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Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal
Open accessAbstract
The expansion of the neocortex during mammalian brain evolution results primarily from an increase in neural progenitor cell divisions in its two principal germinal zones during development, the ventricular zone (VZ) and the subventricular zone (SVZ). Using mRNA sequencing, we analyzed the transcriptomes of fetal human and embryonic mouse VZ, SVZ, and cortical plate. In mouse, the transcriptome of the SVZ was more similar to that of the cortical plate than that of the VZ, whereas in human the opposite was the case, with the inner and outer SVZ being highly related to each other despite their cytoarchitectonic differences. We describe sets of genes that are up- or down-regulated in each germinal zone. These data suggest that cell adhesion and cell–extracellular matrix interactions promote the proliferation and self-renewal of neural progenitors in the developing human neocortex. Notably, relevant extracellular matrix-associated genes include distinct sets of collagens, laminins, proteoglycans, and integrins, along with specific sets of growth factors and morphogens. Our data establish a basis for identifying novel cell-type markers and open up avenues to unravel the molecular basis of neocortex expansion during evolution.
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“These results are consistent with a previous study of laminar enrichment in 13–16pcw human prenatal cortex, which also found few genes specifically enriched in SZo (55) or SZi (61)2.”
From Transcriptional landscape of the prenatal human brain (2014) · cites this paper as [2]
In the citing paper
“Species differences in distinct fetal transient zones, including the SZ2, SP17,18, CP6, and SG9, have also been described.”
From Transcriptional landscape of the prenatal human brain (2014) · cites this paper as [2]
In the citing paper
“Several recent studies have assayed a limited set of brain structures1,3–5 and layers2 from prenatal human brain.”
From Transcriptional landscape of the prenatal human brain (2014) · cites this paper as [2]
In the citing paper
“Excitatory neurons, which constitute the majority of neocortical neurons, are derived from neocortical progenitors called radial glial (RG) cells in a germinal zone called the ventricular zone (VZ) (Ayoub et al., 2011; Fietz et al., 2012).”
From Genetic Changes Shaping the Human Brain (2015) · cites this paper as Fietz et al., 2012
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InfluentialBRN2 as a key gene drives the early primate telencephalon development
Zhu, X., Guo, Y., Chu, C., Liu, D., Duan, K., Yin, Y., Si, C., Kang, Y., Yao, J., Du, X., et al. (2022) · Science Advances · doi:10.1126/sciadv.abl7263 · Cited by 15
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“However, as the structure of the human SVZ is very different to the rodent one (Fietz et al., 2012; Lim and Alvarez-Buylla, 2016), the relevance of this finding to human remyelination is unclear.”
BackgroundNon-muscle myosins control radial glial basal endfeet to mediate interneuron organization
D’Arcy, B. R., Lennox, A. L., Musso, C. M., Bracher, A., Escobar-Tomlienovich, C. F., Perez-Sanchez, S., & Silver, D. L. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3001926 · Cited by 14
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BackgroundLi, M., Sun, H., Hou, Z., Hao, S., Jin, L., & Wang, B. (2023) · Small · doi:10.1002/smll.202306451 · Cited by 12
Toward a better understanding of how a gyrified brain develops
Barresi, M., Hickmott, R. A., Bosakhar, A., Quezada, S., Quigley, A. F., Kawasaki, H., Walker, D. W., & Tolcos, M. (2024) · Cerebral Cortex · doi:10.1093/cercor/bhae055 · Cited by 12
The Control of Cortical Folding: Multiple Mechanisms, Multiple Models
Moffat, A., & Schuurmans, C. J. (2023) · The Neuroscientist · doi:10.1177/10738584231190839 · Cited by 12
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InfluentialMultiscale engineering of brain organoids for disease modeling
Xu, C., Alameri, A., Leong, W., Johnson, E., Chen, Z., Xu, B., & Leong, K. W. (2024) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2024.115344 · Cited by 12
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Yuzhalin, A. E. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.09.010 · Cited by 11
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SMPD4 -mediated sphingolipid metabolism regulates brain and primary cilia development
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Molecular Lineages and Spatial Distributions of Subplate Neurons in the Human Fetal Cerebral Cortex
Guo, X., Lee, T., Sun, J., Sun, J., Cai, W., Yang, Q., & Sun, T. (2024) · Advanced Science · doi:10.1002/advs.202407137 · Cited by 10
Canonical and non-canonical PRC1 differentially contribute to regulation of neural stem cell fate
Hoffmann, J., Schütze, T. M., Kolodziejczyk, A., Küster, K., Kränkel, A., Reinhardt, S., Derihaci, R. P., Birdir, C., Wimberger, P., Koseki, H., et al. (2025) · Life Science Alliance · doi:10.26508/lsa.202403006 · Cited by 10
“To analyse the expression of canonical and non-canonical PRC1 components (Fig 1A) in the human developing neocortex (Fig 1B), we fi rst mined RNA-seq data of microdissected human foetal cortex (Fietz et al, 2012).”
Ditzer, N., Senoglu, E., Kolodziejczyk, A., Schütze, T. M., Nikolaidi, A., Küster, K., Sameith, K., Dietz, S., Derihaci, R. P., Birdir, C., et al. (2025) · Neuron · doi:10.1016/j.neuron.2025.06.016 · Cited by 13
Prominin-1 (CD133) and the Cell Biology of Neural Progenitors and Their Progeny
Sykes, A. M., & Huttner, W. Β. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-5894-4_6 · Cited by 10
Self-citationLoss of TAF8 causes TFIID dysfunction and p53-mediated apoptotic neuronal cell death
El-Saafin, F., Bergamasco, M., Chen, Y., May, R. E., Esakky, P., Hediyeh-zadeh, S., Dixon, M. P., Wilcox, S., Davis, M. J., Strasser, A., et al. (2022) · Cell Death and Differentiation · doi:10.1038/s41418-022-00982-5 · Cited by 10
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BackgroundMeng, X., Lin, Q., Zeng, X., Jiang, J., Li, M., Luo, X., Chen, K., Wu, H., Hu, Y., Liu, C., et al. (2023) · National Science Review · doi:10.1093/nsr/nwad281 · Cited by 11
“Given that previous studies have emphasized the significance of the ECM proteins in neural progenitor self-renewal [54 ], our findings highlight the primary role of the ECM in providing essential niches for neuron migration.”
ResultRadial glia progenitor polarity in health and disease
Viola, V., Chinnappa, K., & Francis, F. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1478283 · Cited by 10
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Human dorsal forebrain organoids show differentiation-state-specific protein secretion
Yentür, Z., Kagermeier, T., Sarieva, K., Jarboui, M. A., Becker, K., & Mayer, S. (2025) · iScience · doi:10.1016/j.isci.2025.112935 · Cited by 8
“6 This indicates the dynamic role of the ECM in different layers of the neocortex.”
Evaluation of Possible Consequences of Zika Virus Infection in the Developing Nervous System
Walter, L. T., Higa, G. S. V., Ikebara, J. M., Vedovello, D., Salvador, F. S., Takada, S. H., Kinjo, É. R., Whalley, B. J., Sperança, M. A., & Kihara, A. H. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0442-5 · Cited by 9
Prodromidou, K., & Matsas, R. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-04063-7 · Cited by 11
“Single-cell sequencing demonstrated the previously unappreciated diversity of transcriptional states within both human apical RG and oRG cells, which by contrast appears markedly simplified in mouse [65, 91].”
BackgroundPutative Cellular and Molecular Roles of Zika Virus in Fetal and Pediatric Neuropathologies
Gharbaran, R., & Somenarain, L. (2018) · Pediatric and Developmental Pathology · doi:10.1177/1093526618790742 · Cited by 8
The SVZ stem cell niche–components, functions, and in vitro modelling
Eşiyok, N., & Heide, M. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1332901 · Cited by 7
“The interactions between ECM and neural cells play essential roles during cortical development and neurogenesis (Fietz et al., 2012; Long and Huttner, 2022).”
BackgroundNeurodevelopmental Implications Underpinning Hereditary Spastic Paraplegia
Zhi, Y., Shi, Y., Lu, D., & Xu, D. (2025) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.70260 · Cited by 7
“To investigate the expression profile of HSP genes during cortical development, we used the published database GSE38805 [60] and GSE65000 [61] to monitor the transcriptome expression profiles of SPG4/SPAST and SPG11/KIAA1840, which are the primary causes of AD HSP and AR HSP, respectively, across…”
TSC tunes progenitor balance and upper-layer neuron generation in neocortex
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“To delineate the potential function of TSC genes ( TSC1 , TSC2 and TBC1D7 ) in cerebral cortical development, we analysed their developmental expression in human and mouse brains, particularly in the germinal zone (VZ and SVZ) and the cortical plate of the developing cerebral cortex 37,43–47 .”
Bertino, F., Mukherjee, D., Bonora, M., Bagowski, C. P., Nardelli, J., Metani, L., Venturini, D. I. Z., Chianese, D., Santander, N. G., Salaroglio, I. C., et al. (2024) · Cell Reports Medicine · doi:10.1016/j.xcrm.2024.101647 · Cited by 7
“In the fetal brain, a dataset from Fietz et al. 26 highlighted a peak of FLVCR1a expression in the ventricular zone (VZ) and outer subventricular zone that declined in the cortical plate (Figure S2D).”
Orchestrating human neocortex development across the scales; from micro to macro
Massimo, M., & Long, K. R. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.09.007 · Cited by 6
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BackgroundBeing a Neural Stem Cell: A Matter of Character But Defined by the Microenvironment
Andreopoulou, E., Arampatzis, A., Patsoni, M., & Kazanis, I. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-69194-7_6 · Cited by 7
The One-Stop Gyrification Station - Challenges and New Technologies
Hickmott, R. A., Bosakhar, A., Quezada, S., Barresi, M., Walker, D. W., Ryan, A. L., Quigley, A. F., & Tolcos, M. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.102111 · Cited by 7
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Adducins regulate morphology and fate of neural progenitors during neocortical neurogenesis
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Species-specific chromatin architecture and neurogenesis mediated by a human enhancer
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NeMO Analytics: a compendium of transcriptomic data for the exploration of neocortical development
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Examining the NEUROG2 lineage and associated gene expression in human cortical organoids
Vasan, L., Chinchalongporn, V., Saleh, F., Zinyk, D. L., Ke, C., Suresh, H., Ghazale, H., Belfiore, L., Touahri, Y., Oproescu, A.-M., et al. (2024) · Development · doi:10.1242/dev.202703 · Cited by 8
“…lineage is also observed in human bRG (Pollen et al., 2015), with expansion of the ECM in the oSVZ providing a pro-proliferative niche for basal NPCs (Amin and Borrell, 2020; Arai et al., 2011; Fietz et al., 2012; Florio et al., 2015; Martinez-Martinez et al., 2016; Pollen et al., 2015).”
InfluentialKalebic, N., Long, K. R., & Huttner, W. Β. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-804042-3.00136-6 · Cited by 6
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“In the human brain, NPCs have been postulated to contribute to basal deposition of ECM constituents via vesicular transport in their basal processes (Fietz et al., 2012), thereby polarizing their own niche environment.”
BackgroundMorphoregulatory ADD3 underlies glioblastoma growth and formation of tumor–tumor connections
Barelli, C., Don, F. K., Iannuzzi, R. M., Faletti, S., Bertani, I., Osei, I., Sorrentino, S., Villa, G., Sokolova, V., Campione, A., et al. (2024) · Life Science Alliance · doi:10.26508/lsa.202402823 · Cited by 5
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Shaping the Neocortex: Radial Glia and Astrocytes in Development and Evolution
Mosti, F., Kawasaki, H., Babbitt, C. C., Benedetto, B. D., Silver, D. L., Kalebic, N., & Falcone, C. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1301-25.2025 · Cited by 5
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“Previous studies have demonstrated that genes related to the extracellular matrix (ECM) and cell adhesion are enriched in the ventricular zone (hVZ) and subventricular zone (hSVZ) during the development of the human cortex 28 .”
Chou, F., Chen, C.-Y., Lee, A.-C., & Wang, P. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.821848 · Cited by 4
Three-dimensional models of human brain development
Tobon, A., Caporale, N., Trattaro, S., & Testa, G. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814085-7.00011-8 · Cited by 4
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Diversity and Evolution of Human Cortical Progenitor Cell Types
Pollen, A. A., & Kriegstein, A. R. (2023) · Wiley eBooks · doi:10.1002/9781119860914.ch2 · Cited by 5
KACZYNSKI, J., & Pasenkiewicz‐Gierula, M. (2025) · PLoS ONE · doi:10.1371/journal.pone.0326022 · Cited by 3
“1 is expressed in the cortical plate of human fetal neocortex [48].”
Gim, D. H., Assir, M. Z. K., Soper, O., Fowler, P., Morgan, M. D., Berg, D. A., & Kang, E. (2025) · Nature Communications · doi:10.1038/s41467-025-64381-3 · Cited by 4
“…the ECM transcriptome of the subventricular zone (SVZ) closely resembles that of the ventricular zone (VZ), suggesting a shared microenvironment that supports progenitor cell self-renewal, and includes distinct sets of collagens, laminins, proteoglycans, integrins, and speci fi c growth factors 27 .”
InfluentialJohnson, T. S., Abrams, Z. B., Zhang, Y., & Huang, K. (2016) · Pacific Symposium on Biocomputing (PSB) · doi:10.1142/9789813207813_0055 · Cited by 3
Downregulation of CDC25C in NPCs Disturbed Cortical Neurogenesis
Zhou, X., Lu, D., Yi, W., & Xu, D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24021505 · Cited by 3
“We focus on studying the role of CDC25C in the developing brain because: (i) Cdc25c is preferentially expressed in neural progenitors, including apical radial glial (aRG) and basal radial glial (bRG) of the fetal human neocortex [23,24]; (ii) tumor stem cells share a similar genetic mechanism with NPCs [25], and CDC25…”
BackgroundMethodLu, D., Zhi, Y., Su, H., Lin, X., Lin, J., Shi, Y., Yi, W., Hong, C., Zhang, T., Fu, Z., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113818 · Cited by 3
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An, B., Ando, A., Akuta, H., Morishita, F., & Imamura, T. (2023) · FEBS Letters · doi:10.1002/1873-3468.14756 · Cited by 2
“We also compared published RNA-seq data from human and mouse VZ and SVZ [34].”
ResultBueno, R. J., Fernández‐Zapata, C., Salla, M., Garcia, J. C., Alacam, A., Klein, O., Böttcher, C., Radbruch, H., Paul, F., Starossom, S. C., et al. (2025) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2025.1578467 · Cited by 2
Neocortical neurogenesis: a proneural gene perspective
Vasan, L., Moffat, A., Mattar, P. A., & Schuurmans, C. (2025) · FEBS Journal · doi:10.1111/febs.70158 · Cited by 3
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“…progenitor subtypes, such as the intermediate/basal progenitor (IP/BP) and the outer/basal radial glia (oRG/bRG) (Figure 1) (Betizeau et al., 2013; Fietz et al., 2010, 2012; Florio & Huttner, 2014; Gertz et al., 2014; Hansen et al., 2010; Huttner et al., 2013; Kalebic et al., 2019; Lui et al.,…”
BackgroundTeleost Fish and Organoids: Alternative Windows Into the Development of Healthy and Diseased Brains
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Development and Developmental Disorders of the Cerebral Cortex
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Development and pathology of the germinal matrix
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Proteoglycans, Neurogenesis and Stem Cell Differentiation
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“15 function, consistent with previous studies (32).”
BackgroundDitzer, N., Senoglu, E., Schütze, T. M., Nikolaidi, A., Kolodziejczyk, A., Sameith, K., Dietz, S., Derihaci, R. P., Birdir, C., Eugster, A., et al. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.5017114 · Cited by 2
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The Expansion of the Cortical Sheet in Primates
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Die Rolle humanspezifischer Gene in der Gehirnentwicklung und -evolution
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MIR3607 regulates cerebral cortex development via activation of Wnt/βCat signalingPreprint
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Metadata
- Authors
- Fietz, S. A., Lachmann, R., Brandl, H., Kircher, M., Samusik, N., Schröder, R., Lakshmanaperumal, N., Henry, I., Vogt, J., Riehn, A., Distler, W., Nitsch, R., Enard, W., Pääbo, S., & Huttner, W. B.
- Affiliations
- Max Planck Institute of Molecular Cell Biology and Genetics (DE)
- University Hospital Carl Gustav Carus (DE)
- Max Planck Institute for Evolutionary Anthropology (DE)
- Stiftung Charité (DE)
- Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany;
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-07-02
- Volume
- 109
- Issue
- 29
- Pages
- 11836-11841
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3406833
- OpenAlex
- W2038280158
- Cited by
- 337
- References
- 51
- Citations by year
- 2026: 15 · 2025: 20 · 2024: 28 · 2023: 27 · 2022: 21 · 2021: 33 · 2020: 31 · 2019: 30 · 2018: 20 · 2017: 24 · 2016: 26 · 2015: 23 · 2014: 20 · 2013: 16 · 2012: 3
- FWCI
- 6.67
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- 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
- neocortex development, neural progenitor cells, ventricular zone, subventricular zone, cortical plate, extracellular matrix, progenitor self-renewal, cell adhesion, transcriptome, human-mouse comparison, laminin, collagen, proteoglycans, integrins, growth factors, morphogens, neocortex expansion, brain evolution
- MeSH terms
- Analysis of Variance, Animals, Cell Adhesion, Biological Evolution, Fetus, Humans, Immunohistochemistry, RNA, Messenger, Stem Cells, Cluster Analysis, Polymerase Chain Reaction, Extracellular Matrix Proteins, Sequence Analysis, RNA, DNA Primers, Gene Expression Regulation, Developmental, Neocortex, Gene Expression Profiling, Principal Component Analysis, Mice, Transcriptome, Laser Capture Microdissection
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