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Origin, fate and dynamics of macrophages at central nervous system interfaces
Open accessAbstract
Perivascular, subdural meningeal and choroid plexus macrophages are non-parenchymal macrophages that mediate immune responses at brain boundaries. Although the origin of parenchymal microglia has recently been elucidated, much less is known about the precursors, the underlying transcriptional program and the dynamics of the other macrophages in the central nervous system (CNS). It was assumed that they have a high turnover from blood-borne monocytes. However, using parabiosis and fate-mapping approaches in mice, we found that CNS macrophages arose from hematopoietic precursors during embryonic development and established stable populations, with the notable exception of choroid plexus macrophages, which had dual origins and a shorter life span. The generation of CNS macrophages relied on the transcription factor PU.1, whereas the MYB, BATF3 and NR4A1 transcription factors were not required.
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“Thus, 4 weeks after TAM administration, recombination is largely restricted to microglia and other long-lived macrophages (e.g., perivascular macrophages) in Cx3cr1CreER mouse lines.15”
From A comparative analysis of microglial inducible Cre lines (2023) · cites this paper as [15]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“the Tmem119CreER, HexbCreER, and P2ry12CreER lines do not target border-associated macrophages in the CNS.15,20,21,30”
From A comparative analysis of microglial inducible Cre lines (2023) · cites this paper as [15]
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“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 [363]
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“Of note, using Cx3cr1 CreERT2 mice to delete microglial genes may also affect border-associated macrophages (BAMs) 16 , albeit to a lesser extent as BAMs were shown to be continuously replenished from skull bone marrow, unlike microglia 17 .”
From APOE4 impairs the microglial response in Alzheimer’s disease by inducing TGFβ-mediated checkpoints (2023) · cites this paper as [16]
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“Likewise, also parenchymal brain M F are thought to comprise during the life time of healthy mice exclusively YS-derived microglia and no MoM F 8-10 .”
From Clonal hematopoiesis-associated motoric deficits caused by monocyte-derived microglia accumulating in aging mice (2025) · cites this paper as [9]
In the citing paper
“Residing in the intracerebral perivascular space, delimited by the glia limitans and the vascular basement membrane (Virchow-Robin space), PVMs are closely apposed to the outer vessel wall and originate from hematopoietic precursors (18,20,21).”
From Perivascular macrophages mediate the neurovascular and cognitive dysfunction associated with hypertension (2016) · cites this paper as [18]
In the citing paper
“Based on current FACS and immunohistochemical analysis, the transcription factor SALL1 was identified as a key marker for microglia.”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [20]
In the citing paper
“Both microglia and BAMs are CD11b+/CD45low, making it difficult to distinguish between them without localization patterns.”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [20]
In the citing paper
“High expression of SALL1 in microglia allows distinguishing SALL1+ microglia from SALL1− BAM cells and infiltrating peripheral monocytes [20, 21].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [20]
In the citing paper
“In addition to microglia, new CD38+ resident myeloid cells called CNS border-associated macrophages (BAMs) are embryonically-derived cells that line along the meninges, choroid plexus, and perivascular spaces [20].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [20]
In the citing paper
“Moreover, single microglia nuclei-based analysis allowed us to exclude perivascular macrophages (Cx3cr1+, Tmem119-, and P2ry12-low)35 as potential factors driving the cbMg clearance-promoting gene expression signature.”
From Epigenetic regulation of brain region-specific microglia clearance activity (2018) · cites this paper as [35]
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“Cx3cr1+ perivascular/meningeal macrophages were identified by low Tmem119, low Hexb, and high Mrc1 expression35,84 and excluded from single cell analysis (n=1-5 per plate).”
From Epigenetic regulation of brain region-specific microglia clearance activity (2018) · cites this paper as [35]
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 [71]
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 [71]
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Metadata
- Authors
- Goldmann, T., Wieghofer, P., Jordão, M. J. C., Prutek, F., Hagemeyer, N., Frenzel, K., Amann, L., Staszewski, O., Kierdorf, K., Krueger, M., Locatelli, G., Hochgerner, H., Zeiser, R., Epelman, S., Geissmann, F., Priller, J., Rossi, F. M. V., Bechmann, I., Kerschensteiner, M., Linnarsson, S., Jung, S., & Prinz, M.
- Affiliations
- University Medical Center Freiburg (DE)
- University of Freiburg (DE)
- Leipzig University (DE)
- Institut für Klinische Neuroimmunologie (DE)
- Karolinska Institutet (SE)
- University Health Network (CA)
- Berlin Institute of Health at Charité - Universitätsmedizin Berlin (DE)
- University of British Columbia (CA)
- Munich Cluster for Systems Neurology (DE)
- Weizmann Institute of Science (IL)
- Corresponding author
- Prinz, Marco
- ORCID
- Venue
- Nature Immunology
- Published
- 2016-05-02
- Volume
- 17
- Issue
- 7
- Pages
- 797-805
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- PMC
- PMC4968048
- OpenAlex
- W2345745180
- Cited by
- 1,209
- References
- 52
- Citations by year
- 2026: 94 · 2025: 103 · 2024: 166 · 2023: 134 · 2022: 137 · 2021: 150 · 2020: 134 · 2019: 106 · 2018: 103 · 2017: 65 · 2016: 17
- FWCI
- 53.14
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Immunology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- BORIS (University Library Bern) (submittedVersion)
- DZNE Pub (submittedVersion)
- Spiral (Imperial College London) (submittedVersion)
- OPUS (Augsburg University) (submittedVersion)
- Funders
- National Cancer Institute (P30CA008748)
- 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
- macrophage origin, choroid plexus macrophages, meningeal macrophages, perivascular macrophages, PU.1, parabiosis, macrophage turnover, central nervous system immunity, transcription factors
- MeSH terms
- Proto-Oncogene Protein Spi-1, Animals, Cell Differentiation, Cells, Cultured, Central Nervous System, Hematopoietic Stem Cells, Macrophages, Mice, Inbred C57BL, Mice, Transgenic, Microscopy, Fluorescence, Monocytes, Parabiosis, Proto-Oncogene Proteins, Trans-Activators, Microglia, Mice, Knockout, Mice
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