An intrinsic mechanism of corticogenesis from embryonic stem cells
Open accessAbstract
The cerebral cortex develops through the coordinated generation of dozens of neuronal subtypes, but the mechanisms involved remain unclear. Here we show that mouse embryonic stem cells, cultured without any morphogen but in the presence of a sonic hedgehog inhibitor, recapitulate in vitro the major milestones of cortical development, leading to the sequential generation of a diverse repertoire of neurons that display most salient features of genuine cortical pyramidal neurons. When grafted into the cerebral cortex, these neurons develop patterns of axonal projections corresponding to a wide range of cortical layers, but also to highly specific cortical areas, in particular visual and limbic areas, thereby demonstrating that the identity of a cortical area can be specified without any influence from the brain. The discovery of intrinsic corticogenesis sheds new light on the mechanisms of neuronal specification, and opens new avenues for the modelling and treatment of brain diseases.
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Human cortical pyramidal neurons develop along a prolonged neotenic timescale when xenotransplanted in the fast-developing mouse cortex, pointing to cell-intrinsic mechanisms.
“Human cortical pyramidal neurons (CPNs) develop along a prolonged neotenic timescale when xenotransplanted in the fast-developing mouse cortex, pointing to cell-intrinsic mechanisms.15,16,17,18,19,20”
From Synaptic neoteny of human cortical neurons requires species-specific balancing of SRGAP2-SYNGAP1 cross-inhibition (2024) · cites this paper as [16]
The ‘Cortical axonal projections of ESC neurons’ section describes mouse embryonic-stem-cell-derived cortical neurons grafted into neonatal mouse cortex, and reports evidence for intrinsic corticogenesis. It does not study human neurons transplanted into mice or show that they retain a prolonged neotenic developmental timescale. (LLM, conf=0.86)
Experimental — accuracy not yet measuredMouse neurons transplanted in the mouse cortex mature in only a few weeks as the host cortical neurons.
“This is in stark contrast to mouse neurons transplanted in the mouse cortex, which mature in only a few weeks as the host cortical neurons”
From Xenotransplanted human cortical neurons reveal species-specific development and functional integration into mouse visual circuits (2019) · cites this paper as Gaspard et al., 2008
The ‘Cortical axonal projections of ESC neurons’ section reports that ESC-derived mouse neurons grafted into neonatal mouse cortex displayed landmarks of mature pyramidal neurons after one month. It compares their projections with endogenous cortical projections, but does not show that the grafted neurons matured at the same rate as host cortical neurons. (LLM, conf=0.84)
Experimental — accuracy not yet measuredHuman xenotransplanted CPNs from 2 to 18 months post-transplantation revealed a much more protracted pattern of dendritic spine development than mouse CPNs, confirming cell-intrinsic neuronal neoteny.
“Similar analysis of dendritic spine development in human xenotransplanted CPNs (from 2 to 18 MPT) revealed a much more protracted pattern, confirming the cell-intrinsic neuronal neoteny described previously.15,16,17,18,20”
From Synaptic neoteny of human cortical neurons requires species-specific balancing of SRGAP2-SYNGAP1 cross-inhibition (2024) · cites this paper as [16]
The ‘Cortical axonal projections of ESC neurons’ section describes mouse embryonic-stem-cell-derived neurons grafted into neonatal mice and examined after one month. The ‘Neural differentiation’ section discusses dendrite orientation, not spine development. Searches for human xenotransplanted neurons, the 2–18-month comparison, and neuronal neoteny found no passage addressing the attributed claim. (LLM, conf=0.76)
Experimental — accuracy not yet measuredTransplanted human neurons develop more slowly than similarly transplanted mouse neurons.
“transplanted human neurons develop more slowly than similarly transplanted mouse neurons”
From Xenotransplanted human cortical neurons reveal species-specific development and functional integration into mouse visual circuits (2019) · cites this paper as Gaspard et al., 2008
The “Cortical axonal projections of ESC neurons” section describes neurons grafted into neonatal mice and assessed after one month, but it does not compare transplanted human and mouse neurons. A search for human neurons and species-specific developmental timing found no passage addressing that comparison; page numbers were not available in our copy. (LLM, conf=0.76)
Experimental — accuracy not yet measured
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Self-citationEspuny-Camacho, I., Michelsen, K. A., Linaro, D., Bilheu, A., Acosta-Verdugo, S., Herpoel, A., Giugliano, M., Gaillard, A., & Vanderhaeghen, P. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.04.094 · Cited by 88 · see citing works
Self-citationRosebrock, D., Arora, S., Mutukula, N., Volkman, R., Gralinska, E., Balaskas, A., Aragonés Hernández, A., Buschow, R., Brändl, B., Müller, F.-J., et al. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00929-5 · Cited by 89 · 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
Self-citationOptimizing neuronal differentiation from induced pluripotent stem cells to model ASD
Kim, D.-S., Ross, P. J., Zaslavsky, K., & Ellis, J. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00109 · Cited by 70 · see citing works
Cortical neurogenesis from pluripotent stem cells: complexity emerging from simplicity
Anderson, S., & Vanderhaeghen, P. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.03.012 · Cited by 40 · see citing works
Self-citationGenome engineering of stem cell organoids for disease modeling
Sun, Y., & Ding, Q. (2017) · Protein & Cell · doi:10.1007/s13238-016-0368-0 · Cited by 39 · see citing works
Laminar fate specification in the cerebral cortex
Gaspard, N., & Vanderhaeghen, P. (2011) · F1000 Biology Reports · doi:10.3410/b3-6 · Cited by 36 · see citing works
Self-citationFrom Human Pluripotent Stem Cells to Cortical Circuits
Astick, M., & Vanderhaeghen, P. (2018) · Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2018.02.011 · Cited by 34 · see citing works
Self-citationMetabolic mechanisms of species-specific developmental tempo
Iwata, R., & Vanderhaeghen, P. (2024) · Developmental Cell · doi:10.1016/j.devcel.2024.05.027 · Cited by 32 · see citing works
Self-citationCTNND2 moderates the pace of synaptic maturation and links human evolution to synaptic neoteny
Assendorp, N., Fossati, M., Libé-Philippot, B., Christopoulou, E., Depp, M., Rapone, R., Dingli, F., Loew, D., Vanderhaeghen, P., & Charrier, C. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114797 · Cited by 32 · see citing works
Self-citationAdvances in Cerebral Organoid Systems and their Application in Disease Modeling
Liu, F., Huang, J., Zhang, L., Chen, J., Zeng, Y., Tang, Y., & Liu, Z. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2018.12.013 · Cited by 27 · see citing works
Libé-Philippot, B., Iwata, R., Recupero, A. J., Wierda, K., Bernal Garcia, S., Hammond, L., van Benthem, A., Limame, R., Ditkowska, M., Beckers, S., et al. (2024) · Neuron · doi:10.1016/j.neuron.2024.08.021 · Cited by 22 · see citing works
Self-citationChoi, J., Park, S., & Sockanathan, S. (2014) · Development · doi:10.1242/dev.104505 · Cited by 19 · see citing works
Biphasic cell cycle defect causes impaired neurogenesis in down syndrome
Sharma, V., Nehra, S., Do, L. H., Ghosh, A., Deshpande, A. J., & Singhal, N. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.1007519 · Cited by 14 · see citing works
- Authors
- Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., van den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., Schiffmann, S. N., Gaillard, A., & Vanderhaeghen, P.
- Affiliations
- Université Libre de Bruxelles (BE)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Vanderhaeghen, Pierre
- ORCID
- Venue
- Nature
- Published
- 2008-08-17
- Volume
- 455
- Issue
- 7211
- Pages
- 351-357
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2159884201
- Cited by
- 641
- References
- 47
- Citations by year
- 2026: 12 · 2025: 25 · 2024: 23 · 2023: 21 · 2022: 35 · 2021: 43 · 2020: 39 · 2019: 57 · 2018: 35 · 2017: 45 · 2016: 34 · 2015: 25 · 2014: 42 · 2013: 53 · 2012: 50
- FWCI
- 10.28
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- ORBi (University of Liège) (submittedVersion, other-oa)
- HAL (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion, other-oa)
- Lirias (submittedVersion)
- Funders
- Fonds De La Recherche Scientifique - FNRS
- Centre National de la Recherche Scientifique
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- cortical development, embryonic stem cells, neuronal specification, cortical pyramidal neurons, axonal projections, cortical layers, visual cortex, limbic cortex, in vitro neuronal differentiation
- MeSH terms
- Animals, Axons, Cell Differentiation, Cerebral Cortex, Veratrum Alkaloids, Pyramidal Cells, Cell Lineage, Mice, Embryonic Stem Cells
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