A combination of ontogeny and CNS environment establishes microglial identity
Open accessAbstract
Microglia, the brain's resident macrophages, are dynamic CNS custodians with surprising origins in the extra-embryonic yolk sac. The consequences of their distinct ontogeny are unknown but critical to understanding and treating brain diseases. We created a brain macrophage transplantation system to disentangle how environment and ontogeny specify microglial identity. We find that donor cells extensively engraft in the CNS of microglia-deficient mice, and even after exposure to a cell culture environment, microglia fully regain their identity when returned to the CNS. Though transplanted macrophages from multiple tissues can express microglial genes in the brain, only those of yolk-sac origin fully attain microglial identity. Transplanted macrophages of inappropriate origin, including primary human cells in a humanized host, express disease-associated genes and specific ontogeny markers. Through brain macrophage transplantation, we discover new principles of microglial identity that have broad applications to the study of disease and development of myeloid cell therapies.
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Yolk-sac-derived microglia marker genes are highly enriched in microglia and are not upregulated in monocytes that engraft the brain in microglia-depleted mouse models.
“These genes are highly enriched in microglia and are not upregulated in monocytes that engraft the brain in microglia-depleted mouse models”
From Cross-Species Single-Cell Analysis Reveals Divergence of the Primate Microglia Program (2019) · cites this paper as Bennett et al., 2018
The Results section on ontogeny markers reports that Gpr56 is expressed by yolk-sac-derived cells and microglia but not by engrafted HSC-lineage cells. However, the Results section on CNS-induced gene expression says engrafted cells of diverse origins express many other microglial signature genes at near-microglial levels. The claim is therefore supported for a specific ontogeny marker, not for microglial marker genes generally; page numbers are unavailable in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredWhen macrophages enter the CNS, they adopt a microglia-like phenotype and express markers considered to be microglia-specific, further confounding analysis.
“In addition, when macrophages enter the CNS, they adopt a microglia-like phenotype and express markers considered to be microglia-specific, further confounding analysis (Bennett et al., 2018).”
From Activated microglia drive demyelination via <scp>CSF1R</scp> signaling (2021) · cites this paper as Bennett et al., 2018
The Results section (“HSC-MLCs express markers distinct from YS-MLCs and microglia”) reports that transplanted macrophages can express microglial signature genes and TMEM119 in the brain, complicating attempts to distinguish them from microglia. But it specifies that this occurred in the Csf1r−/− transplantation model and did not occur following conventional bone marrow transplantation. The claim omits that condition and presents the effect as general whenever macrophages enter the CNS. (LLM, conf=0.87)
Experimental — accuracy not yet measuredOnce microglia are impaired by irradiation or genetic deficiencies, HSC-derived macrophages can efficiently and persistently colonize the brain parenchyma.
“Supporting this notion, once microglia are impaired by irradiation or genetic deficiencies, HSC-derived M F can efficiently and persistently colonize the brain parenchyma 14-17 .”
From Clonal hematopoiesis-associated motoric deficits caused by monocyte-derived microglia accumulating in aging mice (2025) · cites this paper as [17]
In Results (“Transplanted cells of diverse ontogeny engraft and ramify in the Csf1r−/− CNS”; page unavailable), the paper reports complete donor-cell coverage of the brain parenchyma by one month and stable occupancy for up to a year in genetically deficient mice. This supports efficient, persistent colonization in that setting. The reported experiment was irradiation-free, so this paper does not directly establish the irradiation part of the claim. (LLM, conf=0.84)
Experimental — accuracy not yet measuredExperimentally seeded parenchymal brain monocyte-derived macrophages retain epigenomes and expression signatures distinct from YS-derived cells and respond differentially to challenges, even after prolonged brain residence.
“Experimentally seeded parenchymal brain MoM F were shown to retain epigenomes and expression signatures distinct from YSderived cells and respond differentially to challenges, even following prolonged brain residence 14-17 .”
From Clonal hematopoiesis-associated motoric deficits caused by monocyte-derived microglia accumulating in aging mice (2025) · cites this paper as [17]
The Results sections on HSC ontogeny and distinct markers (page unavailable) show that engrafted HSC-derived macrophages retain gene-expression differences from YS-derived cells after months in the brain. Our copy does not establish distinct epigenomes or demonstrate that the engrafted populations respond differently when challenged; it only compares their expression profiles with gene sets associated with prior disease and LPS studies. (LLM, conf=0.86)
Experimental — accuracy not yet measuredRecent transplantation experiments suggest that Ms4a7 and other Cluster 6 markers are specific to hematopoietic-derived cells rather than yolk-sac progenitors.
“recent transplantation experiments suggest that Ms4a7 and other markers in Cluster 6 are specific to hematopoietic derived cells versus those derived from yolk-sac progenitors (Bennett et al., 2018).”
From Complex cell-state changes revealed by single cell RNA sequencing of 76,149 microglia throughout the mouse lifespan and in the injured brain (2018) · cites this paper as Bennett et al., 2018
In our dataset, the homeostatic microglial gene P2ry12 was lost from R6/2 striatum (FDR 5 0.1, LogFC = -0.7083 versus control).
“The loss of the homeostatic microglial gene P2ry12 (Bennett et al. , 2018) from the R6/2 striatum in our dataset (FDR 5 0.1, LogFC = -0.7083 versus control)”
From Microglial depletion prevents extracellular matrix changes and striatal volume reduction in a model of Huntington's disease (2020) · cites this paper as Bennett et al. , 2018
Only transplanted macrophages of yolk sac origin achieve full microglial identity.
“This study shows that transplanted macrophages from multiple tissues can express microglial genes in the brain; however, only those of yolk sac origin fully attain microglial identity.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [220]
Macrophages transplanted from various tissues are able to express microglial genes in the brain.
“This study shows that transplanted macrophages from multiple tissues can express microglial genes in the brain; however, only those of yolk sac origin fully attain microglial identity.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [220]
Yolk sac-derived microglia express Tmem119++, Sall1, Gpr56, and Apoe.
“Barres group recently identified Tmem119++/Sall1+/Gpr56+/Apoe+ as yolk sac-derived microglia, whereas hematopoietic stem cell-derived microglia-like cells express Tmem119+/Ms4a7+/Clec12a+/Apoe+++ suggesting lineage-specific microglia markers that can be useful in determining the origin of microglia [18, 19].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [18]
Lineage-specific microglial markers can be useful in determining the origin of microglia.
“suggesting lineage-specific microglia markers that can be useful in determining the origin of microglia [18, 19].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [18]
Microglia express a unique set of genes distinct from infiltrating monocytes and other immune cells.
“Recent genomic and proteomic studies revealed microglia express a unique set of genes distinct from infiltrating monocytes and other immune cells [18, 19].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [18]
Hematopoietic stem cell-derived microglia-like cells express Tmem119, Ms4a7, Clec12a, and high Apoe.
“Barres group recently identified Tmem119++/Sall1+/Gpr56+/Apoe+ as yolk sac-derived microglia, whereas hematopoietic stem cell-derived microglia-like cells express Tmem119+/Ms4a7+/Clec12a+/Apoe+++ suggesting lineage-specific microglia markers that can be useful in determining the origin of microglia [18, 19].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [18]
Additional CNS-specific cues are needed to maintain microglia specification.
“It can be reversed by engraftment of isolated cells into brains lacking microglia, suggesting that additional CNS-specific cues are required to sustain microglia specification [18, 66].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [18]
Engrafting isolated microglia into brains that lack microglia can reverse the immature phenotype.
“It can be reversed by engraftment of isolated cells into brains lacking microglia, suggesting that additional CNS-specific cues are required to sustain microglia specification [18, 66].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [18]
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Stem-cell-derived human microglia transplanted in mouse brain to study human disease
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To Kill a Microglia: A Case for CSF1R Inhibitors
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Beyond Hemostasis: Platelet Innate Immune Interactions and Thromboinflammation
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Microglia in Brain Development, Homeostasis, and Neurodegeneration
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Does tissue imprinting restrict macrophage plasticity?
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“While these cells do not necessarily upregulate genes expressed by homeostatic microglia [25, 66], the phenotypic similarities between populations of resident and infiltrating myeloid cells may approximate one another in neuroinflammation, hampering accurate identification of their respective functions in disease [298…”
BackgroundIntersection of pathological tau and microglia at the synapse
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APOE4 impairs the microglial response in Alzheimer’s disease by inducing TGFβ-mediated checkpoints
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“To distinguish peripheral recruited myeloid cells and BAMs from microglia, we reclustered all microglia-like cells and identified Ms4a7 + and Mrc1 + macrophages 25,26 and Lyve1 + BAMs 27,28 (Extended Data Fig.”
BackgroundAstrocytes and Microglia as Major Players of Myelin Production in Normal and Pathological Conditions
Traiffort, É., Kassoussi, A., Zahaf, A., & Laouarem, Y. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00079 · Cited by 189 · see citing works
Efficient Strategies for Microglia Replacement in the Central Nervous System
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Type-I-interferon-responsive microglia shape cortical development and behavior
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A new genetic strategy for targeting microglia in development and disease
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Microglia as hackers of the matrix: sculpting synapses and the extracellular space
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Microglia and Neurodevelopmental Disorders
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CNS-Native Myeloid Cells Drive Immune Suppression in the Brain Metastatic Niche through Cxcl10
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The microglial component of amyotrophic lateral sclerosis
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Astrocytes and microglia: Models and tools
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Multiomic spatial landscape of innate immune cells at human central nervous system borders
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Activated microglia drive demyelination via <scp>CSF1R</scp> signaling
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“tion, when macrophages enter the CNS, they adopt a microglia-like phenotype and express markers considered to be microglia-specific, further confounding analysis (Bennett et al., 2018).”
BackgroundHuman iPSC‐derived microglia: A growing toolset to study the brain's innate immune cells
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Self-citationTranscriptional and Epigenetic Regulation of Microglia in Health and Disease
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The immune system and psychiatric disease: a basic science perspective
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Self-citationPhenotypic impacts of CSF1R deficiencies in humans and model organisms
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Molecular and metabolic heterogeneity of astrocytes and microglia
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Self-citationTreatment of a genetic brain disease by CNS-wide microglia replacement
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Lymphatic Endothelial Cells Are Essential Components of the Subcapsular Sinus Macrophage Niche
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Isolation and Culture of Microglia
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Self-citationMicroglial Corpse Clearance: Lessons From Macrophages
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Microglial microRNAs mediate sex-specific responses to tau pathology
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Increased Macrophages and C1qA, C3, C4 Transcripts in the Midbrain of People With Schizophrenia
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The expanding world of tissue‐resident macrophages
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Ion Channels and Receptors as Determinants of Microglial Function
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- Authors
- Bennett, F. C., Bennett, M. L., Yaqoob, F., Mulinyawe, S. B., Grant, G. A., Hayden Gephart, M., Plowey, E. D., & Barres, B. A.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Bennett, F. Chris
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2018-06
- Volume
- 98
- Issue
- 6
- Pages
- 1170-1183.e8
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC6023731
- OpenAlex
- W2807609377
- Cited by
- 524
- References
- 59
- Citations by year
- 2026: 44 · 2025: 59 · 2024: 47 · 2023: 67 · 2022: 73 · 2021: 77 · 2020: 75 · 2019: 57 · 2018: 24
- FWCI
- 26.14
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (S10RR025518-01, NS069375, P50AG047366, R37DA01504317)
- NRSA (F31 NS078813, T32MH019938-22, K08MH112120, K08NS901527, R01CA216054-01, K08 NS075144)
- JPB Foundation
- the Dr. Miriam and Sheldon G. Adelson Medical Research Foundation (853, 04-7023433)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Keywords
- microglia, microglial reprogramming, disease-associated microglia, humanized mice, microglial markers
- MeSH terms
- Animals, Brain, Central Nervous System, Hematopoietic Stem Cells, Humans, Macrophages, Receptors, Granulocyte-Macrophage Colony-Stimulating Factor, Microglia, Mice, Knockout, Cell Lineage, Mice
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