High-Dimensional Single-Cell Mapping of Central Nervous System Immune Cells Reveals Distinct Myeloid Subsets in Health, Aging, and Disease
Open accessAbstract
Individual reports suggest that the central nervous system (CNS) contains multiple immune cell types with diverse roles in tissue homeostasis, immune defense, and neurological diseases. It has been challenging to map leukocytes across the entire brain, and in particular in pathology, where phenotypic changes and influx of blood-derived cells prevent a clear distinction between reactive leukocyte populations. Here, we applied high-dimensional single-cell mass and fluorescence cytometry, in parallel with genetic fate mapping systems, to identify, locate, and characterize multiple distinct immune populations within the mammalian CNS. Using this approach, we revealed that microglia, several subsets of border-associated macrophages and dendritic cells coexist in the CNS at steady state and exhibit disease-specific transformations in the immune microenvironment during aging and in models of Alzheimer's disease and multiple sclerosis. Together, these data and the described framework provide a resource for the study of disease mechanisms, potential biomarkers, and therapeutic targets in CNS disease.
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Inflammatory cytokines have been seen previously in a sub-set of microglia in aged C57BL/6 mice.
“inflammatory cytokines have been seen previously in a sub-set of microglia in aged C57BL/6 mice”
From Cross-Species Single-Cell Analysis Reveals Divergence of the Primate Microglia Program (2019) · cites this paper as Mrdjen et al., 2018
The Aging and Neurodegenerative Disease section describes a reactive subset of microglia in geriatric mice, and Figure 5 (p. 389) identifies the mice as C57BL/6. The reported features are surface and activation markers, not inflammatory cytokines detected in those microglia. The Discussion mentions cytokines as possible environmental cues, which does not establish the claimed observation. (LLM, conf=0.88)
Experimental — accuracy not yet measuredCAMs clear harmful substances through phagocytosis, antigen presentation, and cytokine production.
“As immune surveillants, CAMs clear harmful substances through phagocytosis, antigen presentation, and cytokine production [364,368,371,372,373,374,375,376]”
From Revisiting the Pathogenesis of X-Linked Adrenoleukodystrophy (2025) · cites this paper as [368]
The BAM-subsets section (p. 384–385) identifies CNS border-associated macrophages with MHCII expression, a marker relevant to antigen presentation. But the paper does not show BAMs clearing harmful substances by antigen presentation, phagocytosis, or cytokine production; its Discussion describes their functions as subjects for future study. The phagocytosis passage in the Discussion (p. 391) concerns infiltrating monocyte-derived cells, not BAMs. (LLM, conf=0.77)
Experimental — accuracy not yet measuredBAMs display regional heterogeneity and can be classified into multiple subtypes with diverse signatures.
“However, recent studies using high-dimensional single-cell analysis revealed that BAMs display regional heterogeneity and can be classified into multiple subtypes with diverse signatures.515,516”
From Role of neuroinflammation in neurodegeneration development (2023) · cites this paper as [515]
The existence of DAM in mice and humans has recently been confirmed in tauopathy AD models, aging, and other neurodegenerative diseases such as ALS and multiple sclerosis.
“The existence of DAM in mice and humans has recently been confirmed in tauopathy AD models (26, 27), aging (27, 28), and other neurodegenerative diseases, such as amyotrophic lateral sclerosis (ALS) (29) and multiple sclerosis (30).”
From Therapeutic Idol reduction ameliorates amyloidosis and improves cognitive function in APP/PS1 mice (2020) · cites this paper as [27]
Perivascular macrophages belong to CNS border-associated macrophages (CAMs).
“They belong to CNS border-associated macrophages (CAMs) [367,368].”
From Revisiting the Pathogenesis of X-Linked Adrenoleukodystrophy (2025) · cites this paper as [368]
A subset of tissue-resident macrophages co-expresses Lyve1, Fcna, and Cd38.
“Recent reports have characterized gene expression in tissue-resident immune cells and found that Lyve1 and Fcna are expressed along with Cd38 by a subset of tissue-resident macrophages37,38”
From Senescent cells promote tissue NAD+ decline during ageing via the activation of CD38+ macrophages (2020) · cites this paper as [38]
The dural compartment of the meninges is closest to the skull and is predominantly composed of fibroblasts, but also includes fenestrated blood vasculature, an elaborate lymphatic system, and immune cells distinct from the CNS.
“The dural compartment of the meninges, closest to the skull, is predominantly composed of fibroblasts, but also includes fenestrated blood vasculature, an elaborate lymphatic system, as well as immune cells which are distinct from the CNS.”
From Living on the Edge of the CNS: Meninges Cell Diversity in Health and Disease (2021) · cites this paper as Mrdjen et al., 2018
High-dimensional single-cell cytometry found that all microglia are homogenously affected in neuroinflammatory diseases.
“a study that employed high-dimensional single-cell cytometry to characterize myeloid subsets in the brain in health, ageing and in mouse models of AD and multiple sclerosis (MS) found that all microglia are homogenously affected in neuroinflammatory diseases61.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [61]
This suggests a switch from homeostatic to reactive microglial state in a plaque-associated population.
“This suggests a switch from homeostatic to reactive microglial state in specific population associated with amyloid plaques [46].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [46]
In APP/PS1 and 5XFAD AD mouse models, a subset of plaque-associated microglia has elevated Galectin-3 and CLEC7A and reduced P2RY12.
“In mouse models of AD such as amyloid precursor protein (APP)/presenilin-1 (PS1) and 5XFAD transgenic mice, there is a subset of microglia surrounding amyloid plaques with elevated phagocytic and microglial activation markers including Galectin-3 and CLEC7A, and reduced expression of homeostatic markers such as P2RY12.”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [46]
This morphology indicates microglial response to protein accumulation or increased inflammatory mediators.
“indicating microglial response to protein accumulation or increased inflammatory mediators [41, 46-48].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [46]
In AD brains, microglia surrounding amyloid plaques have activated amoeboid morphology with enlarged soma and retracted processes.
“In AD brains, microglia surrounding amyloid plaques display activated amoeboid morphologies with enlarged soma and retracted processes, indicating microglial response to protein accumulation or increased inflammatory mediators [41, 46-48].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [46]
Losses of homeostatic function are not unique to microglia in ND and are seen in the context of aging.
“These losses of homeostatic function are also not unique to microglia in ND and are seen in the context of aging [44,60,61,77,82].”
From Untangling senescent and damage‐associated microglia in the aging and diseased brain (2023) · cites this paper as [82]
Several publications within the last 2 years have employed scRNAseq and mass cytometry of microglia and other CNS immune cells to understand global alterations in immunological gene expression and dynamic changes in immune cell-type abundance as a function of brain anatomy, aging, and neurodegeneration.
“Several publications within the last 2 years have begun to employ scRNAseq and mass cytometry of microglia and other CNS immune cells as ways to understand (i) global alterations in immunological gene expression and (ii) dynamic changes in immune cell-type abundance as a function of brain anatomy, aging, and neurodegeneration (87, 95, 107, 108).”
From The Transcriptional Landscape of Microglial Genes in Aging and Neurodegenerative Disease (2019) · cites this paper as [108]
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Basal lamina changes in neurodegenerative disorders
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Plaque-associated myeloid cells derive from resident microglia in an Alzheimer's disease model
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Self-citationDissecting the human leptomeninges at single-cell resolution
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“Based on previous studies 31,32 , we compiled a panel of surface-receptor antibodies to capture the major immune cell lineages ( Supplementary Table 1 ).”
Method
- Authors
- Mrdjen, D., Pavlovic, A., Hartmann, F. J., Schreiner, B., Utz, S. G., Leung, B. P., Lelios, I., Heppner, F. L., Kipnis, J., Merkler, D., Greter, M., & Becher, B.
- Affiliations
- University of Zurich (CH)
- Charité – Universitätsmedizin Berlin (DE)
- University of Virginia (US)
- University of Geneva (CH)
- Corresponding author
- Becher, Burkhard
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2018-02
- Volume
- 48
- Issue
- 2
- Pages
- 380-395.e6
- ISSN
- 1074-7613 (ISSN-L)
- OpenAlex
- W2787171652
- Cited by
- 1,010
- References
- 74
- Citations by year
- 2026: 102 · 2025: 110 · 2024: 106 · 2023: 130 · 2022: 144 · 2021: 165 · 2020: 112 · 2019: 82 · 2018: 55 · 2012: 1
- FWCI
- 46.43
- Type
- journal article
- Language
- en
- Update notices
- erratum (2018-03-20)
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by-nc-nd)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by-nc-nd)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Swiss national science foundation (PP00P3_144781, 310030_146130, 316030_150768, 310030_170320)
- European Union
- University Priority Project Translational Cancer Research
- National Science Foundation Graduate Research Fellowship Program (DGE1418060)
- Forschungskredit
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Keywords
- microglia, border-associated macrophages, dendritic cells, Alzheimer's disease, multiple sclerosis, immune microenvironment, leukocyte infiltration, genetic fate mapping, single-cell mass cytometry
- MeSH terms
- Aging, Animals, Central Nervous System, Dendritic Cells, Leukocytes, Macrophages, Mice, Inbred C57BL, Microglia, Neurodegenerative Diseases, Mice, Single-Cell Analysis
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