Cited by 384Neurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene RegulationFetal and Pediatric Neurological Disorders

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Role of Intermediate Progenitor Cells in Cerebral Cortex Development

Pontious, Adria, Kowalczyk, Tom, Englund, Chris, Hevner, Robert F.·2008·Developmental Neuroscience

DOI 10.1159/000109848

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Abstract

Intermediate progenitor cells (IPCs) are a type of neurogenic transient amplifying cells in the developing cerebral cortex. IPCs divide symmetrically at basal (abventricular) positions in the neuroepithelium to produce pairs of new neurons or, in amplifying divisions, pairs of new IPCs. In contrast, radial unit progenitors (neuroepithelial cells and radial glia) divide at the apical (ventricular) surface and produce only single neurons or single IPCs by asymmetric division, or self-amplify by symmetric division. Histologically, IPCs are most prominent during the middle and late stages of neurogenesis, when they accumulate in the subventricular zone, a progenitor compartment linked to the genesis of upper neocortical layers (II–IV). Nevertheless, IPCs are present throughout cortical neurogenesis and produce neurons for all layers. In mice, changes in the abundance of IPCs caused by mutations of Pax6, Ngn2, Id4 and other genes are associated with parallel changes in cortical thickness but not surface area. In gyrencephalic brains, IPCs may play broader roles in determining not only laminar thickness, but also cortical surface area and gyral patterns. We propose that regulation of IPC genesis and amplification across developmental stages and regional subdivisions modulates laminar neurogenesis and contributes to the cytoarchitectonic differentiation of cortical areas.

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“Hevner and colleagues demonstrated that some intermediate progenitors contribute to all layers throughout all stages (early, middle, and late) of cortical neurogenesis in mice (Kowalczyk et al., 2009; Pontious et al., 2008).”
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“). Nestin is expressed in both neuroepithelial and radial glial cells but not basal progenitors”
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“…cortical development (Yokota et al., 2010; Figure 2). aRGCs have been extensively studied in the last decades and it is now clear that they contribute to neurogenesis mainly via the generation of a second type of neural progenitor cells: the BPs (Pontious et al., 2008; Kowalczyk et al., 2009).”
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The autism puzzle: Diffuse but not pervasive neuroanatomical abnormalities in children with ASD
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“, 2008); whereas SA is shaped by radial-unit progenitor cells, which divide in the periventricular area and dictate the number of radial units (Chenn and Walsh, 2002; Pontious et al., 2008).”
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Ets transcription factor Pointed promotes the generation of intermediate neural progenitors in Drosophila larval brains
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“…progenitors (INPs) in the VZ (INPvz, also known as short neural precursors, SNPs) and SVZ (INPsvz) (Gal et al., 2006; Corbin et al., 2008; Pontious et al., 2008; Kriegstein and Alvarez-Buylla, 2009; Fietz et al., 2010; Hansen et al., 2010; Stancik et al., 2010; Taverna and Huttner, 2010;…”
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“However, cortical thickness and surface area measurements represent distinct aspects of the cortical architecture and may represent different early neurodevelopmental pathologies (37, 127, 128).”
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Evolution and development of the mammalian cerebral cortex
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“However, other observations suggested that IPs produce the majority of glutamatergic neurons in all cortical layers [Haubensak et al., 2004; Pontious et al., 2008; Kowalczyk et al., 2009].”
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Distinguishing bipolar and major depressive disorders by brain structural morphometry: a pilot study
Fung, G., Deng, Y., Zhao, Q., Li, Z., Qu, M., Li, K., Zeng, Y., Jin, Z. H., Ma, Y., Yu, X., et al. (2015) · BMC Psychiatry · doi:10.1186/s12888-015-0685-5 · Cited by 93
“Surface area, on the other hand, has been associated with the proliferation of radial unit progenitors, which consist of neuroepithelial cells and radial glial cells [13], and functionally involve in the mechanisms of arborization, pruning within grey matter [14], and varying myelination at the grey/white matter inter…”
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MicroRNA-92b regulates the development of intermediate cortical progenitors in embryonic mouse brain
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“…(of age) is plausible given emerging evidence from recent findings that suggest that CT and SA may result from different phylogenetic processes (Pontious et al., 2008; Rakic, 1995), and their etiologymay involve different genetic mechanisms (Chen et al., 2011; Chouinard-Decorte et al., 2014;…”
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Neural stem cell regulation, fibroblast growth factors, and the developmental origins of neuropsychiatric disorders
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“The committed neuronal progenitors of the SVZ, referred to as intermediate progenitor cells (IPCs) express the transcription factor TBR2 and lack the self-renewal properties of true stem cells (Pontious et al., 2008).”
Background
Surface Vulnerability of Cerebral Cortex to Major Depressive Disorder
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“First, cortical thickness might be a sensitive measurement of neuronal density [12, 13], which has been used to assess mental disorders and related pathological changes [14, 15].”
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The protomap is propagated to cortical plate neurons through an Eomes -dependent intermediate map
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Structural abnormalities in cortical volume, thickness, and surface area in 22q11.2 microdeletion syndrome: Relationship with psychotic symptoms
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“…are also believed to arise from different progenitor cells, which create glial cells and neurons at distinct points in corticogenesis, resulting in SA ultimately reflecting the number of cortical columns and CT representing numbers of neurons within the columns (Pontious et al., 2008; Rakic, 1988).”
BackgroundInfluential
EFHC1 interacts with microtubules to regulate cell division and cortical development
de Nijs, L., Léon, C., Nguyen, L., LoTurco, J. J., Delgado‐Escueta, A. V., Grisar, T. M., & Lakaye, B. (2009) · Nature Neuroscience · doi:10.1038/nn.2390 · Cited by 84
“On the other hand, it is now well established that the developing neocortex contains both types of progenitors: radial progenitors dividing at the apical surface (ventricular zone) and basal progenitors dividing at a basal position (SVZ”
Neural Stem Cells to Cerebral Cortex: Emerging Mechanisms Regulating Progenitor Behavior and Productivity
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“The model was revised when cleavage angle failed to always predict daughter fate (Noctor et al., 2008), and mutations that cause irregular cleavage angles affect cortical thickness in some mutants (Postiglione et al., 2011), but not others (Konno et al., 2008).”
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Late Origin of Glia-Restricted Progenitors in the Developing Mouse Cerebral Cortex
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“…developmental period from progenitors located in the ventricular zone (VZ) and subventricular zone (SVZ) in both ventral and dorsal telencephalon (Götz and Huttner 2005; Miller and Gauthier 2007; Pontious et al. 2008), as well as from progenitors in the dorsal marginal zone (Costa et al. 2007).”
Background
RP58/ZNF238 directly modulates proneurogenic gene levels and is required for neuronal differentiation and brain expansion
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MiRNA-128 regulates the proliferation and neurogenesis of neural precursors by targeting PCM1 in the developing cortex
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“Nuclei were counterstained with DAPI, and mitotic cells were immunostained with PH3.”
MethodInfluential
Multiplex genetic fate mapping reveals a novel route of neocortical neurogenesis, which is altered in the Ts65Dn mouse model of down syndrome.
Tyler, W. A., & Haydar, T. F. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.5380-12.2013 · Cited by 81

Authors: Pontious, A., Kowalczyk, T., Englund, C., & Hevner, R. F.
Affiliations: University of Washington (US)
ORCID: Hevner, Robert F.
Venue: Developmental Neuroscience
Publisher: S. Karger AG
Published: 2007-12-13
Volume: 30
Issue: 1-3
Pages: 24-32
ISSN: 0378-5866 (ISSN-L)
1421-9859
DOI: 10.1159/000109848
OpenAlex: W2012470399
Cited by: 378
References: 73
Citations by year: 2026: 3 · 2025: 5 · 2024: 18 · 2023: 13 · 2022: 15 · 2021: 18 · 2020: 22 · 2019: 22 · 2018: 18 · 2017: 19 · 2016: 20 · 2015: 22 · 2014: 30 · 2013: 31 · 2012: 28
FWCI: 2.07
Type: journal article
Language: en
Open access: closed
Licence: www.karger.com/Services/SiteLicenses (vor)
www.karger.com/Services/SiteLicenses (tdm)
Locations: Developmental Neuroscience (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
Keywords: intermediate progenitor cells, cortical development, cortical neurogenesis, subventricular zone, radial glia, neuroepithelial cells, cortical lamination, cortical thickness, cortical surface area, Pax6, Ngn2, Id4, cytoarchitecture, gyrencephaly
MeSH terms: Animals, Cell Differentiation, Cerebral Cortex, Humans, Nerve Growth Factors, Nervous System Malformations, Neural Pathways, Neurons, Stem Cells, Signal Transduction, Gene Expression Regulation, Developmental, Mice

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Role of Intermediate Progenitor Cells in Cerebral Cortex Development

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