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C-Myb+ Erythro-Myeloid Progenitor-Derived Fetal Monocytes Give Rise to Adult Tissue-Resident Macrophages
Open accessAbstract
Although classified as hematopoietic cells, tissue-resident macrophages (MFs) arise from embryonic precursors that seed the tissues prior to birth to generate a self-renewing population, which is maintained independently of adult hematopoiesis. Here we reveal the identity of these embryonic precursors using an in utero MF-depletion strategy and fate-mapping of yolk sac (YS) and fetal liver (FL) hematopoiesis. We show that YS MFs are the main precursors of microglia, while most other MFs derive from fetal monocytes (MOs). Both YS MFs and fetal MOs arise from erythro-myeloid progenitors (EMPs) generated in the YS. In the YS, EMPs gave rise to MFs without monocytic intermediates, while EMP seeding the FL upon the establishment of blood circulation acquired c-Myb expression and gave rise to fetal MOs that then seeded embryonic tissues and differentiated into MFs. Thus, adult tissue-resident MFs established from hematopoietic stem cell-independent embryonic precursors arise from two distinct developmental programs.
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“The transcription factors Spi1 and Irf8 have been shown to be the core orchestrators for microglia development”
From Cross-Species Single-Cell Analysis Reveals Divergence of the Primate Microglia Program (2019) · cites this paper as Hoeffel et al., 2015
Experimental — accuracy not yet measuredIn the citing paper
“consistent with microglia emerging from PU.1 and IRF8-dependent, but MYB-independent cells 34–37.”
From Efficient derivation of microglia-like cells from human pluripotent stem cells (2016) · cites this paper as [36]
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Keirsse, J., Damme, H. V., Geeraerts, X., Beschin, A., Raes, G., & Ginderachter, J. A. V. (2018) · Cellular Immunology · doi:10.1016/j.cellimm.2018.03.010 · Cited by 65
Mass, E. (2018) · International Immunology · doi:10.1093/intimm/dxy044 · Cited by 65
Central metabolic interactions of immune cells and microbes: prospects for defeating infections
Traven, A., & Naderer, T. (2019) · EMBO Reports · doi:10.15252/embr.201947995 · Cited by 60
“…and pathogens, as well as between different innate immune cells, as all tissue-resident macrophages likely originate from yolk sac and foetal liver progenitor cells, and are thus distinct from monocyte differentiated macrophages that originate from bone haematopoietic stem cells [11 – 14].”
Thion, M. S., Mosser, C., Férézou, I., Grisel, P., Baptista, S., Low, D., Ginhoux, F., Garel, S., & Audinat, É. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.086 · Cited by 64
Self-citationSimic, M., Manosalva, I., Spinelli, L., Gentek, R., Shayan, R. R., Siret, C., Girard-Madoux, M. J. H., Wang, S., de Fabritus, L., Verschoor, J., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108004 · Cited by 64
“Similar to other innate immune lineages, such as macrophages and mast cells (Gentek et al., 2018; Hoeffel et al., 2015), in the adult, LTi cells are replaced by cells from definitive HSCs.”
BackgroundBone marrow-derived Ly6C− macrophages promote ischemia-induced chronic kidney disease
Yang, Q., Wang, Y., Pei, G., Deng, X., Jiang, H., Wu, J., Zhou, C., Guo, Y., Yao, Y., Zeng, R., et al. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1531-3 · Cited by 65
Tay, T. L., Carrier, M., & Tremblay, M. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-9913-8_6 · Cited by 61
Iturri, L., Freyer, L., Biton, A., Dardenne, P., Lallemand, Y., & Perdiguero, E. G. (2020) · Immunity · doi:10.1016/j.immuni.2021.04.026 · Cited by 65
“EMPs then enter the bloodstream at the beginning of circulation and colonize the fetal liver, where they expand and differentiate into erythrocytes, megakaryocytes, macrophages, monocytes, granulocytes and mast cells (Gomez Perdiguero et al., 2015; Hoeffel et al., 2015; McGrath et al., 2015; Gentek et al., 2018; Li et…”
BackgroundSkin barrier immunology from early life to adulthood
Trompette, A., & Ubags, N. D. J. (2023) · Mucosal Immunology · doi:10.1016/j.mucimm.2023.02.005 · Cited by 67
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“The pre-microglia progenitor is developmentally distinct from most other resident tissue macrophages in terms of gene expression (Bennett et al., 2018; Hoeffel et al., 2015; Sheng et al., 2015).”
BackgroundInteractions between macrophages and helminths
Coakley, G., & Harris, N. L. (2020) · Parasite Immunology · doi:10.1111/pim.12717 · Cited by 59
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Biology of resident tissue macrophages
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Self-citationMacrophages: Key regulators of steady-state and demand-adapted hematopoiesis
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“28 [13] Hoeffel G, Chen J, Lavin Y, et al.”
BackgroundRedox-signals and macrophage biology
Weigert, A., von Knethen, A., Fuhrmann, D. C., Dehne, N., & Brüne, B. (2018) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2018.01.003 · Cited by 60
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“The transcription factor Myb is essential in the definitive hematopoiesis (Hoeffel et al., 2015).”
InfluentialMacrophages Orchestrate Hematopoietic Programs and Regulate HSC Function During Inflammatory Stress
Seyfried, A. N., Maloney, J., & MacNamara, K. C. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01499 · Cited by 61
“Primitive macrophage progenitors arise from the yolk sac to seed the developing tissues, including brain and fetal liver, giving rise to microglia in the brain and premacrophages in the fetal liver (19, 20).”
BackgroundMast cell ontogeny: From fetal development to life‐long health and disease
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“This paradigm has shifted during the past 5 years (Ginhoux and Jung 2014; Gomez Perdiguero et al. 2015; Guilliams et al. 2014; Hoeffel et al. 2015); fate mapping and lineage-tracing studies have demonstrated that, in the steady state, most tissue-resident MΦ are derived from erythro-myeloid…”
BackgroundHuman iPSC-liver organoid transplantation reduces fibrosis through immunomodulation
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“In the developing liver, stellate cells and ECs express the MF-recruiting factor CSF1, resulting in the influx of yolk sac–derived MFs followed by gradual replacement with monocyte-derived MFs ( 17 , 42 ).”
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Macrophage compartmentalization in the brain and cerebrospinal fluid system
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“However, in contrast to cDCs which arise from bonemarrowHSCs, LCs develop from yolk sac and fetal liver precursors and are thus developmentally related to tissue-resident macrophages (Hoeffel et al., 2012, 2015).”
BackgroundSelf-citationThe Innate Immune Response in Myocardial Infarction, Repair, and Regeneration
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Self-citationDynamic plasticity of macrophage functions in diseased liver
Ritz, T., Krenkel, O., & Tacke, F. (2017) · Cellular Immunology · doi:10.1016/j.cellimm.2017.12.007 · Cited by 58
Interactions among myeloid regulatory cells in cancer
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Metadata
- Authors
- Hoeffel, G., Chen, J., Lavin, Y., Low, D., Almeida, F. F., See, P., Beaudin, A. E., Lum, J., Low, I., Forsberg, E. C., Poidinger, M., Zolezzi, F., Larbi, A., Ng, L. G., Chan, J. K. Y., Greter, M., Becher, B., Samokhvalov, I. M., Merad, M., & Ginhoux, F.
- Affiliations
- Agency for Science, Technology and Research (SG)
- Tisch Cancer Institute (US)
- University of California, Santa Cruz (US)
- University of Zurich (CH)
- Chinese Academy of Sciences (CN)
- Corresponding author
- Ginhoux, Florent
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2015-04
- Volume
- 42
- Issue
- 4
- Pages
- 665-678
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC4545768
- OpenAlex
- W2023666964
- Cited by
- 1,135
- References
- 55
- Citations by year
- 2026: 64 · 2025: 84 · 2024: 111 · 2023: 99 · 2022: 135 · 2021: 122 · 2020: 118 · 2019: 102 · 2018: 107 · 2017: 81 · 2016: 67 · 2015: 44
- FWCI
- 77.82
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- National University of Singapore (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Funders
- National Heart, Lung, and Blood Institute (HL086899, R01HL086899)
- National Cancer Institute (R01CA173861, R01CA112100, CA112100, R01CA190400)
- National Institute of Allergy and Infectious Diseases (AI080884, R01AI080884)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK100917)
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- tissue-resident macrophages, erythro-myeloid progenitors, microglia, yolk sac hematopoiesis, fetal liver hematopoiesis, MYB, fate mapping
- MeSH terms
- Aging, Animals, Cell Differentiation, Embryo, Mammalian, Female, Fetus, Hematopoietic Stem Cells, Kidney, Liver, Lung, Macrophages, Monocytes, Pregnancy, Skin, Yolk Sac, Biomarkers, Microglia, Cell Lineage, Proto-Oncogene Proteins c-myb, Myeloid Progenitor Cells, Mice, Cell Tracking, Primary Cell Culture
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