A new subtype of progenitor cell in the mouse embryonic neocortex
Open accessAbstract
A hallmark of mammalian brain evolution is cortical expansion, which reflects an increase in the number of cortical neurons established by the progenitor cell subtypes present and the number of their neurogenic divisions. Recent studies have revealed a new class of radial glia-like (oRG) progenitor cells in the human brain, which reside in the outer subventricular zone. Expansion of the subventricular zone and appearance of oRG cells may have been essential evolutionary steps leading from lissencephalic to gyrencephalic neocortex. Here we show that oRG-like progenitor cells are present in the mouse embryonic neocortex. They arise from asymmetric divisions of radial glia and undergo self-renewing asymmetric divisions to generate neurons. Moreover, mouse oRG cells undergo mitotic somal translocation whereby centrosome movement into the basal process during interphase precedes nuclear translocation. Our finding of oRG cells in the developing rodent brain fills a gap in our understanding of neocortical expansion.
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The oRG population is largely missing in mouse brain development.
“The oRG population is largely missing in mouse brain development47, and human cellular models therefore provide a unique opportunity to study this cell population.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [47]
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Cites
Specification of Cerebral Cortical Areas
Rakic, P. (1988) · Science · doi:10.1126/science.3291116 · Cited by 3,127 · 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
Self-citationNoctor, S. C., Martínez-Cerdeño, V., Ivic, L., & Kriegstein, A. R. (2004) · Nature Neuroscience · doi:10.1038/nn1172 · Cited by 2,229 · see citing works
Self-citationThe 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
Neurons derived from radial glial cells establish radial units in neocortex
Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S., & Kriegstein, A. R. (2001) · Nature · doi:10.1038/35055553 · Cited by 2,016 · 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
Self-citationEnglund, 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
Rakic, P. (1974) · Science · doi:10.1126/science.183.4123.425 · Cited by 1,161 · see citing works
Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage
Malatesta, P., Hartfuss, E., & Götz, M. (2000) · Development · doi:10.1242/dev.127.24.5253 · Cited by 1,157 · see citing works
Kanda, T., Sullivan, K., & Wahl, G. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70156-3 · Cited by 1,040 · see citing works
Electroporation and RNA interference in the rodent retina in vivo and in vitro
Matsuda, T., & Cepko, C. L. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2235688100 · Cited by 1,032 · 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
Asymmetric Inheritance of Radial Glial Fibers by Cortical Neurons
Miyata, T., Kawaguchi, A., Okano, H., & Ogawa, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00420-2 · Cited by 892 · see citing works
OSVZ 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
Asymmetric 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
Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion
Kriegstein, A., Noctor, S., & Martínez-Cerdeño, V. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn2008 · Cited by 738 · see citing works
Self-citationTabata, H., & Nakajima, K. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00016-1 · Cited by 705 · see citing works
Smart, I. H. M. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.1.37 · Cited by 687 · see citing works
Patterns of neuronal migration in the embryonic cortex
Kriegstein, A. R., & Noctor, S. C. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.05.001 · Cited by 648 · see citing works
Self-citationA 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
Gap junction adhesion is necessary for radial migration in the neocortex
Elias, L., Wang, D. D., & Kriegstein, A. R. (2007) · Nature · doi:10.1038/nature06063 · Cited by 587 · see citing works
Self-citationAsymmetric centrosome inheritance maintains neural progenitors in the neocortex
Wang, X., Tsai, J., Imai, J. H., Lian, W.-N., Vallee, R. B., & Shi, S. (2009) · Nature · doi:10.1038/nature08435 · Cited by 477 · see citing works
Self-citationKosodo, Y., Röper, K., Haubensak, W. E., Marzesco, A., Corbeil, D., & Huttner, W. Β. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600223 · Cited by 435 · see citing works
Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis
Noctor, S. C., Martínez‐Cerdeño, V., & Kriegstein, A. R. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21669 · Cited by 415 · see citing works
Self-citationTsai, J., Chen, Y., Kriegstein, A. R., & Vallee, R. B. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200505166 · Cited by 401 · see citing works
Self-citationElusive radial glial cells: Historical and evolutionary perspective
RAKIC, P. T. (2003) · Glia · doi:10.1002/glia.10244 · Cited by 279 · see citing works
Making 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
Intrinsic polarity of mammalian neuroepithelial cells.
Chenn, A., Zhang, Y. A., Chang, B., & McConnell, S. (1998) · Molecular and cellular neurosciences · doi:10.1006/mcne.1998.0680 · Cited by 228 · see citing works
Neurons from radial glia: the consequences of asymmetric inheritance
Fishell, G., & Kriegstein, A. R. (2003) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(03)00013-8 · Cited by 224 · see citing works
Self-citationPulvers, J. N., Bryk, J., Fish, J. L., Wilsch‐Bräuninger, M., Arai, Y., Schreier, D., Naumann, R., Helppi, J., Habermann, B. H., Vogt, J., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010494107 · Cited by 194 · see citing works
Comparative aspects of cortical neurogenesis in vertebrates
Cheung, A. F. P., Pollen, A. A., Tavare, A. N., DeProto, J., & Molnár, Z. (2007) · Journal of Anatomy · doi:10.1111/j.1469-7580.2007.00769.x · Cited by 137 · see citing works
Kamei, Y., Inagaki, N., Nishizawa, M., Tsutsumi, O., Taketani, Y., & Inagaki, M. (1998) · Glia · doi:10.1002/(sici)1098-1136(199807)23:3 · Cited by 114 · see citing works
Evolution of cortical neurogenesis
Abdel‐Mannan, O., Cheung, A. F. P., & Molnár, Z. (2007) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2007.10.047 · Cited by 67 · see citing works
Neural Stem and Progenitor Cells in Cortical Development
Noctor, S. C., Martínez‐Cerdeño, V., & Kriegstein, A. R. (2008) · Novartis Foundation symposium · doi:10.1002/9780470994030.ch5 · Cited by 60 · see citing works
Self-citationIn Utero Intraventricular Injection and Electroporation of E15 Mouse Embryos
Walantus, W., Castaneda, D., Elias, L., & Kriegstein, A. R. (2007) · Journal of Visualized Experiments · doi:10.3791/239 · Cited by 52 · see citing works
Self-citationCarney, R. S. E., Bystron, I., López‐Bendito, G., & Molnár, Z. (2007) · Brain Structure and Function · doi:10.1007/s00429-007-0142-4 · Cited by 46 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Self-citationKadoshima, T., Sakaguchi, H., Nakano, T., Soen, M., Ando, S., Eiraku, M., & Sasai, Y. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1315710110 · Cited by 999 · see citing works
Molecular 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
Self-citationMolecular logic of neocortical projection neuron specification, development and diversity
Greig, L. C., Woodworth, M. B., Galazo, M. J., Padmanabhan, H., & Macklis, J. D. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3586 · Cited by 863 · see citing works
Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses
Shi, Y., Kirwan, P., Smith, J., Robinson, H. P. C., & Livesey, F. J. (2012) · Nature Neuroscience · doi:10.1038/nn.3041 · Cited by 813 · see citing works
The use of brain organoids to investigate neural development and disease
Di Lullo, E., & Kriegstein, A. R. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.107 · Cited by 788 · see citing works
Self-citationGuided self-organization and cortical plate formation in human brain organoids
Lancaster, M. A., Corsini, N. S., Wolfinger, S., Gustafson, E. H., Phillips, A. W., Burkard, T. R., Otani, T., Livesey, F. J., & Knoblich, J. A. (2017) · Nature Biotechnology · doi:10.1038/nbt.3906 · Cited by 783 · 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
Neural 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
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
Bershteyn, M., Nowakowski, T. J., Pollen, A. A., Di Lullo, E., Nene, A., Wynshaw-Boris, A., & Kriegstein, A. R. (2017) · Cell Stem Cell · doi:10.1016/j.stem.2016.12.007 · Cited by 566 · see citing works
Self-citationDevelopment of cortical folding during evolution and ontogeny
Zilles, K., Palomero‐Gallagher, N., & Amunts, K. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.01.006 · Cited by 552 · see citing works
Growth and folding of the mammalian cerebral cortex: from molecules to malformations
Sun, T., & Hevner, R. F. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3707 · Cited by 471 · see citing works
<i>Drosophila</i> neuroblasts: a model for stem cell biology
Homem, C. C. F., & Knoblich, J. A. (2012) · Development · doi:10.1242/dev.080515 · Cited by 476 · see citing works
Human-Specific NOTCH2NL Genes Expand Cortical Neurogenesis through Delta/Notch Regulation
Suzuki, I. K., Gacquer, D., Van Heurck, R., Kumar, D., Wojno, M., Bilheu, A., Herpoel, A., Lambert, N., Cheron, J., Polleux, F., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.067 · Cited by 471 · 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
Innovation with Limited Resources: Management Lessons from the G erman M ittelstand
Massis, A. D., Audretsch, D. B., Uhlaner, L. M., & Kammerlander, N. H. (2017) · Journal of Product Innovation Management · doi:10.1111/jpim.12373 · Cited by 461 · see citing works
Mitotic Spindle Orientation in Asymmetric and Symmetric Cell Divisions during Animal Development
Morin, X., & Bellaïche, Y. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.06.012 · Cited by 423 · see citing works
Vascularized human cortical organoids (vOrganoids) model cortical development in vivo
Shi, Y., Sun, L., Liu, J., Zhong, S., Wang, M., Li, R., Li, P., Guo, L., Fang, A., Chen, R., et al. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000705 · Cited by 401 · see citing works
Self-citationProliferation control in neural stem and progenitor cells
Homem, C. C. F., Repic, M., & Knoblich, J. A. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn4021 · Cited by 377 · see citing works
Neurogenesis during development of the vertebrate central nervous system
Paridaen, J. T. M. L., & Huttner, W. Β. (2014) · EMBO Reports · doi:10.1002/embr.201438447 · Cited by 390 · 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
Brain organoids for the study of human neurobiology at the interface of in vitro and in vivo
Chiaradia, I., & Lancaster, M. A. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00730-3 · Cited by 343 · see citing works
Fietz, S. A., Lachmann, R., Brandl, H., Kircher, M., Samusik, N., Schröder, R., Lakshmanaperumal, N., Henry, I., Vogt, J., Riehn, A., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209647109 · Cited by 337 · 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
Human cerebral organoids — a new tool for clinical neurology research
Eichmüller, O. L., & Knoblich, J. A. (2022) · Nature Reviews Neurology · doi:10.1038/s41582-022-00723-9 · Cited by 303 · see citing works
Comprehensive cell atlas of the first-trimester developing human brain
Braun, E., Danan-Gotthold, M., Borm, L. E., Vinsland, E., Lee, K. W., Lönnerberg, P., Hu, L., Li, X., He, X., Andrusivová, Ž., et al. (2023) · Science · doi:10.1126/science.adf1226 · Cited by 274 · see citing works
bHLH Factors in Self-Renewal, Multipotency, and Fate Choice of Neural Progenitor Cells
Imayoshi, I., & Kageyama, R. (2014) · Neuron · doi:10.1016/j.neuron.2014.03.018 · Cited by 279 · see citing works
Stahl, R., Walcher, T., Romero, C. D. J., Pilz, G.-A., Cappello, S., Irmler, M., Sanz-Aquela, J. M., Beckers, J., Blum, R., Borrell, V., et al. (2013) · Cell · doi:10.1016/j.cell.2013.03.027 · Cited by 267 · see citing works
Genetic causes of microcephaly and lessons for neuronal development
Gilmore, E. C., & Walsh, C. A. (2012) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.89 · Cited by 244 · see citing works
Deconstructing 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
Decoding the development of the human hippocampus
Zhong, S., Ding, W., Sun, L., Lu, Y., Dong, H., Fan, X., Liu, Z., Chen, R., Zhang, S., Ma, Q., et al. (2020) · Nature · doi:10.1038/s41586-019-1917-5 · Cited by 236 · see citing works
Self-citationMitotic spindle orientation predicts outer radial glial cell generation in human neocortex
Ostrem, B. E. L., Lui, J. H., Hansen, D. V., & Kriegstein, A. R. (2013) · Nature Communications · doi:10.1038/ncomms2647 · Cited by 233 · see citing works
Self-citationHuman 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
Chromatin Remodeling BAF (SWI/SNF) Complexes in Neural Development and Disorders
Sokpor, G., Xie, Y., Rosenbusch, J., & Tuoc, T. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00243 · Cited by 221 · see citing works
Regulation of cerebral cortex size and folding by expansion of basal progenitors
Nonaka‐Kinoshita, M., Reillo, I., Artegiani, B., Ángeles Martínez‐Martínez, M., Nelson, M., Borrell, V., & Calegari, F. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.96 · Cited by 221 · see citing works
Role 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
Shaping Our Minds: Stem and Progenitor Cell Diversity in the Mammalian Neocortex
Franco, S. J., & Müller, U. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.022 · Cited by 219 · see citing works
Neurogenesis at the Brain–Cerebrospinal Fluid Interface
Lehtinen, M. K., & Walsh, C. A. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154026 · Cited by 212 · 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
Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type
Pilz, G.-A., Shitamukai, A., Reillo, I., Pacary, E., Schwausch, J., Stahl, R., Ninkovic, J., Snippert, H. J. G., Clevers, H. C., Godinho, L., et al. (2013) · Nature Communications · doi:10.1038/ncomms3125 · Cited by 212 · see citing works
Martínez-Cerdeño, V., Cunningham, C. L., Camacho, J., Antczak, J. L., Prakash, A. N., Cziep, M. E., Walker, A. I., & Noctor, S. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030178 · Cited by 203 · see citing works
Hedgehog signaling promotes basal progenitor expansion and the growth and folding of the neocortex
Wang, L., Hou, S., & Han, Y.-G. (2016) · Nature Neuroscience · doi:10.1038/nn.4307 · Cited by 190 · see citing works
Zhang, W., Yang, S.-L., Yang, M., Herrlinger, S. A., Shao, Q., Collar, J. L., Fierro, E., Shi, Y., Liu, A., Lü, H., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10497-2 · Cited by 190 · see citing works
Li, J., Pan, L., Pembroke, W. G., Rexach, J. E., Godoy, M. I., Condro, M. C., Alvarado, A. G., Harteni, M., Chen, Y., Stiles, L., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24232-3 · Cited by 187 · see citing works
Emerging roles of neural stem cells in cerebral cortex development and evolution
Borrell, V., & Reillo, I. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22013 · Cited by 185 · see citing works
Cortical neurogenesis in the absence of centrioles
Insolera, R., Bazzi, H., Shao, W., Anderson, K. V., & Shi, S. (2014) · Nature Neuroscience · doi:10.1038/nn.3831 · Cited by 180 · see citing works
Reillo, I., & Borrell, V. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr284 · Cited by 177 · see citing works
Mutations in Eml1 lead to ectopic progenitors and neuronal heterotopia in mouse and human
Kielar, M., Tuy, F. P. D., Bizzotto, S., Lebrand, C., Romero, C. D. J., Poirier, K., Oegema, R., Mancini, G. M. S., Bahi‐Buisson, N., Olaso, R., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3729 · Cited by 174 · see citing works
Guo, C., Eckler, M. J., McKenna, W. L., McKinsey, G. L., Rubenstein, J. L. R., & Chen, B. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.037 · Cited by 170 · see citing works
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
Self-citationA Radial Glia-Specific Role of RhoA in Double Cortex Formation
Cappello, S., Böhringer, C., Bergami, M., Conzelmann, K., Ghanem, A., Tomassy, G. S., Arlotta, P., Mainardi, M., Allegra, M., Caleo, M., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.12.030 · Cited by 171 · see citing works
Postiglione, M. P., Jüschke, C., Xie, Y., Haas, G. A., Charalambous, C., & Knoblich, J. A. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.022 · Cited by 169 · see citing works
Genetics of human brain development
Zhou, Y. F., Song, H., & Ming, G. (2023) · Nature Reviews Genetics · doi:10.1038/s41576-023-00626-5 · Cited by 173 · see citing works
An Adaptive Threshold in Mammalian Neocortical Evolution
Lewitus, É., Kelava, I., Kalinka, A. T., Tomančák, P., & Huttner, W. Β. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1002000 · Cited by 162 · 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
Neural Stem Cells: Historical Perspective and Future Prospects
Breunig, J. J., Haydar, T. F., & RAKIC, P. T. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.005 · Cited by 161 · see citing works
Effects of estradiol in adult neurogenesis and brain repair in zebrafish
Diotel, N., Vaillant, C., Gabbero, C., Mironov, S., Fostier, A., Guéguen, M., Anglade, I., Kah, O., & Pellegrini, E. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.04.003 · Cited by 160 · see citing works
García‐Moreno, F., Vasistha, N. A., Trévia, N., Bourne, J. A., & Molnár, Z. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr312 · Cited by 154 · see citing works
Asymmetric cell division of stem and progenitor cells during homeostasis and cancer
Gómez‐López, S., Lerner, R. G., & Petritsch, C. K. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1386-1 · Cited by 151 · see citing works
Li, R., Sun, L., Fang, A., Li, P., Wu, Q., & Wang, X. (2017) · Protein & Cell · doi:10.1007/s13238-017-0479-2 · Cited by 154 · see citing works
Self-citationThe role of BAF (mSWI/SNF) complexes in mammalian neural development
Son, E., & Crabtree, G. R. (2014) · American Journal of Medical Genetics Part C Seminars in Medical Genetics · doi:10.1002/ajmg.c.31416 · Cited by 151 · see citing works
Integrative Mechanisms of Oriented Neuronal Migration in the Developing Brain
Evsyukova, I. Y., Plestant, C., & Anton, E. S. (2013) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101512-122400 · Cited by 143 · see citing works
Zhang, W., Ma, L., Yang, M., Shao, Q., Xu, J., Lu, Z., Zhao, Z., Chen, R., Chai, Y., & Chen, J. (2020) · Genes & Development · doi:10.1101/gad.332494.119 · Cited by 142 · 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
Self-citationIntermediate progenitors and Tbr2 in cortical development
Hevner, R. F. (2019) · Journal of Anatomy · doi:10.1111/joa.12939 · Cited by 139 · see citing works
Neural Progenitor Cell Terminology
Martínez‐Cerdeño, V., & Noctor, S. C. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00104 · Cited by 141 · see citing works
How Cells Fold the Cerebral Cortex
Borrell, V. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1106-17.2017 · Cited by 139 · see citing works
Cortical Malformations: Lessons in Human Brain Development
Subramanian, L., Calcagnotto, M. E., & Paredes, M. F. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00576 · Cited by 131 · see citing works
OSVZ progenitors in the human cortex: an updated perspective on neurodevelopmental disease
Ostrem, B. E. L., Lui, J. H., Wang, X., & Kriegstein, A. R. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.03.006 · Cited by 130 · see citing works
Self-citationA restricted period for formation of outer subventricular zone defined by Cdh1 and Trnp1 levels
Martínez‐Martínez, M. Á., Romero, C. D. J., Fernández, V., Cárdenas, A., Götz, M., & Borrell, V. (2016) · Nature Communications · doi:10.1038/ncomms11812 · Cited by 129 · see citing works
Mechanisms of radial glia progenitor cell lineage progression
Beattie, R., & Hippenmeyer, S. (2017) · FEBS Letters · doi:10.1002/1873-3468.12906 · Cited by 127 · 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
Regulation of neuronal migration, an emerging topic in autism spectrum disorders
Reiner, O., Karzbrun, E., Kshirsagar, A., & Kaibuchi, K. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13403 · Cited by 123 · see citing works
Human-specific ARHGAP11B induces hallmarks of neocortical expansion in developing ferret neocortex
Kalebic, N., Gilardi, C., Albert, M., Namba, T., Long, K. R., Kostic, M., Langen, B., & Huttner, W. Β. (2018) · eLife · doi:10.7554/elife.41241 · Cited by 129 · see citing works
Cyclin D2 in the basal process of neural progenitors is linked to non‐equivalent cell fates
Tsunekawa, Y., Britto, J. M., Takahashi, M., Polleux, F., Tan, S., & Osumi, N. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.43 · Cited by 124 · see citing works
Abnormal Cell Sorting Underlies the Unique X-Linked Inheritance of PCDH19 Epilepsy
Pederick, D. T., Richards, K., Piltz, S., Kumar, R., Mincheva-Tasheva, S., Mandelstam, S. A., Dale, R. C., Scheffer, I. E., Gécz, J., Petrou, S., et al. (2018) · Neuron · doi:10.1016/j.neuron.2017.12.005 · Cited by 122 · see citing works
Diverse Behaviors of Outer Radial Glia in Developing Ferret and Human Cortex
Gertz, C. C., Lui, J. H., Ostrem, B. E. L., Wang, X., & Kriegstein, A. R. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2645-13.2014 · Cited by 120 · see citing works
Self-citationFunctions of GSK-3 Signaling in Development of the Nervous System
Kim, W. Y., & Snider, W. D. (2011) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2011.00044 · Cited by 121 · 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
Deriving Excitatory Neurons of the Neocortex from Pluripotent Stem Cells
Hansen, D. V., Rubenstein, J. L. R., & Kriegstein, A. R. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.006 · Cited by 116 · see citing works
Self-citationNamba, T., & Huttner, W. Β. (2016) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.256 · Cited by 115 · see citing works
Neuronal migration disorders: Focus on the cytoskeleton and epilepsy
Stouffer, M. A., Golden, J. A., & Francis, F. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.08.003 · Cited by 114 · 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
Control of Outer Radial Glial Stem Cell Mitosis in the Human Brain
Ostrem, B. E. L., Lui, J. H., Gertz, C. C., & Kriegstein, A. R. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.06.058 · Cited by 112 · see citing works
Self-citationOhtaka‐Maruyama, C., & Okado, H. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00447 · Cited by 111 · see citing works
Kyrousi, C., Arbi, M., Pilz, G.-A., Pefani, D., Lalioti, M., Ninkovic, J., Götz, M., Lygerou, Z., & Taraviras, S. L. (2015) · Development · doi:10.1242/dev.126342 · Cited by 109 · 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
Wide dispersion and diversity of clonally related inhibitory interneurons
Harwell, C. C., Fuentealba, L. C., Gonzalez-Cerrillo, A., Parker, P. R. L., Gertz, C. C., Mazzola, E., Garcia, M. T., Alvarez-Buylla, A., Cepko, C. L., & Kriegstein, A. R. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.030 · Cited by 106 · see citing works
Self-citationNeural Progenitor Cell Polarity and Cortical Development
Arai, Y., & Taverna, E. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00384 · Cited by 104 · see citing works
Cortical Gyrification Induced by Fibroblast Growth Factor 2 in the Mouse Brain
Rash, B. G., Tomasi, S., Lim, H., Suh, C. Y., & Vaccarino, F. M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3621-12.2013 · Cited by 103 · see citing works
Beattie, R., Postiglione, M. P., Burnett, L. E., Laukoter, S., Streicher, C., Pauler, F. M., Xiao, G., Klezovitch, O., Vasioukhin, V. I., Ghashghaei, T., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.012 · Cited by 96 · see citing works
Cortical neurogenesis and morphogens: diversity of cues, sources and functions
Tiberi, L., Vanderhaeghen, P., & van den Ameele, J. (2012) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2012.01.010 · Cited by 103 · see citing works
Nelson, B. R., Hodge, R. D., Bedogni, F., & Hevner, R. F. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0791-13.2013 · Cited by 102 · 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
Emerging Roles of Long Non-Coding RNAs as Drivers of Brain Evolution
Zimmer‐Bensch, G. (2019) · Cells · doi:10.3390/cells8111399 · Cited by 98 · 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
Centrosome anchoring regulates progenitor properties and cortical formation
Shao, W., Yang, J., He, M., Yu, X.-Y., Lee, C. H., Yang, Z., Joyner, A. L., Anderson, K. V., Zhang, J., Tsou, M.-F. B., et al. (2020) · Nature · doi:10.1038/s41586-020-2139-6 · Cited by 98 · 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
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
- Authors
- Wang, X., Tsai, J.-W., LaMonica, B., & Kriegstein, A. R.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Wang, Xiaoqun
- Kriegstein, Arnold R
- Venue
- Nature Neuroscience
- Published
- 2011-04-10
- Volume
- 14
- Issue
- 5
- Pages
- 555-561
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3083489
- OpenAlex
- W2072710787
- Cited by
- 507
- References
- 37
- Citations by year
- 2026: 13 · 2025: 24 · 2024: 26 · 2023: 36 · 2022: 29 · 2021: 39 · 2020: 45 · 2019: 42 · 2018: 27 · 2017: 34 · 2016: 19 · 2015: 34 · 2014: 43 · 2013: 50 · 2012: 26
- FWCI
- 14.56
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Bernard Osher Foundation
- National Institute of General Medical Sciences (T32GM007618)
- National Institute of Neurological Disorders and Stroke (R01NS072630, R01NS035710, R01NS021223)
- 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
- outer radial glia, embryonic neocortex, asymmetric cell division, cortical expansion, neurogenesis, mouse brain development
- MeSH terms
- Age Factors, Animals, Cell Differentiation, Cell Division, Cell Movement, Embryo, Mammalian, Luminescent Proteins, Mice, Transgenic, Nerve Tissue Proteins, Neuroglia, Neurons, Organ Culture Techniques, Stem Cells, Time Factors, Centrosome, Gene Expression Regulation, Developmental, Microscopy, Confocal, Neocortex, Green Fluorescent Proteins, Mice
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