Intermediate Neuronal Progenitors (Basal Progenitors) Produce Pyramidal–Projection Neurons for All Layers of Cerebral Cortex

Kowalczyk, Tom; Pontious, Adria; Englund, Chris; Daza, Ray A. M.; Bedogni, Francesco; Hodge, Rebecca D.; Attardo, Alessio; Bell, Chris; Huttner, Wieland B.; Hevner, Robert F.

doi:10.1093/cercor/bhn260

Cited by 378 publications

(400 citation statements)

References 61 publications

(134 reference statements)

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“…2). In agreement with this notion, the occurrence of direct neurogenesis in the mouse cerebral cortex is remarkably infrequent (Attardo et al, 2008; Haubensak et al, 2004; Kowalczyk et al, 2009; Noctor et al, 2004). Hence, two fundamental changes must have occurred during vertebrate evolution between reptiles/birds and mammals leading to the emergence of the neocortex: (1) abundant generation of a novel type of neurogenic progenitor cell populating and dividing at basal positions in the embryonic cortex and (2) near complete suppression of the direct neurogenic program from aRGCs (Fig.…”

Section: Dawn and Expansion Of The Neocortexmentioning

confidence: 73%

Coevolution of radial glial cells and the cerebral cortex

Romero

Borrell

2015

Glia

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Radial glia cells play fundamental roles in the development of the cerebral cortex, acting both as the primary stem and progenitor cells, as well as the guides for neuronal migration and lamination. These critical functions of radial glia cells in cortical development have been discovered mostly during the last 15 years and, more recently, seminal studies have demonstrated the existence of a remarkable diversity of additional cortical progenitor cell types, including a variety of basal radial glia cells with key roles in cortical expansion and folding, both in ontogeny and phylogeny. In this review, we summarize the main cellular and molecular mechanisms known to be involved in cerebral cortex development in mouse, as the currently preferred animal model, and then compare these with known mechanisms in other vertebrates, both mammal and nonmammal, including human. This allows us to present a global picture of how radial glia cells and the cerebral cortex seem to have coevolved, from reptiles to primates, leading to the remarkable diversity of vertebrate cortical phenotypes. GLIA 2015;63:1303–1319

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Section: Dawn and Expansion Of The Neocortexmentioning

confidence: 73%

Coevolution of radial glial cells and the cerebral cortex

Romero

Borrell

2015

Glia

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“…To further confirm this result, we attempted to observe the migration of grafted cells directly through timelapse imaging analysis using an organotypic slice culture of the developing brain [10]. Cortical cells dissociated from embryos of Tbr2-EGFP mice allow us to identify newly born cortical neurons by the fluorescence of GFP driven by the Tbr2 promoter [32]. GFP-positive grafted cells exhibited neuronal migration-like movement in an apical to basal direction, following a trajectory perpendicular to the ventricular surface (Fig.…”

Section: Transplantation Of Cortical Cells Into Developing Brains Trementioning

confidence: 92%

Novel and Robust Transplantation Reveals the Acquisition of Polarized Processes by Cortical Cells Derived from Mouse and Human Pluripotent Stem Cells

Nagashima

Suzuki

Shitamukai

et al. 2014

Stem Cells and Development

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Current stem cell technologies have enabled the induction of cortical progenitors and neurons from embryonic stem cells (ESCs) and induced pluripotent stem cells in vitro. To understand the mechanisms underlying the acquisition of apico-basal polarity and the formation of processes associated with the stemness of cortical cells generated in monolayer culture, here, we developed a novel in utero transplantation system based on the moderate dissociation of adherens junctions in neuroepithelial tissue. This method enables (1) the incorporation of remarkably higher numbers of grafted cells and (2) quantitative morphological analyses at single-cell resolution, including time-lapse recording analyses. We then grafted cortical progenitors induced from mouse ESCs into the developing brain. Importantly, we revealed that the mode of process extension depends on the extrinsic apicobasal polarity of the host epithelial tissue, as well as on the intrinsic differentiation state of the grafted cells. Further, we successfully transplanted cortical progenitors induced from human ESCs, showing that our strategy enables investigation of the neurogenesis of human neural progenitors within the developing mouse cortex. Specifically, human cortical cells exhibit multiple features of radial migration. The robust transplantation method established here could be utilized both to uncover the missing gap between neurogenesis from ESCs and the tissue environment and as an in vivo model of normal and pathological human corticogenesis.

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“…NSPCs initially divide symmetrically to increase their numbers from embryonic day nine (E9) to E11 in mice (the proliferative period). 1,2 As development proceeds to the neurogenic period (starting around E11 in mice), NSPCs become longer and thinner to form "radial glia (RG)" as they support radial migration of cortical neurons. 3,4 The RG cells divide asymmetrically and produce one apical progenitor cell (AP) and one neuronal cell or intermediate progenitor cell (IP).…”

Section: Introductionmentioning

confidence: 99%

How to keep proliferative neural stem/progenitor cells

Tsunekawa

Osumi

2012

Cell Cycle

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I t has long been argued that cell cycle regulators such as cyclins, cyclindependent kinases and their inhibitors affect the fate of neuronal progenitor cells. Recently, we identified that cyclin D2, which localizes at the basal tip of the radial glial cell (i.e., the neural progenitor in the developing neocortex), functions to give differential cell fates to its daughter cells just after cell division. This basally biased localization is due to transportation of cyclin D2 mRNA via its unique cis-regulatory sequence and local translation into cyclin D2 protein at the basal endfoot. During division of the neural progenitor cells, cyclin D2 protein is inherited by the daughter cell that retain the basal process, resulting in asymmetric distribution of cyclin D2 protein between the two daughter cells. Cyclin D2 is similarly localized in the human fetal cortical primordium, suggesting a common mechanism for the maintenance of neural progenitors and a possible scenario in evolution of primate brains. Here we introduce our recent findings and discuss how cyclin D2 functions in mammalian brain development and evolution.

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Intermediate Neuronal Progenitors (Basal Progenitors) Produce Pyramidal–Projection Neurons for All Layers of Cerebral Cortex

Cited by 378 publications

References 61 publications

Coevolution of radial glial cells and the cerebral cortex

Coevolution of radial glial cells and the cerebral cortex

Novel and Robust Transplantation Reveals the Acquisition of Polarized Processes by Cortical Cells Derived from Mouse and Human Pluripotent Stem Cells

How to keep proliferative neural stem/progenitor cells

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