Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage
Abstract
The developing central nervous system of vertebrates contains an abundant cell type designated radial glial cells. These cells are known as guiding cables for migrating neurons, while their role as precursor cells is less clear. Since radial glial cells express a variety of astroglial characteristics and differentiate as astrocytes after completing their guidance function, they have been considered as part of the glial lineage. Using fluorescence-activated cell sorting, we show here that radial glial cells also are neuronal precursors and only later, after neurogenesis, do they shift towards an exclusive generation of astrocytes. These results thus demonstrate a novel function for radial glial cells, namely their ability to generate two major cell types found in the nervous system, neurons and astrocytes.
Integrity signals
Registry
Cites
Statistics
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?
After symmetric divisions, radial glia divide asymmetrically, generating postmitotic excitatory neurons that migrate to their final location in the cerebral cortex by using the basal process of the radial glial cell as a scaffold.
“After this period of symmetric divisions, these progenitor cells — also known as radial glia — divide asymmetrically, generating postmitotic excitatory neurons that will migrate to their final location in the cerebral cortex by using the basal process of the radial glial cell as a scaffold55–58.”
From Consequences of trisomy 21 for brain development in Down syndrome (2024) · cites this paper as [57]
Cites
Subventricular zone astrocytes are neural stem cells in the adult mammalian brain
Doetsch, F., Caillé, I., Lim, D. A., García-Verdugo, J. M., & Alvarez-Buylla, A. (1999) · Cell · doi:10.1016/s0092-8674(00)80783-7 · Cited by 3,898 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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-citationNeurons 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
Astrocytes give rise to new neurons in the adult mammalian hippocampus
Seri, B., Garcı́a-Verdugo, J. M., McEwen, B. S., & Alvarez-Buylla, A. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07153.2001 · Cited by 1,495 · see citing works
Normal development of brain circuits
Tau, G. Z., & Peterson, B. S. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.115 · Cited by 1,391 · 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
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
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
Middeldorp, J., & Hol, E. M. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.01.005 · Cited by 1,080 · see citing works
Origin of oligodendrocytes in the subventricular zone of the adult brain
Menn, B., Garcia-Verdugo, J. M., Yaschine, C., Gonzalez-Perez, O., Rowitch, D., & Alvarez-Buylla, A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1299-06.2006 · Cited by 972 · see citing works
Development of the human cerebral cortex: Boulder Committee revisited
Bystron, I., Blakemore, C., & Rakic, P. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2252 · Cited by 977 · 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
Adult Ependymal Cells Are Postmitotic and Are Derived from Radial Glial Cells during Embryogenesis
Spassky, N., Merkle, F. T., Flames, N., Tramontin, A. D., García-Verdugo, J. M., & Alvarez-Buylla, A. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1108-04.2005 · Cited by 717 · 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
Cell-cycle control and cortical development
Dehay, C., & Kennedy, H. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2097 · Cited by 655 · see citing works
The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord
Deneen, B., Ho, R., Lukaszewicz, A., Hochstim, C. J., Gronostajski, R. M., & Anderson, D. J. (2006) · Neuron · doi:10.1016/j.neuron.2006.11.019 · Cited by 514 · see citing works
The Indispensable Roles of Microglia and Astrocytes during Brain Development
Reemst, K., Noctor, S. C., Lucassen, P. J., & Hol, E. M. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00566 · Cited by 516 · 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
Hochgerner, H., Zeisel, A., Lönnerberg, P., & Linnarsson, S. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0056-2 · Cited by 482 · see citing works
Hypothalamic tanycytes: a key component of brain-endocrine interaction
RODRIGUEZ, E., BLAZQUEZ, J., PASTOR, F., PELAEZ, B., PENA, P., PERUZZO, B., & AMAT, P. (2005) · International review of cytology · doi:10.1016/s0074-7696(05)47003-5 · Cited by 475 · see citing works
Potential for neural regeneration after neurotoxic injury in the adult mammalian retina
Ooto, S., Akagi, T., Kageyama, R., Akita, J., Mandai, M., Honda, Y., & Takahashi, M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402129101 · Cited by 454 · see citing works
Mori, T., Tanaka, K., Buffo, A., Wurst, W., Kühn, R., & Götz, M. (2006) · Glia · doi:10.1002/glia.20350 · Cited by 398 · see citing works
Self-citationGenerating Neuronal Diversity in the Mammalian Cerebral Cortex
Lodato, S., & Arlotta, P. (2015) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100814-125353 · Cited by 389 · see citing works
G1 Phase Regulation, Area-Specific Cell Cycle Control, and Cytoarchitectonics in the Primate Cortex
Lukaszewicz, A., Savatier, P., Cortay, V., Giroud, P., Huissoud, C., Berland, M., Kennedy, H., & Dehay, C. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.032 · Cited by 315 · see citing works
Anatomy of zebrafish cerebellum and screen for mutations affecting its development
Bae, Y.-K., Kani, S., Shimizu, T., Tanabe, K., Nojima, H., Kimura, Y., Higashijima, S.-I., & Hibi, M. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.04.013 · Cited by 293 · see citing works
Specific synapses develop preferentially among sister excitatory neurons in the neocortex
Yu, Y.-C., Bultje, R. S., Wang, X., & Shi, S.-H. (2009) · Nature · doi:10.1038/nature07722 · Cited by 305 · see citing works
Pucilowska, J., Vithayathil, J., Tavares, E. J., Kelly, C., Karlo, J. C., & Landreth, G. E. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.4864-13.2015 · Cited by 207 · 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
Chai, X., Förster, E., Zhao, S., Bock, H. H., & Frotscher, M. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2934-08.2009 · Cited by 202 · see citing works
Cortical and Clonal Contribution of Tbr2 Expressing Progenitors in the Developing Mouse Brain
Vasistha, N. A., García-Moreno, F., Arora, S., Cheung, A. F. P., Arnold, S. J., Robertson, E. J., & Molnár, Z. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhu125 · Cited by 177 · see citing works
Stancik, E. K., Navarro-Quiroga, I., Sellke, R., & Haydar, T. F. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.6131-09.2010 · Cited by 186 · 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
Adult neurogenesis and cellular brain repair with neural progenitors, precursors and stem cells
Shivraj Sohur, U., Emsley, J. G., Mitchell, B. D., & Macklis, J. D. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1887 · Cited by 170 · see citing works
González, M., Cabrera‐Socorro, A., Pérez‐García, C. G., Fraser, J. D., López, F. J., Alonso, R., & Meyer, G. (2007) · Journal of Comparative Neurology · doi:10.1002/cne.21419 · Cited by 167 · see citing works
Regulation of cerebral cortical neurogenesis by the Pax6 transcription factor
Manuel, M. N., Mi, D., Mason, J. O., & Price, D. J. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00070 · Cited by 153 · see citing works
Emerging topics in Reelin function
Förster, E., Bock, H. H., Herz, J., Chai, X., Frotscher, M., & Zhao, S. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07222.x · Cited by 130 · see citing works
Reelin in the years: controlling neuronal migration and maturation in the mammalian brain
D'Arcangelo, G. (2014) · Advances in Neuroscience · doi:10.1155/2014/597395 · Cited by 120 · see citing works
Radial glia cells in the developing human brain
Howard, B. M., Mo, Z., Filipovic, R., Moore, A. R., Antic, S. D., & Zecevic, N. (2008) · The Neuroscientist · doi:10.1177/1073858407313512 · Cited by 97 · see citing works
Distinct Lineage-Dependent Structural and Functional Organization of the Hippocampus
Xu, H.-T., Han, Z., Gao, P., He, S., Li, Z., Shi, W., Kodish, O., Shao, W., Brown, K. N., Huang, K., et al. (2014) · Cell · doi:10.1016/j.cell.2014.03.067 · 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
Prospective isolation of adult neural stem cells from the mouse subependymal zone
Fischer, J., Beckervordersandforth, R., Tripathi, P., Steiner-Mezzadri, A., Ninkovic, J., & Götz, M. (2011) · Nature Protocols · doi:10.1038/nprot.2011.412 · Cited by 71 · see citing works
Self-citationThe G protein-coupled receptor GPRC5B contributes to neurogenesis in the developing mouse neocortex
Kurabayashi, N., Nguyen, M. D., & Sanada, K. (2013) · Development · doi:10.1242/dev.099754 · Cited by 46 · see citing works
Jaber, S. M., Bordt, E. A., Bhatt, N. M., Lewis, D. M., Gerecht, S., Fiskum, G., & Polster, B. M. (2018) · Neurochemistry International · doi:10.1016/j.neuint.2017.09.003 · Cited by 40 · see citing works
Micali, N., Kim, S.-K., Diaz-Bustamante, M., Stein-O’Brien, G., Seo, S., Shin, J.-H., Rash, B. G., Ma, S., Wang, Y., Olivares, N. A., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107599 · Cited by 31 · see citing works
Consequences of trisomy 21 for brain development in Down syndrome
Russo, M. L., Sousa, A. M. M., & Bhattacharyya, A. (2024) · Nature Reviews Neuroscience · doi:10.1038/s41583-024-00866-2 · Cited by 28 · see citing works
Zhang, J., Argueta, D., Tong, X., Vinters, H. V., Mathern, G. W., & Cepeda, C. (2025) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1486315 · Cited by 3 · see citing works
- Authors
- Malatesta, P., Hartfuss, E., & Götz, M.
- Affiliations
- Max Planck Institute of Neurobiology (DE)
- Corresponding author
- Götz, Magdalena
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2000-12-15
- Volume
- 127
- Issue
- 24
- Pages
- 5253-5263
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2168945089
- Cited by
- 1,157
- References
- 1
- Citations by year
- 2026: 16 · 2025: 22 · 2024: 29 · 2023: 24 · 2022: 27 · 2021: 28 · 2020: 47 · 2019: 38 · 2018: 29 · 2017: 29 · 2016: 43 · 2015: 42 · 2014: 56 · 2013: 58 · 2012: 49
- FWCI
- 12.08
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Development (publishedVersion)
- PubMed (publishedVersion)
- CINECA IRIS Institutial Research Information System (University of Genoa) (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
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- radial glia, neuronal lineage, neuronal precursors, astrocyte differentiation, glial lineage, neurogenesis, central nervous system development
- MeSH terms
- Animals, Astrocytes, Cell Differentiation, Cell Separation, Cerebral Cortex, Flow Cytometry, Glial Fibrillary Acidic Protein, Luminescent Proteins, Male, Mice, Inbred C57BL, Mice, Transgenic, Neuroglia, Neurons, Promoter Regions, Genetic, Recombinant Proteins, Stem Cells, Rats, Wistar, ATP-Binding Cassette Transporters, Amino Acid Transport System X-AG, Green Fluorescent Proteins, Mice, Rats
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