Skull and vertebral bone marrow are myeloid cell reservoirs for the meninges and CNS parenchyma
Open accessAbstract
Getting around the blood–brain barrier: The meninges comprise three membranes that surround and protect the central nervous system (CNS). Recent studies have noted the existence of myeloid cells resident there, but little is known about their ontogeny and function, and whether other meningeal immune cell populations have important roles remains unclear (see the Perspective by Nguyen and Kubes). Cugurra et al. found in mice that a large proportion of continuously replenished myeloid cells in the dura mater are not blood derived, but rather transit from cranial bone marrow through specialized channels. In models of CNS injury and neuroinflammation, the authors demonstrated that these myeloid cells have an immunoregulatory phenotype compared with their more inflammatory blood-derived counterparts. Similarly, Brioschi et al. show that the meninges host B cells that are also derived from skull bone marrow, mature locally, and likely acquire a tolerogenic phenotype. They further found that the brains of aging mice are infiltrated by a second population of age-associated B cells, which come from the periphery and may differentiate into autoantibody-secreting plasma cells after encountering CNS antigens. Together, these two studies may inform future treatment of neurological diseases. Science , abf7844, abf9277, this issue p. eabf7844 , p. eabf9277 ; see also abj8183, p. 396
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Cx3cr1 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 [17]
The Discussion (page not available) says skull and vertebral marrow continuously replenish monocytes and neutrophils at CNS borders and that marrow-derived monocytes can become meningeal macrophages. The Introduction describes microglia as self-maintained. The paper does not establish that BAMs as a group are continuously replenished, or that Cx3cr1 CreERT2-mediated deletion affects them to a lesser extent; the latter part of the citing sentence is the portion attached to this citation. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThere is a growing body of evidence from mice that bone marrow-derived myeloid cells can enter the brain during homeostasis.
“There is a growing body of evidence from mice that bone marrow-derived myeloid cells can enter the brain during homeostasis31,32.”
From Clonal hematopoiesis is associated with protection from Alzheimer’s disease (2023) · cites this paper as [31]
The Introduction and Results report that, in mice, bone marrow-derived myeloid cells reach the dural meninges and other brain borders under homeostatic conditions. They distinguish this from entry into CNS parenchyma, which the paper reports following injury or neuroinflammation. Thus the source supports homeostatic entry to brain borders, but not clearly entry into brain tissue during homeostasis. (LLM, conf=0.87)
Experimental — accuracy not yet measuredSkull bone marrow cells can mount a tailored immune response and supply immune cells to the brain borders and parenchyma post-inflammation.
“They can mount a tailored immune response [387,389]. They supply immune cells to the brain borders and parenchyma post-inflammation [388,389].”
From Revisiting the Pathogenesis of X-Linked Adrenoleukodystrophy (2025) · cites this paper as [389]
The Results section reports that myeloid cells from CNS-adjacent bone marrow infiltrate the CNS after injury or neuroinflammation, and the Discussion describes skull bone marrow supplying cells to the meninges. The paper finds differing transcriptional profiles but treats distinct immune roles as a possibility; it does not establish that these cells mount a tailored immune response. The findings are in mice; page numbers are unavailable in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredSystemic chronic inflammation resulting from immunosenescence and non-neurotropic viral infection compels immune cells in the peripheral blood to penetrate the blood-brain barrier and choroid plexus and enter the brain; immune cells originating from the cranial bone marrow migrate to the meninges, thereby promoting neuroinflammation and neuronal dysfunction while inhibiting neurogenesis, and thisc
“Finally, the systemic chronic inflammation resulting from immunosenescence and non-neurotropic viral infection compels immune cells in the peripheral blood to penetrate the blood-brain barrier (BBB) and choroid plexus and enter the brain,345,346 Additionally, immune cells originating from the cranial bone marrow migrate to the meninges,347 thereby promoting neuroinflammation and neuronal”
From Antiageing strategy for neurodegenerative diseases: from mechanisms to clinical advances (2025) · cites this paper as [347]
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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 .”
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- Authors
- Cugurra, A., Mamuladze, T., Rustenhoven, J., Dykstra, T., Beroshvili, G., Greenberg, Z. J., Baker, W., Papadopoulos, Z., Drieu, A., Blackburn, S., Kanamori, M., Brioschi, S., Herz, J., Schuettpelz, L. G., Colonna, M., Smirnov, I., & Kipnis, J.
- Affiliations
- University Medical Center of the Johannes Gutenberg University Mainz (DE)
- Washington University in St. Louis (US)
- University of Virginia (US)
- Department of Pathology and Immunology, Washington University in St. Louis, St. Louis, MO, USA.
- Corresponding author
- Cugurra, Andrea
- Mamuladze, Tornike
- Rustenhoven, Justin
- Kipnis, Jonathan
- ORCID
- Venue
- Science
- Published
- 2021-07-23
- Volume
- 373
- Issue
- 6553
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC8863069
- OpenAlex
- W3164896384
- Cited by
- 681
- References
- 46
- Citations by year
- 2026: 133 · 2025: 136 · 2024: 130 · 2023: 137 · 2022: 106 · 2021: 38 · 2020: 1
- FWCI
- 41.13
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Archivio Istituzionale della Ricerca - Università Vita-Salute San Raffaele (submittedVersion)
- Funders
- National Institutes of Health (AT010416, AG034113, AG057496)
- National Center for Complementary and Alternative Medicine (DP1AT010416-02)
- National Institute of Neurological Disorders and Stroke (R01NS096967)
- JK National Institutes of Health (AG034113, AG057496)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Keywords
- dura mater, skull bone marrow, vertebral bone marrow, neuroinflammation, central nervous system injury, age-associated B cells, blood-brain barrier, meningeal immunity
- MeSH terms
- Animals, Bone Marrow, Bone Marrow Cells, Brain, Cell Movement, Central Nervous System, Central Nervous System Diseases, Dura Mater, Encephalomyelitis, Autoimmune, Experimental, Homeostasis, Meninges, Monocytes, Neutrophils, Skull, Spinal Cord, Spinal Cord Injuries, Spine, Myeloid Cells, Mice
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