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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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“5 (Hoeffel et al., 2015).”
Neuroendocrine Control of Macrophage Development and Function
Jurberg, A. D., Cotta-de-Almeida, V., Temerozo, J. R., Savino, W., Bou‐Habib, D. C., & Riederer, I. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01440 · Cited by 32
Mast Cells Occupy Stable Clonal Territories in Adult Steady-State Skin
Weitzmann, A., Naumann, R., Dudeck, A., Zerjatke, T., Gerbaulet, A., & Roers, A. (2020) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2020.03.963 · Cited by 30
Macrophages and Stem Cells—Two to Tango for Tissue Repair?
Manole, E., Niculite, C. M., Lambrescu, I. M., Gaina, G. F., Ioghen, O. C., Ceafalan, L. C., & Hinescu, M. E. (2021) · Biomolecules · doi:10.3390/biom11050697 · Cited by 33
“KCs are derived from fetal liver monocytic precursors that expand and maintain themselves through the entire life of the organism [78] by influencing liver progenitor cell invasion and phenotype through chemoattractant factors [79].”
BackgroundLu, L., Kuroishi, T., Tanaka, Y., Furukawa, M., Nochi, T., & Sugawara, S. (2022) · Scientific Reports · doi:10.1038/s41598-022-04941-5 · Cited by 31
Shaping immunity for life: Layered development of CD8 + T cells
Tabilas, C., Smith, N. L., & Rudd, B. D. (2023) · Immunological Reviews · doi:10.1111/imr.13185 · Cited by 30
The diverse roles of macrophages in metabolic inflammation and its resolution
Ray, A. G., Odum, O., Wiseman, D., & Weinstock, A. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1147434 · Cited by 31
“These cells are derived from embryonic tissues (yolk sac and the aorta-gonad-mesonephros-fetal liver axis (Yona et al., 2013; Gomez Perdiguero et al., 2015; Hoeffel et al., 2015; Wu and Hirschi, 2020)) and remain in the tissue throughout the lifetime of the organism.”
BackgroundLeveraging macrophage metabolism for anticancer therapy: opportunities and pitfalls
Saha, P., Ettel, P., & Weichhart, T. (2024) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2024.02.005 · Cited by 33
Habib, S., Osborn, G., Willsmore, Z. N., Chew, M. W., Jakubow, S., Fitzpatrick, A., Wu, Y., Sinha, K., Lloyd-Hughes, H., Geh, J. L. C., et al. (2024) · Expert Review of Clinical Immunology · doi:10.1080/1744666x.2024.2326626 · Cited by 30
“TRMs are embryonic-derived, generated during earlier stages of ontogeny that persist throughout life and can be recruited to the TME via the CSF-1/CSF-1 R pathway [9].”
BackgroundWang, Y., Li, T., Wang, F., Yao, X., Bai, Q., Su, H.-W., Li, J., Li, W., & Tan, R. (2024) · International Journal of Biological Sciences · doi:10.7150/ijbs.104404 · Cited by 30
Kordon, A. O., Abdelhamed, H., Ahmed, H. A., Park, J. Y., Karsi, A., & Pinchuk, L. M. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.02638 · Cited by 28
“New evidence has accumulated on the progenitors of adult tissue resident macrophages, embryonic macrophages (Schulz et al., 2012; Hashimoto et al., 2013; Epelman et al., 2014; Hoeffel et al., 2015; Sheng et al., 2015).”
BackgroundThe origin, fate and function of macrophages in the peripheral nervous system—an update
Amann, L., & Prinz, M. (2020) · International Immunology · doi:10.1093/intimm/dxaa030 · Cited by 34
A stratified myeloid system, the challenge of understanding macrophage diversity
Geissmann, F., & Mass, E. (2015) · Seminars in Immunology · doi:10.1016/j.smim.2016.03.016 · Cited by 29
Martín‐Estebané, M., Navascués, J., Sierra, A., Martín‐Guerrero, S. M., Cuadros, M. Á., Carrasco, M., & Marín‐Teva, J. L. (2017) · PLoS ONE · doi:10.1371/journal.pone.0182450 · Cited by 28
Xu, Y., Zhang, J., Hu, Y., Li, X., Sun, L., Yu, P., Sun, Y., Liu, B., Bian, Z., & Rong, Z. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109524 · Cited by 27
Sargeant, T. J., & Fourrier, C. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.09.015 · Cited by 32
The multifaceted role of macrophages during acute liver injury
Hassan, G. S., Molina, M. F., & Shoukry, N. H. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1237042 · Cited by 30
Glioma–Immune Cell Crosstalk in Tumor Progression
Elguindy, M. M., Young, J. S., Mondal, I., Lu, R. O., & Ho, W. S. (2024) · Cancers · doi:10.3390/cancers16020308 · Cited by 31
Embryonic circulating endothelial progenitor cells
del Moral, S. D., Barrena, S., Muñoz‐Chápuli, R., & Carmona, R. (2020) · Angiogenesis · doi:10.1007/s10456-020-09732-y · Cited by 27
No Evidence for Erythro-Myeloid Progenitor-Derived Vascular Endothelial Cells in Multiple Organs
Feng, T., Gao, Z., Kou, S., Huang, X., Jiang, Z., Lu, Z., Meng, J., Lin, C., & Zhang, H. (2020) · Circulation Research · doi:10.1161/circresaha.120.317442 · Cited by 26
Kidney inflammaging is promoted by CCR2+ macrophages and tissue-derived micro-environmental factors
Lefèvre, L., Iacovoni, J. S., Martini, H., Bellière, J., Maggiorani, D., Dutaur, M., Marsal, D. J., Decaunes, P., Pizzinat, N., Mialet‐Perez, J., et al. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03719-0 · Cited by 27
“Macrophages were identified in CD45+ renal immune cells, based on CD64 expression as previously described [6, 7, 9, 11], and monocyte-derived Fig.”
Microglial activation in Alzheimer's disease: The role of flavonoids and microRNAs
Medrano-Jiménez, E., Meza‐Sosa, K. F., Aragon, J. A. U., Secundino, I., Pedraza-Alva, G., & Pérez-Martínez, L. (2022) · Journal of Leukocyte Biology · doi:10.1002/jlb.3mr1021-531r · Cited by 28
Establishment of tissue-resident immune populations in the fetus
Feyaerts, D., Urbschat, C., Gaudilliere, B. L., & Stelzer, I. A. (2022) · Seminars in Immunopathology · doi:10.1007/s00281-022-00931-x · Cited by 30
“The role of fetal liver–derived monocytes in the establishment of AM in the murine fetus was confirmed in a fate-mapping approach [33, 34, 116].”
BackgroundInfluentialHow cell migration helps immune sentinels
Delgado, M., & Lennon‐Duménil, A. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.932472 · Cited by 27
Thomas, J. R., Appios, A., Calderbank, E. F., Yoshida, N., Zhao, X., Hamilton, R. S., Moffett, A., Sharkey, A., Laurenti, E., Hanna, C. W., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37383-2 · Cited by 31
The regulation of acute immune responses to the bacterial lung pathogenLegionella pneumophila
Brown, A. S., Yang, C., Hartland, E. L., & van Driel, I. R. (2016) · Journal of Leukocyte Biology · doi:10.1189/jlb.4mr0816-340r · Cited by 25
“are seeded in the tissue within the first few days after birth [27, 28] and are replenished in situ within the tissue [25, 29, 30].”
Background
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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