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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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The Biology of Dendritic Cells: In Health and Disease
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Developmental Origins of the Heterogeneous Hematopoiesis
Mo, S., & Yen, K. (2025) · American Journal of Hematology · doi:10.1002/ajh.70050 · Cited by 1
“Additionally, studies have shown that EMPs arising from distinct stages of Runx1-positive HE in the yolk sac exhibit distinct cell fate biases [171].”
Recapitulating Hematopoietic Development in a Dish
Vanuytsel, K., Steinberg, M. H., & Murphy, G. J. (2019) · Current human cell research and applications · doi:10.1007/978-981-13-3672-0_4 · Cited by 3
Development of Enteric Neurons and Muscularis Macrophages
Avetisyan, M. (2019) · Open Scholarship Institutional Repository (Washington University in St. Louis) · doi:10.7936/0zpy-av65 · Cited by 1
He, W., Zhang, Y., Cao, Z., Ye, Z., Lu, X., Fan, J., Peng, W., & Li, Z. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.732527 · Cited by 1
“Except microglia, it has been shown that yolk sac-derived EMPs also migrate to the embryonic fetal liver and other tissues (Hoeffel et al., 2015).”
BackgroundElsaid, R., Meunier, S., Burlen‐Defranoux, O., Soares‐da‐Silva, F., Perchet, T., Iturri, L., Freyer, L., Vieira, P., Pereira, P., Golub, R., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/791103 · Cited by 1
“For example, YS cells that contribute to erythropoiesis and megakaryopoiesis are also the source of tissue resident macrophages that persist throughout life (Bertrand, 2005; Gomez Perdiguero et al., 2015a; Hoeffel et al., 2015; McGrath et al., 2015).”
BackgroundThe landscape of human brain immune response in patients with severe COVID-19Preprint
Fullard, J., Lee, H.-C., Voloudakis, G., Suo, S.-B., Shao, Z., Peter, C., Javidfar, B., Zhang, W., Jiang, S., Corvelo, A., et al. (2021) · bioRxiv · doi:10.1101/2021.01.08.425999 · Cited by 1
“We included both brain and blood tissue models to better capture the transcriptome profiling of the microglial cell lineage ( 20, 21 ).”
MethodSureshchandra, S., Chan, C. N., Robino, J. J., Parmelee, L. K., Nash, M. J., Wesolowski, S. R., Pietras, E., Friedman, J., Takahashi, D., Shen, W.-N., et al. (2022) · bioRxiv · doi:10.1101/2021.04.26.441556
Li, F., Okreglicka, K. M., Pohlmeier, L. M., Schneider, C., & Köpf, M. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.06.04.447115 · Cited by 1
“Tissue-resident macrophages (MFTR) are heterogeneous cell populations, present in almost all tissues and play multiple tissue-specific functions in homeostasis and diseases (Davies et al, 2013; Hoeffel & Ginhoux, 2015).”
BackgroundStables, J., Green, E. K., Sehgal, A., Patkar, O. L., Keshvari, S., Taylor, I., Ashcroft, M. E., Grabert, K., Wollscheid-Lengeling, E., Szymkowiak, S., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.29.462493 · Cited by 1
“Csf1r mRNA is expressed in the earliest macrophages produced in the yolk sac (Lichanska et al., 1999) and subsequent development of macrophages in the mouse embryo depends upon CSF1R signalling (Hoeffel et al., 2015; Munro et al., 2020).”
BackgroundPetazzi, P., Ventura, T., Luongo, F. P., May, A., Taylor, H. A., Romanò, N., Forrester, L. M., Menéndez, P. R., & Fidanza, A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.10.04.510611 · Cited by 1
Elsaid, R., Mikdache, A., Quintero-Castillo, K., Salloum, Y., Diabangouaya, P., Gros, G., Feijóo, C. G., & Hernández, P. P. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.20.529211 · Cited by 1
Pancreatic macrophages: from ontogeny to phenotype and function
Ma, Z. (2023) · DR-NTU (Nanyang Technological University) · doi:10.32657/10356/172964 · Cited by 1
Ma, W., Chen, H., Gao, F., Zhao, H., Wu, N., Zhang, S., Zhu, Y., Zijian, X., Lan, Y., Liu, B., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.30.620640 · Cited by 1
Self-citationYolk sac-derived fetal macrophages suppress skin fibrosis and contribute to scarless wound healingPreprint
Sakai, S., Nakajima, Y., Takaya, K., Okabe, K., & Kishi, K. (2025) · Research Square · doi:10.21203/rs.3.rs-7478492/v1 · Cited by 1
Ontogeny and functional potential of founding dendritic cells in the developing lungPreprint
Soysa, R., Abideen, S., Reyes, V. Z., & Headley, M. B. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.30.679620 · Cited by 1
Microglia are not required for normal postnatal brain development and cognitive function in the ratPreprint
Green, E. K., Li, X., Guo, Y., Carter‐Cusack, D., Rojo, R., Lyall, M., Bell, A., Zheng, H., Teenan, O., Till, S. M., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.22.694658 · Cited by 1
Inflammation and immune-mediated neurobehavioral alterations : a critical role for microglia
Lacabanne, C. (2018) · theses.fr (ABES) · doi:10.70675/41a4e2a3zdbb7z4aa0z899dz9553bb07954b · Cited by 1
Primitive Macrophages Drive Coronary Development
Robbins, C. S., & Besla, R. (2016) · Circulation Research · doi:10.1161/circresaha.116.308778
Perfil de expressão gênica da micróglia humana e suas alterações relacionadas ao glioma
Galatro, T. F. D. A. (2016) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.5.2016.tde-17112016-164342
Constitutive heterogeneity and response diversity of microglia in pathological conditions
Gertig, U. (2016) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6043
Monocytes and Macrophages in the Aged Lung and Heart
Thoman, M. L., Bray, W., & Linton, P. (2017) · Springer eBooks · doi:10.1007/978-3-319-64597-1_94-1
Efeitos dos ácidos graxos na função de macrófagos de camundongos com diabetes tipo I induzido.
Braga, M. R. D. (2018) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.42.2018.tde-20022018-150159
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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