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 or SZi.
“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]
Species differences in distinct fetal transient zones, including SZ, SP, CP, and SG, have been described.
“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]
Prior studies have examined only a restricted subset of prenatal human brain regions and cortical layers.
“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]
Excitatory neurons, which constitute the majority of neocortical neurons, are derived from radial glial cells in the ventricular zone.
“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
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 · see citing works
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 · see citing works
Noctor, S. C., Martínez-Cerdeño, V., Ivic, L., & Kriegstein, A. R. (2004) · Nature Neuroscience · doi:10.1038/nn1172 · Cited by 2,229 · see citing works
The cell biology of neurogenesis
Götz, M., & Huttner, W. B. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1739 · Cited by 2,130 · see citing works
Self-citationEvolution of the neocortex: a perspective from developmental biology
Rakic, P. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2719 · Cited by 1,565 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 769 · see citing works
Smart, I. H. M. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.1.37 · Cited by 687 · see citing works
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 630 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Shitamukai, A., Konno, D., & Matsuzaki, F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4773-10.2011 · Cited by 450 · see citing works
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 406 · see citing works
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 · see citing works
Radial glia diversity: A matter of cell fate
Kriegstein, A., & Götz, M. (2003) · Glia · doi:10.1002/glia.10250 · Cited by 376 · see citing works
Neural 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 372 · see citing works
Self-citationoPOSSUM: 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 · see citing works
Osumi, N., Shinohara, H. M., Numayama‐Tsuruta, K., & Maekawa, M. (2008) · Stem Cells · doi:10.1634/stemcells.2007-0884 · Cited by 345 · see citing works
Huttner, W. Β., & Kosodo, Y. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.10.005 · Cited by 295 · see citing works
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 · see citing works
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 270 · see citing works
Self-citationFarkas, L. M., & Huttner, W. Β. (2008) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2008.09.008 · Cited by 247 · see citing works
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 · see citing works
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 212 · see citing works
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 · see citing works
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 · see citing works
Attardo, A., Calegari, F., Haubensak, W. E., Wilsch‐Bräuninger, M., & Huttner, W. Β. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002388 · Cited by 165 · see citing works
Self-citationoPOSSUM: 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 · see citing works
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 155 · see citing works
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 · see citing works
Human 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 152 · see citing works
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 145 · see citing works
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 135 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 101 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Evolution of Cerebral Cortical Development
Molnár, Z. (2011) · Brain Behavior and Evolution · doi:10.1159/000327325 · Cited by 71 · see citing works
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 · see citing works
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 60 · see citing works
Wang, W.-Z., Oeschger, F. M., Lee, S., & Molnár, Z. (2009) · BMC Molecular Biology · doi:10.1186/1471-2199-10-69 · Cited by 56 · see citing works
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 · see citing works
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 · see citing works
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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 · see citing works
Human 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 · see citing works
Self-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 · see citing works
The 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 · see citing works
Taverna, E., Götz, M., & Huttner, W. Β. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101011-155801 · Cited by 737 · see citing works
Self-citationNeural progenitors, neurogenesis and the evolution of the neocortex
Florio, M., & Huttner, W. Β. (2014) · Development · doi:10.1242/dev.090571 · Cited by 624 · see citing works
Self-citationEstablishing Cerebral Organoids as Models of Human-Specific Brain Evolution
Pollen, A. A., Bhaduri, A., Andrews, M. G., Nowakowski, T. J., Meyerson, O. S., Mostajo-Radji, M. A., Di Lullo, E., Alvarado, B., Bedolli, M., Dougherty, M. L., et al. (2019) · Cell · doi:10.1016/j.cell.2019.01.017 · Cited by 600 · see citing works
Human-specific gene <i>ARHGAP11B</i> promotes basal progenitor amplification and neocortex expansion
Florio, M., Albert, M., Taverna, E., Namba, T., Brandl, H., Lewitus, E., Haffner, C., Sykes, A., Wong, F. K., Peters, J., et al. (2015) · Science · doi:10.1126/science.aaa1975 · Cited by 632 · see citing works
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Gage, F. H., & Temple, S. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.037 · Cited by 571 · see citing works
The rise of three-dimensional human brain cultures
Pașca, S. P. (2018) · Nature · doi:10.1038/nature25032 · Cited by 509 · see citing works
Betizeau, M., Cortay, V., Patti, D., Pfister, S., Gautier, E., Bellemin-Ménard, A., Afanassieff, M., Huissoud, C., Douglas, R. J., Kennedy, H., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.032 · Cited by 462 · see citing works
Human brain organoids on a chip reveal the physics of folding
Karzbrun, E., Kshirsagar, A., Cohen, S., Hanna, J. H., & Reiner, O. (2018) · Nature Physics · doi:10.1038/s41567-018-0046-7 · Cited by 421 · see citing works
Stem Cell Models of Human Brain Development
Kelava, I., & Lancaster, M. A. (2016) · Cell stem cell · doi:10.1016/j.stem.2016.05.022 · Cited by 371 · see citing works
Cerebral cortex expansion and folding: what have we learned?
Fernández, V., Llinares-Benadero, C., & Borrell, V. (2016) · The EMBO Journal · doi:10.15252/embj.201593701 · Cited by 357 · see citing works
Cell-Type-Specific Alternative Splicing Governs Cell Fate in the Developing Cerebral Cortex
Zhang, X., Chen, M. H., Wu, X., Kodani, A., Fan, J., Doan, R. N., Ozawa, M., Ma, J., Yoshida, N., Reiter, J. F., et al. (2016) · Cell · doi:10.1016/j.cell.2016.07.025 · Cited by 343 · see citing works
The outer subventricular zone and primate-specific cortical complexification
Dehay, C., Kennedy, H., & Kosik, K. S. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.060 · Cited by 314 · see citing works
Mora‐Bermúdez, F., Badsha, F., Kanton, S., Camp, J. G., Vernot, B., Köhler, K., Voigt, B., Okita, K., Maričić, T., He, Z., et al. (2016) · eLife · doi:10.7554/elife.18683 · Cited by 289 · see citing works
Self-citationSingle-cell analysis reveals transcriptional heterogeneity of neural progenitors in human cortex
Johnson, M. B., Wang, P. P., Atabay, K. D., Murphy, E. A., Doan, R. N., Hecht, J. L., & Walsh, C. A. (2015) · Nature Neuroscience · doi:10.1038/nn.3980 · Cited by 288 · see citing works
NeuroD1 reprograms chromatin and transcription factor landscapes to induce the neuronal program
Pataskar, A., Jung, J., Smialowski, P., Noack, F., Calegari, F., Straub, T., & Tiwari, V. K. (2015) · The EMBO Journal · doi:10.15252/embj.201591206 · Cited by 275 · see citing works
How the extracellular matrix shapes neural development
Long, K. R., & Huttner, W. Β. (2019) · Open Biology · doi:10.1098/rsob.180216 · Cited by 270 · see citing works
Self-citationDeconstructing cortical folding: genetic, cellular and mechanical determinants
Llinares-Benadero, C., & Borrell, V. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0112-2 · Cited by 243 · see citing works
Molecular genetics of human primary microcephaly: an overview
Faheem, M., Naseer, M. I., Rasool, M., Chaudhary, A., Kumosani, T., Ilyas, A. M., Pushparaj, P. N., Ahmed, F., Algahtani, H. A., Al-Qahtani, M. H., et al. (2015) · BMC Medical Genomics · doi:10.1186/1755-8794-8-s1-s4 · Cited by 234 · see citing works
Fixed single-cell transcriptomic characterization of human radial glial diversity
Thomsen, E. R., Mich, J. K., Yao, Z., Hodge, R. D., Doyle, A. M., Jang, S., Shehata, S. I., Nelson, A. M., Shapovalova, N. V., Levi, B. P., et al. (2015) · Nature Methods · doi:10.1038/nmeth.3629 · Cited by 227 · see citing works
Human TKTL1 implies greater neurogenesis in frontal neocortex of modern humans than Neanderthals
Pinson, A., Xing, L., Namba, T., Kalebic, N., Peters, J., Oegema, C. E., Traikov, S., Reppe, K., Riesenberg, S., Maričić, T., et al. (2022) · Science · doi:10.1126/science.abl6422 · Cited by 228 · see citing works
Self-citationRole of radial glial cells in cerebral cortex folding
Borrell, V., & Götz, M. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.02.007 · Cited by 221 · see citing works
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Franco, S. J., & Müller, U. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.022 · Cited by 219 · see citing works
Aprea, J., Prenninger, S., Dori, M., Ghosh, T., Monasor, L. S., Wessendorf, E., Zocher, S., Massalini, S., Alexopoulou, D., Lesche, M., et al. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.245 · Cited by 219 · see citing works
van 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 207 · see citing works
Florio, M., Heide, M., Pinson, A., Brandl, H., Albert, M., Winkler, S., Wimberger, P., Huttner, W. Β., & Hiller, M. (2018) · eLife · doi:10.7554/elife.32332 · Cited by 201 · see citing works
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Long, K. R., Newland, B., Florio, M., Kalebic, N., Langen, B., Kolterer, A., Wimberger, P., & Huttner, W. B. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.013 · Cited by 196 · see citing works
Self-citationVieira, M. S., Santos, A. K., Vasconcellos, R., Goulart, V. A. M., Parreira, R. C., Kihara, A. H., Ulrich, H., & Resende, R. R. (2018) · Biotechnology Advances · doi:10.1016/j.biotechadv.2018.08.002 · Cited by 191 · see citing works
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Ju, X.-C., Hou, Q.-Q., Sheng, A.-L., Wu, K.-Y., Zhou, Y., Jin, Y., Wen, T., Yang, Z., Wang, X., & Luo, Z. (2016) · eLife · doi:10.7554/elife.18197 · Cited by 169 · see citing works
Klaus, J., Kanton, S., Kyrousi, C., Ayo-Martin, A. C., Di Giaimo, R., Riesenberg, S., O’Neill, A. C., Camp, J. G., Tocco, C., Santel, M., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0371-0 · Cited by 169 · see citing works
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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 · see citing works
Defining 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 · see citing works
Kalebic, N., Gilardi, C., Stepien, B. K., Wilsch‐Bräuninger, M., Long, K. R., Namba, T., Florio, M., Langen, B., Lombardot, B., Shevchenko, A., et al. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.02.017 · Cited by 161 · see citing works
Self-citationSystematic profiling of spatiotemporal tissue and cellular stiffness in the developing brain
Iwashita, M., Kataoka, N., Toida, K., & Kosodo, Y. (2014) · Development · doi:10.1242/dev.109637 · Cited by 154 · see citing works
Genetic 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 · see citing works
Liu, 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 138 · see citing works
Cortical organoids model early brain development disrupted by 16p11.2 copy number variants in autism
Urresti, J., Zhang, P., Losada, P. M., Yu, N., Negraes, P. D., Trujillo, C. A., Antaki, D., Amar, M., Chau, K. K., Pramod, A. B., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01243-6 · Cited by 133 · see citing works
Zhang, X., Ling, J., Barcia, G., Jing, L., Wu, J., Barry, B. J., Mochida, G. H., Hill, R. S., Weimer, J. M., Stein, Q., et al. (2014) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2014.03.003 · Cited by 133 · see citing works
Regulation of Cerebral Cortex Folding by Controlling Neuronal Migration via FLRT Adhesion Molecules
del Toro, D., Ruff, T., Cederfjäll, E. A., Villalba, A., Seyit-Bremer, G., Borrell, V., & Klein, R. (2017) · Cell · doi:10.1016/j.cell.2017.04.012 · Cited by 138 · see citing works
Genetics and mechanisms leading to human cortical malformations
Romero, D. M., Bahi‐Buisson, N., & Francis, F. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.09.031 · Cited by 126 · see citing works
Lewitus, É., Kelava, I., & Huttner, W. Β. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00424 · Cited by 121 · see citing works
Self-citationCerebral cortex development: an outside‐in perspective
Agirman, G., Broix, L., & Nguyen, L. (2017) · FEBS Letters · doi:10.1002/1873-3468.12924 · Cited by 119 · see citing works
Namba, T., & Huttner, W. Β. (2016) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.256 · Cited by 115 · see citing works
Self-citationThe extracellular matrix compartment of neural stem and glial progenitor cells
Faissner, A., & Reinhard, J. (2015) · Glia · doi:10.1002/glia.22839 · Cited by 117 · see citing works
Towards 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 117 · see citing works
Kinetochore 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 · see citing works
Integrin 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 114 · see citing works
Self-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 110 · see citing works
Probing 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 107 · see citing works
Lavado, A., He, Y. Y., Paré, J., Neale, G. A. M., Olson, E. N., Giovannini, M., & Cao, X. (2013) · Development · doi:10.1242/dev.096537 · Cited by 108 · see citing works
Human 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 106 · see citing works
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 · see citing works
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 96 · see citing works
Self-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 97 · see citing works
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 96 · see citing works
Self-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 96 · see citing works
Self-citationTranscriptomic 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 · see citing works
Cortical 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 89 · see citing works
Lindsay, S., Xu, Y., Lisgo, S., Harkin, L. F., Copp, A. J., Gerrelli, D., Clowry, G. J., Talbot, A., Keogh, M. J., Coxhead, J. M., et al. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00086 · Cited by 91 · see citing works
Shaping 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 97 · see citing works
Coevolution of radial glial cells and the cerebral cortex
Romero, C. D. J., & Borrell, V. (2015) · Glia · doi:10.1002/glia.22827 · Cited by 96 · see citing works
Gene 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 88 · see citing works
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 89 · see citing works
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 86 · see citing works
Transformation and model choice for RNA-seq co-expression analysis
Rau, A., & Maugis-Rabusseau, C. (2016) · Briefings in Bioinformatics · doi:10.1093/bib/bbw128 · Cited by 85 · see citing works
Basal Progenitor Morphology and Neocortex Evolution
Kalebic, N., & Huttner, W. Β. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.07.009 · Cited by 85 · see citing works
Self-citationTavano, S., Taverna, E., Kalebic, N., Haffner, C., Namba, T., Dahl, A., Wilsch‐Bräuninger, M., Paridaen, J. T. M. L., & Huttner, W. Β. (2018) · Neuron · doi:10.1016/j.neuron.2018.01.052 · Cited by 82 · see citing works
Self-citationArcila, M. L., Betizeau, M., Cambronne, X. A., Guzman, E., Doerflinger, N., Bouhallier, F., Zhou, H., Wu, B., Rani, N., Bassett, D. S., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.017 · Cited by 80 · see citing works
Cellular and Molecular Mechanisms Linking Human Cortical Development and Evolution
Libé-Philippot, B., & Vanderhaeghen, P. (2021) · Annual Review of Genetics · doi:10.1146/annurev-genet-071719-020705 · Cited by 78 · see citing works
Mechanisms of brain evolution: Regulation of neural progenitor cell diversity and cell cycle length
Borrell, V., & Calegari, F. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.04.004 · Cited by 78 · see citing works
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 71 · see citing works
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 · see citing works
Folding brains: from development to disease modeling
Del-Valle-Anton, L., & Borrell, V. (2021) · Physiological Reviews · doi:10.1152/physrev.00016.2021 · Cited by 78 · see citing works
Dillen, Y., Kemps, H., Gervois, P., Wolfs, E., & Bronckaers, A. (2019) · Translational Stroke Research · doi:10.1007/s12975-019-00717-8 · Cited by 75 · see citing works
The regulation of cortical neurogenesis
Villalba, A., Götz, M., & Borrell, V. (2020) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2020.10.003 · Cited by 74 · see citing works
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 73 · see citing works
Self-citationGodichon‐Baggioni, A., Maugis-Rabusseau, C., & Rau, A. (2018) · Journal of Applied Statistics · doi:10.1080/02664763.2018.1454894 · Cited by 71 · see citing works
Xiao, X., Moreno-Moral, A., Rotival, M., Bottolo, L., & Petretto, E. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004006 · Cited by 63 · see citing works
Spatial 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 69 · see citing works
Long, K. R., Moss, L., Laursen, L. S., Boulter, L., & ffrench‐Constant, C. (2016) · Nature Communications · doi:10.1038/ncomms10354 · Cited by 69 · see citing works
Wang, H., Xiao, Z., Zheng, J., Wu, J., Hu, X.-L., Yang, X., & Shen, Q. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.081 · Cited by 69 · see citing works
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 · see citing works
Sahu, S. K., Tiwari, N., Pataskar, A., Zhuang, Y., Borisova, M. E., Diken, M., Strand, S., Beli, P., & Tiwari, V. K. (2017) · Nature Communications · doi:10.1038/s41467-017-01366-x · Cited by 69 · see citing works
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 68 · see citing works
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 · see citing works
Loss of PCLO function underlies pontocerebellar hypoplasia type III
Ahmed, M. Y., Chioza, B. A., Rajab, A., Schmitz‐Abe, K., Al‐Khayat, A., Al-Turki, S., Baple, E. L., Patton, M. A., Al‐Memar, A., Hurles, M. E., et al. (2015) · Neurology · doi:10.1212/wnl.0000000000001523 · Cited by 66 · see citing works
Ferent, J., Zaidi, D., & Francis, F. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.578341 · Cited by 64 · see citing works
MyT1 Counteracts the Neural Progenitor Program to Promote Vertebrate Neurogenesis
Vasconcelos, F. F., Sessa, A., Laranjeira, C., Raposo, A. A. S. F., Teixeira, V., Hagey, D. W., Tomaz, D. M., Muhr, J., Broccoli, V., & Castro, D. S. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.09.024 · Cited by 62 · see citing works
Hickey, S. L., Berto, S., & Konopka, G. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.044 · Cited by 63 · see citing works
Human brain evolution: Emerging roles for regulatory DNA and RNA
Liu, J., Mosti, F., & Silver, D. L. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.11.005 · Cited by 63 · see citing works
Extracellular LGALS3BP regulates neural progenitor position and relates to human cortical complexity
Kyrousi, C., O’Neill, A. C., Brazovskaja, A., He, Z., Kielkowski, P., Coquand, L., Giaimo, R. D., Andrea, P. D., Belka, A., Forero, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26447-w · Cited by 60 · see citing works
Diverse Roles for Hyaluronan and Hyaluronan Receptors in the Developing and Adult Nervous System
Peters, A., & Sherman, L. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21175988 · Cited by 61 · see citing works
ECE2 regulates neurogenesis and neuronal migration during human cortical development
Buchsbaum, I. Y., Kielkowski, P., Giorgio, G., O’Neill, A. C., Giaimo, R. D., Kyrousi, C., Khattak, S., Sieber, S. A., Robertson, S. P., & Cappello, S. (2020) · EMBO Reports · doi:10.15252/embr.201948204 · Cited by 61 · see citing works
- 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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