Infection drives meningeal engraftment by inflammatory monocytes that impairs CNS immunity
Open accessAbstract
Tissue macrophages have an embryonic origin and can be replenished in some tissues under steady-state conditions by blood monocytes. However, little is known about the residency and properties of infiltrating monocytes after an inflammatory challenge. The meninges of the central nervous system (CNS) are populated by a dense network of macrophages that act as resident immune sentinels. Here we show that, following lymphocytic choriomeningitis virus infection, resident meningeal macrophages (MMs) acquired viral antigen and interacted directly with infiltrating cytotoxic T lymphocytes, which led to macrophage depletion. Concurrently, the meninges were infiltrated by inflammatory monocytes that engrafted the meningeal niche and remained in situ for months after viral clearance. This engraftment led to interferon-γ-dependent functional changes in the pool of MMs, including loss of bacterial and immunoregulatory sensors. Collectively, these data indicate that peripheral monocytes can engraft the meninges after an inflammatory challenge, imprinting the compartment with long-term defects in immune function.
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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 [72]
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 [72]
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References 56 · Cited by 123
- Authors
- Rua, R., Lee, J. Y., Silva, A. B., Swafford, I. S., Maric, D., Johnson, K. R., & McGavern, D. B.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- McGavern, Dorian B.
- Venue
- Nature Immunology
- Published
- 2019-03-18
- Volume
- 20
- Issue
- 4
- Pages
- 407-419
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- PMC
- PMC6481670
- OpenAlex
- W2922321673
- Cited by
- 123
- References
- 56
- Citations by year
- 2026: 15 · 2025: 21 · 2024: 17 · 2023: 19 · 2022: 25 · 2021: 12 · 2020: 3 · 2019: 11
- FWCI
- 5.61
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Immunology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (ZIANS003112)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Keywords
- meningeal macrophages, inflammatory monocytes, lymphocytic choriomeningitis virus, interferon-gamma, cytotoxic T lymphocytes, macrophage depletion, bone marrow-derived monocytes, bacterial sensing, viral infection
- MeSH terms
- Animals, Central Nervous System, Immunity, Inflammation, Interferon-gamma, Macrophages, Meninges, Meningitis, Viral, Monocytes, Mice
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