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Embryonic Origin of Postnatal Neural Stem Cells
Open accessAbstract
Adult neural stem/progenitor (B1) cells within the walls of the lateral ventricles generate different types of neurons for the olfactory bulb (OB). The location of B1 cells determines the types of OB neurons they generate. Here we show that the majority of mouse B1 cell precursors are produced between embryonic days (E) 13.5 and 15.5 and remain largely quiescent until they become reactivated postnatally. Using a retroviral library carrying over 100,000 genetic tags, we found that B1 cells share a common progenitor with embryonic cells of the cortex, striatum, and septum, but this lineage relationship is lost before E15.5. The regional specification of B1 cells is evident as early as E11.5 and is spatially linked to the production of neurons that populate different areas of the forebrain. This study reveals an early embryonic regional specification of postnatal neural stem cells and the lineage relationship between them and embryonic progenitor cells.
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“Adult V-SVZ NSCs are set aside during embryogenesis, remaining largely quiescent until adulthood (Fuentealba et al., 2015; Furutachi et al., 2015), and reside in a complex microenvironment comprising diverse cell types and local and long-range signals (Silva-Vargas et al., 2013).”
From Single-Cell Analysis of Regional Differences in Adult V-SVZ Neural Stem Cell Lineages (2019) · cites this paper as Fuentealba et al., 2015
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Will a mAb-Based Immunotherapy Directed against Cancer Stem Cells Be Feasible?
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“Recent advances on adult neurogenesis demonstrate that neural stem cells (NSCs) at the subventricular zone (SVZ) are largely derived during mid-embryonic neurogenesis from a subset of cells, which slow down in their pace of cell division,(1) become quiescent cells and can be reactivated in need.(2) The NSCs at birth c…”
BackgroundRevisit the Candidacy of Brain Cell Types as the Cell(s) of Origin for Human High-Grade Glioma
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“Moreover, consistent with the embryonic origin of adult NSPCs (Fuentealba et al., 2015; Furutachi et al., 2015), many of the cellular and molecular mechanisms controlling adult neurogenesis are notably similar to those acting during development but often display contextual differences (for review; Lim and AlvarezBuyll…”
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An epigenetic circuit controls neurogenic programs during neocortex development
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“Indeed, during embryonic forebrain neurogenesis neural stem cells are set aside and do not participate in the massive proliferation and differentiation that leads to the development of structures like the cortex, the basal ganglia, or the septum (Fuentealba et al., 2015).”
BackgroundDNA Damage-p53/P21 Response Contributes to Ependymal Cell Development
Ortiz-Álvarez, G., Fortoul, A., Srivastava, A., Moreau, M. X., Bouloudi, B., Mailhes‐Hamon, C., Delgehyr, N., Faucourt, M., Bahin, M., Blugeon, C., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2022.111810 · Cited by 18
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InfluentialEnriched expression of the ciliopathy gene Ick in cell proliferating regions of adult mice
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BackgroundThyroid hormone action in adult neurogliogenic niches: the known and unknown
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Brockman, A. A., Mobley, B. C., & Ihrie, R. A. (2021) · Journal of Histochemistry & Cytochemistry · doi:10.1369/00221554211032003 · Cited by 14
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BackgroundImported Stem Cells Strike against Stroke
Péron, S., & Berninger, B. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.10.006 · Cited by 14
“…5, 2015 ª2 SVZ-derived NSCs or local astrocytes and their progenies using ‘‘confetti’’ mice (Calzolari et al., 2015) or viral barcoding techniques (Fuentealba et al., 2015) could resolve the relative importance of invading versus resident cells as source of scar-forming RAs in vivo and…”
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Syndecan-1 Stimulates Adult Neurogenesis in the Mouse Ventricular-Subventricular Zone after Injury
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A Spacetime Odyssey of Neural Progenitors to Generate Neuronal Diversity
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Transcriptional regulation of adult neural stem/progenitor cells: tales from the subventricular zone
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“In the SVZ, we found CAR in two different cell populations: in SOX2, GFAP and nestin cells, which is consistent with expression of CAR in stem cells and type B1 cells (Codega et al., 2014; Fuentealba et al., 2015; Llorens-Bobadilla et al., 2015), and DCX cells, which correspond to type A or neuroblasts (reviewed by Mi…”
BackgroundChongtham, M. C., Wang, H., Christina Thaller, B., Hsiao, N., Vachkov, I. H., Pavlov, S., Williamson, L. H., Yamashima, T., Stoykova, A., Yan, J., et al. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.584314 · Cited by 13
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“In lateral ventricles, RGC give rise to B1 and ependymal cells (Fuentealba et al., 2015).”
BackgroundHomemade: building the structure of the neurogenic niche
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From Vessels to Neurons—The Role of Hypoxia Pathway Proteins in Embryonic Neurogenesis
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“The embryonic NPCs also contain a subpopulation of dividing cells that persists beyond the perinatal period and give rise to the adult progenitor cells of the subependymal SVZ [81,82] (Figure 1E).”
BackgroundA Thymic Epithelial Stem Cell Pool Persists throughout Ontogeny and Is Modulated by TGF-β
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“A study lends support to this notion by demonstrating that fetal and adult neural SCs have a common origin in early embryonic development (Fuentealba et al., 2015).”
ResultTaking Advantage of Nature’s Gift: Can Endogenous Neural Stem Cells Improve Myelin Regeneration?
Akkermann, R., Jadasz, J. J., Azim, K., & Küry, P. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17111895 · Cited by 12
“5, and these cells are activated in postnatal life [59].”
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Fine-tuned Rest: Unveiling the Regulatory Landscape of Adult Quiescent Neural Stem Cells
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Neural stem cell heterogeneity in adult hippocampus
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“5) until adulthood (Fuentealba et al. 2015; Furutachi et al. 2015).”
Environmental Enrichment Induces Meningeal Niche Remodeling through TrkB-Mediated Signaling
Zorzin, S., Corsi, A., Ciarpella, F., Bottani, E., Dolci, S., Malpeli, G., Pino, A., Amenta, A., Fumagalli, G. F., Chiamulera, C., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910657 · Cited by 10
rAAV2-Mediated Restoration of GALC in Neural Stem Cells from Krabbe Patient-Derived iPSCs
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“NSCs could release several trophic factors into the microenvironment and restore neuronal cell populations [20,21].”
BackgroundSpecific Methyl-CpG Configurations Define Cell Identity through Gene Expression Regulation
Improda, T., Morgera, V., Vitale, M., Chiariotti, L., Passaro, F., Feola, A., Porcellini, A., Cuomo, M., & Pezone, A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24129951 · Cited by 11
Postnatal Neural Stem Cells: Probing Their Competence for Cortical Repair
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“In the case of the V-SVZ, a fraction of forebrain radial glial cells (RGCs) in the lateral ganglionic eminences (LGEs) and pallium becomes quiescent (Young et al., 2007; Fuentealba et al., 2015).”
BackgroundHaemmerle, C. A. D. S., Nogueira, M. I., & Watanabe, I. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00134 · Cited by 10
“…brain are B1- astrocytes (Doetsch et al., 1999), which remain active in the adult V-SVZ; similar to B1 cells, radial astrocytes remain actives in the subgranular zone of dentate gyrus (Morshead et al., 1994; Doetsch et al., 1999; Kriegstein and Alvarez-Buylla, 2009; Fuentealba et al., 2012, 2015).”
BackgroundMethodInfluentialLee, K. H., Nam, H., Jeong, D. E., Kim, S., Song, H. J., Pyeon, H., Kang, K., Hong, S., Nam, D., & Joo, K. M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0158639 · Cited by 10
Singular Adult Neural Stem Cells Do Not Exist
Petřík, D., Jörgensen, S. K. M., Eftychidis, V., & Siebzehnrübl, F. A. (2022) · Cells · doi:10.3390/cells11040722 · Cited by 13
“5 in mice, radial glia cells from the ventricular zone, which act as Pax6+ embryonic neural stem cells [35], give rise to aNSCs of the adult SVZ [36,37].”
BackgroundLineage hierarchies and stochasticity ensure the long-term maintenance of adult neural stem cellsPreprint
Than‐Trong, E., Kiani, B., Dray, N., Ortica, S., Simons, B. D., Rulands, S., Alunni, A., & Bally‐Cuif, L. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/663922 · Cited by 10
Nanoparticle and Stem Cell Combination Therapy for the Management of Stroke
Salatin, S., Farhoudi, M., Sadigh‐Eteghad, S., & Farjami, A. (2022) · Current Pharmaceutical Design · doi:10.2174/1381612829666221213113119 · Cited by 9
Huang, H., Wang, N., Lin, J.-T., Qiu, Y.-K., Wu, W.-F., Liu, Q., Chen, C., Wang, H., Liu, Y., Dong, W., et al. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-03921-2 · Cited by 9
Angelova, A., Platel, J., Béclin, C., Cremer, H., & Coré, N. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24621 · Cited by 9
Sánchez‐González, R., Figueres‐Oñate, M., Ojalvo‐Sanz, A. C., & López‐Mascaraque, L. (2020) · Genes · doi:10.3390/genes11030305 · Cited by 12
“These interneurons arise from progenitors located within the ganglionic eminences that migrate tangentially to their destination in the OB [8,9].”
BackgroundNam, H.-S., & Capecchi, M. R. (2023) · Neural Development · doi:10.1186/s13064-022-00169-1 · Cited by 9
Aberrations of Genomic Imprinting in Glioblastoma Formation
Lozano-Ureña, A., Jiménez-Villalba, E., Pinedo‐Serrano, A., Jordán‐Pla, A., Kirstein, M., & Ferrón, S. R. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.630482 · Cited by 9
“5 and remain largely quiescent until they become reactivated postnatally (34, 35).”
BackgroundThe Adult Neurogenesis Theory of Alzheimer’s Disease
Abbate, C. (2023) · Journal of Alzheimer s Disease · doi:10.3233/jad-221279 · Cited by 11
TIMP3 promotes the maintenance of neural stem-progenitor cells in the mouse subventricular zone
Fang, L., Kuniya, T., Harada, Y., Yasuda, O., Maeda, N., Suzuki, Y., Kawaguchi, D., & Gotoh, Y. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1149603 · Cited by 8
Spatial transcriptomics map of the embryonic mouse brain – a tool to explore neurogenesis
Marco, B. D., Vázquez-Marín, J., Monyer, H., Centanin, L., & Alfonso, J. (2023) · Biology Open · doi:10.1242/bio.060151 · Cited by 8
Foucault, L., Capeliez, T., Angonin, D., Lentini, C., Bezin, L., Heinrich, C., Parras, C. M., Donega, V., Marcy, G., & Raineteau, O. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113734 · Cited by 8
“29 Labeling and fate mapping of cycling cells was performed using single or repeated BrdU (or EdU) injections at E13 and E15 and between P3 to P11 as well as between P11 to P12.”
Ouzikov, S., Edwards, K. M., Anandampillai, T., Watanabe, S., Casasbuenas, D. L., Siu, K. K. W., Harkins, D., Dou, A., Jeong, D., Lee, J. E., et al. (2024) · Communications Biology · doi:10.1038/s42003-024-06524-8 · Cited by 8
“Secondly,westainedolfactorybulbsectionsfromthesemiceformarkersof olfactorybulb(OB)interneuronsCalbindin(CalB)andCalretinin(CalR) whicharederivedfromNSCsintheventralanddorsalareasoftheV-SVZ, respectively 7,25 (Fig.”
Lahti, L., Volakakis, N., Gillberg, L., Salmani, B. Y., Tiklová, K., Kee, N., Lundén-Miguel, H., Werkman, M. H., Piper, M., Gronostajski, R. M., et al. (2025) · Development · doi:10.1242/dev.204421 · Cited by 8
Distinct Developmental Features of Olfactory Bulb Interneurons.
Kim, J. Y., & Choe, J. (2020) · Europe PMC (PubMed Central) · doi:10.14348/molcells.2020.0033 · Cited by 8
“1 (Fuentealba et al., 2015).”
BackgroundInfluentialTracing and tracking epiallele families in complex DNA populations
Pezone, A., Tramontano, A., Scala, G., Cuomo, M., Riccio, P., Nicola, S. M. D., Porcellini, A., Chiariotti, L., & Avvedimento, E. V. (2020) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqaa096 · Cited by 8
“Supplementary Table S4 shows the comparison of MethCoresProfiler with existing tools currently used for methylation analysis of bisulfite sequencing data (26) (see Supplementary Figures S4A and S5C).”
BackgroundMethodThe imaging features and prognosis of gliomas involving the subventricular zone: An MRI study
Zhao, K., Liu, R., Li, Z., Liu, M., Zhao, Y., Xue, Z., Wu, W., Sun, G., & Xu, B. (2022) · Clinical Neurology and Neurosurgery · doi:10.1016/j.clineuro.2022.107465 · Cited by 8
Maintenance of neural stem cell regional identity in culture
Delgado, R. N., Lu, C., & Lim, D. A. (2016) · Neurogenesis · doi:10.1080/23262133.2016.1187321 · Cited by 8
“Recent studies find that after they are generated in the embryo, B1 cell precursors remain quiescent until postnatal life.(15) It is therefore conceivable that the persistence of NKX2.”
BackgroundInfluentialNeuronal Stem Cell Niches of the Brain
Conover, J. C., & Todd, K. L. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-802734-9.00006-8 · Cited by 7
RB: An essential player in adult neurogenesis
Fong, B. C., & Slack, R. S. (2017) · Neurogenesis · doi:10.1080/23262133.2016.1270382 · Cited by 8
“They are believed to originate embryonically, whether during mid-development for slowly-dividing SVZ qNSCs.(8,9) or late development for SGZ qNSCs, in advance of postnatal SGZ formation(10,11) These quiescent cells undergo reversible transition into an activated state, which is believed to be mediated by factors inclu…”
BackgroundWang, X., Qu, L., Chen, J., Hu, K., Zhou, Z., Zhang, J., An, Y., & Zheng, J. (2024) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2024.116567 · Cited by 7
Addressing the Effect of Exercise on Glial Cells: Focus on Ependymal Cells
Maugeri, G., Amato, A., Evola, G., D’Agata, V., & Musumeci, G. (2024) · Journal of Integrative Neuroscience · doi:10.31083/j.jin2312216 · Cited by 7
“Interestingly, in the adult ventricular-subventricular zone, ependymal cells act as a source of niche factors modulating neural stem cell (NSC) function thanks to their close contact with B1 cells [53], a subtype of astroglial cells that retain NSC properties [54].”
Significance of birth in the maintenance of quiescent neural stem cells
Kawase, K., Nakamura, Y., Wolbeck, L., Takemura, S., Zaitsu, K., Ando, T., Jinnou, H., Sawada, M., Nakajima, C., Rydbirk, R., et al. (2025) · Science Advances · doi:10.1126/sciadv.adn6377 · Cited by 7
“Because the majority of postnatal NSCs are maintained in a quiescent state, they can be maintained long term ( 6 , 7 ).”
Chicheportiche, A., Ruat, M., Boussin, F. D., & Daynac, M. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-7371-2_5 · Cited by 7
Cell-autonomous role of GFRα1 in the development of olfactory bulb GABAergic interneurons
Zechel, S., Fernández‐Suárez, D., & Ibáñez, C. F. (2018) · Biology Open · doi:10.1242/bio.033753 · Cited by 7
“B cells) are produced during midembryogenesis, and remain quiescent until they become reactivated postnatally (Fuentealba et al., 2015).”
Płatek, R., Rogujski, P., Mazuryk, J., Wisniewska, M. B., Kaczmarek, L., & Czupryn, A. (2022) · Cells · doi:10.3390/cells11010135 · Cited by 8
SETD4 cells contribute to brain development and maintain adult stem cell reservoir for neurogenesis
Cai, S.-L., Yang, Y.-S., Ding, Y.-F., Yang, S., Jia, X.-Z., Gu, Y.-W., Wood, C., Huang, X.-T., Yang, J., & Yang, W. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.07.017 · Cited by 7
“5, which can then persist for a long period into the adult SVZ (Fuentealba et al., 2015; Furutachi et al., 2015).”
BackgroundTracing the developmental origin of tissue stem cells
Morita, R., & Fujiwara, H. (2022) · Development Growth & Differentiation · doi:10.1111/dgd.12816 · Cited by 6
“Thus, the DNA label-retaining technique was employed to detect and fate map slow-dividing cells during brain development (Fuentealba et al., 2015; Furutachi et al., 2015).”
BackgroundMethodmiR-17∼92 exerts stage-specific effects in adult V-SVZ neural stem cell lineages
Favaloro, F., DeLeo, A. M., Delgado, A. C., & Doetsch, F. K. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111773 · Cited by 7
Kolaj, A., Zahr, S. K., Wang, B. S., Krawec, T., Kazan, H., Yang, G., Kaplan, D. R., & Miller, F. D. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112242 · Cited by 8
Metadata
- Authors
- Fuentealba, L. C., Rompani, S. B., Parraguez, J. I., Obernier, K., Romero, R., Cepko, C. L., & Alvarez-Buylla, A.
- Affiliations
- University of California, San Francisco (US)
- Howard Hughes Medical Institute (US)
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2015-06
- Volume
- 161
- Issue
- 7
- Pages
- 1644-1655
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4475276
- OpenAlex
- W1617074755
- Cited by
- 488
- References
- 55
- Citations by year
- 2026: 22 · 2025: 38 · 2024: 29 · 2023: 43 · 2022: 43 · 2021: 51 · 2020: 62 · 2019: 58 · 2018: 45 · 2017: 47 · 2016: 35 · 2015: 15
- FWCI
- 19.14
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Helen Hay Whitney Foundation
- Deutsche Forschungsgemeinschaft
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (R37NS028478, NS-28478, R01NS028478)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD32116, R37HD032116, R01HD032116)
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- neural stem cells, neural progenitor cells, olfactory bulb, lateral ventricle, embryonic origin, regional specification, lineage tracing, quiescence, forebrain development, striatum, septum, cortex
- MeSH terms
- Animals, Embryo, Mammalian, Olfactory Bulb, Prosencephalon, Cell Lineage, Mice, Adult Stem Cells, Neural Stem Cells
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