Origin, maturation, and astroglial transformation of secondary radial glial cells in the developing dentate gyrus

Brunne, Bianka; Zhao, Shanting; Derouiche, Amin; Herz, Joachim; May, Petra; Frotscher, Michael; Bock, Hans H.

doi:10.1002/glia.21029

Cited by 80 publications

(98 citation statements)

References 64 publications

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“…Vimentin is a marker transiently expressed during radial glial cell development. In the second postnatal week, few astrocytes of the ML express vimentin (Brunne et al, 2010). By coimmunostaining of GFAP and vimentin, we found in P14 mutant DGs that a large portion of those abnormally increased GFAP ϩ cells were colabeled by the two markers (Fig.…”

Section: Loss Of Foxg1 Results In Malformation Of the Secondary Radiamentioning

confidence: 72%

“…3g,gЈ). This cellular morphology may indicate astroglial differentiation (Chiang et al, 1996;McManus et al, 1999;Weiss et al, 2003;Dasgupta and Gutmann, 2005;Brunne et al, 2010). In the infrapyramidal blade, most GFAP ϩ or BLBP ϩ cells displayed excessive arborization, suggestive of a transition to an astrocytic fate.…”

Section: Loss Of Foxg1 Results In Malformation Of the Secondary Radiamentioning

confidence: 99%

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Foxg1Has an Essential Role in Postnatal Development of the Dentate Gyrus

Tian

Gong²,

Yang³

et al. 2012

J. Neurosci.

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Foxg1, formerly BF-1, is expressed continuously in the postnatal and adult hippocampal dentate gyrus (DG). This transcription factor (TF) is thought to be involved in Rett syndrome, which is characterized by reduced hippocampus size, indicating its important role in hippocampal development. Due to the perinatal death of Foxg1 Ϫ/Ϫ mice, the function of Foxg1 in postnatal DG neurogenesis remains to be explored. Here, we describe the generation of a Foxg1 fl/fl mouse line. Foxg1 was conditionally ablated from the DG during prenatal and postnatal development by crossing this line with a Frizzled9-CreER TM line and inducing recombination with tamoxifen. In this study, we first show that disruption of Foxg1 results in the loss of the subgranular zone and a severely disrupted secondary radial glial scaffold, leading to the impaired migration of granule cells. Moreover, detailed analysis reveals that Foxg1 may be necessary for the maintenance of the DG progenitor pool and that the lack of Foxg1 promotes both gliogenesis and neurogenesis. We additionally show that Foxg1 may be required for the survival and maturation of postmitotic neurons and that Foxg1 may be involved in Reelin signaling in regulating postnatal DG development. Last, prenatal deletion of Foxg1 suggests that it is rarely involved in the migration of primordial granule cells. In summary, we report that Foxg1 is critical for DG formation, especially during early postnatal stage.

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Section: Loss Of Foxg1 Results In Malformation Of the Secondary Radiamentioning

confidence: 72%

Section: Loss Of Foxg1 Results In Malformation Of the Secondary Radiamentioning

confidence: 99%

Foxg1Has an Essential Role in Postnatal Development of the Dentate Gyrus

Tian

Gong²,

Yang³

et al. 2012

J. Neurosci.

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“…In the developing dentate gyrus, the first irregular contours of RGL stem cells appear at around postnatal day 3, when their radial processes begin to project across the more tightly packed GCL to the ML (50,51). In the adult dentate gyrus, the NGPα RGL stem cell population is renewing (24,29), and hence new primary processes are constantly extending through the GCL.…”

Section: Discussionmentioning

confidence: 99%

“…Angiogenesis occurs alongside neurogenesis in embryonic development when the BBB is formed, but the BBB does not fully mature until 3 weeks postnatally, when cues from the neuroepithelium are thought to drive the wrapping of vessels by astrocytes (95). This gives plenty of opportunity to RGL stem cells in the developing dentate gyrus (50,51) to receive similar cues and participate in the BBB via the wrapping of blood vessels. Furthermore, exogenous VEGF has been shown to increase the permeability of the BBB (96,97).…”

Section: Discussionmentioning

confidence: 99%

Fine processes of Nestin-GFP–positive radial glia-like stem cells in the adult dentate gyrus ensheathe local synapses and vasculature

Moss

Gebara

Bushong

et al. 2016

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

108

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Adult hippocampal neurogenesis relies on the activation of neural stem cells in the dentate gyrus, their division, and differentiation of their progeny into mature granule neurons. The complex morphology of radial glia-like (RGL) stem cells suggests that these cells establish numerous contacts with the cellular components of the neurogenic niche that may play a crucial role in the regulation of RGL stem cell activity. However, the morphology of RGL stem cells remains poorly described. Here, we used light microscopy and electron microscopy to examine Nestin-GFP transgenic mice and provide a detailed ultrastructural reconstruction analysis of Nestin-GFP-positive RGL cells of the dentate gyrus. We show that their primary processes follow a tortuous path from the subgranular zone through the granule cell layer and ensheathe local synapses and vasculature in the inner molecular layer. They share the ensheathing of synapses and vasculature with astrocytic processes and adhere to the adjacent processes of astrocytes. This extensive interaction of processes with their local environment could allow them to be uniquely receptive to signals from local neurons, glia, and vasculature, which may regulate their fate.adult neurogenesis | adult neural stem cell | neurogenic niche | electron microscopy | hippocampus N eurogenesis in the adult mouse brain primarily occurs within discrete niches, the subventricular zone (SVZ), and the subgranular zone (SGZ) of the dentate gyrus, supplying new neurons to the olfactory bulb and the dentate gyrus, respectively (1-3). Neural stem cells of these niches can be activated to divide and generate other stem cells, astrocytes, or new neurons (4, 5). Newborn neurons of the dentate gyrus have the capacity to integrate into the existing hippocampal circuitry (6-8), influencing processes such as learning and memory (9-11) as well as stress and depression (12).Radial glia-like (RGL) neural stem cells of the SVZ, which supply the olfactory bulb with newborn neurons and astrocytes, express astrocytic markers and form elegant pinwheel structures (13-16). RGL neural stem cells of the adult dentate gyrus also express astrocytic markers, but comprise a heterogeneous population based on the molecular markers they express, the morphologies they exhibit (17-22), and their fate (23-28). Nestin-GFP-positive RGL stem cells account for more than 70% of RGL stem cells in the SGZ of the dentate gyrus (24), but it was recently found that not all Nestin-GFP-positive cells with RGL morphology have stem cell properties (29): type β cells, which arborize in the granule cell layer (GCL) but do not reach the molecular layer (ML) of the dentate gyrus, account for 26% of Nestin-GFP-positive RGL stem cells. They express stem cell (Sox1, Sox2, Prominin 1, GFAP, and Nestin) and astrocytic [GFAP, glial glutamate tranporter 1 (GLT1), and S100β] markers but do not proliferate. In contrast, type α cells, which extend across the GCL and arborize in the inner ML, account for 74% of Nestin-GFP-positive RGL cells. They express stem...

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“…5A′). Next, we investigated the morphology of the secondary (or transgranular) radial glia scaffolding, which is required at postnatal stages for the GC subpial to granular transition (Brunne et al, 2010). By P7, radial glia fibres have reached the molecular layer, and their cell bodies (visualized by BLBP) accumulate along the inner GCL (Fig.…”

Section: Aberrant Glial Scaffolding Prevents Proper Gc Positioning Ofmentioning

confidence: 99%

COUP-TFI mitotically regulates production and migration of dentate granule cells and modulates hippocampal CXCR4 expression

et al. 2017

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Development of the dentate gyrus (DG), the primary gateway for hippocampal inputs, spans embryonic and postnatal stages, and involves complex morphogenetic events. We have previously identified the nuclear receptor COUP-TFI as a novel transcriptional regulator in the postnatal organization and function of the hippocampus. Here, we dissect its role in DG morphogenesis by inactivating it in either granule cell progenitors or granule neurons. Loss of COUP-TFI function in progenitors leads to decreased granule cell proliferative activity, precocious differentiation and increased apoptosis, resulting in a severe DG growth defect in adult mice. COUP-TFI-deficient cells express high levels of the chemokine receptor Cxcr4 and migrate abnormally, forming heterotopic clusters of differentiated granule cells along their paths. Conversely, high COUP-TFI expression levels downregulate Cxcr4 expression, whereas increased Cxcr4 expression in wild-type hippocampal cells affects cell migration. Finally, loss of COUP-TFI in postmitotic cells leads to only minor and transient abnormalities, and to normal Cxcr4 expression. Together, our results indicate that COUP-TFI is required predominantly in DG progenitors for modulating expression of the Cxcr4 receptor during granule cell neurogenesis and migration.

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Origin, maturation, and astroglial transformation of secondary radial glial cells in the developing dentate gyrus

Cited by 80 publications

References 64 publications

Foxg1Has an Essential Role in Postnatal Development of the Dentate Gyrus

Foxg1Has an Essential Role in Postnatal Development of the Dentate Gyrus

Fine processes of Nestin-GFP–positive radial glia-like stem cells in the adult dentate gyrus ensheathe local synapses and vasculature

COUP-TFI mitotically regulates production and migration of dentate granule cells and modulates hippocampal CXCR4 expression

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