, cytoarchitecture, primate cortex, rodent cortex
MeSH terms: Animals, Cell Communication, Cell Cycle, Cell Differentiation, Cerebral Cortex, Humans, Neurons, Stem Cells, Signal Transduction, G1 Phase, Cell Cycle Proteins, Cell Proliferation

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Cell-cycle control and cortical development

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