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Macrophages at CNS interfaces: ontogeny and function in health and disease
Abstract
The segregation and limited regenerative capacity of the CNS necessitate a specialized and tightly regulated resident immune system that continuously guards the CNS against invading pathogens and injury. Immunity in the CNS has generally been attributed to neuron-associated microglia in the parenchyma, whose origin and functions have recently been elucidated. However, there are several other specialized macrophage populations at the CNS borders, including dural, leptomeningeal, perivascular and choroid plexus macrophages (collectively known as CNS-associated macrophages (CAMs)), whose origins and roles in health and disease have remained largely uncharted. CAMs are thought to be involved in regulating the fine balance between the proper segregation of the CNS, on the one hand, and the essential exchange between the CNS parenchyma and the periphery, on the other. Recent studies that have been empowered by major technological advances have shed new light on these cells and suggest central roles for CAMs in CNS physiology and in the pathogenesis of diseases.
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“They belong to CNS border-associated macrophages (CAMs) [367,368].”
From Revisiting the Pathogenesis of X-Linked Adrenoleukodystrophy (2025) · cites this paper as [367]
In the citing paper
“Single-cell profiling suggested functions shared with microglia and astrocytes in maintaining CNS homeostasis [372] and regulating barrier functions [367,378,379,380].”
From Revisiting the Pathogenesis of X-Linked Adrenoleukodystrophy (2025) · cites this paper as [367]
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Sbierski‐Kind, J., Mroz, N. M., & Molofsky, A. B. (2021) · Immunological Reviews · doi:10.1111/imr.12984 · Cited by 35
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“At these CNS barriers, specialized macrophage populations, including dural, leptomeningeal, perivascular, and choroid plexus macrophages, are collectively referred to as CNS-associated macrophages (CAMs) (Kierdorf et al., 2019).”
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Woolf, Z., Stevenson, T. J., Lee, K., Highet, B., Foliaki, J. M., Ratiu, R., Rustenhoven, J., Correia, J. A., Schweder, P. M., Heppner, P. A., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-99867-z · Cited by 40
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Immunopathogenesis of Craniotomy Infection and Niche-Specific Immune Responses to Biofilm
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“Infiltrating border associated macrophages, identified by CD206 staining (28), were primarily present in the leptomeninges and covered a median of 1.”
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Microglia‐leucocyte axis in cerebral ischaemia and inflammation in the developing brain
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“…microglia and non-parenchymal macrophages represent ontologically, phenotypically, and functionally distinct cell populations (Jordao et al., 2019; Masuda et al., 2019; Mrdjen et al., 2018; Munro et al., 2020; Shemer et al., 2018; Utz et al., 2020; Van Hove et al., 2019); however,…”
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“Both parenchymal microglia and CAMs share their origin from MRC1 + yolk sac macrophages and depend on the same transcription factors, although they differentiate in distinct CNS compartments around birth 38,39 .”
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“In contrast to microglia, CNS-associated MACs include resident tissue MACs of barriers and interfaces of the CNS parenchyma and the periphery, such as perivascular space, meninges and the choroid plexus (154) (Table 2).”
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BackgroundNovel insights into the origin and development of CNS macrophage subsets
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Self-citationOligodendrocyte myelin glycoprotein as a novel target for pathogenic autoimmunity in the CNS
Gerhards, R., Pfeffer, L. K., Lorenz, J., Starost, L. J., Nowack, L., Thaler, F., Schlüter, M., Rübsamen, H., Macrini, C., Winklmeier, S., et al. (2020) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-01086-2 · Cited by 28
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“Macrophages are especially abundant, and they can be divided into several molecularly distinct classes that are characterized by different half-lives and capacities for self-renewal ( Mrdjen et al., 2018 ; Kierdorf et al., 2019 ; Van Hove et al., 2019 ; Masuda et al., 2022 ).”
BackgroundExercise rejuvenates microglia and reverses T cell accumulation in the aged female mouse brain
Chauquet, S., Willis, E. F., Grice, L. F., Harley, S. B. R., Powell, J. E., Wray, N. R., Nguyen, Q. H., Ruitenberg, M. J., Shah, S. H., & Vukovic, J. (2024) · Aging Cell · doi:10.1111/acel.14172 · Cited by 29
“…insights into the transcriptional heterogeneity of microglia in mice and humans on both a temporal and spatial axis, providing new insights into the nature of microglia during development, homeostasis, ageing and disease progression (Allen et al., 2023; Hammond et al., 2018; Masuda et al., 2019).”
Reimagining the meninges from a neuroimmune perspective: a boundary, but not peripheral
Zhang, X., Liu, L., Chai, Y., Zhang, J., Deng, Q., & Chen, X. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03286-2 · Cited by 31
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“CAMs are constantly monitoring the CSF, searching for harmful antigens, and also contributing to the drainage of CNS-derived antigens (70, 72, 73).”
Bağdaş, D., Paris, J. J., Carper, M., Wodarski, R., Rice, A. S. C., Knapp, P. E., Hauser, K. F., & Damaj, M. I. (2020) · European Journal of Pain · doi:10.1002/ejp.1618 · Cited by 24
“Since microglial promoters are also found to be expressed by monocyte-derived macrophages (Bottcher et al., 2019; Goldmann et al., 2016; Kierdorf et al., 2019), previous attempts to restrict HIV protein expression to the nervous system have relied on the use of astrocytic promoters such as the…”
BackgroundRobert, S. M., Reeves, B. C., Marlier, A., Duy, P. Q., DeSpenza, T., Kundishora, A. J., Kiziltug, E., Singh, A. K., Allington, G., Alper, S. L., et al. (2021) · Child s Nervous System · doi:10.1007/s00381-021-05255-z · Cited by 24
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“The brain harbors several macrophage populations: parenchymal macrophages (i.e., microglia) and non-parenchymal macrophages, which reside at CNS border regions including the meninges, choroid plexus and perivascular spaces (Kierdorf et al., 2019).”
BackgroundNeurovascular Coupling in Hypertension Is Impaired by IL-17A through Oxidative Stress
Youwakim, J., Vallerand, D., & Girouard, H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043959 · Cited by 24
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“A study in zebrafish showed that pvM Φ can repair the injured BBB [126,128].”
BackgroundEvaluating microglial phenotypes using single-cell technologies
Sankowski, R., Monaco, G., & Prinz, M. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.11.001 · Cited by 25
Self-citationBuenaventura, R. G., Harvey, A. C., Burns, M. P., & Main, B. S. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1210175 · Cited by 23
“Although recent work has uncovered the role of meningeal driven immunity in various chronic neurodegenerative disorders (Filiano et al., 2016; Louveau et al., 2018b; Kierdorf et al., 2019; Alves de Lima et al., 2020; Brioschi et al., 2021), less is known about their role in response to moderate/severe brain injury.”
BackgroundWang, J., Li, S., Lan, Y., Liu, X., & Li, W. (2024) · Current Medicine · doi:10.1007/s44194-024-00031-y · Cited by 24
Bartalska, K., Hübschmann, V., Korkut-Demirbaş, M., Cubero, R. J. A., Venturino, A., Rössler, K., Czech, T., & Siegert, S. (2022) · iScience · doi:10.1016/j.isci.2022.104580 · Cited by 22
“, 2014) and stained with the pan-macrophage marker IBA1/AIF1 (ionized calcium binding adaptor molecule one/allograft inflammatory factor 1), which identifies brain parenchymal- (microglia), blood-derived- (MF), and border-associated- (perivascular pvMF, leptomeningeal mMF, choroid plexus cpMF) macrophages (Imai et al.…”
BackgroundYe, F., Yang, J., Holste, K. G., Koduri, S., Hua, Y., Keep, R. F., Garton, H. J. L., & Xi, G. (2023) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x231173187 · Cited by 23
You, Y., Chen, Z., & Hu, W. (2024) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2024.108606 · Cited by 25
Age-dependent effects of gut microbiota metabolites on brain resident macrophages
Hasavci, D., & Blank, T. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.944526 · Cited by 23
“The different subsets are suggested to be involved in monitoring of the CNS and clearance of cellular debris and pathogens (Nayak et al., 2012; Kierdorf et al., 2019).”
BackgroundSchmidt-Morgenroth, I., Michaud, P., Gasparini, F., & Avraméas, A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241310523 · Cited by 26
Nguyễn, V. Đ., Nguyen, N., Li, Z., Cheng, C., Wang, J., Chiang, L.-C., Song, H., Lo, S., Mac, C., Chang, Y., et al. (2024) · Advanced Functional Materials · doi:10.1002/adfm.202401570 · Cited by 22
The Eclectic Nature of Glioma-Infiltrating Macrophages and Microglia
Arrieta, V. A., Najem, H., Petrosyan, E., Lee-Chang, C., Chen, P., Sonabend, A. M., & Heimberger, A. B. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222413382 · Cited by 23
“Apart from the microglia, specialized subsets of macrophages exist in the CNS borders including the perivascular, leptomeningeal, choroid plexus, and dural niches [29].”
BackgroundXu, X., Han, Y., Zhang, B., Ren, Q., Ma, J., & Liu, S. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-024-01509-w · Cited by 25
Tremblay, M. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.628347 · Cited by 21
“Recent technological advances such as single cell transcriptome analysis have revealed an unprecedented heterogeneity in the nonneuronal cells of the CNS’s molecular signatures (Krasemann et al., 2017; Hammond et al., 2019; Kierdorf et al., 2019; Deczkowska et al., 2020).”
BackgroundRojas, M., Luz‐Crawford, P., Soto‐Rifo, R., Reyes-Cerpa, S., & Toro‐Ascuy, D. (2021) · Cells · doi:10.3390/cells10092378 · Cited by 22
“The newly recognized longevity and self-renewing potential of CNS-associated macrophages [41] suggests that they may be a reservoir for viral infection and renders them a preferred site for replication, in agreement with previous reports [42,43].”
ResultDissecting calvarial bones and sutures at single‐cell resolution
Li, B., Li, J., Fan, Y., Zhao, Z., Li, L., Okano, H., & Ouchi, T. (2023) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12975 · Cited by 21
Metabolic determinants of leukocyte pathogenicity in neurological diseases
Runtsch, M. C., Ferrara, G. B., & Angiari, S. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15169 · Cited by 20
Tuddenham, J. F., Taga, M. F., Haage, V. C., Roostaei, T., White, C. C., Lee, A., Fujita, M., Khairallah, A., Green, G., Hyman, B. T., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.04.494709 · Cited by 20
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“BAMs present mixed origins as they derive from both yolk sac and liver progenitors and are found in the barriers between the blood and brain and CSF (cerebro-spinal fluid) and in the meninges (Kierdorf et al., 2019).”
Getting on in Old Age: How the Gut Microbiota Interferes With Brain Innate Immunity
Mossad, O., & Blank, T. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.698126 · Cited by 18
Wasteosomes (corpora amylacea) of human brain can be phagocytosed and digested by macrophages
Riba, M., Campo-Sabariz, J., Tena, I., Molina‐Porcel, L., Ximelis, T., Calvo, M., Ferrer, R., Martín-Venegas, R., del Valle, J., Vilaplana, J., et al. (2022) · Cell & Bioscience · doi:10.1186/s13578-022-00915-2 · Cited by 18
Neuro-immune crosstalk in depressive symptoms of multiple sclerosis
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“The CNS contains multiple subsets of macrophages (CNS associated macrophages): 1) microglia cells that are resident in the parenchyma, 2) non-parenchymal macrophages in the choroid plexus, perivascular space and meninges; 3) under inflammatory conditions, infiltrating monocytes-derived macrophages that can occupy both…”
BackgroundCNS-associated macrophages shape the inflammatory response in a mouse model of Parkinson’s disease
Frosch, M., Amann, L., & Prinz, M. (2023) · Nature Communications · doi:10.1038/s41467-023-39061-9 · Cited by 21
Self-citationBloomfield, C. L., Gong, J., Droho, S., Makinde, H. M., Gurra, M. G., Stumpf, C. H., Kharel, A., Gadhvi, G. T., Winter, D. R., Cui, W., et al. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1399989 · Cited by 18
Yamasaki, A., Imanishi, I., Tanaka, K. Y., Ohkawa, Y., Tsuda, M., & Masuda, T. (2024) · Communications Biology · doi:10.1038/s42003-024-06607-6 · Cited by 17
Self-citationDeciphering the heterogeneity of myeloid cells during neuroinflammation in the single‐cell era
Borst, K., & Prinz, M. (2020) · Brain Pathology · doi:10.1111/bpa.12910 · Cited by 17
Self-citationThe Neuroimmunology of Multiple Sclerosis: Fictions and Facts
Pachner, A. R. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2021.796378 · Cited by 19
Wang, J. M., Ong, J. X., Nesper, P. L., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-17229-5 · Cited by 18
Niche-specific therapeutic targeting of myeloid cells in the central nervous system
Frosch, M., & Prinz, M. (2025) · Immunity · doi:10.1016/j.immuni.2025.03.016 · Cited by 17
Self-citationMultiple Roles of Peripheral Immune System in Modulating Ischemia/Hypoxia-Induced Neuroinflammation
Guo, L., & Zhu, L. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.752465 · Cited by 17
“Border macrophages participate in CNS homeostasis through multiple ways, including affecting vascular permeability and BBB integrity, carrying out scavenger functions, filtering and draining the CNS, scanning for invading pathogens, and presenting antigens to circulating lymphocytes (Fabriek et al., 2005; Coles et al.…”
BackgroundComplement drives circuit modulation in the adult brain
Parker, S. E., Bellingham, M. C., & Woodruff, T. M. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102282 · Cited by 18
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“…addition to limiting the exchange and access of cells and molecules from the periphery due to its highly specialized anatomical structures, including the meninges, perivascular space (PVS), and choroid plexus (cp), which form an interface between the periphery and the CNS (Kierdorf et al., 2019).”
Peripherally-sourced myeloid antigen presenting cells increase with advanced aging
Honarpisheh, P., Blixt, F. W., Conesa, M. P. B., Won, W. W., d’Aigle, J., Munshi, Y., Hudobenko, J., Furr, J. W., Mobley, A. S., Lee, J., et al. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.08.023 · Cited by 18
“Future mechanistic studies utilizing conditional knock-out mouse models of APCs are required to examine the specific age-dependent role of brain’s peripherally-source myeloid APCs in the recruitment of both innate and adaptive immune cells into the CNS. Brain APCs regulate neuroinflammation by presenting antigens to T…”
BackgroundInfluentialRoles for Microglia in Cryptococcal Brain Dissemination in the Zebrafish Larva
Nielson, J. A., & Davis, J. M. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.04315-22 · Cited by 15
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“Germline variants were removed by comparing against matched whole-genome or whole-exome sequencing data of the same individual.”
MethodSingle‐Cell and Spatial Multiomics: Applications for Diseases
Li, W., Chen, C., Zhu, X., & Zhang, C. (2025) · MedComm · doi:10.1002/mco2.70553 · Cited by 16
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“Microglia not only protect the brain from pathogens and injury, but also serve critical roles in maintaining neuronal viability, proper synaptodendritic function and integrity in development and over the lifespan (20, 21, 37 – 39).”
BackgroundQuarta, A., Berneman, Z. N., & Ponsaerts, P. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.3ru0820-536r · Cited by 17
Metadata
- Authors
- Kierdorf, K., Masuda, T., Jordão, M. J. C., & Prinz, M.
- Affiliations
- University of Freiburg (DE)
- Corresponding author
- Prinz, Marco
- Venue
- Nature Reviews Neuroscience
- Published
- 2019-07-29
- Volume
- 20
- Issue
- 9
- Pages
- 547-562
- ISSN
- 1471-003X (ISSN-L)
- 1471-0048
- OpenAlex
- W2965570118
- Semantic Scholar
- 7aa0033e693c776f7718f0c2d90733dadf1d5769
- Cited by
- 416
- References
- 196
- Citations by year
- 2026: 54 · 2025: 49 · 2024: 74 · 2023: 56 · 2022: 62 · 2021: 70 · 2020: 42 · 2019: 8
- FWCI
- 4.71
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature reviews. Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Health Sciences › Medicine › Clinical Neurology › Cerebrospinal fluid and hydrocephalus
- Keywords
- perivascular macrophages, choroid plexus macrophages, macrophage ontogeny, meninges, blood-brain barrier, neuroinflammation, neurodegenerative diseases
- MeSH terms
- Animals, Central Nervous System, Humans, Macrophages, Neurons, Inflammation Mediators, Neurodegenerative Diseases
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