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A single-cell atlas of mouse brain macrophages reveals unique transcriptional identities shaped by ontogeny and tissue environment
Open accessAbstract
While the roles of parenchymal microglia in brain homeostasis and disease are fairly clear, other brain-resident myeloid cells remain less well understood. By dissecting border regions and combining single-cell RNA-sequencing with high-dimensional cytometry, bulk RNA-sequencing, fate-mapping and microscopy, we reveal the diversity of non-parenchymal brain macrophages. Border-associated macrophages (BAMs) residing in the dura mater, subdural meninges and choroid plexus consisted of distinct subsets with tissue-specific transcriptional signatures, and their cellular composition changed during postnatal development. BAMs exhibited a mixed ontogeny, and subsets displayed distinct self-renewal capacity following depletion and repopulation. Single-cell and fate-mapping analysis both suggested that there is a unique microglial subset residing on the apical surface of the choroid plexus epithelium. Finally, gene network analysis and conditional deletion revealed IRF8 as a master regulator that drives the maturation and diversity of brain macrophages. Our results provide a framework for understanding host-macrophage interactions in both the healthy and diseased brain.
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“Our consensus exAM signature does overlap with the dissociation signature in the study by Van Hove et al.[43] (19 of 25 genes in consensus exAM list; Supplementary Tables 4, 5 and 21a).”
From Dissection of artifactual and confounding glial signatures by single-cell sequencing of mouse and human brain (2022) · cites this paper as Van Hove et al.[43]
In the citing paper
“Consistent with the reports from other tissues in mice, we found that typical enzymatic digestion of mouse brain tissue induced a host of transcriptional alterations34,43,44,65.”
From Dissection of artifactual and confounding glial signatures by single-cell sequencing of mouse and human brain (2022) · cites this paper as [43]
In the citing paper
“However, emerging results from other tissues/cell types have begun to characterize dissociation artifacts following enzymatic digestion43–45,65,66.”
From Dissection of artifactual and confounding glial signatures by single-cell sequencing of mouse and human brain (2022) · cites this paper as [43]
In the citing paper
“No explicit statistical methods were used to predetermine sample sizes but our sample sizes exceed those reported in previous publications32,34,43.”
From Dissection of artifactual and confounding glial signatures by single-cell sequencing of mouse and human brain (2022) · cites this paper as [43]
In the citing paper
“This molecule likely also affects BAMs, as reported in the case of PLX3397 [317], placing an important caveat on the interpretation of data where PLX5622 is assumed to be purely microglia-specific.”
From Microglia and monocytes in inflammatory CNS disease: integrating phenotype and function (2022) · cites this paper as [317]
In the citing paper
“Although microglia represent a heterogeneous cell population [46], they still share several expression profiles with primitive and adult macrophages, including IBA1.”
From The Cuprizone Model: Dos and Do Nots (2020) · cites this paper as [46]
In the citing paper
“In the Aging Mouse Brain Single Cell Portal, Plcg2 expression is highest in microglia and brain macrophages, with lower levels in endothelial cells and oligodendrocyte precursor cells and minimal to no expression in neurons, astrocytes, and mature oligodendrocytes [30, 72–74].”
From PLCγ2 deficiency compromises systemic immune tolerance and erodes myelin homeostasis while enhancing oxidative metabolism in the mouse brain (2026) · cites this paper as [74]
In the citing paper
“In the Brain Immune Atlas aggregate of CD45+ cells from brain and meningeal regions, Plcg2 transcripts are detected in 18% of immune cells across parenchymal microglia and multiple border-associated macrophage (BAM) subsets, with choroid plexus surface and dural BAMs contributing many Plcg2+ cells and a small B-cell cluster displaying the highest per-cell Plcg2 expression in the dataset [74].”
From PLCγ2 deficiency compromises systemic immune tolerance and erodes myelin homeostasis while enhancing oxidative metabolism in the mouse brain (2026) · cites this paper as [74]
In the citing paper
“We identified a classical monocyte cluster that highly express Ly6c2, and a non-classical monocyte cluster highly express Itgal, similarly as a published single cell RNA-seq study.88”
From TET2-mutant myeloid cells mitigate Alzheimer’s disease progression via CNS infiltration and enhanced phagocytosis in mice (2025) · cites this paper as [88]
In the citing paper
“In addition, we confirmed previous findings of elevated expression of lipid-related genes in BAMs (31) and observed an increase in LD content within these cells over time and during disease progression.”
From Reducing microglial lipid load enhances β amyloid phagocytosis in an Alzheimer’s disease mouse model (2025) · cites this paper as [31]
In the citing paper
“MHCII+ macrophages are most abundant in the choroid plexus and meninges [37], and we similarly observe widespread uptake of L2-siRNA in this population (Fig. 5F).”
From Elucidating brain transport pathways and cell type-dependent gene silencing of a durable lipid–siRNA conjugate administered into cerebrospinal fluid (2025) · cites this paper as [37]
In the citing paper
“MHCII+ macrophages are most abundant in the choroid plexus and meninges,43 and we similarly observe widespread uptake of L2-siRNA in this population (Fig. 5F).”
From Lipid-siRNA conjugate accesses a perivascular transport mechanism and achieves widespread and durable knockdown in the central nervous system (2024) · cites this paper as [43]
In the citing paper
“The yolk sac-derived precursors of resident macrophages are only in the perivascular compartment [360,361], where they maintain their cellular origin in adulthood [362,363,364].”
From Revisiting the Pathogenesis of X-Linked Adrenoleukodystrophy (2025) · cites this paper as [364]
In the citing paper
“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 [364]
In the citing paper
“CD38 expression was associated with neuroinflammation with greater amounts of proinflammatory macrophages/microglia in mouse brains160,165.”
From NAD+ metabolism and its roles in cellular processes during ageing (2021) · cites this paper as [165]
In the citing paper
“This contrasts with macrophages in the choroid plexus and dura mater, which do turn over and receive some input from peripheral blood monocytes during adulthood (71-73).”
From The anatomy and immunology of vasculature in the central nervous system (2019) · cites this paper as [73]
In the citing paper
“Like microglia, most macrophages residing in the leptomeninges and perivascular spaces are derived from early yolk sac–derived erythromyeloid progenitors, and during steady state, these cells have minimal turnover.”
From The anatomy and immunology of vasculature in the central nervous system (2019) · cites this paper as [73]
In the citing paper
“On the basis of high-parameter mass cytometry and single-cell RNA-sequencing studies, the dural macrophages appear to be distinct from those residing in the pia and underlying parenchyma (73, 94).”
From The anatomy and immunology of vasculature in the central nervous system (2019) · cites this paper as [73]
In the citing paper
“The macrophages expressed markers of border associated macrophages (BAMs) (e.g., Apoe, Ms4a7, Ms4a6c) recently identified in periluminal regions, meninges, and ChP (Van Hove et al., 2019).”
From A cellular and spatial map of the choroid plexus across brain ventricles and ages (2021) · cites this paper as Van Hove et al., 2019
In the citing paper
“Similarly, we found a subset of macrophages expressing markers previously defined as subdural-specific BAMs (e.g., Lyve1, Ednrb, Colec12; Van Hove et al., 2019) that were enriched in embryonic ChP macrophages in our dataset (Figure S5H).”
From A cellular and spatial map of the choroid plexus across brain ventricles and ages (2021) · cites this paper as Van Hove et al., 2019
In the citing paper
“However, in contrast to Van Hove et al., our data revealed that this separation was age-dependent and potentially represented a maturation-dependent shift from MHC IIlow to MHC IIhigh (Figure 5I, S5I,J, Table S6).”
From A cellular and spatial map of the choroid plexus across brain ventricles and ages (2021) · cites this paper as Van Hove et al., 2019
In the citing paper
“In agreement with recent reports (Van Hove et al., 2019), we found diversity within the BAMs, which segregated into two subsets defined as major histocompatibility complex (MHC) class IIlow and MHC IIhigh.”
From A cellular and spatial map of the choroid plexus across brain ventricles and ages (2021) · cites this paper as Van Hove et al., 2019
In the citing paper
“These maturation dependent changes agree with a recent report of BAMs (Van Hove et al., 2019).”
From A cellular and spatial map of the choroid plexus across brain ventricles and ages (2021) · cites this paper as Van Hove et al., 2019
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“Similar findings have been shown in tissues such as the spleen, brain, skin, and intestine 19,23,24 .”
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“Using the expression of previously described cell-type specific markers 11,14–16 we could identify epithelial cells, endothelial cells, pericyte-like cells, macrophages and a mix of immune cells.”
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“…based on the following observations: (i) genes universally upregulated in these macrophage populations are associated with blood vessel development [35]; (ii) perivascular macrophages, together with laminin-containing basement membranes, form a vascular barrier in the rat area postrema [36]; (iii)…”
Strehle, J., Somnuke, P., Li, S., Wang, S., Hirnet, T., Wang, Y., & Schäfer, M. K. E. (2025) · Acta Neuropathologica Communications · doi:10.1186/s40478-025-02156-z · Cited by 9
Eme‐Scolan, E., Gomes, M., Bani, A., Romano, A., Kassem, O., Roussel‐Queval, A., Casel, B., Slimani, L., Lawrence, T., & Rua, R. (2025) · Immunity · doi:10.1016/j.immuni.2025.11.019 · Cited by 11
Li, T., Zhang, J., Song, H., Zhang, R., Fan, F., Huang, Z., Zeng, M., Peng, B., & Zhang, J. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03631-z · Cited by 11
Trained immunity in acute and chronic neurological diseases
Zhang, S., & Liesz, A. (2026) · eLife · doi:10.7554/elife.106037 · Cited by 7
“While perivascular and subdural macrophages are long-lived and do not rely on replenishment from bone marrow-derived monocytes, choroid plexus BAMs are gradually replaced by bone marrow-derived precursors ( Utz et al., 2020 ; Van Hove et al., 2019 ).”
Neuroinflammation in stroke—A review of implications for precision immunomodulation
Zharikova, T. M., Petrova, E. A., Makarov, I., Preobrazhenskaya, U., Pontes-Silva, A., & Zharikov, Y. (2026) · Neuroscience · doi:10.1016/j.neuroscience.2026.03.054 · Cited by 7
Yoon, J. K., Schindler, J. W., Loperfido, M., Baricordi, C., DeAndrade, M. P., Jacobs, M. E., Treleaven, C. M., Plasschaert, R. N., Yan, A., Barese, C. N., et al. (2024) · Molecular Therapy · doi:10.1016/j.ymthe.2024.09.024 · Cited by 7
Nör, C., Kharas, K., Rasnitsyn, A., Vladoiu, M. C., Cho, N. W., Young, J. S., Nör, F., Mankahla, N., Haapasalo, J. A., Nordfors, K., et al. (2025) · Developmental Cell · doi:10.1016/j.devcel.2025.06.016 · Cited by 7
New advances in immune components mediating viral control in the CNS
Vincenti, I., & Merkler, D. (2021) · Current Opinion in Virology · doi:10.1016/j.coviro.2021.02.001 · Cited by 6
Innate and adaptive immune mechanisms regulating central nervous system remyelination
Creswell, R., & Dombrowski, Y. (2022) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2021.12.002 · Cited by 6
Li, H., Hu, M., Huang, Z., Wang, Y., Xu, Y., Deng, J., Zhu, M., Feng, W., & Xu, X. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1056447 · Cited by 6
Li, H., Yu, S., Liu, H., Chen, L., Liu, H., Liu, X., & Shen, C. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1274982 · Cited by 6
Bone marrow-derived myeloid progenitors in the leptomeninges of adult mice
Koeniger, T., Bell, L., Mifka, A., Enders, M., Hautmann, V., Mekala, S. R., Kirchner, P., Ekici, A. B., Schulz, C., Wörsdörfer, P., et al. (2020) · Stem Cells · doi:10.1002/stem.3311 · Cited by 6
New Insights in the Complexity and Functionality of the Neurovascular Unit
Schaffenrath, J., & Keller, A. (2020) · Handbook of experimental pharmacology · doi:10.1007/164_2020_424 · Cited by 8
Microbial and immune factors regulate brain maintenance and aging
Travier, L., Singh, R., Fernández, D. S., & Deczkowska, A. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102607 · Cited by 6
The dural sinus hub: more than just a brain drain
Mundt, S., Keller, A., & Greter, M. (2021) · Cell · doi:10.1016/j.cell.2021.01.040 · Cited by 6
Hamel, R., Peruzzotti‐Jametti, L., Ridley, K., Testa, V., Yu, B., Rowitch, D. H., Marioni, J. C., & Pluchino, S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.21.346635 · Cited by 7
Choi, H., Lee, E. J., Shin, J. S., Kim, H., Bae, S., Choi, Y., & Lee, D. S. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.06.28.450154 · Cited by 6
TIA1 Mediates Divergent Inflammatory Responses to Tauopathy in Microglia and MacrophagesPreprint
Webber, C. J., van der Spek, S. J. F., Cruz, A. L., Puri, S., Zhang, C., Aw, J. T. M., Papadimitriou, G.-Z., Roberts, R., Jiang, K., Tran, T., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.06.622325 · Cited by 6
Foley, K. E., Weekman, E. M., Krick, K. E., Johnson, S. N., Sudduth, T. L., & Wilcock, D. M. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1456-24.2024 · Cited by 6
Jiang, X. J., Mei, J., Zhu, J., Tian, Y., Wu, T., Li, Z., Wu, Z., Abdelaal, T., Li, F., Li, N., et al. (2025) · Communications Biology · doi:10.1038/s42003-025-08748-8 · Cited by 7
“Consistent with previous research 6,42 , CD206 + BAMs form the largest part of the BAM population in healthy brains, while we found monocyte-derived macrophages still drove acute in fl ammation through adhesion molecule upregulation.”
Neuroinflammation in fungal infections: from pathogen recognition to pathological manifestations
Dangarembizi, R., Awala, A. N., & de Lange, A. (2025) · Disease Models & Mechanisms · doi:10.1242/dmm.052344 · Cited by 6
Decoding brain border immunity to enable future therapeutic avenues
Hoecke, L. V., Acker, L. V., & Vandenbroucke, R. E. (2026) · Trends in Immunology · doi:10.1016/j.it.2025.12.007 · Cited by 5
Self-citationCNS border macrophages in health and disease
Fliegauf, M., Amann, L., & Prinz, M. (2026) · The Journal of Immunology · doi:10.1093/jimmun/vkaf308 · Cited by 5
García‐Bonilla, M., Swarup, R., Limbrick, O. W., Vohra, H. Z., Otun, A., McKalip, K., Bernhardt, W., Shumilov, K., Michenkova, M., Crouthamel, J., et al. (2026) · Fluids and Barriers of the CNS · doi:10.1186/s12987-026-00800-x · Cited by 9
Brain metastases exhibit distinct spatial patterns of resident and infiltrating macrophages
Ratzabi, A., Caspit, I. M., Telechi, I., Kim, J.-S., Vaknine, H., Blinder, P., Jung, S., & Stein, R. (2026) · Cell Death Discovery · doi:10.1038/s41420-026-03084-0 · Cited by 8
Activity-dependent protein synthesis in neurons requires microglial-metabolic coupling
Adler, D. I., Martín‐Ávila, A., Cheng, E., Oliveira, M. M., Zhang, M., Evans, H. T., Yuan, D., Sam, R., Zhang, N., Sellés, M. C., et al. (2026) · Cell Metabolism · doi:10.1016/j.cmet.2026.05.006 · Cited by 7
Ernst, K., Okonechnikov, K., Bageritz, J., Perera, A. A., Mallm, J., Wittmann, A., Maaß, K. K., Leible, S., Boutros, M., Pfister, S. M., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-97053-9 · Cited by 18
“The most highly variable unique gene for example, MRC1 , is a marker for border-associated macrophages 49 (Fig.”
Brain tumors: Cancer stem-like cells interact with tumor microenvironment
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Extrinsic factors associated with the response to immunotherapy in glioblastoma
Bi, H., & Zhang, C. (2021) · Cancer Letters · doi:10.1016/j.canlet.2021.04.018 · Cited by 5
Applications of single‐cell multi‐omics sequencing in deep understanding of brain diseases
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Meningeal lymphatic vasculature, a general target for glioblastoma therapy?
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“In addition to B cells, there are also a substantial number of border-associated macrophages (BAMs) within the dura mater [16] .”
BackgroundChrono‐Gerontology: Integrating Circadian Rhythms and Aging in Stroke Research
Kara, N. Z., Iweka, C. A., & Blacher, E. (2023) · Advanced Biology · doi:10.1002/adbi.202300048 · Cited by 5
Advances in understanding the immunity of the brain and its borders: Focus on brain macrophages
Süß, P., Diebold, M., & Sankowski, R. (2024) · Clinical and Translational Medicine · doi:10.1002/ctm2.70014 · Cited by 5
Frontiers of Neurodegenerative Disease Treatment: Targeting Immune Cells in Brain Border Regions
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Kiss, M., Lebegge, E., Murgaski, A., Damme, H. V., Kancheva, D., Brughmans, J., Scheyltjens, I., Talebi, A., Awad, R. M., Elkrim, Y., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1003975 · Cited by 6
“Sample preparation for sort: To limit dissociation-induced gene expression, tumors were dissociated in the presence of actinomycin D (ActD), following a protocol described before (18).”
MethodSelf-citationHematopoietic Stem Cell Requirement for Macrophage Regeneration Is Tissue Specific
Eddins, D. J., Kosters, A., Waters, J., Sosa, J., Phillips, M., Yadava, K., Herzenberg, L. A., Kuipers, H. F., & Ghosn, E. (2021) · The Journal of Immunology · doi:10.4049/jimmunol.2100344 · Cited by 6
Perivascular SPP1 Mediates Microglial Engulfment of Synapses in Alzheimer’s Disease ModelsPreprint
Schepper, S. D., Ge, J. Z., Crowley, G., Ferreira, L. S. S., Garceau, D. T., Toomey, C. E., Sokolova, D., Childs, T., Lashley, T., Burden, J. J., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.04.486547 · Cited by 5
“3A)(12), which allows to monitor microglia- and complement-mediated synapse engulfment in contralateral hippocampus of WT mice post intracerebroventricular (ICV) injection of oAβ [Aβ (1-40) S26C dimers].”
MethodSelf-citationPuype, H., Deschildre, J., & Vermeirssen, V. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.23.529626 · Cited by 4
Rovira, M., Ferrero, G., Miserocchi, M., Montanari, A., Lattuca, R., & Wittamer, V. (2025) · eLife · doi:10.1101/2023.07.27.550829 · Cited by 9
Rovira, M., Ferrero, G., Miserocchi, M., Montanari, A., Lattuca, R., & Wittamer, V. (2024) · eLife · doi:10.7554/elife.91427 · Cited by 7
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“Cluster 7 was identified as a population of brain border-associated macrophages, marked by MRC1, CD163, and LYVE1 53 .”
BackgroundEpigenetic heterogeneity shapes the transcriptional landscape of regional microgliaPreprint
Margetts, A. V., Vilca, S. J., Bourgain‐Guglielmetti, F., & Tuesta, L. M. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.08.607229 · Cited by 6
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Functional border-associated macrophages limit Alzheimer’s Disease progressionPreprint
Adler, D. I., Pinheiro-Rosa, N., Millet, A., Gajic, Z. Z., Cheng, E., Gamallo‐Lana, B., Morizawa, Y. M., Klann, E., Gan, W., Mar, A. C., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.31.703045 · Cited by 8
Microglial colonization routes and their impacts on cellular diversity
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“Recent advancements in single-cell transcriptomic analyses have provided key insights into microglial diversity in both mice (Hammond et al., 2019, Van Hove et al., 2019) and humans (Kracht et al., 2020).”
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Bringing natural killer cells to the clinic: Opportunities beyond cancer
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BMAL1-GPX3 axis in the choroid plexus mitigates Aβ pathology in an amyloid mouse model
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The meninges as a neuroimmune interface: structure, barriers and roles in CNS disease
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Metadata
- Authors
- Van Hove, H., Martens, L., Scheyltjens, I., De Vlaminck, K., Pombo Antunes, A. R., De Prijck, S., Vandamme, N., De Schepper, S., Van Isterdael, G., Scott, C. L., Aerts, J., Berx, G., Boeckxstaens, G. E., Vandenbroucke, R. E., Vereecke, L., Moechars, D., Guilliams, M., Van Ginderachter, J. A., Saeys, Y., & Movahedi, K.
- Affiliations
- Ghent University (BE)
- Vrije Universiteit Brussel (BE)
- Janssen (Belgium) (BE)
- KU Leuven (BE)
- Ghent University Hospital (BE)
- Corresponding author
- Movahedi, Kiavash
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2019-05-06
- Volume
- 22
- Issue
- 6
- Pages
- 1021-1035
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2943220296
- Cited by
- 1,074
- References
- 68
- Citations by year
- 2026: 160 · 2025: 156 · 2024: 187 · 2023: 152 · 2022: 148 · 2021: 151 · 2020: 90 · 2019: 29
- FWCI
- 46.98
- Type
- journal article
- Language
- en
- Open access
- green
- lirias.kuleuven.be
- Licence
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- Lirias (submittedVersion, other-oa)
- VUBIR (Vrije Universiteit Brussel) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- brain macrophages, border-associated macrophages, choroid plexus, dura mater, microglia, IRF8, macrophage ontogeny, postnatal brain development, self-renewal, cerebrospinal fluid
- MeSH terms
- Interferon Regulatory Factor-8, Animals, Brain, Cell Differentiation, Female, Macrophages, Male, Mice, Inbred C57BL, Microglia, Cell Lineage, Interferon Regulatory Factors, Mice
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