Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion

Kriegstein, Arnold R.; Noctor, Stephen C.; Martínez‐Cerdeño, Verónica

doi:10.1038/nrn2008

Cited by 662 publications

(645 citation statements)

References 90 publications

Supporting

Mentioning

604

Contrasting

Unclassified

Order By: Relevance

“…1L). These progenitors have been considered fundamental for the generation of neocortical neurons and for cortical surface expansion (Kriegstein et al, 2006). However, they do not seem to play a major role in ferret corticogenesis, where they are far less abundant than in mouse (Arai et al, 2011) or primate — both macaque (Betizeau et al, 2013) and human (Hansen et al, 2010) — cortices, throughout the neurogenic period and across different areas, although a greater proportion of these progenitors is actively cycling in the ferret (Poluch and Juliano, 2015; Reillo and Borrell, 2012; Reillo et al, 2011; present study).…”

Section: Discussionmentioning

confidence: 99%

“…The neocortex of these species is folded into grooves (sulci) and ridges (gyri), a trait known as gyrencephaly, as opposed to lissencephaly, in which the cortical surface is smooth (Lewitus et al, 2013; Zilles et al, 2013). To understand cortical expansion, it is necessary to study the developmental mechanisms underlying it, especially the roles played by the various types of neural progenitors with varying degrees of self‐renewing and neurogenic capacities and the processes that regulate their neuron output (Fietz and Huttner, 2011; Florio and Huttner, 2014; Franco and Muller, 2013; Kriegstein et al, 2006; Lewitus et al, 2013; Lui et al, 2011; Zilles et al, 2013). …”

mentioning

confidence: 99%

“…In many mammalian species, this area is progressively subdivided into two subregions, the inner subventricular zone (ISVZ) and the outer subventricular zone (OSVZ), which appears later in development and is greatly expanded in gyrencephalic species (Cheung et al, 2007; Fish et al, 2008; Franco and Muller, 2013; Kriegstein et al, 2006; Lui et al, 2011; Martinez‐Cerdeno et al, 2012; Smart et al, 2002). The SVZ harbors a variety of neural progenitors, collectively referred to as basal progenitors, which eventually become the main source of neocortical neurons.…”

mentioning

confidence: 99%

See 2 more Smart Citations

S‐phase duration is the main target of cell cycle regulation in neural progenitors of developing ferret neocortex

García

Chang

Arai

et al. 2015

J of Comparative Neurology

View full text Add to dashboard Cite

The evolutionary expansion of the neocortex primarily reflects increases in abundance and proliferative capacity of cortical progenitors and in the length of the neurogenic period during development. Cell cycle parameters of neocortical progenitors are an important determinant of cortical development. The ferret (Mustela putorius furo), a gyrencephalic mammal, has gained increasing importance as a model for studying corticogenesis. Here, we have studied the abundance, proliferation, and cell cycle parameters of different neural progenitor types, defined by their differential expression of the transcription factors Pax6 and Tbr2, in the various germinal zones of developing ferret neocortex. We focused our analyses on postnatal day 1, a late stage of cortical neurogenesis when upper‐layer neurons are produced. Based on cumulative 5‐ethynyl‐2′‐deoxyuridine (EdU) labeling as well as Ki67 and proliferating cell nuclear antigen (PCNA) immunofluorescence, we determined the duration of the various cell cycle phases of the different neocortical progenitor subpopulations. Ferret neocortical progenitors were found to exhibit longer cell cycles than those of rodents and little variation in the duration of G1 among distinct progenitor types, also in contrast to rodents. Remarkably, the main difference in cell cycle parameters among the various progenitor types was the duration of S‐phase, which became shorter as progenitors progressively changed transcription factor expression from patterns characteristic of self‐renewal to those of neuron production. Hence, S‐phase duration emerges as major target of cell cycle regulation in cortical progenitors of this gyrencephalic mammal. J. Comp. Neurol. 524:456–470, 2016. © 2015 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.

show abstract

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

S‐phase duration is the main target of cell cycle regulation in neural progenitors of developing ferret neocortex

García

Chang

Arai

et al. 2015

J of Comparative Neurology

View full text Add to dashboard Cite

show abstract

“…Although many intrinsic and extrinsic factors may influence cortical size and cytoarchitecture, such as patterns of neuronal migration (Letinic et al, 2002;Kriegstein and Noctor, 2004;Bystron et al, 2006), thalamic afferents (Windrem and Finlay, 1991;Dehay et al, 2001) and the diversification of subventricular zone neural progenitors (Smart et al, 2002;Haubensak et al, 2004;Miyata et al, 2004;Noctor et al, 2004;Fish et al, 2008), an increase in neuron number during brain development and evolution is ultimately controlled by the number and modes of division of neural progenitors in the embryonic ventricular and subventricular zones (Götz and Huttner, 2005;Kriegstein et al, 2006;Fish et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Brca1 is required for embryonic development of the mouse cerebral cortex to normal size by preventing apoptosis of early neural progenitors

Pulvers

Huttner

2009

Development

View full text Add to dashboard Cite

The extent of apoptosis of neural progenitors is known to influence the size of the cerebral cortex. Mouse embryos lacking Brca1, the ortholog of the human breast cancer susceptibility gene BRCA1, show apoptosis in the neural tube, but the consequences of this for brain development have not been studied. Here we investigated the role of Brca1 during mouse embryonic cortical development by deleting floxed Brca1 using Emx1-Cre, which leads to conditional gene ablation specifically in the dorsal telencephalon after embryonic day (E) 9.5. The postnatal Brca1-ablated cerebral cortex was substantially reduced in size with regard to both cortical thickness and surface area. Remarkably, although the thickness of the cortical layers (except for the upper-most layer) was decreased, cortical layering as such was essentially unperturbed. High levels of apoptosis were found at E11.5 and E13.5, but dropped to near-control levels by E16.5. The apoptosis at the early stage of neurogenesis occurred in both BrdU pulse-labeled neural progenitors and the neurons derived therefrom. No changes were observed in the mitotic index of apical (neuroepithelial, radial glial) progenitors and basal (intermediate) progenitors, indicating that Brca1 ablation did not affect cell cycle progression. Brca1 ablation did, however, result in the nuclear translocation of p53 in neural progenitors, suggesting that their apoptosis involved activation of the p53 pathway. Our results show that Brca1 is required for the cerebral cortex to develop to normal size by preventing the apoptosis of early cortical progenitors and their immediate progeny. Development 136, 1859Development 136, -1868Development 136, (2009Development 136, ) doi:10.1242 Max Planck Institute for Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany. . Brca1 is widely expressed in proliferating tissues and is also expressed in the ventricular neuroepithelium of the neural tube (Korhonen et al., 2003). KEY WORDS: Brca1, Apoptosis, Cerebral cortexThe relevance of apoptosis in cortical development (Haydar et al., 1999), the increased apoptosis of neuroepithelial cells observed in systemic Brca1 knockouts (Gowen et al., 1996;Xu et al., 2001), and the expression pattern of Brca1 in neural progenitors, when considered together, raise the intriguing possibility that Brca1 might have a role in the development of the cerebral cortex. Moreover, the apparent link between BRCA1 and the primary microcephaly genes ASPM (Bond et al., 2002;Zhong et al., 2005) and MCPH1 (Xu et al., 2004;Lin et al., 2005), whereby knockdown of either microcephaly gene leads to a decrease in BRCA1 levels, also leads to the question of whether BRCA1 has a role in brain size regulation. In this context, it is interesting to note that BRCA1 has undergone positive selection in the primate lineage (Huttley et al., 2000), raising the possibility that it might have been selected owing to a function in brain development. Here, we have investigated this issue by conditional ablation of Brca1 in cor...

show abstract

“…It is known that differential planar expansions of the neuroepithelium, combined with restrictions to expansion at specific zones, contribute to model the neural tube morphology (Concha and Adams, 1998;Ciruna et al, 2006;Kriegstein et al, 2006). The identification of ZHMDs displaying characteristic positional changes as a function of the time allow proposing a step-by-step model of OT morphogenesis based on a sequence of simple but significant morphogenetic changes mediated by space-dependent differences in NEcs proliferation.…”

Section: Discussionmentioning

confidence: 99%

Optic tectum morphogenesis: A step‐by‐step model based on the temporal–spatial organization of the cell proliferation. Significance of deterministic and stochastic components subsumed in the spatial organization

Rapacioli

Duarte

Celin

et al. 2012

Developmental Dynamics

View full text Add to dashboard Cite

Background: Cell proliferation plays an important morphogenetic role. This work analyzes the temporalspatial organization of cell proliferation as an attempt to understand its contribution to the chick optic tectum (OT) morphogenesis. Results: A morphogenetic model based on space-dependent differences in cell proliferation is presented. Step1: a medial zone of high mitotic density (mZHMD) appears at the caudal zone. Step2: the mZHMD expands cephalically forming the dorsal curvature and then duplicates into two bilateral ZHMDs (bZHMD). Step3: the bZHMDs move toward the central region of each hemitectum. Step4: the planar expansion of both bZHMD and a relative decrement in the dorsal midline growth produces a dorsal medial groove separating the tectal hemispheres. Step5: a relative caudal displacement of the bZHMDs produces the OT caudal curvature. Numerical sequences derived from records of mitotic cells spatial coordinates, analyzed as stochastic point processes, show that they correspond to 1/f (b) processes. The spatial organization subsumes deterministic and stochastic components. Conclusions: The deterministic component describes the presence of a long-range influence that installs an asymmetric distribution of cell proliferation, i.e., an asymmetrically located ZHMD that print space-dependent differences onto the tectal corticogenesis. The stochastic component reveals short-range anti-correlations reflecting spatial clusterization and synchronization between neighboring cells. Developmental Dynamics 241:1043-1061, 2012. V C 2012 Wiley Periodicals, Inc.Key words: developing CNS; mitotic cell organization; nonlinear analyses; morphogenesis Key findings:The signals representing the mitotic cell spatial organization display 1/f type spectrum. The signals subsume deterministic components that reveal the existence of long-range influences. The signals subsume stochastic fluctuations revealing short-range anti-correlations between adjacent cells. The differential displacements of zones of high mitotic density regulate planar expansion. The asymmetric proliferation prints space-dependent histogenetic changes to the tectal corticogenesis.

show abstract

Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion

Cited by 662 publications

References 90 publications

S‐phase duration is the main target of cell cycle regulation in neural progenitors of developing ferret neocortex

S‐phase duration is the main target of cell cycle regulation in neural progenitors of developing ferret neocortex

Brca1 is required for embryonic development of the mouse cerebral cortex to normal size by preventing apoptosis of early neural progenitors

Optic tectum morphogenesis: A step‐by‐step model based on the temporal–spatial organization of the cell proliferation. Significance of deterministic and stochastic components subsumed in the spatial organization

Contact Info

Product

Resources

About