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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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BackgroundNovel insights into embryonic cardiac macrophages
Gula, G., & Ratajska, A. (2022) · Developmental Biology · doi:10.1016/j.ydbio.2022.05.003 · Cited by 12
Larkin, C. J., Arrieta, V. A., Najem, H., Li, G., Zhang, P., Miska, J. M., Chen, P., James, C. D., Sonabend, A. M., & Heimberger, A. B. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.907605 · Cited by 9
“Evidence for this includes that these yolk sac-derived macrophages do not rely on the transcription factor c-Myb, which is necessary for differentiation of erythroid-myeloid progenitors into monocytes prior to differentiation into macrophages (18), providing a clear distinction from monocyte-derived macrophages (19, 2…”
BackgroundThe evolving views of hematopoiesis: from embryo to adulthood and from in vivo to in vitro
Zhang, Y., & Liu, F. (2023) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2023.09.005 · Cited by 9
A subset of megakaryocytes regulates development of hematopoietic stem cell precursors
Lan, W., Li, J., Ye, Z., Liu, Y., Luo, S., Lu, X., Cao, Z., Chen, Y., Chen, H., & Li, Z. (2024) · The EMBO Journal · doi:10.1038/s44318-024-00079-4 · Cited by 10
“One day later, erythroid-myeloid progenitors (EMP) have the ability to generate Mks in the yolk sac, independent of Myb (Tober et al, 2007; Tober et al, 2008; Xu et al, 2001).”
The Role of Cardiac Tissue Macrophages in Homeostasis and Disease
Ilinykh, A., & Pinto, A. R. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-57613-8_6 · Cited by 10
Kitic, M., See, P., Bruttger, J., Ginhoux, F., & Waisman, A. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9658-2_16 · Cited by 11
Self-citationSignaling pathways that control mRNA translation initiation in macrophages
Tabatabaei, N., Hou, S., Kim, K.-W., & Tahmasebi, S. (2020) · Cellular Signalling · doi:10.1016/j.cellsig.2020.109700 · Cited by 10
Tissue-specific features of microglial innate immune responses
Timmerman, R., Burm, S. M., & Bajramovic, J. J. (2020) · Neurochemistry International · doi:10.1016/j.neuint.2020.104924 · Cited by 10
Worthington, A. K., Cool, T., Poscablo, D. M., Hussaini, A., Beaudin, A. E., & Forsberg, E. C. (2022) · Development · doi:10.1242/dev.200139 · Cited by 11
Self-citationHan, M., Geng, J., Zhang, S., Rao, J., Zhu, Y., Xu, S., Wang, F., Ma, F., Zhou, M., & Zhou, H. (2023) · European Journal of Immunology · doi:10.1002/eji.202350474 · Cited by 12
Baer, J. M., Zuo, C., Kang, L., de la Lastra, A. A., Borcherding, N. C., Knolhoff, B. L., Bogner, S. J., Zhu, Y., Lewis, M. A., Zhang, N., et al. (2022) · SSRN Electronic Journal · doi:10.1101/2022.02.09.479745 · Cited by 10
“…with monocyte-derived cells over time, to varying extents determined at a tissue-specific level (Bain et al., 2016; Epelman et al., 2014a; Ginhoux et al., 2010; Ginhoux and Guilliams, 2016; Hashimoto et al., 2013; Hoeffel et al., 2015; Liu et al., 2019; Schulz et al., 2012; Yona et al., 2013).”
BackgroundRosin, J. M., Tretiakov, N., Hanniman, E., Hampton, K., & Kurrasch, D. M. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.830399 · Cited by 10
“…ng/mL (Nesan et al., 2021), while human studies show BPA levels in maternal serum can vary considerably and range anywhere between 0.46 and 22 ng/mL (Ikezuki et al., 2002; Schonfelder et al., 2002; Kuroda et al., 2003; Padmanabhan et al., 2008), which is 1.15–55-fold higher than what was measured…”
BackgroundInfluentialThe ontogenesis and heterogeneity of basophils
Park, J., & Kang, S. (2024) · Discovery Immunology · doi:10.1093/discim/kyae003 · Cited by 10
“Late EMP-derived fetal liver monocytes replace YS macrophages in many organs during the perinatal period, including the liver, lung, and epidermis [122].”
BackgroundBiswas, M. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1375528 · Cited by 11
“Cell fate mapping and antibody depletion studies proved that YS-derived macrophages are F4/80 hi in MG, persist lifelong, and express canonical macrophage markers (CD64, MerTK, CD206, C1qa, CSfr1, and Spi) but lack dendritic cell markers (CD11c, Zbtb46, and Itgax) (28, 29).”
BackgroundPongma, C., Keawvilai, P., Boonmee, A., Wongprom, B., Pattarakankul, T., Sittplangkoon, C., Alameh, M., Kueanjinda, P., Heyes, J. A., Lam, K., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-85234-5 · Cited by 9
“KCs are of embryonic origin and are capable of self-renewal with limited contributions from circulating monocytes 5 .”
Shaping immunity: the influence of the maternal gut bacteria on fetal immune development
Faas, M. M., & Smink, A. M. (2025) · Seminars in Immunopathology · doi:10.1007/s00281-025-01039-8 · Cited by 12
“These macrophages are thought to replace the fetal macrophages arising from the first yolk sac-derived primitive progenitors in most tissues, except for the brain, and remain in the tissues in adult life [87, 89–93].”
InfluentialTissue-resident macrophages and renal diseases: landscapes and treatment directions
Qu, Z., Chu, J., Jin, S., Yang, C., Zang, J., Zhang, J., Xu, D., & Cheng, M. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1548053 · Cited by 8
Weinhaus, B., Homan, S. M., Kincaid, M., Tadwalkar, A., Gu, X., Kumar, S. R., Slaughter, A., Zhang, J., Wu, Q., Kofron, M. J., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-59058-w · Cited by 9
“4,20,21 and Fig.”
InfluentialTissue-resident macrophages: from zebrafish to mouse
Lin, X., Wen, Z., & Xu, J. (2019) · Blood Science · doi:10.1097/bs9.0000000000000013 · Cited by 9
“to predominantly generate microglia in adult mice, whereas the late emergedMyb EMPs, which likely depend onMyb function, gave rise to other adult TRMs.(13,14) Although the EMP-origin theory of TRMs has become the prevailing view, dissonance still”
BackgroundInfluentialAkula, S., Lara, S., Olsson, A., & Hellman, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23105818 · Cited by 10
Wu, X., Ni, Y., Li, W., Yang, B., Yang, X., Zhu, Z., Zhang, J., Wu, X., Shen, Q., Liao, Z., et al. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.105556 · Cited by 9
“The fi rst wave occurs in the yolk sac and generates primitive macrophages, which migrate to the brain and form microglia (18 – 22).”
BackgroundStable biomarker for plastic microglia
Segal, B. M., & Giger, R. J. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1601669113 · Cited by 9
Tsc1 controls the development and function of alveolar macrophages
Chen, S., Yang, Q., Liu, J., Huang, H., Shi, M., & Feng, X. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.03.027 · Cited by 7
The Role of Macrophages in Oocyte Donation Pregnancy: A Systematic Review
Tian, X., Eikmans, M., & van der Hoorn, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21030939 · Cited by 9
“In addition, once the fetal liver is operational, erythro-myeloid progenitors that seed in the fetal liver start to differentiate into tissue-resident macrophages [22].”
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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