The DOI matches its Crossref record; 51 of the 51 references it cites were found in a registry or an index.
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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
Citations
Cites
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.211 · Cited by 35,890
The Glial Nature of Embryonic and Adult Neural Stem Cells
Kriegstein, A., & Alvarez-Buylla, A. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135600 · Cited by 2,475
Noctor, S. C., Martínez-Cerdeño, V., Ivic, L., & Kriegstein, A. R. (2004) · Nature Neuroscience · doi:10.1038/nn1172 · Cited by 2,229
The cell biology of neurogenesis
Götz, M., & Huttner, W. B. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1739 · Cited by 2,130
Self-citationEvolution of the neocortex: a perspective from developmental biology
Rakic, P. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2719 · Cited by 1,565
Neurogenic radial glia in the outer subventricular zone of human neocortex
Hansen, D. V., Lui, J. H., Parker, P. R. L., & Kriegstein, A. R. (2010) · Nature · doi:10.1038/nature08845 · Cited by 1,388
Development and Evolution of the Human Neocortex
Lui, J. H., Hansen, D. V., & Kriegstein, A. R. (2011) · Cell · doi:10.1016/j.cell.2011.06.030 · Cited by 1,342
Englund, C., Fink, A., Lau, C., Pham, D., Daza, R. A. M., Bulfone, A., Kowalczyk, T., & Hevner, R. F. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2899-04.2005 · Cited by 1,261
Haubensak, W. E., Attardo, A., Denk, W. T., & Huttner, W. Β. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308600100 · Cited by 1,004
Self-citationOSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling
Fietz, S. A., Kelava, I., Vogt, J., Wilsch-Bräuninger, M., Stenzel, D., Fish, J. L., Corbeil, D., Riehn, A., Distler, W., Nitsch, R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2553 · Cited by 830
Self-citation
Cited by
Sorted by citations
Items 301–336 of 336
Investigating prenatal stress in a stem cell model of human neuronal development
Papst, L. (2019) · Elektronische Hochschulschriften der LMU München (Ludwig-Maximilians-Universität München) · doi:10.5282/edoc.25120
Brain organoids as a model system for human neurodevelopment in health and disease
Reiner, O., & Karzbrun, E. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814405-3.00010-2
Molecular mechanisms underlying malformations of cortical development
Oishi, S. (2020) · The University of Queensland · doi:10.14264/uql.2020.1023
de Wolf, B. (2020) · Utrecht University Repository (Utrecht University) · doi:10.33540/239
Bartlett, T. E. (2021) · BMC Bioinformatics · doi:10.1101/2021.05.18.444638 · Cited by 2
Proteoglycans of the Neural Stem Cell Niche
Roll, L., & Faissner, A. (2021) · Biology of extracellular matrix · doi:10.1007/978-3-030-73453-4_8
Sakib, M. S. (2021) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-8870 · Cited by 1
Muotri, A. R. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.726777864.793560529
Mira, H., Díez del Corral, R., & Morales, A. V. (2020) · Frontiers research topics · doi:10.3389/978-2-88963-988-5
Konopka, G. (2018) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.725998661.793545857
Post-transcriptional Gene Regulation During Cortical Development
Serdar, L. D., Musso, C. M., & Silver, D. L. (2022) · Springer eBooks · doi:10.1007/978-1-4614-6434-1_184-1
Mubuchi, A., Takechi, M., Nishio, S., Matsuda, T., Itoh, Y., Sato, C., Kitajima, K., Kitagawa, H., & Miyata, S. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.09.03.506497
“Basal/outer radial glial cells are characterized by the high gene expression of several ECM molecules, including TNC ( Fietz et al., 2012 ; Control (Con); Dunnett’s test.”
BackgroundWu, Q., Bilgic, M., & Matsuzaki, F. (2023) · Wiley eBooks · doi:10.1002/9781119860914.ch9
Mubuchi, A., Takechi, M., Nishio, S., Matsuda, T., Itoh, Y., Sato, C., Kitajima, K., Kitagawa, H., & Miyata, S. (2023) · eLife · doi:10.7554/elife.92342.1
Mubuchi, A., Takechi, M., Nishio, S., Matsuda, T., Itoh, Y., Sato, C., Kitajima, K., Kitagawa, H., & Miyata, S. (2024) · eLife · doi:10.7554/elife.92342.2
Extracellular matrix of the nervous system
Nazir, S., Feresten, A. H., Lin, L. D., Hutter, H., & Julian, L. M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-95730-4.00002-0
Liu, D., Talevi, V., Tavares, J. F., Wang, R., Imtiaz, M. A., Melas, K., Teumer, A., Wittfeld, K., Hillary, R. F., Vojinović, D., et al. (2024) · medRxiv · doi:10.1101/2024.12.20.24319418
Barresi, M., Johnstone, A. C., & Tolcos, M. (2025) · Developmental Neuroscience · doi:10.1159/000545713
“In the developing human cortex, FOXM1 has been identi fi ed in proliferative cells within the germinal zones (i.e., VZ, inner SVZ, and oSVZ) [14], and single-cell RNA sequencing data has shown that FOXM1 is highly enriched in bRGCs [8].”
Genomic basis of human-specific brain features
Mosti, F., & Silver, D. L. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-27380-3.00062-2
Transitions in development – an interview with Katie Long
(2026) · Development · doi:10.1242/dev.205551
Betizeau, M. (2013) · theses.fr (ABES) · doi:10.70675/96b2fd4ez61cfz4afeza473z7811a8b1fda6
Molecular mechanisms orchestrating commissural axon guidance
Roig‐Puiggros, S. (2019) · theses.fr (ABES) · doi:10.70675/9709d6aaz37b7z4de2za537zd7f1bf648566
Diversity of visual projections in vertebrates
Vigouroux, R. J. (2020) · theses.fr (ABES) · doi:10.70675/4e013149z524az4f80za5c1z99a2ca079cb0
Rôle physiologique et pathologique de la kinésine Kif21b au cours de la migration neuronale
Alvarez, J. R. (2022) · theses.fr (ABES) · doi:10.70675/7fc29459z67a7z4bedzacbczf5ca6affb824
Molecular mechanisms underlying the surface organization of the NMDA receptors during development
Bénac, N. (2024) · theses.fr (ABES) · doi:10.70675/e3508a2ezb62ez4f99zb27bz156201271974
Drlje, M., Trnski, S., Škokić, S., Censo, D. D., Bobić‐Rasonja, M., Kim, E., Kirchbaum, I., Štajduhar, A., Ilić, K., Cash, D., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.07.723460
Liu, D., Talevi, V., Tavares, J. F., Wang, R., Imtiaz, M. A., Melas, K., Teumer, A., Wittfeld, K., Hillary, R. F., Vojinović, D., et al. (2026) · EBioMedicine · doi:10.1016/j.ebiom.2026.106289
“55 Nutritional patterns associated with reduced inflammation and enhanced immune resilience, such as the EAT-Lancet, AHEI, and Nordic diets, may influence the regulation of CD300LB .”
Neurobiologie in der Petrischale – Chancen und Herausforderungen
Stephens, K. P., Yentür, Z., & Mayer, S. (2026) · BIOspektrum · doi:10.1007/s12268-026-2777-9
Betancourt, C. M. B., Ingravallo, I. N., Göloğlu, İ. B., Begenova, D., Puig-Segui, M. S., Costa, A. M., Reshetar, M., Heide, S., Ivanov, M. N., Veleva, L. V., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.07.27.740929
“Cells were sorted into 500 µL of lysis buffer (Micro RNeasy kit, Qiagen) prior to RNA extraction, as described above.”
Barresi, M., Johnstone, A., Quezada, S., Quigley, A. F., & Tolcos, M. (2026) · Brain Structure and Function · doi:10.1007/s00429-026-03178-6
“Previous studies have reported strong enrichment of ECM components and related signalling molecules in the oSVZ compared with the VZ and inner SVZ of 14-16-week human fetal brains (approxi - mately equivalent to P3-4 in the ferret) prior to the onset of cortical folding (Fietz et al. 2012 ).”
Transcriptome of fetal cortex of tree shrew underlying the emergence of outer subventricular zone
Hu, T., Wen, Y., Tan, Y., Kong, Y., Yuan, L., Yi, S. V., & Shi, L. (2026) · Communications Biology · doi:10.1038/s42003-026-10802-y
“Human, macaque, tree shrew and mouse lamina RNA-seq data Raw count data and FPKM values forhuman, macaque,tree shrewE37VZ, ISVZ, OSVZ, CP, and mouse neocortical laminae were obtained from the Gene Expression Omnibus (GEO) database (GSE38805) and from our previous studies 42,57,58 .”
CCNB1IP1 regulatory evolution underlies gradual increases in cortical size and folding in primates
Hu, T., Ma, P., Kong, Y., Tan, Y., Sun, X., Wang, J., Xiang, K., Mao, B., Wu, Q., Yi, S. V., et al. (2026) · Nature Genetics · doi:10.1038/s41588-026-02773-x · Cited by 2
“A summary of published data 7,26–29,”
Human-biased MEIS1 expression by a promoter noncoding RNA regulates neural stem cell proliferation
Uchida, H., Kameda, T., Zenno, S., Nakashima, H., Minato, Y., Aritsuka, Y., Nishida, S., An, B., Honda, M., Morishita, F., et al. (2026) · Life Science Alliance · doi:10.26508/lsa.202603708
“…available DRIP-seq data in human NPCs (Yan et al, 2020) suggested that pancMEIS1 forms an R-loop structure in a region (A) Expression level of MEIS1 , as analyzed using public RNA-seq data (aRGs and bRGs: [Florio et al, 2015]: [N = 4], VZ, ISVZ, OSVZ, and SVZ: [Fietz et al, 2012]: [N = 1]).”
Reaping what you grow: rethinking apoptosis in cortical folding
Barresi, M., & Tolcos, M. (2026) · Cerebral Cortex · doi:10.1093/cercor/bhag180
“Each cortical layer exhibits a unique transcriptional profile, captured by sequencing experiments ( Fietz et al. 2012).”
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
