The DOI matches its Crossref record; 55 of the 55 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Fate Mapping Analysis Reveals That Adult Microglia Derive from Primitive Macrophages
Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., Mehler, M. F., Conway, S. J., Ng, L. G., Stanley, E. R., et al. (2010) · Science · doi:10.1126/science.1194637 · Cited by 5,175
Self-citationBlood Monocytes Consist of Two Principal Subsets with Distinct Migratory Properties
Geissmann, F., Jung, S., & Littman, D. R. (2003) · Immunity · doi:10.1016/s1074-7613(03)00174-2 · Cited by 3,504
Fate Mapping Reveals Origins and Dynamics of Monocytes and Tissue Macrophages under Homeostasis
Yona, S., Kim, K.-W., Wolf, Y., Mildner, A., Varol, D., Breker, M., Strauss-Ayali, D., Viukov, S., Guilliams, M., Misharin, A., et al. (2013) · Immunity · doi:10.1016/j.immuni.2012.12.001 · Cited by 3,245
CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis
Qian, B.-Z., Li, J., Zhang, H., Kitamura, T., Zhang, J., Campion, L. R., Kaiser, E. A., Snyder, L. A., & Pollard, J. W. (2011) · Nature · doi:10.1038/nature10138 · Cited by 2,874
A Lineage of Myeloid Cells Independent of Myb and Hematopoietic Stem Cells
Schulz, C., Perdiguero, E. G., Chorro, L., Szabo-Rogers, H., Cagnard, N., Kierdorf, K., Prinz, M., Wu, B., Jacobsen, S. E. W., Pollard, J. W., et al. (2012) · Science · doi:10.1126/science.1219179 · Cited by 2,578
Hematopoiesis: An Evolving Paradigm for Stem Cell Biology
Orkin, S. H., & Zon, L. I. (2008) · Cell · doi:10.1016/j.cell.2008.01.025 · Cited by 2,570
Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors
Gomez Perdiguero, E., Klapproth, K., Schulz, C., Busch, K., Azzoni, E., Crozet, L., Garner, H., Trouillet, C., de Bruijn, M. F., Geissmann, F., et al. (2015) · Nature · doi:10.1038/nature13989 · Cited by 2,339
Hashimoto, D., Chow, A., Noizat, C., Teo, P., Beasley, M. B., Leboeuf, M., Becker, C. D., See, P., Price, J., Lucas, D., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.04.004 · Cited by 2,311
Self-citationVisualizing Spatiotemporal Dynamics of Multicellular Cell-Cycle Progression
Sakaue-Sawano, A., Kurokawa, H., Morimura, T., Hanyu, A., Hama, H., Osawa, H., Kashiwagi, S., Fukami, K., Miyata, T., Miyoshi, H., et al. (2008) · Cell · doi:10.1016/j.cell.2007.12.033 · Cited by 2,194
Pericytes are required for blood–brain barrier integrity during embryogenesis
Daneman, R., Zhou, L., Kebede, A. A., & Barres, B. A. (2010) · Nature · doi:10.1038/nature09513 · Cited by 2,128
Flagged first, then by citations
Cited by
Sorted by citations
Items 201–300 of 1,000
Alveolar and lung interstitial macrophages: Definitions, functions, and roles in lung fibrosis
Shi, T., Denney, L., An, H., Ho, L., & Zheng, Y. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.3ru0720-418r · Cited by 146
Human and Mouse Mononuclear Phagocyte Networks: A Tale of Two Species?
Reynolds, G., & Haniffa, M. A. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00330 · Cited by 138
Macrophage activation in human diseases
Schultze, J. L., Schmieder, A., & Goerdt, S. (2015) · Seminars in Immunology · doi:10.1016/j.smim.2015.07.003 · Cited by 134
Two distinct ontogenies confer heterogeneity to mouse brain microglia
De, S., Deren, D. A. V., Peden, E., Hockin, M., Boulet, A. M., Titen, S. W. A., & Capecchi, M. R. (2018) · Development · doi:10.1242/dev.152306 · Cited by 139
Sphingosine-1-Phosphate and Macrophage Biology—How the Sphinx Tames the Big Eater
Weigert, A., Olesch, C., & Brüne, B. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01706 · Cited by 130
“They can be derived from early hematopoiesis in the yolk sac (11–17) or the fetal liver, without transitioning through a monocytic intermediate stage (16, 17).”
BackgroundPhenotypic impacts of CSF1R deficiencies in humans and model organisms
Hume, D. A., Caruso, M., Ferrari-Cestari, M., SUMMERS, K. M., Pridans, C., & Irvine, K. M. (2019) · Journal of Leukocyte Biology · doi:10.1002/jlb.mr0519-143r · Cited by 125
Differential Location and Distribution of Hepatic Immune Cells
Freitas-Lopes, M., Mafra, K., David, B., Carvalho-Gontijo, R., & Menezes, G. (2017) · Cells · doi:10.3390/cells6040048 · Cited by 126
“DCs may be also classified into two main subsets that include classical/conventional DCs (cDCs) and plasmacytoid DCs (pDCs) [76].”
BackgroundThe influence of environment and origin on brain resident macrophages and implications for therapy
Bennett, M. L., & Bennett, F. C. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0545-6 · Cited by 136
Hou, S., Li, Z., Zheng, X., Gao, Y., Dong, J., Ni, Y., Wang, X., Li, Y., Ding, X., Chang, Z., et al. (2020) · Cell Research · doi:10.1038/s41422-020-0300-2 · Cited by 127
Macrophages and Cardiovascular Health
Frodermann, V., & Nahrendorf, M. (2018) · Physiological Reviews · doi:10.1152/physrev.00068.2017 · Cited by 128
Targeting innate immunity for neurodegenerative disorders of the central nervous system
Andreasson, K. I., Bachstetter, A. D., Colonna, M., Ginhoux, F., Holmes, C., Lamb, B., Landreth, G., Lee, D. C., Low, D., Lynch, M. A., et al. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13667 · Cited by 126
Self-citationImmunology of the ageing kidney
Sato, Y., & Yanagita, M. (2019) · Nature Reviews Nephrology · doi:10.1038/s41581-019-0185-9 · Cited by 126
Guilliams, M., & van de Laar, L. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00406 · Cited by 135
“The Level1 that forms the scaffold of the herein proposed classification system is in part based on elegant murine fate-mapping systems developed to study the cellular origin of MΦs (33, 34, 38, 39, 43, 44) and DCs [(123) and (124) in this issue].”
BackgroundMacrophages and Dendritic Cells
Cybulsky, M. I., Cheong, C., & Robbins, C. S. (2016) · Circulation Research · doi:10.1161/circresaha.115.306542 · Cited by 130
Perdiguero, E. G., Klapproth, K., Schulz, C., Busch, K., Bruijn, M. F. T. R. D., Rodewald, H.-R., & Geissmann, F. (2015) · Immunity · doi:10.1016/j.immuni.2015.11.022 · Cited by 122
“A subsequent report confirmed our findings that yolk-sacderived EMPs are the origin of tissuemac- rophages and further suggested that macrophages arise either directly from EMPs or later from fetal monocytes that are, however, also derived from EMPs (Hoeffel et al., 2015).”
ResultNayak, D. K., Zhou, F., Xu, M., Huang, J., Tsuji, M., Hachem, R. R., & Mohanakumar, T. (2016) · American Journal of Transplantation · doi:10.1111/ajt.13819 · Cited by 127
“Freshly collected BAL cells were incubated with human BD Fc Block (BD Biosciences) and human TruStain FcX (Biolegend, San Diego, CA) to inhibit Fc-specific binding, followed by staining with following Abs (obtained from Biolegend and eBioscience, San Diego, CA): CD45-Alexa Fluor 488 (HI30), CD11b-Phycoerythrin/Cyanine…”
MethodNew perspectives on the origins and heterogeneity of mast cells
John, A. L. S., Rathore, A. P. S., & Ginhoux, F. (2022) · Nature reviews. Immunology · doi:10.1038/s41577-022-00731-2 · Cited by 127
Self-citationSingle-cell transcriptomics reveal the dynamic of haematopoietic stem cell production in the aorta
Baron, C. S., Kester, L. A., Klaus, A., Boisset, J.-C., Thambyrajah, R., Yvernogeau, L., Kouskoff, V., Lacaud, G., van Oudenaarden, A., & Robin, C. (2018) · Nature Communications · doi:10.1038/s41467-018-04893-3 · Cited by 115
Langerhans cell origin and regulation
Collin, M., & Milne, P. (2016) · Current Opinion in Hematology · doi:10.1097/moh.0000000000000202 · Cited by 120
Ferrero, G., Mahony, C. B., Dupuis, E., Yvernogeau, L., Ruggiero, E. D., Miserocchi, M., Caron, M., Robin, C., Traver, D. J., Bertrand, J. Y., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.066 · Cited by 124
“In a recent report, Hoeffel et al. (2015) proposed to categorize the mouse EMP population into early c-Myb -independent EMPs and late c-Myb -dependent EMPs, emerging in the yolk sac at E7.”
BackgroundInfluentialNiche-specific functional heterogeneity of intestinal resident macrophages
Viola, M. F., & Boeckxstaens, G. E. (2020) · Gut · doi:10.1136/gutjnl-2020-323121 · Cited by 122
“20 However, the exact contribution of each wave of embryonic precursors to the different mature macrophage pools in the adult is subject to intense debate; as yet, not all transcription factors involved have been identified.”
BackgroundScalable production of tissue-like vascularized liver organoids from human PSCs
Harrison, S. P., Siller, R., Tanaka, Y., Chollet, M. E., de la Morena-Barrio, M. E., Xiang, Y., Patterson, B., Andersen, E., Bravo-Pérez, C., Kempf, H., et al. (2023) · Experimental & Molecular Medicine · doi:10.1038/s12276-023-01074-1 · Cited by 119
McMenamin, P. G., Saban, D. R., & Dando, S. J. (2019) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2018.12.002 · Cited by 115
“The seminal paper from Ginhoux et al. demonstrated that adult brain MG arise directly from the yolk sac (Ginhoux et al., 2010), by early erythromyeloid progenitors (EMP) (Gomez Perdiguero et al., 2015; Hoeffel et al., 2015; Kierdorf et al., 2013).”
BackgroundThe Origins and Functions of Tissue-Resident Macrophages in Kidney Development
Munro, D. A. D., & Hughes, J. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00837 · Cited by 124
“The trends shown in the yolk sac-derived and monocyte-derived macrophage graphs are based on fate-mapping experiments by Hoeffel et al. (2015).”
BackgroundInfluentialStudying tissue macrophages in vitro: are iPSC-derived cells the answer?
Lee, C., Kozaki, T., & Ginhoux, F. (2018) · Nature reviews. Immunology · doi:10.1038/s41577-018-0054-y · Cited by 124
Self-citationCheng, M. L., Nakib, D., Perciani, C. T., & MacParland, S. A. (2021) · Clinical Science · doi:10.1042/cs20190654 · Cited by 130
Capturing the Fantastic Voyage of Monocytes Through Time and Space
Teh, Y. C., Ding, J. L., Ng, L. G., & Chong, S. Z. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00834 · Cited by 120
“Functionally, fetal monocytes share many common traits with adult BM-derived monocytes but have reduced expression of antigen presentation and pathogen recognition-associated genes (26).”
BackgroundSelf-citationBurgess, M. O., Wicks, K., Gardasevic, M., & Mace, K. A. (2019) · ImmunoHorizons · doi:10.4049/immunohorizons.1900038 · Cited by 119
Specification and function of hemogenic endothelium during embryogenesis
Gritz, E. C., & Hirschi, K. K. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2134-0 · Cited by 114
Macrophage Modification Strategies for Efficient Cell Therapy
Poltavets, A. S., Vishnyakova, P., Elchaninov, A. V., Sukhikh, G. T., & Fatkhudinov, T. (2020) · Cells · doi:10.3390/cells9061535 · Cited by 117
A limited capacity for microglial repopulation in the adult brain
Najafi, A. R., Crapser, J., Jiang, S., Ng, W., Mortazavi, A., West, B. L., & Green, K. N. (2018) · Glia · doi:10.1002/glia.23477 · Cited by 99
“Unique among myeloid cell types, microglia directly derive from yolk sac macrophage precursors, and colonize the CNS early in development (Ginhoux et al., 2010; Hoeffel et al., 2015).”
BackgroundRosin, J. M., Vora, S. R., & Kurrasch, D. M. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.07.023 · Cited by 113
Epidermal γδ T cells originate from yolk sac hematopoiesis and clonally self-renew in the adult
Gentek, R., Ghigo, C., Hoeffel, G., Jorquera, A., Msallam, R., Wienert, S., Klauschen, F., Ginhoux, F., & Bajénoff, M. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20181206 · Cited by 112
Self-citationUnderstanding the heterogeneity of resident liver macrophages
Blériot, C., & Ginhoux, F. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02694 · Cited by 107
Self-citationDevelopment and Functions of Alveolar Macrophages
Woo, Y. D., Jeong, D., & Chung, D. H. (2021) · Molecules and Cells · doi:10.14348/molcells.2021.0058 · Cited by 110
“Moreover, the tdTomato signals of Mx1-cre × R26Tomato and S100a4-cre × R26Tomato fate-mapping mice were high in circulating monocytes, but low in AMs, indicating that circulating monocytes rarely serve as precursors of AMs (Hoeffel et al., 2015).”
BackgroundMethodInfluentialThe early life education of the immune system: Moms, microbes and (missed) opportunities
Jain, N. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1824564 · Cited by 119
Resident Innate Immune Cells in the Cornea
Liu, J., & Li, Z. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.620284 · Cited by 114
“5 or after birth, hematopoietic stem cells (HSCs) are differentiated into monocytes, and some of these monocytes migrate into peripheral tissue and differentiate into macrophages (81, 82).”
BackgroundFullard, J. F., Lee, H.-C., Voloudakis, G., Suo, S., Javidfar, B., Shao, Z., Peter, C. J., Zhang, W., Jiang, S., Corvelo, A., et al. (2021) · Genome Medicine · doi:10.1186/s13073-021-00933-8 · Cited by 108
“6% of all cells in the brain parenchyma [37], we also included blood tissue models corresponding to immune cells which are close to the microglial cell lineage [38, 39].”
BackgroundMacrophages in periodontitis: A dynamic shift between tissue destruction and repair
Yin, L., Li, X., & Hou, J. L. (2022) · Japanese Dental Science Review · doi:10.1016/j.jdsr.2022.10.002 · Cited by 119
Gao, S., Shi, Q., Zhang, Y., Liang, G., Kang, Z., Huang, B., Ma, D., Wang, L., Jiao, J., Fang, X., et al. (2021) · Cell Research · doi:10.1038/s41422-021-00540-7 · Cited by 113
Heterogeneous origins and functions of mouse skeletal muscle-resident macrophages
Wang, X., Sathe, A. A., Smith, G. R., Ruf-Zamojski, F. M., Nair, V., Lavine, K. J., Xing, C., Sealfon, S. C., & Zhou, L. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1915950117 · Cited by 120
“Fetal liver MOs seed numerous embryonic tissues except for brain (14).”
BackgroundInfluentialUnderstanding the Biology of Self-Renewing Macrophages
Rőszer, T. (2018) · Cells · doi:10.3390/cells7080103 · Cited by 115
Generation of mature kupffer cells from human induced pluripotent stem cells
Tasnim, F., Xing, J., Huang, X., Mo, S., Wei, X., Tan, M., & Yu, H. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.11.016 · Cited by 111
Yamazaki, T., Nalbandian, A., Uchida, Y., Li, W., Arnold, T. D., Kubota, Y., Yamamoto, S., Ema, M., & Mukouyama, Y. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.069 · Cited by 105
“Specifically, in the central nervous system, pericytes are an important contributor to the integrity of the blood-brain barrier (BBB) (Armulik et al., 2011; Hirschi and D’Amore, 1996).”
BackgroundInfluentialYe, Y., Zhao, J., Lu, Y., Gao, C.-C., Yang, Y., Liang, S.-Q., Lu, Y., Wang, L., Yue, S., Dou, K., et al. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-1691 · Cited by 107
Role of the Monocyte–Macrophage System in Normal Pregnancy and Preeclampsia
Vishnyakova, P., Elchaninov, A. V., Fatkhudinov, T., & Sukhikh, G. T. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20153695 · Cited by 106
“Microglial precursors migrate directly to the central nervous system and mature within [6].”
BackgroundWang, M., Yang, Y., Cansever, D., Wang, Y., Kantores, C., Messiaen, S., Moison, D., Livera, G., Chakarov, S., Weinberger, T., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2013686117 · Cited by 108
“During steady-state development brain microglia, epidermal LCs, liver KCs, and lung AMs are minimally replaced with circulatory monocytes (7).”
BackgroundInfluentialSelf-citationCrosstalk between macrophages and cardiac cells after myocardial infarction
Jian, Y., Zhou, X. J., Shan, W., Chen, C., Ge, W., Cui, J., Yi, W., & Sun, Y. (2023) · Cell Communication and Signaling · doi:10.1186/s12964-023-01105-4 · Cited by 114
Platelets and diseases: signal transduction and advances in targeted therapy
Tian, Y., Yao, Z., Pang, Y., Zheng, Z., Ma, Y., Zhang, C., & Gao, J. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02198-8 · Cited by 134
“…MKs. 18 At fi rst, multifunctional hematopoietic stem cells undergo directed differentiation in hematopoietic tissue to form primitive MKs. 19,20 23 Besides, research has shown that lungs are the main site where late-stage platelets are produced, with many MKs circulating in the lungs and…”
liu, J., Xue, Y., Dong, D., Xiao, C., Lin, C., Wang, H., Song, F., Fu, T., Wang, Z., Chen, J., et al. (2017) · Mucosal Immunology · doi:10.1038/mi.2016.139 · Cited by 104
“5 or after birth, HSCs differentiate into monocytes and migrate into peripheral tissues where a proportion of these monocytes differentiate into macrophages.(13,14) Thus, macrophages are a heterogeneous cell population, and each population of macrophages migrates into peripheral tissues during different stages of deve…”
BackgroundSelf-citationPuranik, A. S., Leaf, I. A., Jensen, M. A., Hedayat, A. F., Saad, A., Kim, K.-W., Saadalla, A. M., Woollard, J. R., Kashyap, S., Textor, S. C., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-31887-4 · Cited by 109
Tissue-resident macrophages regulate lymphatic vessel growth and patterning in the developing heart
Cahill, T. J., Sun, X., Ravaud, C., del Campo, C. V., Klaourakis, K., Lupu, I.-E., Lord, A. M., Browne, C., Jacobsen, S. E. W., Greaves, D. R., et al. (2021) · Development · doi:10.1242/dev.194563 · Cited by 105
Macrophage Heterogeneity in Kidney Injury and Fibrosis
Wen, Y., Yan, H.-R., Wang, B., & Liu, B. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.681748 · Cited by 102
“F4/80 ADGRE1 Human, Mouse Cell Membrane Receptor (13, 18, 30, 36, 40, 44, 45, 55, 56, 81, 82)”
BackgroundInfluentialThe origins and roles of osteoclasts in bone development, homeostasis and repair
Yahara, Y., Nguyen, T., Ishikawa, K., Kamei, K., & Alman, B. A. (2022) · Development · doi:10.1242/dev.199908 · Cited by 111
Functional regulation of decidual macrophages during pregnancy
Sun, F., Wang, S., & Du, M. (2020) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2020.103264 · Cited by 104
Origins and diversity of macrophages in health and disease
Sreejit, G., Fleetwood, A. J., Murphy, A. J., & Nagareddy, P. R. (2020) · Clinical & Translational Immunology · doi:10.1002/cti2.1222 · Cited by 112
“replaced by non-labelled precursors before birth.(19,67,68) Contributions of YS versus foetal liver-derived precursors, however, vary between”
BackgroundHeterogeneity and Function of Kupffer Cells in Liver Injury
Li, W., Chang, N., & Li, L. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.940867 · Cited by 102
“Then, partial YS-macrophages migrate into fetal liver and develop into KCs (10).”
BackgroundTraining the Fetal Immune System Through Maternal Inflammation—A Layered Hygiene Hypothesis
Apostol, A. C., Jensen, K. D. C., & Beaudin, A. E. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00123 · Cited by 101
Self-citationThe role of IL-10 in kidney disease
Wei, W., Zhao, Y., Zhang, Y., Jin, H., & Shou, S. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.108917 · Cited by 100
Nahrendorf, M., & Swirski, F. K. (2016) · European Heart Journal · doi:10.1093/eurheartj/ehv453 · Cited by 95
“macrophages derive from embryonic cells that originated in the yolk sac and/or foetal liver.(17,21) Long-term parabiosis leads to”
BackgroundVarvel, N. H., Grathwohl, S. A., Degenhardt, K., Resch, C., Bosch, A., Jucker, M., & Neher, J. J. (2015) · Journal of Experimental Medicine · doi:10.1084/jem.20150478 · Cited by 99
“Microglia, the brain’s resident macrophages, are a myeloid population that is developmentally and functionally distinct from circulating monocytes (Lavin et al., 2014; Hoeffel et al., 2015).”
BackgroundKawamura, S., Onai, N., Miya, F., Sato, T., Tsunoda, T., Kurabayashi, K., Yotsumoto, S., Kuroda, S., Takenaka, K., Akashi, K., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.04.019 · Cited by 113
Generation, localization and functions of macrophages during the development of testis
Lokka, E., Lintukorpi, L., Cisneros-Montalvo, S., Mäkelä, J., Tyystjärvi, S., Ojasalo, V., Gerke, H., Toppari, J., Rantakari, P., & Salmi, M. (2020) · Nature Communications · doi:10.1038/s41467-020-18206-0 · Cited by 102
Occurrences and Functions of Ly6Chi and Ly6Clo Macrophages in Health and Disease
Li, Y., Zhang, Y., Pan, G., Xiang, L., Luo, D., & Shao, J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.901672 · Cited by 109
“In mice, yolk sac- or fetal liver-derived macrophages are located in different adult tissues, including the brain, epidermis and kidneys, and contribute to tissue homeostasis independent of bone marrow-derived monocytic precursors (5, 24, 25).”
BackgroundLysophosphatidic acid converts monocytes into macrophages in both mice and humans
Ray, R., & Rai, V. (2017) · Blood · doi:10.1182/blood-2016-10-743757 · Cited by 99
Human anti-PSCA CAR macrophages possess potent antitumor activity against pancreatic cancer
Shah, Z., Tian, L., Li, Z., Jin, L., Zhang, J., Li, Z., Barr, T., Tang, H., Feng, M., Caligiuri, M. A., et al. (2024) · Cell stem cell · doi:10.1016/j.stem.2024.03.018 · Cited by 107
Otsuka, M., Egawa, G., & Kabashima, K. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01768 · Cited by 112
Interleukin-6 signaling regulates hematopoietic stem cell emergence
Tie, R., Li, H., Cai, S., Liang, Z., Shan, W., Wang, B., Tan, Y., Zheng, W., & Huang, H. (2019) · Experimental & Molecular Medicine · doi:10.1038/s12276-019-0320-5 · Cited by 97
A temporal perspective for tumor-associated macrophage identities and functions
Blériot, C., Dunsmore, G., Alonso‐Curbelo, D., & Ginhoux, F. (2024) · Cancer Cell · doi:10.1016/j.ccell.2024.04.002 · Cited by 105
Self-citationInfiltrating monocytes in liver injury and repair
Brempelis, K. J., & Crispe, I. N. (2016) · Clinical & Translational Immunology · doi:10.1038/cti.2016.62 · Cited by 97
Alveolar Macrophages in Allergic Asthma: the Forgotten Cell Awakes
Draijer, C., & Peters-Golden, M. L. (2017) · Current Allergy and Asthma Reports · doi:10.1007/s11882-017-0681-6 · Cited by 95
The immunophenotype of amniotic fluid leukocytes in normal and complicated pregnancies
Gomez‐Lopez, N., Romero, R. J., Xu, Y., Miller, D., Leng, Y., Panaitescu, B., Silva, P. R. D. O., Faro, J. P., Alhousseini, A., Gill, N., et al. (2018) · American Journal of Reproductive Immunology · doi:10.1111/aji.12827 · Cited by 97
Dege, C., Fegan, K. H., Creamer, J. P., Berrien-Elliott, M. M., Luff, S. A., Kim, D., Wagner, J. A., Kingsley, P. D., McGrath, K. E., Fehniger, T. A., et al. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.02.016 · Cited by 96
“To test this hypothesis, we utilized the tamoxifen-inducible Csf1rMerCreMerRosa26YFP mouse model, which has been used to lineage trace the macrophage potential of EMP (Gomez Perdiguero et al., 2015; Hoeffel et al., 2015).”
MethodNeuroplasticity related to chronic pain and its modulation by microglia
Hiraga, S.-I., Itokazu, T., Nishibe, M., & Yamashita, T. (2022) · Inflammation and Regeneration · doi:10.1186/s41232-022-00199-6 · Cited by 101
Exploring tumor-associated macrophages in glioblastoma: from diversity to therapy
Zhao, W., Zhang, Z., Xie, M., Ding, F., Zheng, X., Sun, S., & Du, J. (2025) · npj Precision Oncology · doi:10.1038/s41698-025-00920-x · Cited by 112
“Emerging evidence suggests that microglia originate from erythromyeloid progenitors (EMPs) in the yolk sac and migrate into the brain, where they colonize, differentiate, and mature, ultimately maintaining immune homeostasis in the CNS environment 17,18 .”
Olgasi, C., Cucci, A., & Follenzi, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21176215 · Cited by 100
The Role of Myeloid-Derived Cells in the Progression of Liver Disease
Weston, C. J., Zimmermann, H. W., & Adams, D. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00893 · Cited by 92
“Kupffer Cells The liver contains a population of self-renewing resident macrophages, termed Kupffer cells (KC), derived from yolk sac-derived progenitor cells (8, 9) or hematopoietic stem cells (10).”
BackgroundThibaut, R., Gage, M., Pineda‐Torra, I., Chabrier, G., Venteclef, N., & Alzaïd, F. (2021) · FEBS Journal · doi:10.1111/febs.15877 · Cited by 97
Paschalis, E. I., Lei, F., Zhou, C., Kapoulea, V., Dana, R., Chodosh, J., Vavvas, D. G., & Dohlman, C. H. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1807123115 · Cited by 91
“The ability of CSF1R-independent embryonic precursors to functionally replace yolk-sac–derived microglia during development has been demonstrated (30), suggesting that other tissue macrophages may assume the role of microglia under certain conditions.”
BackgroundNew insights into mononuclear phagocyte biology from the visual system
Reyes, N. S., O’Koren, E. G., & Saban, D. R. (2017) · Nature reviews. Immunology · doi:10.1038/nri.2017.13 · Cited by 95
Endocardially Derived Macrophages Are Essential for Valvular Remodeling
Shigeta, A., Huang, V. H., Zuo, J., Besada, R. H., Nakashima, Y., Lu, Y., Ding, Y., Pellegrini, M. A., Kulkarni, R. P., Hsiai, T. K., et al. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.01.021 · Cited by 93
The Role of Osteopontin in Tumor Progression Through Tumor-Associated Macrophages
Tan, Y., Zhao, L., Yang, Y., & Liu, W. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.953283 · Cited by 94
Chen, H., Chen, C., Kuo, Y.-M., Chen, B., Kuan, I. S., Huang, H., Lee, J., Anthony, N. R., Kuan, C.-Y., & Sun, Y. (2021) · Theranostics · doi:10.7150/thno.64033 · Cited by 96
Oncofetal reprogramming in tumour development and progression
Sharma, A., Blériot, C., Currenti, J., & Ginhoux, F. (2022) · Nature reviews. Cancer · doi:10.1038/s41568-022-00497-8 · Cited by 104
Self-citationYe, Z., Ai, X., Yang, K., Yang, Z., Fei, F., Liao, X., Qiu, Z., Gimple, R. C., Yuan, H., Huang, H., et al. (2023) · Cancer Discovery · doi:10.1158/2159-8290.cd-22-0455 · Cited by 93
Baer, J. M., Zuo, C., Kang, L., de la Lastra, A. A., Borcherding, N. C., Knolhoff, B. L., Bogner, S. J., Zhu, Y., Yang, L., Poursine‐Laurent, J., et al. (2022) · Nature Immunology · doi:10.1038/s41590-023-01579-x · Cited by 104
Wang, L., Wang, D., Zhang, T., Ma, Y., Tong, X., & Fan, H. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1117548 · Cited by 100
Skeletal muscle inflammation and atrophy in heart failure
Lavine, K. J., & Sierra, O. L. (2017) · Heart Failure Reviews · doi:10.1007/s10741-016-9593-0 · Cited by 96
“heart, lung, kidney, liver, and skin [28, 45].”
BackgroundInnate Immune Signaling and Alcohol Use Disorders
Coleman, L. G., & Crews, F. T. (2018) · Handbook of experimental pharmacology · doi:10.1007/164_2018_92 · Cited by 97
“Microglia are the only myeloid cells that originate from yolk-sac progenitor cells[1, 2].”
BackgroundFirst blood: the endothelial origins of hematopoietic progenitors
Canu, G., & Ruhrberg, C. (2021) · Angiogenesis · doi:10.1007/s10456-021-09783-9 · Cited by 98
Macrophages: Subtypes, Distribution, Polarization, Immunomodulatory Functions, and Therapeutics
Peng, M., Li, N., Wang, H., Li, Y., Liu, H., Luo, Y., Lang, B., Zhang, W., Li, S., Tian, L., et al. (2025) · MedComm · doi:10.1002/mco2.70304 · Cited by 98
Transcriptomic and epigenetic mechanisms underlying myeloid diversity in the lung
Sajti, E., Link, V. M., Ouyang, Z., Spann, N. J., Westin, E. M., Romanoski, C. E., Fonseca, G. J., Prince, L. S., & Glass, C. K. (2020) · Nature Immunology · doi:10.1038/s41590-019-0582-z · Cited by 84
Origin and Differentiation of Nerve-Associated Macrophages
Kolter, J., Kierdorf, K., & Henneke, P. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1901077 · Cited by 91
The Many Roles of Macrophages in Skeletal Muscle Injury and Repair
Wang, X., & Zhou, L. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.952249 · Cited by 101
“Fetal monocytes seed all other embryonic tissues except for brain (Hoeffel et al., 2015).”
BackgroundSalei, N., Rambichler, S., Salvermoser, J., Papaioannou, N. E., Schuchert, R., Pakalniškytė, D., Li, N., Marschner, J. A., Lichtnekert, J., Stremmel, C., et al. (2020) · Journal of the American Society of Nephrology · doi:10.1681/asn.2019040419 · Cited by 89
Developmental control of macrophage function
Bonnardel, J., & Guilliams, M. (2017) · Current Opinion in Immunology · doi:10.1016/j.coi.2017.12.001 · Cited by 87
Role of adipose tissue macrophages in obesity-related disorders
Chakarov, S., Blériot, C., & Ginhoux, F. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20211948 · Cited by 91
“…but many studies have now revealed that the vastmajority of RTMpopulations are actually established during embryonic development and subsequently self-maintained (Epelman et al., 2014; Ginhoux et al., 2010; Guilliams et al., 2013; Hoeffel et al., 2015; Schneider et al., 2014; Schulz et al., 2012).”
BackgroundSelf-citationCytokine Networks between Innate Lymphoid Cells and Myeloid Cells
Mortha, A., & Burrows, K. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00191 · Cited by 88
“These cells seed the developing organs and locally self-renew in the steady state, while chronic inflammation fosters the replacement of tissue-resident myeloid cells by progeny arising from circulating precursors (89, 90).”
BackgroundRahman, M. S., & Woollard, K. J. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-57613-8_7 · Cited by 87
Effects of dyslipidaemia on monocyte production and function in cardiovascular disease
Rahman, M. S., Murphy, A. J., & Woollard, K. J. (2017) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2017.34 · Cited by 86
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
