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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Four weeks after TAM administration, recombination is largely restricted to microglia and other long-lived macrophages in Cx3cr1CreER mouse lines.
“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]
The Results section, “Maintenance of pvMΦ, mMΦ and cpMΦ in adulthood,” reports persistent labeling of microglia and perivascular macrophages while blood monocytes lose their label. It documents this distinction at eight weeks after TAM, but the passages do not establish the claim’s specific four-week time point. (LLM, conf=0.82)
Experimental — accuracy not yet measuredThe Tmem119CreER, HexbCreER, and P2ry12CreER lines do not target border-associated macrophages in the CNS.
“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]
The Discussion (page unavailable) says P2ry12 was expressed only by microglia, supporting the distinction from macrophages at CNS interfaces. But gene expression does not establish whether a P2ry12CreER line targets those macrophages, and our copy does not assess the Tmem119CreER or HexbCreER lines. The Methods (Mice; page unavailable) list Cx3cr1CreER and Flt3Cre instead. (LLM, conf=0.85)
Experimental — accuracy not yet measuredYolk sac-derived precursors of resident macrophages are only in the perivascular compartment and maintain their cellular origin in adulthood.
“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]
The Results section (‘Prenatal yolk sac origin of CNS macrophages’) reports that perivascular and meningeal macrophages retained yolk sac lineage labels in adult mice, supporting persistence into adulthood. It also identifies yolk sac-derived macrophages in the meninges and choroid plexus, so they are not only in the perivascular compartment; choroid plexus macrophages, unlike the other two populations, lost their labels over time. (LLM, conf=0.90)
Experimental — accuracy not yet measuredCx3cr1 CreERT2-mediated deletion of microglial genes may also affect BAMs, albeit to a lesser extent.
“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]
The parenchymal brain macrophage compartment of unchallenged healthy mice is thought to comprise exclusively YS-derived microglia and no monocyte-derived macrophages.
“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]
PVMs are resident brain macrophages located in the intracerebral perivascular space, closely apposed to the outer vessel wall, and derived from hematopoietic precursors.
“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]
SALL1 was identified as a key marker for microglia based on FACS and immunohistochemical analysis.
“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]
Both microglia and BAMs are CD11b+/CD45low, making them difficult to distinguish without localization patterns.
“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]
High SALL1 expression distinguishes SALL1+ microglia from SALL1− BAM cells and infiltrating peripheral monocytes.
“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]
CD38+ resident myeloid cells called CNS border-associated macrophages are embryonically derived and line the meninges, choroid plexus, and perivascular spaces.
“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]
Single microglia nuclei-based analysis allowed exclusion of perivascular macrophages (Cx3cr1+, Tmem119-, P2ry12-low) as potential factors driving the cerebellar microglia clearance-promoting gene expression signature.
“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]
Cx3cr1+ perivascular/meningeal macrophages, identified by low Tmem119, low Hexb, and high Mrc1, were excluded from single-cell analysis.
“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]
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.
“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]
Macrophages in the choroid plexus and dura mater turn over and receive some input from peripheral blood monocytes during adulthood.
“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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Stifter, S. A., & Greter, M. (2020) · European Journal of Immunology · doi:10.1002/eji.202048546 · Cited by 48 · see citing works
- 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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