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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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BackgroundEarly antitumor activity of oral Langerhans cells is compromised by a carcinogen
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“The contribution of circulating monocytes to the resident macrophage pool is instead dominant in inflammatory contexts, such as infection and cancer.((33,35-38)) The origin of TAMs notwithstanding, a large body of literature indicates that these cells—in particular in the M2 polarized state—tend to have strong protumo…”
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“Do microglia originate from primitive Mac [100,101] or from early EMPs [97,102,103]? Is it possible that we are calling the same cells with different names? Progenitors of microglia have a CD45− c-Kit+ immunophenotype, the same as the progenitors of primitive Mac [94,102].”
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BackgroundMouse placenta fetal macrophages arise from endothelial cells outside the placenta
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“These Mφ can self-renew, but recent studies have shown their input from the bone marrow as well (Gomez Perdiguero et al., 2015; Hoeffel et al., 2015; Scott et al., 2016).”
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Self-citationCross Talk Between Macrophages and Cancer Cells in the Bone Metastatic Environment
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“5) from yolk sac-derived erythromyeloid precursors and share a common transcriptional program that diverges with time in their respective tissues of residence (Hoeffel et al., 2015; Mass et al., 2016).”
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BackgroundNew concepts in macrophage ontogeny in the adult neural retina
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Macrophages Orchestrate the Liver Tumor Microenvironment
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InfluentialMesenchymal stem cells-based therapy in liver diseases
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BackgroundMultiple waves of fetal‐derived immune cells constitute adult immune system
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“Under steady state conditions, the local population of KCs is maintained by self-renewal (McDonald and Kubes, 2016) independent of bone marrow (BM)-derived progenitors (Yona et al., 2013; Hoeffel et al., 2015).”
BackgroundCx3cr1 controls kidney resident macrophage heterogeneity
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Self-citationCell competition for neuron-derived trophic factor controls the turnover and lifespan of microglia
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“Interestingly, the primitive population of YS-MACs seems to persist after birth in peripheral and perivascular locations.”
BackgroundMethodInfluentialIntercellular genetic tracing of cardiac endothelium in the developing heart
Liu, K., Jin, H., Zhang, S., Tang, M., Meng, X., Li, Y., Pu, W., Lui, K. O., & Zhou, B. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.05.021 · Cited by 20
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Zhao, L., Wang, Z., Tan, Y., Ma, J., Huang, W., Zhang, X., Jin, C., Zhang, T., Liu, W., & Yang, Y. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.115039 · Cited by 20
The Biological Function of Kupffer Cells in Liver Disease
Ma, Y., Yang, M., He, Z., Wei, Q., & Li, J. (2017) · InTech eBooks · doi:10.5772/67673 · Cited by 21
The developing immune network in human prenatal skin
Botting, R. A., & Haniffa, M. A. (2020) · Immunology · doi:10.1111/imm.13192 · Cited by 19
Alveolar Macrophages in Viral Respiratory Infections: Sentinels and Saboteurs of Lung Defense
Pöpperl, P., Stoff, M., & Beineke, A. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26010407 · Cited by 21
“AlvM ϕ originate from fetal precursors and seed the lung during the embryogenesis phase [8–10].”
Placental chemokine compartmentalisation: A novel mammalian molecular control mechanism
Lee, K. M., Wilson, G. J., Pingen, M., Fukuoka, A., Hansell, C. A. H., Bartolini, R., Medina‐Ruiz, L., & Graham, G. J. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000287 · Cited by 18
KIT Is Required for Fetal Liver Hematopoiesis
Fantin, A., Plein, A., Tacconi, C., Villa, E., Ceccacci, E., Denti, L., & Ruhrberg, C. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.648630 · Cited by 18
Macrophage-Associated Disorders: Pathophysiology, Treatment Challenges, and Possible Solutions
Yadav, D. K., Pradhan, M., Singh, D., & Singh, M. R. (2022) · Springer eBooks · doi:10.1007/978-3-030-84164-5_4 · Cited by 20
Ander, S. E., Li, F. S., Carpentier, K. S., & Morrison, T. E. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010474 · Cited by 20
An improved organotypic cell culture system to study tissue-resident macrophages ex vivo
Aktories, P., Petry, P., Glatz, P., Andrieux, G., Oschwald, A., Botterer, H., Gorka, O., Erny, D., Boerries, M., Henneke, P., et al. (2022) · Cell Reports Methods · doi:10.1016/j.crmeth.2022.100260 · Cited by 19
Zhao, Y. X., Song, J., Bao, X. W., Zhang, J., Wu, J. C., Wang, L. Y., He, C., Shao, W., Bai, X. L., Liang, T., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113364 · Cited by 21
Bobotis, B. C., Halvorson, T., Carrier, M., & Tremblay, M. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1317125 · Cited by 22
Sheng, J., Ruedl, C., & Karjalainen, K. (2015) · Immunity · doi:10.1016/j.immuni.2015.11.023 · Cited by 19
“Interestingly though, the study of Hoeffel et al. (2015) recently showed that a wave of fetal monocytes replaced the early EMP-derived macrophages in all tissues, and we would argue that this wave was the product of fetal HSCs and not EMPs as the authors speculate (Hoeffel et al., 2015).”
ResultPolarization of M2 Tumor-Associated Macrophages (TAMs) in Cancer Immunotherapy
Bui, I., & Bonavida, B. (2024) · Critical Reviews™ in Oncogenesis · doi:10.1615/critrevoncog.2024053830 · Cited by 18
A Comprehensive Outlook on Pulmonary Alveolar Proteinosis—A Review
Wołoszczak, J., Wrześniewska, M., Hrapkowicz, A., Janowska, K., Szydziak, J., & Gomułka, K. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25137092 · Cited by 18
“Circulating monocytes have only a partial contribution to the AMs composition, as they mostly derive from the embryonic monocyte progenitors of the yolk sac or fetal liver into the lung, where they differentiate into AMs [12,15].”
BackgroundElchaninov, A. V., Lokhonina, А. V., Nikitina, M., Vishnyakova, P., Макаров, А. В., Arutyunyan, I. V., Poltavets, A. S., Kananykhina, E. Y., Kovalchuk, S. I., Karpulevich, E., et al. (2020) · Biomedicines · doi:10.3390/biomedicines8120627 · Cited by 17
“The proportion of bone marrow macrophages in the liver of mice may constitute about 7% [7], whereas other authors (by using a different, more specific set of markers) reduce this estimation to 2–5% [5,8].”
BackgroundA new method for obtaining bankable and expandable adult-like microglia in mice
You, M., Rim, C., Kang, Y., & Kwon, M. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02351-4 · Cited by 16
“5 and surround the neuroepithelial layer (NEL) in the part corresponding to the head [1, 13].”
BackgroundXu, Y., Schrank, P. R., & Williams, J. W. (2022) · Current Protocols · doi:10.1002/cpz1.456 · Cited by 16
“Conclusions were supplemented with key work from other Xu et al. 15 of 22 Current Protocols groups applying additional CX3CR1creER, Flt3cre, and RunxMerCreMer fate-mapping systems (Bain et al., 2014; Bain et al., 2016; Epelman et al., 2014; Hoeffel et al., 2015; Yona et al., 2013).”
MethodFetal CCL2 signaling mediates offspring social behavior and recapitulates effects of prenatal stress
Chen, H. J., Galley, J. D., Verosky, B. G., Yang, F. T., Rajasekera, T. A., Bailey, M. T., & Gur, T. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.10.032 · Cited by 18
Tissue‐resident macrophages — how to humanize our knowledge
Schlitzer, A., & Schultze, J. L. (2016) · Immunology and Cell Biology · doi:10.1038/icb.2016.82 · Cited by 20
Resident Macrophages in Cystic Kidney Disease
Li, Z., Zimmerman, K. A., & Yoder, B. K. (2020) · Kidney360 · doi:10.34067/kid.0006052020 · Cited by 18
“They are derived in a Myb-independent manner from erythro-myeloid progenitors that are first generated in the fetal yolk sac, colonize the fetal liver, and migrate into the kidney during early development (12, 13, 17).”
BackgroundTang, W., He, J., Huang, T., Bai, Z., Wang, C., Wang, H., Yang, R., Ni, Y., Hou, J. W., Wang, J., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.728057 · Cited by 17
Ehlers, G., Tödtmann, A. M., Holsten, L., Willers, M., Heckmann, J., Schöning, J., Richter, M., Heinemann, A. S., Pirr, S. M., Heinz, A., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-57357-w · Cited by 20
“3f-i (see our answer to point 8-b).”
Microglia and neuroinflammation: function, heterogeneity, and crosstalk
Zong, S., Cui, X., Wu, S., & Lu, Z. (2026) · Cellular and Molecular Immunology · doi:10.1038/s41423-026-01438-3 · Cited by 28
“5, abundant FL monocytes in fi ltrate nearly all peripheral tissues but fail to invade the brain [16].”
Zhou, Z., Pan, X., & Li, L. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1070208 · Cited by 19
Hu, Z., Jin, X., Hong, W., Sui, Q., Zhao, M., Huang, Y., Li, M., Wang, Q., Zhan, C., & Chen, Z. (2023) · Cellular Oncology · doi:10.1007/s13402-023-00816-7 · Cited by 18
Microglia, synaptic dynamics and forgetting
Wang, C., Wang, L., & Gu, Y. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.06.005 · Cited by 20
Rasaei, R., Tyagi, A., Rasaei, S., Lee, S., Yang, S., Kim, K.-S., Ramakrishna, S., & Hong, S. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-03136-z · Cited by 18
Ahamed, F., Eppler, N., Jones, E., & Zhang, Y. (2024) · Livers · doi:10.3390/livers4030033 · Cited by 17
“…in rats, their lifespan extends from several weeks to months [60,61]. are of embryonic origin, with some derived from hematopoietic stem cells [58,59 The average half-life of mouse KCs is KCs are self-renewing and can proliferate into mature cells, making their replenishment in a steady state…”
Defining the Hoxb8 cell lineage during murine definitive hematopoiesis
Deren, D. A. V., De, S., Xu, B., Eschenbacher, K. M., Zhang, S., & Capecchi, M. R. (2022) · Development · doi:10.1242/dev.200200 · Cited by 18
Li, Z., Zimmerman, K. A., Cherakara, S., Chumley, P. H., Collawn, J. F., Wang, J., Haycraft, C. J., Song, C. J., Chacana, T., Andersen, R. S., et al. (2022) · Disease Models & Mechanisms · doi:10.1242/dmm.049810 · Cited by 16
“In mice, renal macrophages can be categorized into two populations based on their origin (Munro and Hughes, 2017; Liu et al., 2020; Hoeffel et al., 2015; Gomez Perdiguero et al., 2015; Zimmerman et al., 2019a).”
Coffee, antioxidants, and brain inflammation
Rai, S. P., Ansari, A. H., Singh, D., & Singh, S. (2024) · Progress in brain research · doi:10.1016/bs.pbr.2024.06.005 · Cited by 20
Wnt-5A/B Signaling in Hematopoiesis throughout Life
de Rezende, M. M., Justo, G. Z., Paredes‐Gamero, E. J., & Gosens, R. (2020) · Cells · doi:10.3390/cells9081801 · Cited by 17
“In this context, it is noteworthy that other cells than HSC also seem to have roles in hematopoietic cell production, as described for tissue macrophages [57,58].”
Quarta, A., Berneman, Z. N., & Ponsaerts, P. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.3ru0820-536r · Cited by 17
CSF1R as a Therapeutic Target in Bone Diseases: Obvious but Not so Simple
Hume, D. A., Batoon, L., Sehgal, A., Keshvari, S., & Irvine, K. M. (2022) · Current Osteoporosis Reports · doi:10.1007/s11914-022-00757-4 · Cited by 17
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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