Cited by 371Neuroinflammation and Neurodegeneration MechanismsSingle-cell and spatial transcriptomicsMultiple Sclerosis Research Studies

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Dual ontogeny of disease-associated microglia and disease inflammatory macrophages in aging and neurodegeneration

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Silvin, Aymeric, Uderhardt, Stefan, Piot, Cecile, Da Mesquita, Sandro, Yang, Katharine, Geirsdottir, Laufey, Mulder, Kevin, Eyal, David, Liu, Zhaoyuan, Bridlance, Cecile, Thion, Morgane Sonia, Zhang, Xiao Meng, Kong, Wan Ting, Deloger, Marc, Fontes, Vasco, Weiner, Assaf, Ee, Rachel, Dress, Regine, Hang, Jing Wen, Balachander, Akhila, Chakarov, Svetoslav, Malleret, Benoit, Dunsmore, Garett, Cexus, Olivier, Chen, Jinmiao, Garel, Sonia, Dutertre, Charles Antoine, Amit, Ido, Kipnis, Jonathan, Ginhoux, Florent·2022·Immunity

DOI 10.1016/j.immuni.2022.07.004

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Abstract

Brain macrophage populations include parenchymal microglia, border-associated macrophages, and recruited monocyte-derived cells; together, they control brain development and homeostasis but are also implicated in aging pathogenesis and neurodegeneration. The phenotypes, localization, and functions of each population in different contexts have yet to be resolved. We generated a murine brain myeloid scRNA-seq integration to systematically delineate brain macrophage populations. We show that the previously identified disease-associated microglia (DAM) population detected in murine Alzheimer's disease models actually comprises two ontogenetically and functionally distinct cell lineages: embryonically derived triggering receptor expressed on myeloid cells 2 (TREM2)-dependent DAM expressing a neuroprotective signature and monocyte-derived TREM2-expressing disease inflammatory macrophages (DIMs) accumulating in the brain during aging. These two distinct populations appear to also be conserved in the human brain. Herein, we generate an ontogeny-resolved model of brain myeloid cell heterogeneity in development, homeostasis, and disease and identify cellular targets for the treatment of neurodegeneration.

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Authors: Silvin, A., Uderhardt, S., Piot, C., Da Mesquita, S., Yang, K., Geirsdottir, L., Mulder, K., Eyal, D., Liu, Z., Bridlance, C., Thion, M. S., Zhang, X. M., Kong, W. T., Deloger, M., Fontes, V., Weiner, A., Ee, R., Dress, R., Hang, J. W., Balachander, A., Chakarov, S., Malleret, B., Dunsmore, G., Cexus, O., Chen, J., Garel, S., Dutertre, C. A., Amit, I., Kipnis, J., & Ginhoux, F.
Affiliations: Agency for Science, Technology and Research (SG)
Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
Inserm (FR)
Shanghai Jiao Tong University (CN)
Centre National de la Recherche Scientifique (FR)
Weizmann Institute of Science (IL)
National University of Singapore (SG)
Washington University in St. Louis (US)
Corresponding author: Ginhoux, Florent
ORCID: Silvin, Aymeric
Uderhardt, Stefan
Yang, Katharine
Mulder, Kevin
Liu, Zhaoyuan
Thion, Morgane Sonia
Zhang, Xiao Meng
Kong, Wan Ting
Deloger, Marc
Fontes, Vasco
Weiner, Assaf
Dress, Regine
Hang, Jing Wen
Balachander, Akhila
Chakarov, Svetoslav
Dunsmore, Garett
Cexus, Olivier
Chen, Jinmiao
Garel, Sonia
Dutertre, Charles Antoine
Amit, Ido
Kipnis, Jonathan
Ginhoux, Florent
Venue: Immunity
Publisher: Elsevier BV
Published: 2022-08
Volume: 55
Issue: 8
Pages: 1448-1465.e6
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/j.immuni.2022.07.004
OpenAlex: W4289794258
Cited by: 368
References: 69
Citations by year: 2026: 80 · 2025: 99 · 2024: 100 · 2023: 77 · 2022: 10
FWCI: 25.27
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 660 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Immunity (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
Keywords: disease-associated microglia, brain macrophages, TREM2, monocyte-derived macrophages, border-associated macrophages, aging, neurodegeneration, Alzheimer's disease, neuroprotection, single-cell transcriptomics
MeSH terms: Aging, Alzheimer Disease, Animals, Brain, Humans, Macrophages, Membrane Glycoproteins, Receptors, Immunologic, Microglia, Mice

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Dual ontogeny of disease-associated microglia and disease inflammatory macrophages in aging and neurodegeneration

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