The Cell Biology of Neurogenesis: Toward an Understanding of the Development and Evolution of the Neocortex

Taverna, Elena; Götz, Magdalena; Huttner, Wieland B.

doi:10.1146/annurev-cellbio-101011-155801

Cited by 638 publications

(784 citation statements)

References 260 publications

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“…The structure and function of a given brain area is determined during ontogeny by the regulation of cell proliferation and migration (Cheung et al, 2010; Lui et al, 2011; Borrell and Calegari, 2014; Florio and Huttner, 2014; Taverna et al, 2014). Recent investigations have tried to establish links between the organization of the germinal zones and telencephalic structures in various species.…”

Section: Subventricular Zone In Sauropsids and Mammalsmentioning

confidence: 99%

From sauropsids to mammals and back: New approaches to comparative cortical development

Montiel

Vasistha

García-Moreno

et al. 2015

J of Comparative Neurology

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Evolution of the mammalian neocortex (isocortex) has been a persisting problem in neurobiology. While recent studies have attempted to understand the evolutionary expansion of the human neocortex from rodents, similar approaches have been used to study the changes between reptiles, birds, and mammals. We review here findings from the past decades on the development, organization, and gene expression patterns in various extant species. This review aims to compare cortical cell numbers and neuronal cell types to the elaboration of progenitor populations and their proliferation in these species. Several progenitors, such as the ventricular radial glia, the subventricular intermediate progenitors, and the subventricular (outer) radial glia, have been identified but the contribution of each to cortical layers and cell types through specific lineages, their possible roles in determining brain size or cortical folding, are not yet understood. Across species, larger, more diverse progenitors relate to cortical size and cell diversity. The challenge is to relate the radial and tangential expansion of the neocortex to the changes in the proliferative compartments during mammalian evolution and with the changes in gene expression and lineages evident in various sectors of the developing brain. We also review the use of recent lineage tracing and transcriptomic approaches to revisit theories and to provide novel understanding of molecular processes involved in specification of cortical regions. J. Comp. Neurol. 524:630–645, 2016. © 2015 The Authors. The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.

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Section: Subventricular Zone In Sauropsids and Mammalsmentioning

confidence: 99%

From sauropsids to mammals and back: New approaches to comparative cortical development

Montiel

Vasistha

García-Moreno

et al. 2015

J of Comparative Neurology

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“…In humans, both aRG and bRG are able to self-amplify by symmetric proliferative divisions. They also share the capacity to divide asymmetrically to self-renew while producing neurons either directly or via bIPs (3)(4)(5)(6). In humans, bIPs further amplify the neuronal output of aRG and bRG by undergoing additional rounds of symmetric division before self-consuming into pairs of neurons (1,7).…”

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confidence: 99%

Human cerebral organoids recapitulate gene expression programs of fetal neocortex development

Camp

Badsha

Florio

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Cerebral organoids-3D cultures of human cerebral tissue derived from pluripotent stem cells-have emerged as models of human cortical development. However, the extent to which in vitro organoid systems recapitulate neural progenitor cell proliferation and neuronal differentiation programs observed in vivo remains unclear.Here we use single-cell RNA sequencing (scRNA-seq) to dissect and compare cell composition and progenitor-to-neuron lineage relationships in human cerebral organoids and fetal neocortex. Covariation network analysis using the fetal neocortex data reveals known and previously unidentified interactions among genes central to neural progenitor proliferation and neuronal differentiation. In the organoid, we detect diverse progenitors and differentiated cell types of neuronal and mesenchymal lineages and identify cells that derived from regions resembling the fetal neocortex. We find that these organoid cortical cells use gene expression programs remarkably similar to those of the fetal tissue to organize into cerebral cortex-like regions. Our comparison of in vivo and in vitro cortical single-cell transcriptomes illuminates the genetic features underlying human cortical development that can be studied in organoid cultures.

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“…They exhibit apicobasal polarity, with cellular processes contacting both the apical (ventricular) and the basal (pial) surfaces of the cortical wall. APs divide at the ventricular surface, initially in a symmetric self‐renewing manner that expands the progenitor pool, later switching to an asymmetric self‐renewing mode that maintains the pool while generating neurons and other progenitor types (Götz and Huttner, 2005; Kriegstein and Alvarez‐Buylla, 2009; Taverna et al, 2014). …”

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confidence: 99%

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

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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.

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The Cell Biology of Neurogenesis: Toward an Understanding of the Development and Evolution of the Neocortex

Cited by 638 publications

References 260 publications

From sauropsids to mammals and back: New approaches to comparative cortical development

From sauropsids to mammals and back: New approaches to comparative cortical development

Human cerebral organoids recapitulate gene expression programs of fetal neocortex development

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

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