Radial glial cells: defined and major intermediates between embryonic stem cells and CNS neurons

doi:10.1016/J.NEURON.2005.04.012

Home
/
Papers
/
Radial glial cells: defined and major intermediates between embryonic stem cells and CNS neurons

Journal Article•DOI•

Radial glial cells: defined and major intermediates between embryonic stem cells and CNS neurons

Magdalena Götz, Yves-Alain Barde¹•Institutions (1)

University of Basel¹

05 May 2005-Neuron (Elsevier)-Vol. 46, Iss: 3, pp 369-372

TL;DR: Evidence for the distinct "glial" nature of radial glial cells is reviewed and progenitors with clear glial antigenic characteristics act as cellular intermediates are contrasted with the neuroepithelial cells.

read less

About: This article is published in Neuron.The article was published on 2005-05-05 and is currently open access. It has received 333 citations till now. The article focuses on the topics: Neuroepithelial cell & Neurogenesis.

...read moreread less

Citations

PDF

Open Access

More filters

Journal Article•DOI•

The origin and development of glial cells in peripheral nerves

[...]

Kristjan R. Jessen¹, Rhona Mirsky¹•Institutions (1)

University College London¹

01 Sep 2005-Nature Reviews Neuroscience

TL;DR: Embryonic nerves offer a particular opportunity to analyse the early steps of gliogenesis from transient multipotent stem cells, and to understand how this process is integrated with organogenesis of peripheral nerves.

...read moreread less

Abstract: During the development of peripheral nerves, neural crest cells generate myelinating and non-myelinating glial cells in a process that parallels gliogenesis from the germinal layers of the CNS. Unlike central gliogenesis, neural crest development involves a protracted embryonic phase devoted to the generation of, first, the Schwann cell precursor and then the immature Schwann cell, a cell whose fate as a myelinating or non-myelinating cell has yet to be determined. Embryonic nerves therefore offer a particular opportunity to analyse the early steps of gliogenesis from transient multipotent stem cells, and to understand how this process is integrated with organogenesis of peripheral nerves.

...read moreread less

1,216 citations

Journal Article•DOI•

Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors

[...]

Fabio Mohn¹, Michael Weber¹, Michael Rebhan¹, Tim Roloff¹, Jens Richter², Michael B. Stadler¹, Miriam Bibel², Dirk Schübeler¹ - Show less +4 more•Institutions (2)

Friedrich Miescher Institute for Biomedical Research¹, Novartis²

20 Jun 2008-Molecular Cell

TL;DR: A model how de novo DNA methylation and dynamic switches in Polycomb targets restrict pluripotency and define the developmental potential of progenitor cells is suggested.

...read moreread less

901 citations

Cites background from "Radial glial cells: defined and maj..."

...In CNS neurogenesis, for example, radial glial cells have been identified as progenitors that can differentiate into diverse neuronal subtypes (Goldman, 2003; Gotz and Barde, 2005)....
[...]

Journal Article•DOI•

Development of the human cerebral cortex: Boulder Committee revisited

[...]

Irina Bystron¹, Colin Blakemore¹, Pasko Rakic²•Institutions (2)

University of Oxford¹, Yale University²

01 Feb 2008-Nature Reviews Neuroscience

TL;DR: Current data on the development of the human cerebral cortex is reviewed and the classical model of how the structure that makes us human is formed is updated.

...read moreread less

Abstract: In 1970 the Boulder Committee described the basic principles of the development of the CNS, derived from observations on the human embryonic cerebrum Since then, numerous studies have significantly advanced our knowledge of the timing, sequence and complexity of developmental events, and revealed important inter-species differences We review current data on the development of the human cerebral cortex and update the classical model of how the structure that makes us human is formed

...read moreread less

828 citations

Journal Article•DOI•

Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage

[...]

Yechiel Elkabetz¹, Georgia Panagiotakos, George Al Shamy, Nicholas D. Socci, Viviane Tabar, Lorenz Studer - Show less +2 more•Institutions (1)

Kettering University¹

15 Jan 2008-Genes & Development

TL;DR: It is proposed that R-NSCs represent the first characterized NSC stage capable of responding to patterning cues that direct differentiation toward region-specific neuronal fates, and offer new tools for harnessing the differentiation potential of human ESCs.

...read moreread less

Abstract: Neural stem cells (NSCs) yield both neuronal and glial progeny, but their differentiation potential toward multiple region-specific neuron types remains remarkably poor. In contrast, embryonic stem cell (ESC) progeny readily yield region-specific neuronal fates in response to appropriate developmental signals. Here we demonstrate prospective and clonal isolation of neural rosette cells (termed R-NSCs), a novel NSC type with broad differentiation potential toward CNS and PNS fates and capable of in vivo engraftment. R-NSCs can be derived from human and mouse ESCs or from neural plate stage embryos. While R-NSCs express markers classically associated with NSC fate, we identified a set of genes that specifically mark the R-NSC state. Maintenance of R-NSCs is promoted by activation of SHH and Notch pathways. In the absence of these signals, R-NSCs rapidly lose rosette organization and progress to a more restricted NSC stage. We propose that R-NSCs represent the first characterized NSC stage capable of responding to patterning cues that direct differentiation toward region-specific neuronal fates. In addition, the R-NSC-specific genetic markers presented here offer new tools for harnessing the differentiation potential of human ESCs.

...read moreread less

692 citations

Cites background from "Radial glial cells: defined and maj..."

...In early development, neural precursors transit from nestin single-layer neurepithelial cells into FABP7 radial glial cells that progress to a S100B stage and eventually give rise to GFAP-expressing adult NSCs (Gotz and Barde 2005)....
[...]
...In early development, neural precursors transit from nestin+ single-layer neurepithelial cells into FABP7+ radial glial cells that progress to a S100B+ stage and eventually give rise to GFAP-expressing adult NSCs (Gotz and Barde 2005)....
[...]

Journal Article•DOI•

Late-Stage Neuronal Progenitors in the Retina Are Radial Müller Glia That Function as Retinal Stem Cells

[...]

Rebecca Bernardos¹, Linda K. Barthel¹, Jason R. Meyers¹, Pamela A. Raymond•Institutions (1)

University of Michigan¹

27 Jun 2007-The Journal of Neuroscience

TL;DR: It is concluded that zebrafish Müller glia function as multipotent retinal stem cells that generate retinal neurons by homeostatic and regenerative developmental mechanisms.

...read moreread less

Abstract: Neuronal progenitors in the mammalian brain derive from radial glia or specialized astrocytes. In developing neural retina, radial glia-like Muller cells are generated late in neurogenesis and are not considered to be neuronal progenitors, but they do proliferate after injury and can express neuronal markers, suggesting a latent neurogenic capacity. To examine the neurogenic capacity of retinal glial cells, we used lineage tracing in transgenic zebrafish with a glial-specific promoter (gfap, for glial fibrillary acid protein) driving green fluorescent protein in differentiated Muller glia. We found that all Muller glia in the zebrafish retina express low levels of the multipotent progenitor marker Pax6 (paired box gene 6), and they proliferate at a low frequency in the intact, uninjured retina. Muller glia-derived progenitors express Crx (cone rod homeobox) and are late retinal progenitors that generate the rod photoreceptor lineage in the postembryonic retina. These Muller glia-derived progenitors also remain competent to produce earlier neuronal lineages, in that they respond to loss of cone photoreceptors by specifically regenerating the missing neurons. We conclude that zebrafish Muller glia function as multipotent retinal stem cells that generate retinal neurons by homeostatic and regenerative developmental mechanisms.

...read moreread less

577 citations

1
2
3
4
…
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67

Collapse

References

PDF

Open Access

More filters

Journal Article•DOI•

Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases

[...]

Stephen C. Noctor¹, Verónica Martínez-Cerdeño¹, Lidija Ivic¹, Arnold R. Kriegstein¹•Institutions (1)

Columbia University¹

01 Feb 2004-Nature Neuroscience

TL;DR: It is shown here that neurons are generated in two proliferative zones by distinct patterns of division, and newborn neurons do not migrate directly to the cortex; instead, most exhibit four distinct phases of migration, including a phase of retrograde movement toward the ventricle before migration to the cortical plate.

...read moreread less

Abstract: Precise patterns of cell division and migration are crucial to transform the neuroepithelium of the embryonic forebrain into the adult cerebral cortex. Using time-lapse imaging of clonal cells in rat cortex over several generations, we show here that neurons are generated in two proliferative zones by distinct patterns of division. Neurons arise directly from radial glial cells in the ventricular zone (VZ) and indirectly from intermediate progenitor cells in the subventricular zone (SVZ). Furthermore, newborn neurons do not migrate directly to the cortex; instead, most exhibit four distinct phases of migration, including a phase of retrograde movement toward the ventricle before migration to the cortical plate. These findings provide a comprehensive and new view of the dynamics of cortical neurogenesis and migration.

...read moreread less

2,062 citations

"Radial glial cells: defined and maj..." refers background or result in this paper

...…results are further consistent with observations using time-lapse video microscopy, indicating that cortical radial glial cells generate postmitotic neurons directly (Noctor et al., 2004), while radial glial cells in the ventral telencephalon rarely do so (A. Kriegstein, personal communication)....
[...]
...…neurons are generated from neuroepithelial cells s as well as from the earliest basal progenitors (Hauben- v sak et al., 2004; Miyata et al., 2004; Noctor et al., 2004). a The latter are defined by the absence of ventricular i (apical) contact and their cell division at significant dis- t tances…...
[...]
...The radial glia is then prepsent until the end of neurogenesis and neuronal migrartion, when their remainder transforms into astrocytes t(Noctor et al., 2004; for review, see Mori et al., 2005)....
[...]

Journal Article•DOI•

Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture.

[...]

Qi-Long Ying¹, Marios P. Stavridis¹, Dean Griffiths¹, Meng Li¹, Austin Smith¹ - Show less +1 more•Institutions (1)

University of Edinburgh¹

13 Jan 2003-Nature Biotechnology

TL;DR: It is reported that neither multicellular aggregation nor coculture is necessary for ES cells to commit efficiently to a neural fate and this system provides a platform for defining the molecular machinery of neural commitment and optimizing the efficiency of neuronal and glial cell production from pluripotent mammalian stem cells.

...read moreread less

Abstract: Mouse embryonic stem (ES) cells are competent for production of all fetal and adult cell types. However, the utility of ES cells as a developmental model or as a source of defined cell populations for pharmaceutical screening or transplantation is compromised because their differentiation in vitro is poorly controlled. Specification of primary lineages is not understood and consequently differentiation protocols are empirical, yielding variable and heterogeneous outcomes. Here we report that neither multicellular aggregation nor coculture is necessary for ES cells to commit efficiently to a neural fate. In adherent monoculture, elimination of inductive signals for alternative fates is sufficient for ES cells to develop into neural precursors. This process is not a simple default pathway, however, but requires autocrine fibroblast growth factor (FGF). Using flow cytometry quantitation and recording of individual colonies, we establish that the bulk of ES cells undergo neural conversion. The neural precursors can be purified to homogeneity by fluorescence activated cell sorting (FACS) or drug selection. This system provides a platform for defining the molecular machinery of neural commitment and optimizing the efficiency of neuronal and glial cell production from pluripotent mammalian stem cells.

...read moreread less

1,535 citations

"Radial glial cells: defined and maj..." refers background in this paper

...…the observation that an ES cell differentiation protocol that differs in major aspects (e.g., no retinoic acid treatment, monolayer differentiation; Ying et al., 2003) from that described by Bibel et al. also leads to the generation of Pax6-positive radial glial cells (S. Pollard and A. Smith,…...
[...]

Journal Article•DOI•

Pax6, Tbr2, and Tbr1 Are Expressed Sequentially by Radial Glia, Intermediate Progenitor Cells, and Postmitotic Neurons in Developing Neocortex

[...]

Chris Englund¹, Andy Fink¹, Charmaine Lau¹, Diane Pham¹, Ray A. M. Daza¹, Alessandro Bulfone², Tom Kowalczyk¹, Robert F. Hevner¹ - Show less +4 more•Institutions (2)

University of Washington¹, Vita-Salute San Raffaele University²

05 Jan 2005-The Journal of Neuroscience

TL;DR: It is shown that the transition from radial glia to intermediate progenitor cell is associated with upregulation of Tbr2, a T-domain transcription factor, and downregulation of Pax6, a homeodomain transcription factor.

...read moreread less

Abstract: The developing neocortex contains two types of progenitor cells for glutamatergic, pyramidal-projection neurons. The first type, radial glia, produce neurons and glia, divide at the ventricular surface, and express Pax6, a homeodomain transcription factor. The second type, intermediate progenitor cells, are derived from radial glia, produce only neurons, and divide away from the ventricular surface. Here we show that the transition from radial glia to intermediate progenitor cell is associated with upregulation of Tbr2, a T-domain transcription factor, and downregulation of Pax6. Accordingly, Tbr2 expression in progenitor compartments (the subventricular zone and ventricular zone) rises and falls with cortical plate neurogenesis. The subsequent transition from intermediate progenitor cell to postmitotic neuron is marked by downregulation of Tbr2 and upregulation of Tbr1, another T-domain transcription factor. These findings delineate the transcription factor sequence Pax6 --> Tbr2 --> Tbr1 in the differentiation of radial glia --> intermediate progenitor cell --> postmitotic projection neuron. This transcription factor sequence is modified in preplate neurons, in which Tbr2 is transiently coexpressed with Tbr1, and in the direct differentiation pathway from radial glia --> postmitotic projection neuron, in which Tbr2 is expressed briefly or not at all.

...read moreread less

1,197 citations

"Radial glial cells: defined and maj..." refers background in this paper

...Before the appearance of radial glial g cells, neurons are generated from neuroepithelial cells s as well as from the earliest basal progenitors (Hauben- v sak et al., 2004; Miyata et al., 2004; Noctor et al., 2004). a The latter are defined by the absence of ventricular i (apical) contact and their cell division at significant dis- t tances from the ventricle at further basal positions. n Basal progenitors are molecularly distinct from the api- b cal-located neuroepithelial and radial glial cells, e.g., by m the expression of Tbr2 (Englund et al., 2005) and Ngn2 H (Miyata et al., 2004) and the lack of GLAST or Pax6 t (Malatesta et al., 2003; Haubst et al., 2004)....
[...]
...…basal positions. n Basal progenitors are molecularly distinct from the api- b cal-located neuroepithelial and radial glial cells, e.g., by m the expression of Tbr2 (Englund et al., 2005) and Ngn2 H (Miyata et al., 2004) and the lack of GLAST or Pax6 t (Malatesta et al., 2003; Haubst et al., 2004)....
[...]

Journal Article•DOI•

Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage.

[...]

Paolo Malatesta¹, Eva Hartfuss¹, Magdalena Götz¹•Institutions (1)

Max Planck Society¹

15 Dec 2000-Development

TL;DR: Using fluorescence-activated cell sorting, it is shown that radial glial cells also are neuronal precursors and only later, after neurogenesis, do they shift towards an exclusive generation of astrocytes.

...read moreread less

Abstract: The developing central nervous system of vertebrates contains an abundant cell type designated radial glial cells. These cells are known as guiding cables for migrating neurons, while their role as precursor cells is less clear. Since radial glial cells express a variety of astroglial characteristics and differentiate as astrocytes after completing their guidance function, they have been considered as part of the glial lineage. Using fluorescence-activated cell sorting, we show here that radial glial cells also are neuronal precursors and only later, after neurogenesis, do they shift towards an exclusive generation of astrocytes. These results thus demonstrate a novel function for radial glial cells, namely their ability to generate two major cell types found in the nervous system, neurons and astrocytes.

...read moreread less

1,123 citations

"Radial glial cells: defined and maj..." refers background in this paper

...…the recombinase Cre under the control of the human GFAP promoter (that drives Cre in the GLAST-immunopositive radial glial cells at E13/E14, i.e., the fully differentiated radial glia stage; Malatesta et al., 2000; Malatesta et al., 2003) differ in the dorsal and the ventral telencephalon....
[...]
...…radial glial cells isolated at midneurogenesis from the ventral telencephalon (using mice expressing GFP under the human GFAP promoter) hardly generate any neurons, in marked contrast with radial glial cells from the dorsal telencephalon (Malatesta et al., 2003; see also Malatesta et al., 2000)....
[...]

Journal Article•DOI•

A unified hypothesis on the lineage of neural stem cells.

[...]

Arturo Alvarez-Buylla, José Manuel García-Verdugo, Anthony D. Tramontin

01 Apr 2001-Nature Reviews Neuroscience

TL;DR: It is proposed that the stem cells in the central nervous system are contained within the neuroepithelial → radial glia → astrocyte lineage.

...read moreread less

Abstract: For many years, it was assumed that neurons and glia in the central nervous system were produced from two distinct precursor pools that diverged early during embryonic development This theory was partially based on the idea that neurogenesis and gliogenesis occurred during different periods of development, and that neurogenesis ceased perinatally However, there is now abundant evidence that neural stem cells persist in the adult brain and support ongoing neurogenesis in restricted regions of the central nervous system Surprisingly, these stem cells have the characteristics of fully differentiated glia Neuroepithelial stem cells in the embryonic neural tube do not show glial characteristics, raising questions about the putative lineage from embryonic to adult stem cells In the developing brain, radial glia have long been known to produce cortical astrocytes, but recent data indicate that radial glia might also divide asymmetrically to produce cortical neurons Here we review these new developments and propose that the stem cells in the central nervous system are contained within the neuroepithelial → radial glia → astrocyte lineage

...read moreread less

1,003 citations

"Radial glial cells: defined and maj..." refers background in this paper

...Importantly, the so-called type B cells, which are astrocytes acting as neural stem cells in the adult subependymal zone, also express the same set of molecules (GLAST, S100β, GS, GFAP, vimentin, TN-C; Alvarez-Buylla et al., 2001; Mori et al., 2005)....
[...]