Replacement of microglia in the aged brain reverses cognitive, synaptic, and neuronal deficits in mice
Open accessAbstract
Microglia, the resident immune cell of the brain, can be eliminated via pharmacological inhibition of the colony‐stimulating factor 1 receptor (CSF1R). Withdrawal of CSF1R inhibition then stimulates microglial repopulation, effectively replacing the microglial compartment. In the aged brain, microglia take on a “primed” phenotype and studies indicate that this coincides with age‐related cognitive decline. Here, we investigated the effects of replacing the aged microglial compartment with new microglia using CSF1R inhibitor‐induced microglial repopulation. With 28 days of repopulation, replacement of resident microglia in aged mice (24 months) improved spatial memory and restored physical microglial tissue characteristics (cell densities and morphologies) to those found in young adult animals (4 months). However, inflammation‐related gene expression was not broadly altered with repopulation nor the response to immune challenges. Instead, microglial repopulation resulted in a reversal of age‐related changes in neuronal gene expression, including expression of genes associated with actin cytoskeleton remodeling and synaptogenesis. Age‐related changes in hippocampal neuronal complexity were reversed with both microglial elimination and repopulation, while microglial elimination increased both neurogenesis and dendritic spine densities. These changes were accompanied by a full rescue of age‐induced deficits in long‐term potentiation with microglial repopulation. Thus, several key aspects of the aged brain can be reversed by acute noninvasive replacement of microglia.
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Under normal conditions microglia sculpt neuronal brain connections, and increased phagocytic activity by PU.1 overexpression may result in elevated removal of dendritic spines contributing to neuronal loss in disease.
“On the other hand, under normal conditions microglia sculpt neuronal brain connections and increased phagocytic activity by PU.1 overexpression may result in elevated removal of dendritic spines contributing to neuronal loss in disease based on studies of microglia depletion in mouse models (Elmore et al., 2018).”
From Alzheimer's-associated PU.1 expression levels regulate microglial inflammatory response (2021) · cites this paper as Elmore et al., 2018
The Results section (page unavailable) reports that microglial elimination increased dendritic spine density in aged mice and that replacement microglia sculpted the synaptic landscape. The paper does not connect PU.1 overexpression to increased phagocytosis, excess spine removal, or neuronal loss in disease. (LLM, conf=0.88)
Experimental — accuracy not yet measuredRestoring microglial phagocytosis is therapeutically important.
“Many studies have underscored the therapeutic importance of restoring microglial phagocytosis (54–56).”
From Reducing microglial lipid load enhances β amyloid phagocytosis in an Alzheimer’s disease mouse model (2025) · cites this paper as [56]
The Introduction (page unavailable) describes impaired phagocytosis as an age-related microglial change and suggests that microglial replacement may benefit impaired brain function. The Results (page unavailable) report improved spatial memory after replacement in aged mice, but do not show that phagocytosis was restored or that its restoration produced the benefit. The paper therefore supports the therapeutic potential of microglial replacement, not the specific claim about restoring phagocytosis. (LLM, conf=0.82)
Experimental — accuracy not yet measuredMicroglial repopulation after depletion reversed age-related deficits in long-term potentiation as initial elimination of microglia increased neurogenesis and dendritic spine densities.
“Moreover, microglial repopulation after depletion reversed age-related deficits in long-term potentiation as initial elimination of microglia increased neurogenesis and dendritic spine densities (Elmore et al., 2018).”
From Alzheimer's-associated PU.1 expression levels regulate microglial inflammatory response (2021) · cites this paper as Elmore et al., 2018
Previous studies identified the capacity of microglia to repopulate following experimental depletion in healthy, aged, irradiated, or neurodegenerating brain, but this feature can also serve to reinstate microglia after naturally occurring death following white matter injury, while regulating microglia activation.
“Although previous studies identified the capacity of microglia to repopulate following experimental depletion in healthy13–15, aged17, irradiated18, or neurodegenerating brain19, we show that this feature can also serve to reinstate microglia after naturally occurring death following white matter injury, while regulating microglia activation.”
From Central nervous system regeneration is driven by microglia necroptosis and repopulation (2019) · cites this paper as [17]
Microglia interact with and modulate neuronal and synaptic elements, with direct effects on learning and memory.
“evidence indicates that these cells interact with and modulate neuronal and synaptic elements, with direct effects on learning and memory [14], [15], [16], [17], [18], [19].”
From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [15]
Microglia can be indefinitely depleted via the continued administration of CSF1R inhibitors, and the microglial compartment can also be repopulated upon CSF1R inhibitor withdrawal.
“While microglia can be indefinitely depleted via the continued administration of CSF1R inhibitors, the microglial compartment can also be repopulated upon CSF1R inhibitor withdrawal17,40,41.”
From Sustained microglial depletion with CSF1R inhibitor impairs parenchymal plaque development in an Alzheimer’s disease model (2019) · cites this paper as [40]
Microglial repopulation in naturally aged mice led to a rescue in age-related cognitive, synaptic, and neuronal deficits.
“For example, microglial repopulation in naturally aged mice led to a rescue in age-related cognitive, synaptic and neuronal deficits [71].”
From Untangling senescent and damage‐associated microglia in the aging and diseased brain (2023) · cites this paper as [71]
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- Authors
- Elmore, M. R. P., Hohsfield, L. A., Kramár, E. A., Soreq, L., Lee, R. J., Pham, S. T., Najafi, A. R., Spangenberg, E. E., Wood, M. A., West, B. L., & Green, K. N.
- Affiliations
- University of California, Irvine (US)
- The Francis Crick Institute (GB)
- Plexxikon (United States) (US)
- Corresponding author
- Green, Kim N.
- Venue
- Aging Cell
- Publisher
- Wiley
- Published
- 2018-10-02
- Volume
- 17
- Issue
- 6
- Pages
- e12832-e12832
- ISSN
- 1474-9718 (ISSN-L)
- 1474-9726
- PMC
- PMC6260908
- OpenAlex
- W2894787694
- Cited by
- 380
- References
- 48
- Citations by year
- 2026: 36 · 2025: 39 · 2024: 50 · 2023: 67 · 2022: 57 · 2021: 49 · 2020: 56 · 2019: 25 · 2018: 1
- FWCI
- 14.63
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Aging Cell (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- National Institute on Aging (AG016573, AG00096)
- Glenn Family Foundation
- National Institute of Neurological Disorders and Stroke (R01NS083801)
- Alzheimer's Association (AARF-16-442762)
- American Foundation for Aging Research
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
- Keywords
- microglia, microglial repopulation, CSF1R inhibition, brain aging, age-related cognitive decline, spatial memory, hippocampus, synaptogenesis, actin cytoskeleton remodeling, dendritic spines, neurogenesis, long-term potentiation, neuroinflammation, neuronal gene expression
- MeSH terms
- Aging, Animals, Cell Count, Cognition, Cytoskeleton, Gene Expression Regulation, Inflammation, Lipopolysaccharides, Male, Mice, Inbred C57BL, Neurons, Synapses, Receptors, Granulocyte-Macrophage Colony-Stimulating Factor, Microglia, Long-Term Potentiation, Cell Shape, Dendritic Spines, Neurogenesis
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