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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Spi1 and Irf8 are core orchestrators for microglia development.
“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
The Introduction and Results describe the yolk-sac macrophage origin of microglia, but do not identify Spi1 or Irf8 as regulators of their development. Searches for Spi1, Irf8, PU.1, and IRF8 found no passage in our copy addressing that claim; page numbers were unavailable. (LLM, conf=0.75)
Experimental — accuracy not yet measuredThe PU.1-high, IRF8-high, MYB-low expression pattern in pMGLs is consistent with microglia emerging from PU.1- and IRF8-dependent but MYB-independent cells.
“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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Park, M. D., Silvin, A., Ginhoux, F., & Merad, M. (2022) · Cell · doi:10.1016/j.cell.2022.10.007 · Cited by 644 · see citing works
Self-citationPathological sequelae of long-haul COVID
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Mechanisms of Organ Injury and Repair by Macrophages
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Efficient derivation of microglia-like cells from human pluripotent stem cells
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“Contrary to the long-held mononuclear phagocyte system hypothesis that macrophages derive solely from circulating monocytes (van Furth and Cohn, 1968), recent studies have described three distinct macrophage precursors that are produced in independent waves during development (Christensen et al., 2004; Ginhoux and Jun…”
BackgroundResultInfluentialThe development and maintenance of resident macrophages
Perdiguero, E. G., & Geissmann, F. (2015) · Nature Immunology · doi:10.1038/ni.3341 · Cited by 634 · see citing works
Bonnardel, J., T’Jonck, W., Gaublomme, D., Browaeys, R., Scott, C. L., Martens, L., Vanneste, B., De Prijck, S., Nedospasov, S. A., Kremer, A., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.08.017 · Cited by 631 · see citing works
“Under homeostatic conditions, monocytes circulate in the liver sinusoids but do not contribute to the adult KC pool (Hoeffel et al., 2015; Schulz et al., 2012; Scott et al., 2016; Yona et al., 2013).”
BackgroundBiology of lung macrophages in health and disease
Aegerter, H., Lambrecht, B. N., & Jakubzick, C. (2022) · Immunity · doi:10.1016/j.immuni.2022.08.010 · Cited by 628 · see citing works
Microglia are an essential component of the neuroprotective scar that forms after spinal cord injury
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Self-citationMicroglia and Central Nervous System–Associated Macrophages—From Origin to Disease Modulation
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“Our own work (Buchrieser et al., 2017) and that of others (Hoeffel et al., 2015) indicates that this protocol produces MYB-independent myeloid cells, recapitulating an embryonic ontogeny, and lineage-tracking studies in mouse have demonstrated that microglia derive from primitive, yolk sac…”
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“…yolk sac (YS) primitive macrophages (Ginhoux et al. 2010; Hoeffel et al. 2012; Schulz et al. 2012; Kierdorf et al. 2013; Gomez Perdiguero et al. 2015; Hoeffel et al. 2015), reside in the brain throughout life, and maintain their numbers through a process of self-renewal (Hashimoto et al. 2013).”
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“Therefore, we individually transplanted whole tissues and sorted myeloid cells into the Csf1r / CNS at P0–P4, including YSderived cells from yolk sac and fetal brain, HSC-derived cells from blood and bonemarrow (BM), andmonocytes from the fetal liver, which, at embryonic day 13 (E13)–E14, contains a mix of HSC- and YS…”
Microglial subtypes: diversity within the microglial community
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“5 (Hoeffel et al , 2015), and fully during the first postnatal weeks (Squarzoni et al , 2014).”
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BackgroundInfluentialYao, Y., Jeyanathan, M., Haddadi, S., Barra, N. G., Vaseghi‐Shanjani, M., Damjanovic, D., Lai, R., Afkhami, S., Chen, Y., Dvorkin‐Gheva, A., et al. (2018) · Cell · doi:10.1016/j.cell.2018.09.042 · Cited by 520 · see citing works
“AMs turn over slowly and are of embryonic origin and self-maintained in steady state (Gomez Perdiguero et al., 2015; Guilliams et al., 2013b; Hoeffel et al., 2015).”
Microglial regional heterogeneity and its role in the brain
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Self-citationDeterminants of resident tissue macrophage identity and function
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Self-citationMicroglia in Central Nervous System Inflammation and Multiple Sclerosis Pathology
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Microglia and Beyond: Innate Immune Cells As Regulators of Brain Development and Behavioral Function
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“Microglia arise from yolk-sac fetal macrophages, whereas other tissue macrophages arise from precursors generated slightly later in development (20, 21).”
BackgroundMost Tissue-Resident Macrophages Except Microglia Are Derived from Fetal Hematopoietic Stem Cells
Sheng, J., Ruedl, C., & Karjalainen, K. (2015) · Immunity · doi:10.1016/j.immuni.2015.07.016 · Cited by 482 · see citing works
“showed very recently that FL monocytes can replace earlier YS-derived macrophages in most tissues (Hoeffel et al., 2015).”
Microbiome–microglia connections via the gut–brain axis
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Three Unique Interstitial Macrophages in the Murine Lung at Steady State
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Self-citationCross-Species Single-Cell Analysis Reveals Divergence of the Primate Microglia Program
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Self-citationChemokine-Induced Macrophage Polarization in Inflammatory Conditions
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“5 yolk sac prior to formation of the fetal liver (Tober et al. 2007; Perdiguero et al. 2014; Hoeffel et al. 2015).”
BackgroundResultInfluentialEarly Fate Defines Microglia and Non-parenchymal Brain Macrophage Development
Utz, S. G., See, P., Mildenberger, W., Thion, M. S., Silvin, A., Lutz, M., Ingelfinger, F., Rayan, N. A., Lelios, I., Buttgereit, A., et al. (2020) · Cell · doi:10.1016/j.cell.2020.03.021 · Cited by 436 · see citing works
Self-citationMacrophages and lipid metabolism
Remmerie, A., & Scott, C. L. (2018) · Cellular Immunology · doi:10.1016/j.cellimm.2018.01.020 · Cited by 385 · see citing works
The roles of tumor-associated macrophages in tumor angiogenesis and metastasis.
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“…from fetal monocytes or hematopoietic stem cells, leading to either complete replacement of yolk sack–derived macrophages or mixed populations that are dominated by cells of the fetal monocyte or hematopoietic stem cell lineage (Epelman et al., 2014; Hoeffel et al., 2015; Sheng et al., 2015).”
BackgroundInfluentialAmit, I., Winter, D. R., & Jung, S. (2015) · Nature Immunology · doi:10.1038/ni.3325 · Cited by 406 · see citing works
Does niche competition determine the origin of tissue-resident macrophages?
Guilliams, M., & Scott, C. L. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.42 · Cited by 409 · see citing works
Liver macrophages in health and disease
Guilliams, M., & Scott, C. L. (2022) · Immunity · doi:10.1016/j.immuni.2022.08.002 · Cited by 395 · see citing works
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Fetal monocytes and the origins of tissue-resident macrophages
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Self-citationOntogeny and homeostasis of CNS myeloid cells
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Tissue-resident macrophages in the intestine are long lived and defined by Tim-4 and CD4 expression
Shaw, T. N., Houston, S. A., Wemyss, K., Bridgeman, H. M., Barbera, T. A., Zangerle-Murray, T., Strangward, P., Ridley, A. J. L., Wang, P., Tamoutounour, S., et al. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20180019 · Cited by 382 · see citing works
“…often arising from embryonic or perinatal precursors that are maintained locally and independently of blood monocytes at homeostasis (Ginhoux et al., 2010; Hoeffel et al., 2012, 2015; Schulz et al., 2012; Hashimoto et al., 2013; Yona et al., 2013; Sheng et al., 2015; Ginhoux and Guilliams, 2016).”
BackgroundImmune dysregulation in amyotrophic lateral sclerosis: mechanisms and emerging therapies
Beers, D. R., & Appel, S. H. (2019) · The Lancet Neurology · doi:10.1016/s1474-4422(18)30394-6 · Cited by 387 · see citing works
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Macrophage Polarization and Osteoporosis: A Review
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Neuroinflammation: Microglia and T Cells Get Ready to Tango
Schetters, S. T. T., Gómez‐Nicola, D., García-Vallejo, J. J., & van Kooyk, Y. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01905 · Cited by 378 · see citing works
“This could have two important consequences: (1) the insoluble antigen is unable to drain to secondary lymphoid structures where T cells are primed and (2) the insoluble antigen may harbor neo-antigens that can be presented by microglia on MHCII.”
BackgroundInfluentialEnsan, S., Li, A., Besla, R., Degousee, N., Cosme, J., Roufaiel, M., Shikatani, E. A., El-Maklizi, M., Williams, J. W., Robins, L., et al. (2016) · Nature Immunology · doi:10.1038/ni.3343 · Cited by 372 · see citing works
Monocytes and macrophages in tissue repair: Implications for immunoregenerative biomaterial design
Ogle, M. E., Segar, C. E., Sridhar, S., & Botchwey, E. A. (2016) · Experimental Biology and Medicine · doi:10.1177/1535370216650293 · Cited by 378 · see citing works
Tissue macrophages: origin, heterogenity, biological functions, diseases and therapeutic targets
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Macrophages in intestinal homeostasis and inflammatory bowel disease
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Macrophage-Mediated Inflammation in Skin Wound Healing
Hassanshahi, A., Moradzad, M., Ghalamkari, S., Fadaei, M., Cowin, A. J., & Hassanshahi, M. (2022) · Cells · doi:10.3390/cells11192953 · Cited by 364 · see citing works
Ontogeny of Tissue-Resident Macrophages
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“The use of the S100a4-Cre fate-mapping model in our hands supports these observations and similar conclusions were obtained for BM and peritoneal macrophages (15).”
BackgroundMethodResultInfluentialSelf-citationMacrophages: An Inflammatory Link Between Angiogenesis and Lymphangiogenesis
Corliss, B. A., Azimi, M. S., Munson, J. M., Peirce, S. M., & Murfee, W. L. (2016) · Microcirculation · doi:10.1111/micc.12259 · Cited by 356 · see citing works
“Early EMPs give rise to YS-Mac that eventually populate the brain to become microglia, the tissue-resident macrophage for that organ [113].”
BackgroundThe Cytokine TGF-β Promotes the Development and Homeostasis of Alveolar Macrophages
Yu, X., Buttgereit, A., Lelios, I., Utz, S. G., Cansever, D., Becher, B., & Greter, M. (2017) · Immunity · doi:10.1016/j.immuni.2017.10.007 · Cited by 346 · see citing works
Self-citationTakata, K., Kozaki, T., Lee, C., Thion, M. S., Otsuka, M., Lim, S. H., Utami, K. H., Fidan, K., Park, D. S., Malleret, B., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.06.017 · Cited by 352 · see citing works
Self-citationOrigin, Differentiation, and Function of Intestinal Macrophages
Bain, C. C., & Schridde, A. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02733 · Cited by 348 · see citing works
Bain, C. C., Hawley, C. A., Garner, H., Scott, C. L., Schridde, A., Steers, N. J., Mack, M., Joshi, A., Guilliams, M., Mowat, A. M. I., et al. (2016) · Nature Communications · doi:10.1038/ncomms11852 · Cited by 527 · see citing works
Roles of macrophages in tumor development: a spatiotemporal perspective
Bied, M., Ho, W. W., Ginhoux, F., & Blériot, C. (2023) · Cellular and Molecular Immunology · doi:10.1038/s41423-023-01061-6 · Cited by 360 · see citing works
Self-citationHemogenic Endothelial Fate Mapping Reveals Dual Developmental Origin of Mast Cells
Gentek, R., Ghigo, C., Hoeffel, G., Bulle, M. J., Msallam, R., Gautier, G., Launay, P., Chen, J., Ginhoux, F., & Bajénoff, M. (2018) · Immunity · doi:10.1016/j.immuni.2018.04.025 · Cited by 338 · see citing works
Self-citationPrimitive Embryonic Macrophages are Required for Coronary Development and Maturation
Leid, J. M., Carrelha, J., Boukarabila, H., Epelman, S., Jacobsen, S. E. W., & Lavine, K. J. (2016) · Circulation Research · doi:10.1161/circresaha.115.308270 · Cited by 327 · see citing works
“sac–derived erythromyeloid progenitor that migrates from the yolk sac to the liver during midgestation.(13) For example,”
Molecular and epigenetic basis of macrophage polarized activation
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Epigenetic regulation of macrophages: from homeostasis maintenance to host defense
Chen, S., Yang, J., Wei, Y., & Wei, X. (2019) · Cellular and Molecular Immunology · doi:10.1038/s41423-019-0315-0 · Cited by 317 · see citing works
“Fetal monocytes differentiate into macrophages when recruited to fetal tissues, replacing the main components of the existing yolk-sac-derived macrophages gradually with the exception of microglia.(35) With the growth of host tissues, these primitive macrophages differentiate through proliferating in their respective…”
BackgroundTumor-associated macrophages in cancer: recent advancements in cancer nanoimmunotherapies
Kumari, N., & Choi, S. H. (2022) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-022-02272-x · Cited by 324 · see citing works
Pulmonary Macrophages: A New Therapeutic Pathway in Fibrosing Lung Disease?
Byrne, A. J., Maher, T. M., & Lloyd, C. M. (2016) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2016.02.004 · Cited by 314 · see citing works
“Subsequently, this work was confirmed using depletion and fate-mapping mouse models of yolk sac and fetal liver macrophages, respectively [26,27].”
Revisiting Mouse Peritoneal Macrophages: Heterogeneity, Development, and Function
Cassado, A. D. A., D’Império Lima, M. R., & Bortoluci, K. R. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00225 · Cited by 315 · see citing works
Neuroinflammation in Alzheimer’s Disease
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“Other tissue macrophages develop from precursors that emerge later in life [103,104].”
BackgroundMacrophages as Key Drivers of Cancer Progression and Metastasis
Nielsen, S. R., & Schmid, M. C. (2017) · Mediators of Inflammation · doi:10.1155/2017/9624760 · Cited by 281 · see citing works
“Fate mapping has identified yolk sac-derived macrophages as the main precursor for brain microglia [11], whereas fetal liverderived monocytes are the main precursor of liver Kupffer cells and lung alveolar macrophages [12, 13], while bone marrow-derived monocytes replenish intestinal and cardiac macrophages in the ste…”
Background
- 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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