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Increased post-mitotic senescence in aged human neurons is a pathological feature of Alzheimer’s disease
Open accessAbstract
The concept of senescence as a phenomenon limited to proliferating cells has been challenged by growing evidence of senescence-like features in terminally differentiated cells, including neurons. The persistence of senescent cells late in life is associated with tissue dysfunction and increased risk of age-related disease. We found that Alzheimer's disease (AD) brains have significantly higher proportions of neurons that express senescence markers, and their distribution indicates bystander effects. AD patient-derived directly induced neurons (iNs) exhibit strong transcriptomic, epigenetic, and molecular biomarker signatures, indicating a specific human neuronal senescence-like state. AD iN single-cell transcriptomics revealed that senescent-like neurons face oncogenic challenges and metabolic dysfunction as well as display a pro-inflammatory signature. Integrative profiling of the inflammatory secretome of AD iNs and patient cerebral spinal fluid revealed a neuronal senescence-associated secretory phenotype that could trigger astrogliosis in human astrocytes. Finally, we show that targeting senescence-like neurons with senotherapeutics could be a strategy for preventing or treating AD.
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“However, features of premature senescence associated particularly with DNA double-strand breaks (DSBs) and p16 expression also have been described in post-mitotic cells such as neurons[16, 18, 29].”
From Characterisation of premature cell senescence in Alzheimer's disease using single nuclear transcriptomics (2024) · cites this paper as [29]
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“but no AD hallmark neuropathology was shown.”
From Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming (2024) · cites this paper as [24]
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“These severely affected donors had lower transcription and reduced chromatin accessibility that may correspond to senescent states97, or global epigenome dysregulation that is indicative of cell identity loss98.”
From Integrated multimodal cell atlas of Alzheimer’s disease (2024) · cites this paper as [97]
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“Recent studies have directly induced neurons from individuals with AD through NGN2/ASCL1 overexpression.”
From Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming (2024) · cites this paper as [24]
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“These neurons exhibited several age-associated dysregulations such as instability of mature neuronal fate, increased cellular senescence, and metabolic shifts (11, 24, 25)”
From Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming (2024) · cites this paper as [24]
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Metadata
- Authors
- Herdy, J. R., Traxler, L., Agarwal, R. K., Karbacher, L., Schlachetzki, J. C. M., Boehnke, L., Zangwill, D., Galasko, D., Glass, C. K., Mertens, J., & Gage, F. H.
- Affiliations
- Salk Institute for Biological Studies (US)
- Universität Innsbruck (AT)
- University of California San Diego (US)
- Corresponding author
- Herdy, Joseph R.
- Gage, Fred H.
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2022-12
- Volume
- 29
- Issue
- 12
- Pages
- 1637-1652.e6
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- PMC
- PMC10093780
- OpenAlex
- W4310496865
- Cited by
- 208
- References
- 79
- Citations by year
- 2026: 59 · 2025: 63 · 2024: 63 · 2023: 23
- FWCI
- 23.04
- 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, 365 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)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Michael J. Fox Foundation for Parkinson's Research
- California Institute for Regenerative Medicine
- American Heart Association (H2020, 19PABH134610000, 19PABHI34610000)
- BrightFocus Foundation (A2019562S, ERC-STG-2019-852086, H2020-MSCA-IF-2017-797205)
- Waitt Foundation
- European Commission (H2020-MSCA-IF-2017., H2020, 797205, H2020‐MSCA‐IF, H2020-MSCA)
- Austrian Science Fund (FWF-I5057)
- National Institutes of Health (P30 014195, RT2-01927, 1s10od023689-01a1, H2020, AG062429, AG051449)
- University of California, San Diego
- Horizon 2020 Framework Programme (H2020-MSCA, H2020-MSCA-IF-2017)
- National Institute on Aging (K99AG056679, R01AG056306, R01AG057706, R01AG056511, T32AG000216, P30AG062429, RF1AG056306, P01AG051449, R37AG072502)
- National Cancer Institute (S10-OD023689, P30014195)
- National Institute of General Medical Sciences (T32GM007198)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- neuronal senescence, Alzheimer's disease, senescence-associated secretory phenotype, senotherapeutics, astrocyte activation, neuroinflammation, senescence markers
- MeSH terms
- Aged, Alzheimer Disease, Astrocytes, Brain, Humans, Neurons, Oncogenes
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