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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]
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“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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Microglia promote remyelination independent of their role in clearing myelin debris
Baaklini, C. S., Ho, M. F. S., Lange, T., Hammond, B. P., Panda, S. P., Zirngibl, M., Zia, S., Himmelsbach, K., Rana, H., Phillips, B., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113574 · Cited by 73
Distinct Features of Brain-Resident Macrophages: Microglia and Non-Parenchymal Brain Macrophages
Lee, E., Eo, J.-C., Lee, C., & Yu, J. (2021) · Molecules and Cells · doi:10.14348/molcells.2021.0060 · Cited by 83
“Although functional studies are limited, CAMs reportedly monitor or filter the CSF for any harmful antigens and metabolites (Kierdorf et al., 2019), and also contribute to the drainage of CNS-derived antigens (Mundt et al.”
BackgroundResultInfluentialBenhar, I., Ding, J., Yan, W., Whitney, I. E., Jacobi, A., Sud, M., Burgin, G., Shekhar, K., Tran, N. M., Wang, C., et al. (2023) · Nature Immunology · doi:10.1038/s41590-023-01437-w · Cited by 69
“Notably, resident macrophages are prone to replacement by blood-derived myeloid cells after injurious perturbations, such as irradiation (Bechmann et al., 2001; Hickey and Kimura, 1988; Kierdorf et al., 2019; Xu et al., 2007b).”
BackgroundMapunda, J. A., Pareja, J. R., Vladymyrov, M., Bouillet, E., Hélie, P., Pleskač, P., Barcos, S., Andræ, J., Vestweber, D., McDonald, D. M., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-41580-4 · Cited by 72
Microglia Diversity in Health and Multiple Sclerosis
Zia, S., Rawji, K. S., Michaels, N. J., Burr, M. K., Kerr, B. J., Healy, L. M., & Plemel, J. R. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.588021 · Cited by 70
Cholinergic Modulation of the Immune System in Neuroinflammatory Diseases
Reale, M., & Costantini, E. (2021) · Diseases · doi:10.3390/diseases9020029 · Cited by 76
“Circulating monocytes can migrate in the brain, and together with resident microglial cells, respond to inflammatory stimuli and increase the immune response [56] playing a key role in neurodegenerative disease progression.”
BackgroundThe molecular anatomy and functions of the choroid plexus in healthy and diseased brain
Kratzer, I., Ek, C. J., & Stolp, H. B. (2020) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2020.183430 · Cited by 74
Brain Parenchymal and Extraparenchymal Macrophages in Development, Homeostasis, and Disease
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“However, whether microglia and BAMs arise from a unique YSderived progenitor or develop through independent pathways is still unknown (170).”
BackgroundDissecting the complexities of Alzheimer disease with in vitro models of the human brain
Blanchard, J., Victor, M. B., & Tsai, L. (2021) · Nature Reviews Neurology · doi:10.1038/s41582-021-00578-6 · Cited by 68
The Role of Osteopontin in Microglia Biology: Current Concepts and Future Perspectives
Rosmus, D.-D., Lange, C., Ludwig, F., Ajami, B., & Wieghofer, P. (2022) · Biomedicines · doi:10.3390/biomedicines10040840 · Cited by 70
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“We found that cells expressing CM-DiI at 2 and 5 days were perivascular or meningeal macrophages, which are a unique macrophage population that can be genetically distinguished from parenchymal microglia and other central nervous system macrophage populations.(29,30) In our study, we did not identify parenchymal micro…”
BackgroundChowdhury, E. A., Noorani, B., Alqahtani, F., Bhalerao, A., Raut, S., Sivandzade, F., & Cucullo, L. (2021) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x20985946 · Cited by 77
“Other than this the perivascular spaces also contain resident macrophages (known as perivascular macrophages) that may be involved in the clearance of different endogenous molecules.(32,33) CSF is constantly secreted by the choroid plexus which is present along the Blood-Cerebrospinal fluid barrier (BCSFB) in the late…”
BackgroundMuñoz-Castro, C., Mejias-Ortega, M., Sanchez-Mejias, E., Navarro, V., Trujillo-Estrada, L., Jimenez, S., Garcia-Leon, J. A., Fernandez-Valenzuela, J. J., Sanchez-Mico, M. V., Romero-Molina, C., et al. (2023) · Acta Neuropathologica Communications · doi:10.1186/s40478-023-01530-z · Cited by 66
“Typical examples are infiltration of lymphocytes and monocyte-derived cells (MDC) in multiple sclerosis and amyotrophic lateral sclerosis, which seem to play an important role in the development of these neurodegenerative conditions [3, 26, 42, 66].”
BackgroundThe CNS mononuclear phagocyte system in health and disease
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The Ins and Outs of Central Nervous System Inflammation—Lessons Learned from Multiple Sclerosis
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Tackling the glial scar in spinal cord regeneration: new discoveries and future directions
Shafqat, A., Albalkhi, I., Magableh, H. M., Saleh, T., AlKattan, K. M., & Yaqinuddin, A. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1180825 · Cited by 71
“However, their distinct roles in SCI remain largely uncharted (Jordão et al., 2019; Kierdorf et al., 2019; De Schepper et al., 2023).”
BackgroundNakahashi-Oda, C., Fujiyama, S., Nakazawa, Y., Kanemaru, K., Wang, Y., Lyu, W., Shichita, T., Kitaura, J., Abe, F., & Shibuya, A. (2021) · Science Immunology · doi:10.1126/sciimmunol.abe7915 · Cited by 63
“On the basis of these results and previous reports (23, 24), CD45.”
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The Expanding Cell Diversity of the Brain Vasculature
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“PVMs serve a vital role in the phagocytosis of blood-borne pathogens and antigen presentation to induce protective immune responses (Lapenna et al., 2018; Kierdorf et al., 2019).”
BackgroundThe impact of stress on immune systems and its relevance to mental illness
Ishikawa, Y., & Furuyashiki, T. (2021) · Neuroscience Research · doi:10.1016/j.neures.2021.09.005 · Cited by 73
Visceral adiposity, inflammation, and hippocampal function in obesity
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The niche matters: Origin, function and fate of CNS-associated macrophages during health and disease
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“We also do not know to what extent CNS macrophages reciprocally instruct the profiles of their niche neighbors in the brain and its border compartments [for additional open questions regarding BAMs and microglia, see (3, 37)].”
BackgroundMethodInfluentialMicroglial Priming in Infections and Its Risk to Neurodegenerative Diseases
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Understanding microglial diversity and implications for neuronal function in health and disease
Schepper, S. D., Crowley, G., & Hong, S. Y. (2020) · Developmental Neurobiology · doi:10.1002/dneu.22777 · Cited by 54
“Besides microglia, the CNS myeloid compartment consists of BAMs that reside at brain borders, including meninges, perivascular space, and choroid plexus (Goldmann et al., 2016; Kierdorf et al., 2019).”
BackgroundRedefining our vision: an updated guide to the ocular immune system
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Dwellers and Trespassers: Mononuclear Phagocytes at the Borders of the Central Nervous System
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Choroid plexus mast cells drive tumor-associated hydrocephalus
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Hallmarks of neurodegenerative disease: A systems pharmacology perspective
Bloomingdale, P., Karelina, T., Ramakrishnan, V., Bakshi, S., Véronneau‐Veilleux, F., Moye, M., Sekiguchi, K., Meno‐Tetang, G. M. L., Mohan, A., Maithreye, R., et al. (2022) · CPT Pharmacometrics & Systems Pharmacology · doi:10.1002/psp4.12852 · Cited by 54
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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