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-citationAsymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells
Miyata, T., Kawaguchi, A., Saito, K., Kawano, M., Muto, T., & Ogawa, M. (2004) · Development · doi:10.1242/dev.01173 · Cited by 791
Smart, I. H. M. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.1.37 · Cited by 687
A Role for Intermediate Radial Glia in the Tangential Expansion of the Mammalian Cerebral Cortex
Reillo, I., Romero, C. D. J., García‐Cabezas, M. Á., & Borrell, V. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq238 · Cited by 655
Johnson, M. B., Kawasawa, Y. I., Mason, C. E., Krsnik, Ž., Coppola, G., Bogdanović, D., Geschwind, D. H., Mane, S. M., State, M. W., & Šestan, N. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.027 · Cited by 603
A new subtype of progenitor cell in the mouse embryonic neocortex
Wang, X., Tsai, J.-W., LaMonica, B., & Kriegstein, A. R. (2011) · Nature Neuroscience · doi:10.1038/nn.2807 · Cited by 507
Extracellular Matrix: Functions in the Nervous System
Barros, C. S., Franco, S. J., & Muller, U. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005108 · Cited by 506
Shitamukai, A., Konno, D., & Matsuzaki, F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4773-10.2011 · Cited by 474
Kowalczyk, T., Pontious, A., Englund, C., Daza, R. A. M., Bedogni, F., Hodge, R. D., Attardo, A., Bell, C., Huttner, W. Β., & Hevner, R. F. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn260 · Cited by 438
Self-citationNeural stem and progenitor cells shorten S-phase on commitment to neuron production
Arai, Y., Pulvers, J. N., Haffner, C., Schilling, B., Nüsslein, I., Calegari, F., & Huttner, W. Β. (2011) · Nature Communications · doi:10.1038/ncomms1155 · Cited by 399
Self-citationRole of Intermediate Progenitor Cells in Cerebral Cortex Development
Pontious, A., Kowalczyk, T., Englund, C., & Hevner, R. F. (2008) · Developmental Neuroscience · doi:10.1159/000109848 · Cited by 378
Radial glia diversity: A matter of cell fate
Kriegstein, A., & Götz, M. (2003) · Glia · doi:10.1002/glia.10250 · Cited by 376
oPOSSUM: identification of over-represented transcription factor binding sites in co-expressed genes
Sui, S. J. H. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki624 · Cited by 370
Osumi, N., Shinohara, H. M., Numayama‐Tsuruta, K., & Maekawa, M. (2008) · Stem Cells · doi:10.1634/stemcells.2007-0884 · Cited by 360
Huttner, W. Β., & Kosodo, Y. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.10.005 · Cited by 305
Self-citationCortical progenitor expansion, self-renewal and neurogenesis—a polarized perspective
Fietz, S. A., & Huttner, W. Β. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.10.002 · Cited by 277
Self-citationMaking bigger brains–the evolution of neural-progenitor-cell division
Fish, J. L., Dehay, C., Kennedy, H., & Huttner, W. B. (2008) · Journal of Cell Science · doi:10.1242/jcs.023465 · Cited by 274
Self-citationFarkas, L. M., & Huttner, W. Β. (2008) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2008.09.008 · Cited by 263
Self-citationArikawa‐Hirasawa, E., Wilcox, W. R., Le, A. H., Silverman, N. S., Govindraj, P., Hassell, J. R., & Yamada, Y. (2001) · Nature Genetics · doi:10.1038/86941 · Cited by 238
Kelava, I., Reillo, I., Murayama, A. Y., Kalinka, A. T., Stenzel, D., Tomančák, P., Matsuzaki, F., Lebrand, C., Sasaki, E., Schwamborn, J. C., et al. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr301 · Cited by 217
Self-citationSingle-cell gene profiling defines differential progenitor subclasses in mammalian neurogenesis
Kawaguchi, A., Ikawa, T., Kasukawa, T., Ueda, H. R., Kurimoto, K., Saitou, M., & Matsuzaki, F. (2008) · Development · doi:10.1242/dev.022616 · Cited by 193
β1 Integrin Maintains Integrity of the Embryonic Neocortical Stem Cell Niche
Loulier, K., Lathia, J. D., Marthiens, V., Relucio, J. L. V., Mughal, M. R., Tang, S., Coksaygan, T., Hall, P. E., Chigurupati, S., Patton, B. L., et al. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000176 · Cited by 184
Attardo, A., Calegari, F., Haubensak, W. E., Wilsch‐Bräuninger, M., & Huttner, W. Β. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002388 · Cited by 180
Self-citationHuman disorders of cortical development: from past to present
Francis, F., Meyer, G., Fallet‐Bianco, C., Moreno, S., Kappeler, C., Socorro, A. C., Tuy, F. P. D., Beldjord, C., & Chelly, J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04649.x · Cited by 166
Adhesion molecules in the stem cell niche – more than just staying in shape?
Marthiens, V., Kazanis, I., Moss, L., Long, K. R., & ffrench‐Constant, C. (2010) · Journal of Cell Science · doi:10.1242/jcs.054312 · Cited by 164
oPOSSUM: integrated tools for analysis of regulatory motif over-representation
Sui, S. J. H., Fulton, D. L., Arenillas, D. J., Kwon, A. T.-J., & Wasserman, W. W. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm427 · Cited by 162
A Stem Cell Niche for Intermediate Progenitor Cells of the Embryonic Cortex
Javaherian, A., & Kriegstein, A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp029 · Cited by 155
Regulation of neural progenitor cell development in the nervous system
Corbin, J. G., Gaiano, N., Juliano, S. L., Poluch, S., Stancik, E. K., & Haydar, T. F. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05522.x · Cited by 149
Patterns of laminins and integrins in the embryonic ventricular zone of the CNS
Lathia, J. D., Patton, B. L., Eckley, D. M., Magnus, T., Mughal, M. R., Sasaki, T., Caldwell, M. A., Rao, M. S., Mattson, M. P., & ffrench‐Constant, C. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21520 · Cited by 141
Neurovascular Congruence during Cerebral Cortical Development
Stubbs, D., DeProto, J., Nie, K., Englund, C., Mahmud, I., Hevner, R., & Molnár, Z. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp040 · Cited by 133
Ayoub, A. E., Oh, S., Xie, Y., Leng, J., Cotney, J., Dominguez, M. H., Noonan, J. P., & Rakic, P. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1112213108 · Cited by 129
Oligodendrocyte development in the spinal cord and telencephalon: common themes and new perspectives
Woodruff, R., Tekki-Kessaris, N., Stiles, C., Rowitch, D., & Richardson, W. (2001) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(00)00083-6 · Cited by 124
Ochiai, W., Nakatani, S., Takahara, T., Kainuma, M., Masaoka, M., Minobe, S., Namihira, M., Nakashima, K., Sakakibara, A., Ogawa, M., et al. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.10.007 · Cited by 104
Perlecan controls neurogenesis in the developing telencephalon
Girós, A., Morante, J., Gil, C., Fairén, A., & Costell, M. (2007) · BMC Developmental Biology · doi:10.1186/1471-213x-7-29 · Cited by 101
Saito, K., Dubreuil, V., Arai, Y., Wilsch-Bräuninger, M., Schwudke, D., Saher, G., Miyata, T., Breier, G., Thiele, C., Shevchenko, A., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903541106 · Cited by 88
Self-citationMechanisms that regulate the number of neurons during mouse neocortical development
Miyata, T., Kawaguchi, D., Kawaguchi, A., & Gotoh, Y. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.01.001 · Cited by 78
Evolution of Cerebral Cortical Development
Molnár, Z. (2011) · Brain Behavior and Evolution · doi:10.1159/000327325 · Cited by 75
Hoyer, J., Kraus, C. S., Hammersen, G., Geppert, J., & Rauch, A. M. (2009) · Clinical Genetics · doi:10.1111/j.1399-0004.2009.01204.x · Cited by 63
The microenvironment of the embryonic neural stem cell: Lessons from adult niches?
Lathia, J. D., Rao, M. S., Mattson, M. P., & ffrench‐Constant, C. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21319 · Cited by 61
Wang, W.-Z., Oeschger, F. M., Lee, S., & Molnár, Z. (2009) · BMC Molecular Biology · doi:10.1186/1471-2199-10-69 · Cited by 56
Membrane traffic in polarized neurons
Bradke, F., & Dotti, C. G. (1998) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(98)00060-3 · Cited by 53
The evolution of Olig genes and their roles in myelination
Li, H., & Richardson, W. (2008) · Neuron Glia Biology · doi:10.1017/s1740925x09990251 · Cited by 39
Cited by
Sorted by citations
Transcriptional landscape of the prenatal human brain
Miller, J. A., Ding, S.-L., Sunkin, S. M., Smith, K. A., Ng, L., Szafer, A., Ebbert, A., Riley, Z. L., Royall, J. J., Aiona, K., et al. (2014) · Nature · doi:10.1038/nature13185 · Cited by 1,325
“Data for samples passing QC were normalized in three steps: (1) ‘within-batch’ normalization to the 75th percentile expression values; (2) ‘cross-batch’ bias reduction using ComBat(57); and (3) ‘cross-brain’ normalization as in step 1.”
MethodHuman cerebral organoids recapitulate gene expression programs of fetal neocortex development
Camp, J. G., Badsha, F., Florio, M., Kanton, S., Gerber, T., Wilsch-Bräuninger, M., Lewitus, E., Sykes, A., Hevers, W., Lancaster, M., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1520760112 · Cited by 1,130
“We next used all expressed genes to characterize cells based on their maximum correlation with bulk RNA-seq data from laser-dissected germinal zones, namely VZ (containing a majority of aRG), iSVZ and oSVZ (containing a majority of bIPs, bRG neurons, and migrating neurons), and CP (containing mature neurons) (18), or…”
BackgroundMethodSelf-citationMolecular Identity of Human Outer Radial Glia during Cortical Development
Pollen, A. A., Nowakowski, T. J., Chen, J., Retallack, H., Sandoval-Espinosa, C., Nicholas, C. R., Shuga, J., Liu, S. J., Oldham, M. C., Diaz, A., et al. (2015) · Cell · doi:10.1016/j.cell.2015.09.004 · Cited by 908
“Previous studies have attempted to identify genes uniquely expressed in oRG cells using a variety of transcriptional profiling strategies, including comparisons between microdissected samples (Fietz et al., 2012; Miller et al., 2014) and between cell populations expressing particular surface proteins (Florio et al.”
InfluentialThe Cellular and Molecular Landscapes of the Developing Human Central Nervous System
Silbereis, J. C., Pochareddy, S., Zhu, Y., Li, M., & Sestan, N. (2016) · Neuron · doi:10.1016/j.neuron.2015.12.008 · Cited by 818
“In a complementary approach, Florio et al. (2015) used differential labeling of apical (iRG) and basal (oRG) RG cells to sort these two populations for RNA sequencing in mouse and human fetal neocortex.”
Taverna, E., Götz, M., & Huttner, W. Β. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101011-155801 · Cited by 780
Self-citation
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
