Cell Fate Specification and Symmetrical/Asymmetrical Divisions in the Developing Cerebral Cortex

Mione, Maria Caterina; Cavanagh, J.F.R.; Harris, Brett S.; Parnavelas, John G.

doi:10.1523/jneurosci.17-06-02018.1997

Cited by 128 publications

(85 citation statements)

References 62 publications

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“…The more recent use of a retroviral marker in combination with bromodeoxyuridine (BrdU) has shown that only pyramidal neurons maintain a close spatial relationship with their clonal relatives in the developing cortex, which can be achieved through radial migration (25). In contrast, labeled nonpyramidal cells were found, in agreement with earlier lineage analyses, as isolated cells or pairs of clonally neurons.…”

Section: Development Of Neuronal Lineagessupporting

confidence: 73%

The origin of cortical neurons

Parnavelas

2002

Braz J Med Biol Res

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Neurons of the mammalian cerebral cortex comprise two broad classes: pyramidal neurons, which project to distant targets, and the inhibitory nonpyramidal cells, the cortical interneurons. Pyramidal neurons are generated in the germinal ventricular zone, which lines the lateral ventricles, and migrate along the processes of radial glial cells to their positions in the developing cortex in an inside-out sequence. The GABA-containing nonpyramidal cells originate for the most part in the ganglionic eminence, the primordium of the basal ganglia in the ventral telencephalon. These cells follow tangential migratory routes to enter the cortex and are in close association with the corticofugal axonal system. Once they enter the cortex, they move towards the ventricular zone, possibly to obtain positional information, before they migrate radially in the direction of the pial surface to take up their positions in the developing cortex. The mechanisms that guide interneurons throughout these long and complex migratory routes are currently under investigation. Correspondence

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Section: Development Of Neuronal Lineagessupporting

confidence: 73%

The origin of cortical neurons

Parnavelas

2002

Braz J Med Biol Res

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“…In contrast, consistent with retroviral lineage tracing studies in vivo (5,(15)(16)(17)(18), analysis of the division patterns of isolated NE cells and their progeny has documented the coexistence, in vitro, of asymmetric and symmetric neurongenerating divisions of progenitors at the onset of neurogenesis (19)(20)(21). One possible explanation for this apparent discrepancy is the existence of neuronal progenitors other than the canonical NE cell dividing at the apical surface of the neuroepithelium.…”

mentioning

confidence: 76%

“…Retroviral lineage studies (5,15,16,18) and clonal analysis of isolated neuronal progenitors (19)(20)(21) have shown that neurons can be generated from both symmetric and asymmetric divisions. However, only asymmetric divisions have previously been reported from time-lapse analyses of neurongenerating divisions of NE͞radial glial cells occurring at the apical side of the VZ (7-9).…”

Section: Discussionmentioning

confidence: 99%

Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: A major site of neurogenesis

Haubensak

Attardo

Denk

et al. 2004

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

894

1,006

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Neurons of the mammalian CNS are thought to originate from progenitors dividing at the apical surface of the neuroepithelium. Here we use mouse embryos expressing GFP from the Tis21 locus, a gene expressed throughout the neural tube in most, if not all, neuron-generating progenitors, to specifically reveal the cell divisions that produce CNS neurons. In addition to the apical, asymmetric divisions of neuroepithelial (NE) cells that generate another NE cell and a neuron, we find, from the onset of neurogenesis, a second population of progenitors that divide in the basal region of the neuroepithelium and generate two neurons. Basal progenitors are most frequent in the telencephalon, where they outnumber the apically dividing neuron-generating NE cells. Our observations reconcile previous data on the origin and lineage of CNS neurons and show that basal, rather than apical, progenitors are the major source of the neurons of the mammalian neocortex.A ll neurons generated during the development of the mammalian CNS derive from neuroepithelial (NE) cells (see Supporting Text, which is published as supporting information on the PNAS web site). NE cells undergo three principal kinds of cell division, (i) symmetric, proliferative divisions (two NE cells) (see Supporting Text for terminology), (ii) asymmetric divisions (one NE cell, one neuron) and (iii) symmetric, differentiating divisions (two neurons) (1-6). It remains to be settled whether, at the very onset of neurogenesis, NE cells switch only to asymmetric division, or to both asymmetric and symmetric differentiating divisions.Real-time imaging studies of cells dividing at the apical surface of the neuroepithelium (7-9) and analyses of intrinsic cell fate determinants with a polarized distribution in mitotic NE cells (7, 10, 11) have provided evidence in support of the widely held view that during early neurogenesis, neurons are generated from NE cells by asymmetric rather than symmetric differentiating divisions (2,6,(12)(13)(14). In contrast, consistent with retroviral lineage tracing studies in vivo (5,(15)(16)(17)(18), analysis of the division patterns of isolated NE cells and their progeny has documented the coexistence, in vitro, of asymmetric and symmetric neurongenerating divisions of progenitors at the onset of neurogenesis (19-21). One possible explanation for this apparent discrepancy is the existence of neuronal progenitors other than the canonical NE cell dividing at the apical surface of the neuroepithelium.One of the problems in studying the divisions of NE cells that generate neurons has been the lack of a marker that allows one to distinguish between proliferating and neuron-generating NE cells and to identify the latter before they enter mitosis. Our group previously reported the first such marker, Tis21, an antiproliferative gene that within the neural tube is selectively expressed in neuron-generating, but not proliferating, NE cells, nor in neurons (22). Moreover, given that Ͼ95% of the newborn CNS neurons appear to inherit TIS21 protein from t...

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“…Notably, early-born, deep-layer neurons are thought to be primarily derived from asymmetric neurogenic divisions of radial glial cells in the VZ, which are multipotent progenitors throughout the CNS (Heins et al, 2002;Malatesta et al, 2003). In contrast, later-born, upperlayer neurons are thought to be derived from the SVZ, a model that is currently supported by lineage tracing (Goldman, 1995), gene expression analyses (Ishii et al, 2000;Tarabykin et al, 2001) and the preferential occurrence of symmetrical neurogenic cell divisions in the SVZ (Haubensak et al, 2004;Kornack and Rakic, 1995;Mione et al, 1997;Miyata et al, 2004;Noctor et al, 2002Noctor et al, , 2004. Notably, in utero electroporation selectively targets apical VZ progenitors, while previous BrdU birthdating experiments identified the time of neuronal birth in each layer by labeling both VZ and SVZ progenitors.…”

Section: The Position Of Cells Electroporated and Birthdated At E155mentioning

confidence: 99%

Validating in utero electroporation for the rapid analysis of gene regulatory elements in the murine telencephalon

Langevin

Mattar

Scardigli

et al. 2007

Developmental Dynamics

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With the ultimate goal of understanding how genetic modules have evolved in the telencephalon, we set out to modernize the functional analysis of cross-species cis-regulatory elements in mouse. In utero electroporation is rapidly replacing transgenesis as the method of choice for gain-and loss-of-function studies in the murine telencephalon, but the application of this technique to the analysis of transcriptional regulation has yet to be fully explored and exploited. To empirically define the developmental stages required to target specific populations of neurons in the dorsal telencephalon, or pallium, which gives rise to the neocortex in mouse, we performed a temporal and spatial analysis of the migratory properties of electroporated versus birth-dated cells. Next, we compared the activities of two known Ngn2 enhancers via transgenesis and in utero electroporation, demonstrating that the latter technique more faithfully reports the endogenous telencephalic expression pattern observed in an Ngn2lacZ knock-in line. Finally, we used this approach to test the telencephalic activities of a series of deletion constructs comprised of the zebrafish ER81 upstream regulatory region, allowing us to identify a previously uncharacterized enhancer that displays cross-species activity in the murine piriform cortex and lateral neocortex, yet not in more medial domains of the forebrain. Taken together, our data supports the contention that in utero technology can be exploited to rapidly examine the architecture and evolution of pallial-specific cis-regulatory elements.

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Cell Fate Specification and Symmetrical/Asymmetrical Divisions in the Developing Cerebral Cortex

Cited by 128 publications

References 62 publications

The origin of cortical neurons

The origin of cortical neurons

Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: A major site of neurogenesis

Validating in utero electroporation for the rapid analysis of gene regulatory elements in the murine telencephalon

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