Competitive repopulation of an empty microglial niche yields functionally distinct subsets of microglia-like cells
Open accessAbstract
Circulating monocytes can compete for virtually any tissue macrophage niche and become long-lived replacements that are phenotypically indistinguishable from their embryonic counterparts. As the factors regulating this process are incompletely understood, we studied niche competition in the brain by depleting microglia with >95% efficiency using Cx3cr1 CreER/+ R26 DTA/+ mice and monitored long-term repopulation. Here we show that the microglial niche is repopulated within weeks by a combination of local proliferation of CX3CR1 + F4/80 low Clec12a – microglia and infiltration of CX3CR1 + F4/80 hi Clec12a + macrophages that arise directly from Ly6C hi monocytes. This colonization is independent of blood brain barrier breakdown, paralleled by vascular activation, and regulated by type I interferon. Ly6C hi monocytes upregulate microglia gene expression and adopt microglia DNA methylation signatures, but retain a distinct gene signature from proliferating microglia, displaying altered surface marker expression, phagocytic capacity and cytokine production. Our results demonstrate that monocytes are imprinted by the CNS microenvironment but remain transcriptionally, epigenetically and functionally distinct.
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During aging or neurodegeneration, bone marrow-derived blood monocytes can infiltrate the brain through a disrupted blood-brain barrier and differentiate into microglia-like cells.
“Moreover, recent studies have reported that during aging or neurodegeneration, bone marrow-derived blood monocytes can infiltrate the brain through a disrupted blood-brain barrier (BBB) and differentiate into microglia-like cells, exhibiting transcriptional and functional similarity to brain-resident microglia13–15.”
From Somatic cancer variants enriched in Alzheimer’s disease microglia-like cells drive inflammatory and proliferative states (2026) · cites this paper as [13]
The Results and Discussion report that bone marrow-derived monocytes entered the brain and became microglia-like cells after experimental microglial depletion, but explicitly state that engraftment occurred without blood-brain barrier breakdown. The paper does not establish this process during aging or neurodegeneration. (LLM, conf=0.88)
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Experimental — accuracy not yet measuredMonocyte-derived microglia and to a lesser extent HSC-macrophages displayed expression of Sall1 compared to leptomeningeal macrophages.
“Interestingly, MoMg and to a lesser extend HSC-M F displayed expression of Sall1 , as compared to leptomeningeal M F ( Fig. 4f ), suggesting that also engrafted cells in BM chimeras can acquire this proposed 'microglia signature' marker 14,18,19 .”
From Clonal hematopoiesis-associated motoric deficits caused by monocyte-derived microglia accumulating in aging mice (2025) · cites this paper as [19]
The Discussion explicitly states that Sall1 was not expressed in monocyte-derived macrophages, contrary to the claim that monocyte-derived microglia displayed Sall1 expression. The Results section ‘Engrafting macrophages adopt TGF-β driven transcription’ likewise lists Sall1 as an exception among microglia-associated transcription factors detected in engrafting macrophages. Page numbers are not available in the supplied copy. (LLM, conf=0.90)
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Experimental — accuracy not yet measuredMarrow-derived cells may have an ameliorative effect on neurodegenerative phenotypes in mice, possibly due to their superior phagocytic capacity.
“Marrow-derived cells may have an ameliorative effect on neurodegenerative phenotypes in mice33,34, possibly due to their superior phagocytic capacity35.”
From Clonal hematopoiesis is associated with protection from Alzheimer’s disease (2023) · cites this paper as [35]
Experimentally seeded parenchymal brain monocyte-derived macrophages lack expression of Sall1, a proposed hallmark of microglia identity.
“This includes, for instance, lack of expression of the transcriptional repressor Spalt Like Transcription Factor 1 (Sall1), a proposed hallmark of microglia identity 14,18,19 .”
From Clonal hematopoiesis-associated motoric deficits caused by monocyte-derived microglia accumulating in aging mice (2025) · cites this paper as [19]
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- Authors
- Lund, H., Pieber, M., Parsa, R., Han, J., Grommisch, D., Ewing, E., Kular, L., Needhamsen, M., Espinosa, A., Nilsson, E., Överby, A. K., Butovsky, O., Jagodic, M., Zhang, X.-M., & Harris, R. A.
- Affiliations
- Karolinska University Hospital (SE)
- Umeå University (SE)
- Brigham and Women's Hospital (US)
- Corresponding author
- Harris, Robert A.
- ORCID
- Venue
- Nature Communications
- Published
- 2018-11-19
- Volume
- 9
- Issue
- 1
- Pages
- 4845-4845
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC6242869
- OpenAlex
- W2901905540
- Cited by
- 249
- References
- 70
- Citations by year
- 2026: 23 · 2025: 36 · 2024: 39 · 2023: 33 · 2022: 36 · 2021: 26 · 2020: 39 · 2019: 17
- FWCI
- 9.20
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- KTH Publication Database DiVA (KTH Royal Institute of Technology) (submittedVersion, other-oa)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Hjärnfonden
- Karolinska Institutet
- Vetenskapsrådet
- Alzheimerfonden
- Science for Life Laboratory
- Servier
- National Institute of Neurological Disorders and Stroke (R01NS088137)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Keywords
- microglia, niche competition, CX3CR1, CLEC12A, Ly6Chi monocytes, microglia-like cells, type I interferon, DNA methylation, epigenetic imprinting, phagocytosis, microglial proliferation, brain macrophages, vascular activation, blood-brain barrier
- MeSH terms
- CX3C Chemokine Receptor 1, Animals, Antigens, Differentiation, Antigens, Ly, Bacterial Proteins, Bone Marrow Cells, Brain, Gene Expression Regulation, Interferon Type I, Luminescent Proteins, Macrophages, Mice, Transgenic, Monocytes, Phagocytosis, Receptors, Mitogen, Whole-Body Irradiation, Signal Transduction, Microglia, Genes, Reporter, Transplantation Chimera, Cell Lineage, DNA Methylation, Adoptive Transfer, Lectins, C-Type, Cell Proliferation, Green Fluorescent Proteins, Mice
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