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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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Namba, T., & Huttner, W. Β. (2024) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-112122-032521 · Cited by 27
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“…evolutionary process of expansion of the embryonic NSC pool through diversification has not been cell-autonomous, with the embryonic microenvironment (the extracellular matrix, for example) playing a crucial role (Garcion et al., 2004; Loulier et al., 2009; Fietz et al., 2012; Pollen et al., 2015).”
BackgroundNovel gene function and regulation in neocortex expansion
Heide, M., Long, K. R., & Huttner, W. Β. (2017) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2017.11.008 · Cited by 25
Self-citationAltered extracellular matrix structure and elevated stiffness in a brain organoid model for disease
Zur, M. K., Bhattacharya, B., Solomonov, I., Dror, S. B., Savidor, A., Levin, Y., Prior, A., Sapir, T., Harris, T., Olender, T., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-59252-w · Cited by 23
“ECM has been proposed to be a crucial element in the structural organization of the developing brain and the formation of human brain folds 22,23 .”
Hess, J., Quinn, T. P., Akbarian, S., & Glatt, S. J. (2014) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32284 · Cited by 21
“Standard measures of RNA integrity (i.e., RIN, RQI) were reported in these studies; all samples were indicated as having high quality for RNA-seq (RQI 6.0 [Wu et al., 2012], RIN> 8.5 [Fietz et al., 2012]).”
InfluentialSecondary loss of miR-3607 reduced cortical progenitor amplification during rodent evolution
Chinnappa, K., Cárdenas, A., Prieto‐Colomina, A., Villalba, A., Márquez-Galera, Á., Soler, R., Nomura, Y., Llorens, E., Tomasello, U., López‐Atalaya, J. P., et al. (2022) · Science Advances · doi:10.1126/sciadv.abj4010 · Cited by 22
“…have identified significant differences in expression levels of highly conserved genes: (i) between mouse and macaque or human embryos ( 20 , 22 ), (ii) between aRGCs that self-amplify and those that self-consume to form bRGCs ( 23 ), and (iii) related to the differential expansion of the…”
Molecular drivers of human cerebral cortical evolution
Suzuki, I. (2019) · Neuroscience Research · doi:10.1016/j.neures.2019.05.007 · Cited by 22
Phf21b imprints the spatiotemporal epigenetic switch essential for neural stem cell differentiationPreprint
Basu, A., Mestres, I., Sahu, S. K., Tiwari, N., Khongwir, B., Baumgart, J., Singh, A. P., Calegari, F., & Tiwari, V. K. (2020) · Genes & Development · doi:10.1101/gad.333906.119 · Cited by 24
“By taking advantage of previous transcriptome studies of the developing cortex (Fietz et al. 2012; Aprea et al. 2013), we found that Phf21b was expressed at higher levels in the basal radial glial cells (bRG) as compared with the apical radial glial cells (aRG) and maintained at high levels in…”
Shi, L., Hu, E., Wang, Z., Liu, J., Li, J., Li, M., Chen, H., Yu, C., Jiang, T., & Su, B. (2017) · Human Genetics · doi:10.1007/s00439-016-1748-5 · Cited by 20
Iwashita, M., Nomura, T., Suetsugu, T., Matsuzaki, F., Kojima, S., & Kosodo, Y. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.574619 · Cited by 23
Cubillos, P., Ditzer, N., Kolodziejczyk, A., Schwenk, G., Hoffmann, J., Schütze, T. M., Derihaci, R. P., Birdir, C., Köllner, J. E. M., Petzold, A., et al. (2024) · The EMBO Journal · doi:10.1038/s44318-024-00068-7 · Cited by 26
“…resulting in an inner and outer layer (ISVZ/OSVZ), which represents an additional proliferative niche away from the ventricle and the signals of the cerebrospinal fl uid (Fietz et al, 2012; Florio and Huttner, 2014; Lehtinen et al, 2011; Libe-Philippot and Vanderhaeghen, 2021; Pollen et al, 2015).”
Human-Specific Hypomethylation of CENPJ, a Key Brain Size Regulator
Shi, L., Lin, Q., & Su, B. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst231 · Cited by 21
Bouschet, T., Dubois, E., Reynès, C., Kota, S. K., Rialle, S., Maupetit‐Mehouas, S., Pezet, M. G., Digarcher, A. L., Nidelet, S., Demolombe, V., et al. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw102 · Cited by 22
“This confirms previous RNA-seq experiments on developing cortex (Fietz et al. 2012).”
ResultHuman-specific gene expansions contribute to brain evolution
(2025) · doi:10.1016/j.cell.2025.06.037 · Cited by 25
Postembryonic Fish Brain Proliferation Zones Exhibit Neuroepithelial-Type Gene Expression Profile
Dambroise, E., Simion, M., Bourquard, T., Bouffard, S., Rizzi, B., Jaszczyszyn, Y., Bourge, M., Affaticati, P., Heuzé, A., Jouralet, J., et al. (2017) · Stem Cells · doi:10.1002/stem.2588 · Cited by 20
Identification of characteristic genes distinguishing neural stem cells from astrocytes
Qin, S., Huang, X., Wang, D., Hu, X., Yuan, Y., Sun, X. Z., Tan, Z., Gu, Y., Cheng, X.-Y., He, C., et al. (2018) · Gene · doi:10.1016/j.gene.2018.09.044 · Cited by 19
Integrative Omics Reveals Rapidly Evolving Regulatory Sequences Driving Primate Brain Evolution
Zhuang, X.-L., Zhang, J., Shao, Y., Ye, Y., Chen, C., Zhou, L., Wang, Z., Luo, X., Su, B., Yao, Y., et al. (2023) · Molecular Biology and Evolution · doi:10.1093/molbev/msad173 · Cited by 22
“no Bmp7 expression in the fetal brain of mouse (Fietz et al. 2012; Florio et al. 2015) (fig.”
BackgroundInfluentialJohansson, M. M., Geystelen, A. V., Larmuseau, M., Djurovic, S., Andreassen, O. A., Agartz, I., & JAZIN, E. E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137223 · Cited by 19
Developing guinea pig brain as a model for cortical folding
Hatakeyama, J., Sato, H., & Shimamura, K. (2017) · Development Growth & Differentiation · doi:10.1111/dgd.12371 · Cited by 18
“These defects could be mediated through the basal progenitors, given that the meninges have been suggested to be required for their maintenance (Fietz et al. 2012; Stenzel et al. 2014).”
BackgroundMay, M., Denecke, B., Schroeder, T., Götz, M., & Faissner, A. (2018) · Biology Open · doi:10.1242/bio.027730 · Cited by 18
“In the human brain, the VZ, the inner SVZ and the outer SVZdisplayaspecific ECMcomposition,which mightmodulatethe proliferative capacity of human basal progenitors (Fietz et al., 2012).”
Human SERPINA3 induces neocortical folding and improves cognitive ability in mice
Zhao, J., Feng, C., Wang, W., Su, L., & Jiao, J. (2022) · Cell Discovery · doi:10.1038/s41421-022-00469-0 · Cited by 17
Teng, P., Li, Y., Ku, L., Wang, F., Goldsmith, D. R., Wen, Z., Yao, B., & Feng, Y. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.06.009 · Cited by 18
“…the recently published transcriptomic datasets that examined various germinal zones when NPCs migrate and differentiate during human fetal neocortex formation (Fietz et al., 2012), we found low levels of GOMAFU in the ventricular zone (VZ) enriched of proliferating apical progenitors (APs) (Fig.”
Bąk, M., van Nimwegen, E., Kouzel, I. U., Gür, T., Schmidt, R. L. J., Zavolan, M., & Gruber, A. J. (2024) · Nature Communications · doi:10.1038/s41467-024-48046-1 · Cited by 17
“To investigate this further from a splicing perspective, we used MAPP, comparing cells from the ventricular zone (VZ) to cells from the cortical plate (CP) 45 .”
MethodHuman organoids to model the developing human neocortex in health and disease
Khakipoor, S., Crouch, E. E., & Mayer, S. (2020) · Brain Research · doi:10.1016/j.brainres.2020.146803 · Cited by 17
Chowdhury, R., Wang, Y., Campbell, M., Goderie, S. K., Doyle, F., Tenenbaum, S. A., Kusek, G., Kiehl, T. R., Ansari, S. A., Boles, N. C., et al. (2021) · Development · doi:10.1242/dev.199376 · Cited by 17
Cai, Q., Feng, I., Costa, A. R., Pinto‐Costa, R., Partlow, J. N., Caluseriu, O., Li, D., Ganetzky, R. D., Brasch‐Andersen, C., Fagerberg, C. R., et al. (2021) · Genetics in Medicine · doi:10.1016/j.gim.2021.09.014 · Cited by 20
Comparative genomics of brain size evolution
Enard, W. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00345 · Cited by 16
“…did find evidence for positive selection across some primate lineages for several genes (reviewed in Gilbert et al., 2005), the correlation with changes in brain size was usually not explicitly tested, impeding the interpretation of these findings (Woods et al., 2005; Montgomery et al., 2014).”
Self-citationKullmann, J. A., Meyer, S., Pipicelli, F., Kyrousi, C., Schneider, F., Bartels, N., Cappello, S., & Rust, M. B. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz321 · Cited by 16
Exploring the Complexity of Cortical Development Using Single-Cell Transcriptomics
Jeong, H., & Tiwari, V. K. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00031 · Cited by 16
“For example, Camp et al. performed unsupervised clustering of 226 single-cells from human embryonic neocortex, and examined the characteristics of each clusters (Camp et al., 2015) using the correlation with existing bulk-cell RNA-seq profiled from cortical layers (VZ, ISVZ, OSVZ, and CP; Fietz et al., 2012) and FAC-s…”
BackgroundMethodIndirect neurogenesis in space and time
Thor, S. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00833-x · Cited by 17
“ARHGAP11B encodes Rho guanosine triphosphatase-activating protein 11B and is expressed in RGCs and oRG in the embryonic human neocortex 221,222,241 .”
Liu, Y., Luo, X., Sun, Y., Chen, K., Hu, T., You, B., Xu, J., Zhang, F., Cheng, Q., Meng, X., et al. (2024) · Developmental Cell · doi:10.1016/j.devcel.2024.10.005 · Cited by 18
Ahmed, M., Marziali, L. N., Arenas, E., Feltri, M. L., & ffrench‐Constant, C. (2019) · Development · doi:10.1242/dev.172668 · Cited by 16
“Previous studies examining laminin expression in the brain describe the murine neocortex as being rich in lm-α2 and lm-α4, with expression greatest at the ventricular surface (Fietz et al., 2012; Lathia et al., 2007).”
BackgroundAprea, J., Lesche, M., Massalini, S., Prenninger, S., Alexopoulou, D., Dahl, A., Hiller, M., & Calegari, F. (2015) · Neurogenesis · doi:10.1080/23262133.2014.995524 · Cited by 13
Brain Organization and Human Diseases
Sapir, T., Sela‐Donenfeld, D., Zur, M. K., & Reiner, O. (2022) · Cells · doi:10.3390/cells11101642 · Cited by 15
Zychowicz, M., Méhn, D., Ruiz, A., Frontczak‐Baniewicz, M., Rossi, F., & Bużańska, L. (2012) · Acta Neurobiologiae Experimentalis · doi:10.55782/ane-2012-1905 · Cited by 15
“It refers to natural niches of stem cells in vivo or artificial structures/systems mimicking natural environment of stem cell niche in vitro (Taverna et al. 2011, Fietz et al. 2012).”
Background
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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