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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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InfluentialSelf-citationSingle-cell analysis reveals transcriptional heterogeneity of neural progenitors in human cortex
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“Using RNA-seq datasets (Table EV1) (Fietz et al, 2012; Shen et al, 2012; Yue et al, 2014) from embryonic tissues that are representative of all three lineages, as well as from various layers of embryonic cortex, we found that NeuroD1 was highly expressed in the ventricular zone (VZ), was…”
MethodInfluentialHow the extracellular matrix shapes neural development
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Self-citationRole of radial glial cells in cerebral cortex folding
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“Intriguingly, recent studies in primates suggest that integrins and their ECM ligands might have important roles in the oSVZ, where bRGCs reside (Fietz et al., 2010; 2012), raising the possibility that cell-ECM interactions affect specific progenitor subpopulations.”
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BackgroundInfluentialvan de Leemput, J., Boles, N. C., Kiehl, T. R., Corneo, B., Lederman, P. L., Menon, V., Lee, C., Martinez, R. A., Levi, B. P., Thompson, C. L., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.013 · Cited by 210
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An Adaptive Threshold in Mammalian Neocortical Evolution
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Lui, J. H., Nowakowski, T. J., Pollen, A. A., Javaherian, A., Kriegstein, A. R., & Oldham, M. C. (2014) · Nature · doi:10.1038/nature13973 · Cited by 166
“Fusion of PDGF receptor b to a novel ets-like gene, tel, in chronic myelomonocytic leukemia with t(5;12) chromosomal translocation.”
BackgroundDefining the Adult Neural Stem Cell Niche Proteome Identifies Key Regulators of Adult Neurogenesis
Kjell, J., Fischer-Sternjak, J., Thompson, A. J., Friess, C., Sticco, M. J., Salinas, F., Cox, J., Martinelli, D. C., Ninkovic, J., Franze, K., et al. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.01.002 · Cited by 163
“Notably, the SEZ-enriched matrisome unraveled here differs profoundly from the enrichments found recently by RNA-seq of NSC niches in the developing Cx of murine or human samples (Fietz et al., 2012).”
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“Long basal processes of bRG allows them to receive signals from the ECM components located at the basal lamina, which was shown to be important for proliferative capacity (Fietz et al., 2010).”
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BackgroundGenetic Changes Shaping the Human Brain
Bae, B.-I., Jayaraman, D., & Walsh, C. A. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.01.035 · Cited by 135
“The other theory is that lineage-restricted or distinct subtypes of progenitors co-exist and are pre-specified to generate different subtypes of neurons (Franco et al., 2012).”
BackgroundLiu, J., Liu, W., Yang, L., Wu, Q., Zhang, H., Fang, A., Li, L., Xu, X., Sun, L., Zhang, J., et al. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.08.013 · Cited by 143
“…genes uniquely expressed in oRG cells, such as transcriptome analyses of microdissected VZ and SVZ tissues from rodents, primates, and humans (Fietz et al., 2012; Hawrylycz et al., 2012; Johnson et al., 2009, 2015; Kang et al., 2011; Lui et al., 2014; Miller et al., 2014; Pollen et al.,…”
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Regulation of Cerebral Cortex Folding by Controlling Neuronal Migration via FLRT Adhesion Molecules
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Genetics and mechanisms leading to human cortical malformations
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BackgroundSelf-citationCerebral cortex development: an outside‐in perspective
Agirman, G., Broix, L., & Nguyen, L. (2017) · FEBS Letters · doi:10.1002/1873-3468.12924 · Cited by 132
Namba, T., & Huttner, W. Β. (2016) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.256 · Cited by 120
“Comparative transcriptomics of proliferative aRGCs and nbIPs from mouse embryonic neocortex had pointed to a potential role of PDGF signaling in NPC proliferation.95 Indeed, a recent study has provided compelling evidence for a role of human PDGFD and PDGF receptor β (PDGFRβ).92,93 Specifically, in the fetal human neo…”
BackgroundInfluentialSelf-citationThe extracellular matrix compartment of neural stem and glial progenitor cells
Faissner, A., & Reinhard, J. (2015) · Glia · doi:10.1002/glia.22839 · Cited by 116
“In this approach, a strong and highly significant enrichment of ECM-constituents and ECM-related signaling was recorded, in close association with NSC proliferation (Fietz et al., 2012).”
BackgroundInfluentialTowards extracellular matrix normalization for improved treatment of solid tumors
Abyaneh, H. S., Regenold, M., McKee, T. D., Allen, C. J., & Gauthier, M. A. (2020) · Theranostics · doi:10.7150/thno.39995 · Cited by 120
“This evolutionary expansion of the human brain leads to higher cognitive function [44].”
BackgroundKinetochore KMN network gene CASC5 mutated in primary microcephaly
Genin, A., Desir, J., Lambert, N., Biervliet, M., Van Der Aa, N., Pierquin, G., Killian, A., Tosi, M., Urbina, M., Lefort, A., et al. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds386 · Cited by 116
“analyzed the transcriptome of the germinal zone of the human fetal neocortex at 13–16 gestational weeks by RNA sequencing (25).”
MethodIntegrin αvβ3 and thyroid hormones promote expansion of progenitors in embryonic neocortex
Stenzel, D., Wilsch‐Bräuninger, M., Wong, F. K., Heuer, H., & Huttner, W. Β. (2014) · Development · doi:10.1242/dev.101907 · Cited by 118
“TAPs), which is a characteristic feature of developing human, but not mouse, neocortex and which has been proposed to be linked to the greater BP-autonomous ECM production in human than mouse (Fietz et al., 2012), can indeed be induced by itgαvβ3 activation.”
BackgroundInfluentialSelf-citationNonparametric expression analysis using inferential replicate counts
Zhu, A., Srivastava, A., Ibrahim, J. G., Patro, R., & Love, M. I. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz622 · Cited by 112
“(46) dataset to have highest correlation with clusters 7 and 5 from the scRNA-seq dataset: the VZ is enriched with progenitor cells marked by Eomes, while the CP is enriched with differentiated neurons marked by Neurod2.”
BackgroundMethodInfluentialProbing human brain evolution and development in organoids
Giandomenico, S. L., & Lancaster, M. A. (2017) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2017.01.001 · Cited by 111
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“Because cell adhesions and ECM interactions play essential roles in stem cell self-renewal (Fietz et al., 2012; Marthiens et al., 2010), it is plausible that a direct role of Yap/Taz in NPC maintenance is to regulate genes involved in cell-cell and cell-matrix interactions.”
BackgroundHuman fetal brain self-organizes into long-term expanding organoids
Hendriks, D. F. G., Pagliaro, A., Andreatta, F., Ma, Z., van Giessen, J., Massalini, S., López‐Iglesias, C., van Son, G. J. F., DeMartino, J., Damen, M. J. A., et al. (2024) · Cell · doi:10.1016/j.cell.2023.12.012 · Cited by 108
Genes and Mechanisms Involved in the Generation and Amplification of Basal Radial Glial Cells
Penisson, M., Ladewig, J., Belvindrah, R., & Francis, F. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00381 · Cited by 97
Sustained Pax6 Expression Generates Primate-like Basal Radial Glia in Developing Mouse Neocortex
Wong, F. K., Fei, J., Mora‐Bermúdez, F., Taverna, E., Haffner, C., Fu, J., Anastassiadis, K., Stewart, A. F., & Huttner, W. Β. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002217 · Cited by 101
“Moreover, although Pax6 mRNA levels are generally lower in BPs than APs, this down-regulation is much greater for mouse than human [50].”
BackgroundInfluentialSelf-citationMechanotransduction in neuronal cell development and functioning
Chighizola, M., Dini, T., Lenardi, C., Milani, P., Podestà, A., & Schulte, C. (2019) · Biophysical Reviews · doi:10.1007/s12551-019-00587-2 · Cited by 101
A novel population of Hopx-dependent basal radial glial cells in the developing mouse neocortex
Vaid, S., Camp, J. G., Hersemann, L., Oegema, C. E., Heninger, A., Winkler, S., Brandl, H., Sarov, M., Treutlein, B., Huttner, W. Β., et al. (2018) · Development · doi:10.1242/dev.169276 · Cited by 98
“, 2016), have not been found to be expressed in mouse bRGCs in the dorsolateral telencephalon during embryonic corticogenesis (Fietz et al., 2012; Florio et al., 2015), although Hopx has been reported to be strongly expressed in the dentate gyrus of adult mouse hippocampus”
BackgroundInfluentialSelf-citationHuman-specific genomic signatures of neocortical expansion
Florio, M., Borrell, V., & Huttner, W. Β. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.11.004 · Cited by 100
Self-citationCortical progenitor biology: key features mediating proliferation versus differentiation
Uzquiano, A., Gladwyn-Ng, I. E., Nguyen, L., Reiner, O., Götz, M., Matsuzaki, F., & Francis, F. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14338 · Cited by 96
“Transcriptome analyses point towards a role for extracellular matrix (ECM) components produced in a cell-autonomous manner in controlling bRG proliferation (Fietz et al., 2012, Florio and Huttner, 2014, Pollen et al., 2015).”
BackgroundTranscriptomic Perspectives on Neocortical Structure, Development, Evolution, and Disease
Lein, E. S., Belgard, T. G., Hawrylycz, M., & Molnár, Z. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-013858 · Cited by 92
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“…of human development are hampered by difficulties in obtaining tissue which means that publicly available large-scale data sets are particularly useful because data can be used and re-used (Kang et al., 2011; Zhang et al., 2011; Fietz et al., 2012; Miller et al., 2014; Darmanis et al., 2015).”
BackgroundShaping the brain: The emergence of cortical structure and folding
Akula, S. K., Exposito-Alonso, D., & Walsh, C. A. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.11.004 · Cited by 104
“These include elevated expression of ECM proteins, 45,103,147 responsiveness to extracellular signaling cues through innovations in receptor expression, 148–150 molecular pathways controlling fatty acid synthesis, 84 specialized mitochondrial dynamics and metabolism, 151,152 and ciliary dynamics…”
BackgroundCoevolution of radial glial cells and the cerebral cortex
Romero, C. D. J., & Borrell, V. (2015) · Glia · doi:10.1002/glia.22827 · Cited by 102
“Significantly, this study also led to the intriguing finding that extracellular matrix (ECM) components are highly enriched in the OSVZ of the human fetal cortex compared with mouse (Fietz et al., 2012).”
BackgroundGene regulation and priming by topoisomerase IIα in embryonic stem cells
Thakurela, S., Garding, A., Jung, J., Schübeler, D., Burger, L., & Tiwari, V. K. (2013) · Nature Communications · doi:10.1038/ncomms3478 · Cited by 91
Tenascin-C in the matrisome of neural stem and progenitor cells
Faissner, A., Roll, L., & Theocharidis, U. (2016) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2016.11.003 · Cited by 87
“In this outer SVZ, the so-called basal radial glia or outer radial glia that does not contact the ventricular space is thought to promote further cortical growth and gyrification (Borrell and Gotz, 2014; Fietz and Huttner, 2011; Florio and Huttner, 2014; Hansen et al., 2010; Taverna et al., 2014).”
The extracellular matrix niche microenvironment of neural and cancer stem cells in the brain
Reinhard, J., Brösicke, N., Theocharidis, U., & Faissner, A. (2016) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2016.05.002 · Cited by 87
Transformation and model choice for RNA-seq co-expression analysis
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“[29] mouse data had a conditional probability of 24.”
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“, 2016), that is, throughout the developing cortical wall (Hirano and Takeichi, 2012; Fietz et al., 2012; Florio et al., 2015).”
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Mechanisms of brain evolution: Regulation of neural progenitor cell diversity and cell cycle length
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Cellular and Molecular Mechanisms Linking Human Cortical Development and Evolution
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Progenitor cell diversity in the developing mouse neocortex
Ruan, X., Kang, B., Qi, C., Lin, W., Wang, J., & Zhang, X. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2018866118 · Cited by 74
From sauropsids to mammals and back: New approaches to comparative cortical development
Montiel, J. F., Vasistha, N. A., García‐Moreno, F., & Molnár, Z. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23871 · Cited by 74
“Developmental compartments have been shown to express specific gene-signatures (Ayoub et al., 2011; Fietz et al., 2012) differing across ontogeny.”
BackgroundResultFolding brains: from development to disease modeling
Del-Valle-Anton, L., & Borrell, V. (2021) · Physiological Reviews · doi:10.1152/physrev.00016.2021 · Cited by 79
Dillen, Y., Kemps, H., Gervois, P., Wolfs, E., & Bronckaers, A. (2019) · Translational Stroke Research · doi:10.1007/s12975-019-00717-8 · Cited by 79
The regulation of cortical neurogenesis
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Neocortex expansion in development and evolution — from cell biology to single genes
Wilsch‐Bräuninger, M., Florio, M., & Huttner, W. Β. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.05.004 · Cited by 76
Self-citationGodichon‐Baggioni, A., Maugis-Rabusseau, C., & Rau, A. (2018) · Journal of Applied Statistics · doi:10.1080/02664763.2018.1454894 · Cited by 70
“[17] studied the expansion of the neocortex in five embryonic (day 14.5) mice by analyzing the transcriptome of the ventricular zone (VZ), subventricular zone (SVZ) and cortical place (CP).”
MethodInfluentialSpatial centrosome proteome of human neural cells uncovers disease-relevant heterogeneity
O’Neill, A. C., Uzbaş, F., Antognolli, G., Merino, F., Draganova, K., Jäck, A., Zhang, S., Pedini, G., Schessner, J. P., Cramer, K., et al. (2022) · Science · doi:10.1126/science.abf9088 · Cited by 71
“To probe when the genes misspliced upon PRPF6 expression may have the greatest effect, we examined their expression using data from the developing mouse cortex (45).”
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Heterogeneity and Plasticity of Breast Cancer Stem Cells
Sousa, B., Ribeiro, A. S., & Paredes, J. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-14366-4_5 · Cited by 69
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Kostic, M., Paridaen, J. T. M. L., Long, K. R., Kalebic, N., Langen, B., Grübling, N., Wimberger, P., Kawasaki, H., Namba, T., & Huttner, W. Β. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.03.091 · Cited by 67
Self-citationLaminin-Inspired Cell-Instructive Microenvironments for Neural Stem Cells
Barros, D., Amaral, I. F., & Pêgo, A. P. (2019) · Biomacromolecules · doi:10.1021/acs.biomac.9b01319 · Cited by 67
Loss of PCLO function underlies pontocerebellar hypoplasia type III
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“We also analyzed an additional RNA sequencing dataset of human fetal brain (13–16 weeks postconception).(9) In this dataset, PCLO expression was very low in the ventricular zone (0.”
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MyT1 Counteracts the Neural Progenitor Program to Promote Vertebrate Neurogenesis
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“5 mouse embryonic cortex (Fietz et al., 2012).”
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“In addition, our analysis revealed a distinct functionally-coherent network (human cluster 2) related to development of later cognitive functions in developing brain, which was not reported in the original study [32].”
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Human brain evolution: Emerging roles for regulatory DNA and RNA
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Extracellular LGALS3BP regulates neural progenitor position and relates to human cortical complexity
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ECE2 regulates neurogenesis and neuronal migration during human cortical development
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“Extracellular matrix proteins such as collagens, galectins and lumican have been implicated both in neuronal migration and differentiation and in cortical expansion and folding [67 – 69], with human-enriched ECM components contributing to interspecies differences such as in gyrification [70].”
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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