Early stem cell aging in the mature brain
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Abstract
Stem cell dysfunction drives many age-related disorders. Identifying mechanisms that initially compromise stem cell behavior represent early targets to promote tissue function later in life. Here, we pinpoint multiple factors that disrupt neural stem cell (NSC) behavior in the adult hippocampus. Clonal tracing showed that NSCs exhibit asynchronous depletion by identifying short-term NSCs (ST-NSCs) and long-term NSCs (LT-NSCs). ST-NSCs divide rapidly to generate neurons and deplete in the young brain. Meanwhile, multipotent LT-NSCs are maintained for months but are pushed out of homeostasis by lengthening quiescence. Single-cell transcriptome analysis of deep NSC quiescence revealed several hallmarks of molecular aging in the mature brain and identified tyrosine-protein kinase Abl1 as an NSC aging factor. Treatment with the Abl inhibitor imatinib increased NSC activation without impairing NSC maintenance in the middle-aged brain. Our study indicates that hippocampal NSCs are particularly vulnerable and adaptable to cellular aging.
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In the mouse brain, single-cell RNA-seq analyses indicate that the number of activated neural stem cells (NSCs) and neuroblasts decreases with ageing in both the subventricular zone (SVZ) NSC niche and the hippocampal NSC niche.
“For example, in the mouse brain, single-cell RNA-seq analyses indicate that the number of activated neural stem cells (NSCs) and neuroblasts (progeny) decreases with ageing in both the subventricular zone (SVZ) NSC niche and the hippocampal NSC niche6–9 — the main locations of NSCs.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [9]
Lineage tracing uncovered a subset of early-declining NSCs in the hippocampal neurogenic niche.
“Lineage tracing uncovered a subset of early-declining NSCs in the hippocampal neurogenic niche9.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [9]
Activated NSCs exhibit fewer overall transcriptomic changes with ageing than quiescent NSCs.
“Interestingly, activated NSCs exhibit fewer overall transcriptomic changes with ageing than quiescent NSCs6–9,63,64, perhaps because activated NSCs are recently generated and do not have the time to accumulate damage, or because they ‘dilute’ the damage as they proliferate.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [9]
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Regulation of neurogenesis in the adult and aging brain
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Stem cells: Aging and transcriptional fingerprints
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Expression of Cre recombinase in dopaminoceptive neurons
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Function and Dysfunction of Adult Hippocampal Neurogenesis in Regeneration and Disease
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Ageing and rejuvenation of tissue stem cells and their niches
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- Authors
- Ibrayeva, A., Bay, M., Pu, E., Jörg, D. J., Peng, L., Jun, H., Zhang, N., Aaron, D., Lin, C., Resler, G., Hidalgo, A., Jang, M.-H., Simons, B. D., & Bonaguidi, M. A.
- Affiliations
- University of Southern California (US)
- University of Cambridge (GB)
- Mayo Clinic (US)
- Corresponding author
- Bonaguidi, Michael A.
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2021-05
- Volume
- 28
- Issue
- 5
- Pages
- 955-966.e7
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- PMC
- PMC10069280
- OpenAlex
- W3153549711
- Cited by
- 137
- References
- 112
- Citations by year
- 2026: 14 · 2025: 29 · 2024: 25 · 2023: 37 · 2022: 21 · 2021: 9 · 2020: 1 · 2019: 1
- FWCI
- 8.31
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 370 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell stem cell (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Apollo (University of Cambridge) (submittedVersion, cc-by-nc-nd)
- Apollo
- Funders
- University of South China
- University of Southern California
- Donald E. and Delia B. Baxter Foundation
- National Institutes of Health (R00NS080913, R56AG064077)
- L. K. Whittier Foundation
- Eli and Edythe Broad Foundation (RO1AG0585560)
- Wellcome Trust (098357/Z/12/Z)
- AFAR
- Royal Society (RP\R1\180165)
- American Foundation for Aging Research (T32HD060549-08)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- neural stem cells, stem cell aging, hippocampus, stem cell quiescence, stem cell depletion, imatinib, clonal tracing, single-cell transcriptomics, age-related neurodegeneration
- MeSH terms
- Brain, Hippocampus, Cellular Senescence, Neurogenesis, Neural Stem Cells
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.
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