Ontogeny of Tissue-Resident Macrophages
Open accessAbstract
The origin of tissue-resident macrophages, crucial for homeostasis and immunity, has remained controversial until recently. Originally described as part of the mononuclear phagocyte system, macrophages were long thought to derive solely from adult blood circulating monocytes. However, accumulating evidence now shows that certain macrophage populations are in fact independent from monocyte and even from adult bone marrow hematopoiesis. These tissue-resident macrophages derive from sequential seeding of tissues by two precursors during embryonic development. Primitive macrophages generated in the yolk sac (YS) from early erythro-myeloid progenitors (EMPs), independently of the transcription factor c-Myb and bypassing monocytic intermediates, first give rise to microglia. Later, fetal monocytes, generated from c-Myb(+) EMPs that initially seed the fetal liver (FL), then give rise to the majority of other adult macrophages. Thus, hematopoietic stem cell-independent embryonic precursors transiently present in the YS and the FL give rise to long-lasting self-renewing macrophage populations.
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These markers have been identified in mouse as markers of early yolk sac myelogenesis before definitive hematopoiesis or embryonic circulation.
“which have been identified in mouse as markers of early yolk sac myelogenesis before definitive hematopoiesis or the establishment of embryonic circulation (<E8.5) 19.”
From Efficient derivation of microglia-like cells from human pluripotent stem cells (2016) · cites this paper as [19]
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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 · see citing works
Self-citationMacrophage biology in development, homeostasis and disease
Wynn, T. A., Chawla, A., & Pollard, J. W. (2013) · Nature · doi:10.1038/nature12034 · Cited by 4,684 · cited 2× · see citing works
“Macrophages are exquisitely adapted to their local environment, acquiring organ-specific functionalities during developmental stages and the steady state (4).”
BackgroundTumor-Associated Macrophages: From Mechanisms to Therapy
Noy, R., & Pollard, J. W. (2014) · Immunity · doi:10.1016/j.immuni.2014.06.010 · Cited by 4,089 · see citing works
Blood 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 3,366 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Macrophages in atherosclerosis: a dynamic balance
Moore, K. J., Sheedy, F. J., & Fisher, E. A. (2013) · Nature reviews. Immunology · doi:10.1038/nri3520 · Cited by 2,559 · see citing works
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 · cited 14× · see citing works
“More recently, Perdiguero et al. used the CSF-1R-iCre fate-mapping model to show that YS macrophages are derived from CSF-1R+ EMPs (14).”
BackgroundMethodInfluentialHashimoto, 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 · see citing works
Self-citationTissue-Resident Macrophage Enhancer Landscapes Are Shaped by the Local Microenvironment
Lavin, Y., Winter, D., Blecher-Gonen, R., David, E., Keren-Shaul, H., Merad, M., Jung, S., & Amit, I. (2014) · Cell · doi:10.1016/j.cell.2014.11.018 · Cited by 2,167 · see citing works
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 · see citing works
Local self-renewal can sustain CNS microglia maintenance and function throughout adult life
Ajami, B., Bennett, J. L., Krieger, C., Tetzlaff, W., & Rossi, F. M. V. (2007) · Nature Neuroscience · doi:10.1038/nn2014 · Cited by 1,643 · see citing works
THE ORIGIN AND KINETICS OF MONONUCLEAR PHAGOCYTES
van Furth, R., & Cohn, Z. A. (1968) · The Journal of Experimental Medicine · doi:10.1084/jem.128.3.415 · Cited by 1,564 · see citing works
Epelman, S., Lavine, K. J., Beaudin, A. E., Sojka, D. K., Carrero, J. A., Calderon, B., Brija, T., Gautier, E. L., Ivanov, S., Satpathy, A. T., et al. (2014) · Immunity · doi:10.1016/j.immuni.2013.11.019 · Cited by 1,494 · see citing works
Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways
Kierdorf, K., Erny, D., Goldmann, T., Sander, V., Schulz, C., Perdiguero, E. G., Wieghofer, P., Heinrich, A., Riemke, P., Hölscher, C., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3318 · Cited by 1,457 · see citing works
Jenkins, S., Ruckerl, D., Cook, P., Jones, L., Finkelman, F., van Rooijen, N., MacDonald, A., & Allen, J. (2011) · Science · doi:10.1126/science.1204351 · Cited by 1,427 · see citing works
Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease
Prinz, M., & Priller, J. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3722 · Cited by 1,329 · see citing works
Guilliams, M., de Kleer, I., Henri, S., Post, S., Vanhoutte, L., Prijck, S. D., Deswarte, K., MALISSEN, B., Hammad, H., & Lambrecht, B. N. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20131199 · Cited by 1,259 · see citing works
Identification of Flt3+ Lympho-Myeloid Stem Cells Lacking Erythro-Megakaryocytic Potential
Adolfsson, J., Månsson, R., Buza-Vidas, N., Hultquist, A., Liuba, K., Jensen, C. T., Bryder, D., Yang, L., Borge, O. J., Thorén, L., et al. (2005) · Cell · doi:10.1016/j.cell.2005.02.013 · Cited by 1,229 · see citing works
Bain, C. C., Bravo-Blas, A., Scott, C. L., Gomez Perdiguero, E., Geissmann, F., Henri, S., Malissen, B., Osborne, L. C., Artis, D., & Mowat, A. M. (2014) · Nature Immunology · doi:10.1038/ni.2967 · Cited by 1,178 · see citing works
Hoeffel, G., Chen, J., Lavin, Y., Low, D., Almeida, F. F., See, P., Beaudin, A. E., Lum, J., Low, I., Forsberg, E. C., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.03.011 · Cited by 1,135 · cited 13× · see citing works
“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-citationvan Furth, R., Cohn, Z. A., Jg, H., Humphrey, J., Spector, W. G., & Langevoort, H. L. (1972) · PubMed Central · Cited by 1,133 · see citing works
Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse
Palis, J., Robertson, S. M., Kennedy, M., Wall, C., & Keller, G. M. (1999) · Development · doi:10.1242/dev.126.22.5073 · Cited by 1,050 · see citing works
Local proliferation dominates lesional macrophage accumulation in atherosclerosis
Robbins, C. S., Hilgendorf, I., Weber, G. F., Theurl, I., Iwamoto, Y., Figueiredo, J.-L., Gorbatov, R., Sukhova, G. K., Gerhardt, L. M. S., Smyth, D., et al. (2013) · Nature Medicine · doi:10.1038/nm.3258 · Cited by 1,041 · see citing works
A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis
Mucenski, M. L., McLain, K., Kier, A. B., Swerdlow, S. H., Schreiner, C. M., Miller, T. A., Pietryga, D. W., Scott, W. J., & Potter, S. S. (1991) · Cell · doi:10.1016/0092-8674(91)90099-k · Cited by 1,041 · see citing works
Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter
Chen, M. J., Yokomizo, T., Zeigler, B. M., Dzierzak, E. A., & Speck, N. A. (2009) · Nature · doi:10.1038/nature07619 · Cited by 1,016 · see citing works
Langerhans cells renew in the skin throughout life under steady-state conditions
Mérad, M., Manz, M. G., Karsunky, H., Wagers, A. J., Peters, W., Charo, I. F., Weissman, I. L., Cyster, J. G., & Engleman, E. G. (2002) · Nature Immunology · doi:10.1038/ni852 · Cited by 976 · see citing works
In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium
Boisset, J.-C., van Cappellen, W. A., Andrieu‐Soler, C., Galjart, N., Dzierzak, E. A., & Robin, C. (2010) · Nature · doi:10.1038/nature08764 · Cited by 951 · see citing works
Development of hematopoietic stem cell activity in the mouse embryo
Müller, A. M., Medvinsky, A., Strouboulis, J., Grosveld, F. G., & Dzierzakt, E. (1994) · Immunity · doi:10.1016/1074-7613(94)90081-7 · Cited by 901 · see citing works
Hoeffel, G., Wang, Y., Greter, M., See, P., Teo, P., Malleret, B., Leboeuf, M., Low, D., Oller, G., Almeida, F., et al. (2012) · Journal of Experimental Medicine · doi:10.1084/jem.20120340 · Cited by 786 · see citing works
Self-citationTamoutounour, S., Guilliams, M., Montanana Sanchis, F., Liu, H., Terhorst, D., Malosse, C., Pollet, E., Ardouin, L., Luche, H., Sanchez, C., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.10.004 · Cited by 783 · see citing works
Fundamental properties of unperturbed haematopoiesis from stem cells in vivo
Busch, K., Klapproth, K., Barile, M., Flossdorf, M., Holland-Letz, T., Schlenner, S. M., Reth, M., Höfer, T., & Rodewald, H.-R. (2015) · Nature · doi:10.1038/nature14242 · Cited by 769 · see citing works
Jakubzick, C. V., Gautier, E., Gibbings, S. L., Sojka, D. K., Schlitzer, A., Johnson, T. E., Ivanov, S., Duan, Q., Bala, S., Condon, T., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.08.007 · Cited by 762 · see citing works
Self-citationMacrophages, Immunity, and Metabolic Disease
McNelis, J., & Olefsky, J. M. (2014) · Immunity · doi:10.1016/j.immuni.2014.05.010 · Cited by 728 · see citing works
Of lineage and legacy: the development of mammalian hematopoietic stem cells
Dzierzak, E., & Speck, N. A. (2008) · Nature Immunology · doi:10.1038/ni1560 · Cited by 707 · see citing works
The Placenta Is a Niche for Hematopoietic Stem Cells
Gekas, C., Dieterlen‐Lièvre, F., Orkin, S. H., & Mikkola, H. K. A. (2005) · Developmental Cell · doi:10.1016/j.devcel.2004.12.016 · Cited by 664 · see citing works
Oguro, H., Ding, L., & Morrison, S. J. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.05.014 · Cited by 657 · see citing works
Microglia Modulate Wiring of the Embryonic Forebrain
Squarzoni, P., Oller, G., Hoeffel, G., Pont‐Lezica, L., Rostaing, P., Low, D., Bessis, A., Ginhoux, F., & Garel, S. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.042 · Cited by 655 · see citing works
Self-citationOrigin of monocytes and macrophages in a committed progenitor
Hettinger, J., Richards, D. M., Hansson, J., Barra, M. M., Joschko, A.-C., Krijgsveld, J., & Feuerer, M. (2013) · Nature Immunology · doi:10.1038/ni.2638 · Cited by 643 · see citing works
Bruijn, M. F. T. R. D., Speck, N. A., Peeters, M. C. E., & Dzierzak, E. (2000) · The EMBO Journal · doi:10.1093/emboj/19.11.2465 · Cited by 617 · see citing works
Schneider, C., Nobs, S. P., Kurrer, M. O., Rehrauer, H., Thiele, C., & Köpf, M. (2014) · Nature Immunology · doi:10.1038/ni.3005 · Cited by 603 · see citing works
New insights into the development of lymphoid tissues
van de Pavert, S. A., & Mebius, R. E. (2010) · Nature reviews. Immunology · doi:10.1038/nri2832 · Cited by 597 · see citing works
The journey of developing hematopoietic stem cells
Mikkola, H. K. A., & Orkin, S. H. (2006) · Development · doi:10.1242/dev.02568 · Cited by 577 · see citing works
Cumano, A., Dieterlen‐Lièvre, F., & Godin, I. (1996) · Cell · doi:10.1016/s0092-8674(00)80166-x · Cited by 567 · see citing works
Progressive replacement of embryo-derived cardiac macrophages with age
Molawi, K., Wolf, Y., Kandalla, P. K., Favret, J., Hagemeyer, N., Frenzel, K., Pinto, A. R., Klapproth, K., Henri, S., MALISSEN, B., et al. (2014) · The Journal of Experimental Medicine · doi:10.1084/jem.20140639 · Cited by 504 · see citing works
Most 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
Cell tracing shows the contribution of the yolk sac to adult haematopoiesis
Samokhvalov, I. M., Samokhvalova, N. I., & Nishikawa, S. (2007) · Nature · doi:10.1038/nature05725 · Cited by 461 · see citing works
Primitive and definitive erythropoiesis in mammals
Palis, J. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00003 · Cited by 442 · see citing works
Kumaravelu, P., Hook, L., Morrison, A. M., Ure, J. M., Zhao, S., Zuyev, S., Ansell, J., & Medvinsky, A. (2002) · Development · doi:10.1242/dev.129.21.4891 · Cited by 435 · see citing works
McGrath, K. E., Frame, J. M., Fegan, K. H., Bowen, J. R., Conway, S. J., Catherman, S. C., Kingsley, P. D., Koniski, A. D., & Palis, J. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.05.036 · Cited by 434 · see citing works
Ontogeny of the Hematopoietic System
Cumano, A., & Godin, I. (2007) · Annual Review of Immunology · doi:10.1146/annurev.immunol.25.022106.141538 · Cited by 432 · see citing works
Heme-mediated SPI-C induction promotes monocyte differentiation into iron-recycling macrophages
Haldar, M., Kohyama, M., So, A. Y.-L., KC, W., Wu, X., Briseño, C. G., Satpathy, A. T., Kretzer, N. M., Arase, H., Rajasekaran, N. S., et al. (2014) · Cell · doi:10.1016/j.cell.2014.01.069 · Cited by 431 · see citing works
Auffray, C., Fogg, D. K., Narni-Mancinelli, E., Senechal, B., Trouillet, C., Saederup, N., Leemput, J., Bigot, K., Campisi, L., Abitbol, M., et al. (2009) · Journal of Experimental Medicine · doi:10.1084/jem.20081385 · Cited by 422 · see citing works
Characterization of Definitive Lymphohematopoietic Stem Cells in the Day 9 Murine Yolk Sac
Yöder, M. C., Hiatt, K. K., Dutt, P., Mukherjee, P., Bodine, D. M., & Orlic, D. (1997) · Immunity · doi:10.1016/s1074-7613(00)80355-6 · Cited by 419 · see citing works
Metchnikoff and the phagocytosis theory
Tauber, A. I. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1244 · Cited by 413 · see citing works
Embryonic origin of the adult hematopoietic system: advances and questions
Medvinsky, A., Александрович, Р. С., & Taoudi, S. (2011) · Development · doi:10.1242/dev.040998 · Cited by 403 · see citing works
M-CSF inhibition selectively targets pathological angiogenesis and lymphangiogenesis
Kubota, Y., Takubo, K., Shimizu, T., Ohno, H., Kishi, K., Shibuya, M., Saya, H., & Suda, T. (2009) · The Journal of Experimental Medicine · doi:10.1084/jem.20081605 · Cited by 388 · see citing works
Godin, I., Dieterlen‐Lièvre, F., & Cumano, A. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.3.773 · Cited by 366 · see citing works
Circulation and Chemotaxis of Fetal Hematopoietic Stem Cells
Christensen, J. L., Wright, D. E., Wagers, A. J., & Weissman, I. L. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020075 · Cited by 358 · see citing works
Development of Secondary Lymphoid Organs
Randall, T. D., Carragher, D. M., & Rangel‐Moreno, J. (2008) · Annual Review of Immunology · doi:10.1146/annurev.immunol.26.021607.090257 · Cited by 339 · see citing works
CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo
Ferkowicz, M. J., Starr, M. D., Xie, X., Li, W., Johnson, S. A., Shelley, W. C., Morrison, P. R., & Yöder, M. C. (2003) · Development · doi:10.1242/dev.00632 · Cited by 333 · see citing works
Bertrand, J. Y., Kim, A. D., Violette, E. P., Stachura, D. L., Schwedler, J. L., & Traver, D. J. (2007) · Development · doi:10.1242/dev.012385 · Cited by 330 · see citing works
Tober, J. M., Koniski, A. D., McGrath, K. E., Vemishetti, R., Emerson, R. L., Bentley, K. L. D. M., Waugh, R. E., & Palis, J. (2006) · Blood · doi:10.1182/blood-2006-06-031898 · Cited by 328 · see citing works
Three pathways to mature macrophages in the early mouse yolk sac
Bertrand, J. Y., Jalil, A., Klaine, M., Jung, S., Cumano, A., & Godin, I. (2005) · Blood · doi:10.1182/blood-2005-02-0461 · Cited by 315 · see citing works
Studying the mononuclear phagocyte system in the molecular age
Chow, A. T., Brown, B. D., & Mérad, M. (2011) · Nature reviews. Immunology · doi:10.1038/nri3087 · Cited by 315 · see citing works
Circulation is established in a stepwise pattern in the mammalian embryo
McGrath, K. E., Koniski, A. D., Malik, J. T., & Palis, J. (2003) · Blood · doi:10.1182/blood-2002-08-2531 · Cited by 291 · see citing works
Yoshimoto, M., Montecino‐Rodriguez, E., Ferkowicz, M. J., Porayette, P., Shelley, W. C., Conway, S. J., Dorshkind, K. A., & Yöder, M. C. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015841108 · Cited by 283 · see citing works
Gray, E. E., & Cyster, J. G. (2012) · Journal of Innate Immunity · doi:10.1159/000337007 · Cited by 282 · see citing works
Böiers, C., Carrelha, J., Lutteropp, M., Luc, S., Green, J. C. A., Azzoni, E., Woll, P. S., Mead, A. J., Hultquist, A., Swiers, G., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.08.012 · Cited by 279 · see citing works
Macrophage recruitment during limb development and wound healing in the embryonic and foetal mouse
Hopkinson-Woolley, J. A., Hughes, D. A., Gordon, S., & Martin, P. B. (1994) · Journal of Cell Science · doi:10.1242/jcs.107.5.1159 · Cited by 279 · see citing works
Chen, M. J., Li, Y., Obaldia, M. E. D., Yang, Q., Yzaguirre, A. D., Yamada-Inagawa, T., Vink, C. S., Bhandoola, A., Dzierzak, E. A., & Speck, N. A. (2011) · Cell stem cell · doi:10.1016/j.stem.2011.10.003 · Cited by 260 · see citing works
Embryonic development of the human hematopoietic system
Tavian, M., & Peault, B. (2005) · The International Journal of Developmental Biology · doi:10.1387/ijdb.041957mt · Cited by 254 · see citing works
Boyer, S. W., Schroeder, A. V., Smith‐Berdan, S., & Forsberg, E. C. (2011) · Cell stem cell · doi:10.1016/j.stem.2011.04.021 · Cited by 245 · see citing works
Takahashi, K., Yamamura, F., & Naito, M. (1989) · Journal of Leukocyte Biology · doi:10.1002/jlb.45.2.87 · Cited by 242 · see citing works
The Human Embryo, but Not Its Yolk Sac, Generates Lympho-Myeloid Stem Cells
Tavian, M., Robin, C., Coulombel, L., & Péault, B. (2001) · Immunity · doi:10.1016/s1074-7613(01)00193-5 · Cited by 231 · see citing works
Wood, W., Turmaine, M., Weber, R., Camp, V., Maki, R. A., McKercher, S. R., & Martin, P. B. (2000) · Development · doi:10.1242/dev.127.24.5245 · Cited by 201 · see citing works
Palis, J., Chan, R. J., Koniski, A. D., Patel, R., Starr, M. D., & Yöder, M. C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.071002398 · Cited by 192 · see citing works
The nuclear receptor LXRα controls the functional specialization of splenic macrophages
A-González, N., Guillén, J. Á., Gallardo, G., Diaz, M., de la Rosa, J. V., Hernández, I., Casanova-Acebes, M., López, F., Tabraue, C., Beceiro, S., et al. (2013) · Nature Immunology · doi:10.1038/ni.2622 · Cited by 187 · see citing works
HEMATOPOIETIC ORIGIN OF MACROPHAGES AS STUDIED BY CHROMOSOME MARKERS IN MICE
Virolainen, M. J. (1968) · The Journal of Experimental Medicine · doi:10.1084/jem.127.5.943 · Cited by 184 · see citing works
Autonomous murine T-cell progenitor production in the extra-embryonic yolk sac before HSC emergence
Yoshimoto, M., Porayette, P., Glosson, N. L., Conway, S. J., Carlesso, N., Cardoso, A. A., Kaplan, M. H., & Yoder, M. C. (2012) · Blood · doi:10.1182/blood-2011-12-397489 · Cited by 178 · see citing works
Some New Aspects of the Langerhans Cell
Hashimoto, K. (1968) · Archives of Dermatology · doi:10.1001/archderm.1968.01610100090015 · Cited by 173 · see citing works
Development, differentiation, and phenotypic heterogeneity of murine tissue macrophages
Naito, M., Umeda, S., Yamamoto, T., Moriyama, H., Umezu, H., Hasegawa, G., Usuda, H., Shultz, L. D., & Takahashi, K. (1996) · Journal of Leukocyte Biology · doi:10.1002/jlb.59.2.133 · Cited by 169 · see citing works
Frame, J. M., McGrath, K. E., & Palis, J. (2013) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2013.09.006 · Cited by 155 · see citing works
Self-Renewal of Pulmonary Alveolar Macrophages: Evidence From Radiation Chimera Studies
Tarling, J. D., Lin, H.-S., & Hsu, S. (1987) · Journal of Leukocyte Biology · doi:10.1002/jlb.42.5.443 · Cited by 153 · see citing works
From the Reticuloendothelial to Mononuclear Phagocyte System – The Unaccounted Years
Yona, S., & Gordon, S. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00328 · Cited by 150 · see citing works
Origins and functions of phagocytes in the embryo
Lichanska, A. M., & Hume, D. A. (2000) · Experimental Hematology · doi:10.1016/s0301-472x(00)00157-0 · Cited by 150 · see citing works
Gordon, E. J., Rao, S., Pollard, J. W., Nutt, S. L., Lang, R. A., & Harvey, N. L. (2010) · Development · doi:10.1242/dev.050021 · Cited by 146 · see citing works
Placenta as a site for hematopoietic stem cell development
Mikkola, H. K. A., Gekas, C., Orkin, S. H., et al. (2005) · Experimental Hematology · doi:10.1016/j.exphem.2005.06.011 · Cited by 139 · see citing works
Coşkun, S., Chao, H., Vasavada, H. H., Heydari, K., Gonzales, N. M., Zhou, X., Crombrugghe, B. D., & Hirschi, K. K. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.09.013 · Cited by 133 · see citing works
The historical milestones in the understanding of leukocyte biology initiated by Elie Metchnikoff
Cavaillon, J. (2011) · Journal of Leukocyte Biology · doi:10.1189/jlb.0211094 · Cited by 128 · see citing works
Embryonic Origin of the Mouse Macrophage
Cline, M. J., & Moore, M. A. S. (1972) · Blood · doi:10.1182/blood.v39.6.842.842 · Cited by 126 · see citing works
McGrath, K. E., Kingsley, P. D., Koniski, A. D., Porter, R. L., Bushnell, T. P., & Palis, J. (2007) · Blood · doi:10.1182/blood-2007-08-107581 · Cited by 122 · see citing works
Immature hematopoietic stem cells undergo maturation in the fetal liver
Kieusseian, A., de la Grange, P. B., Burlen‐Defranoux, O., Godin, I., & Cumano, A. (2012) · Development · doi:10.1242/dev.079210 · Cited by 121 · see citing works
Kawamoto, H., & Katsura, Y. (2009) · Trends in Immunology · doi:10.1016/j.it.2009.03.001 · Cited by 118 · see citing works
Development, Differentiation, and Maturation of Macrophages in the Fetal Mouse Liver
Naito, M., Takahashi, K., & Nishikawa, S.-L. (1990) · Journal of Leukocyte Biology · doi:10.1002/jlb.48.1.27 · Cited by 115 · see citing works
Sumner, R., Crawford, A., Mucenski, M. L., & Frampton, J. (2000) · Oncogene · doi:10.1038/sj.onc.1203660 · Cited by 115 · see citing works
Golub, R., & Cumano, A. (2013) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2013.08.004 · Cited by 113 · see citing works
Epidermal Langerhans Cells—A Cycling Cell Population
Czernielewski, J., Vaigot, P., & PRUNIERAS, M. (1985) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12265523 · Cited by 94 · see citing works
Development, Differentiation, and Maturation of Fetal Mouse Yolk Sac Macrophages in Cultures
Naito, M., Yamamura, F., Nishikawa, S.-L., & Takahashi, K. (1989) · Journal of Leukocyte Biology · doi:10.1002/jlb.46.1.1 · Cited by 91 · see citing works
Yamada, M. G., Naito, M., & Takahashi, K. (1990) · Journal of Leukocyte Biology · doi:10.1002/jlb.47.3.195 · Cited by 90 · see citing works
Identification of a Fetal Hematopoietic Precursor with B Cell, T Cell, and Macrophage Potential
Lacaud, G., Carlsson, L., & Keller, G. M. (1998) · Immunity · doi:10.1016/s1074-7613(00)80648-2 · Cited by 90 · see citing works
Lymphoid Progenitor Emergence in the Murine Embryo and Yolk Sac Precedes Stem Cell Detection
Lin, Y., Yöder, M. C., & Yoshimoto, M. (2014) · Stem Cells and Development · doi:10.1089/scd.2013.0536 · Cited by 80 · see citing works
Krueger, G. G., Daynes, R. A., & Emam, M. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.6.1650 · Cited by 72 · see citing works
A short history of hemogenic endothelium
Swiers, G., Rode, C., Azzoni, E., & Bruijn, M. F. T. R. D. (2013) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2013.09.005 · Cited by 70 · see citing works
Ontogeny of Ia-Positive and Thy-1-Positive Leukocytes of Murine Epidermis
Romani, N., Schuler, G., & Fritsch, P. O. (1986) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12284135 · Cited by 69 · see citing works
Development, differentiation, and proliferation of macrophages in the rat yolk sac
Takahashi, K., & Naito, M. (1993) · Tissue and Cell · doi:10.1016/0040-8166(93)90077-x · Cited by 51 · see citing works
Naito, M., & Takahashi, K. (1991) · PubMed · Cited by 50 · see citing works
Morioka, Y., Naito, M., Sato, T., & Takahashi, K. (1994) · Journal of Leukocyte Biology · doi:10.1002/jlb.55.5.642 · Cited by 44 · see citing works
Ultrastructural and functional development of macrophages in the dermal tissue of rat fetuses
Takahashi, K., Takahashi, H., Naito, M., et al. (1983) · Cell and Tissue Research · doi:10.1007/bf00216427 · Cited by 42 · see citing works
Clarke, D., Vegiopoulos, A., Crawford, A., Mucenski, M. L., Bonifer, C., & Frampton, J. (2000) · Oncogene · doi:10.1038/sj.onc.1203661 · Cited by 42 · see citing works
Different macrophage populations develop from embryonic/fetal and adult hematopoietic tissues.
Faust, N., Huber, M. C., Sippel, A. E., et al. (1997) · PubMed · Cited by 33 · see citing works
Mizoguchi, S., Takahashi, K., Takeya, M., Naito, M., & Morioka, T. (1992) · Journal of Leukocyte Biology · doi:10.1002/jlb.52.1.52 · Cited by 24 · see citing works
Sorokin, S. P., McNelly, N. A. F., Blunt, D. G., et al. (1992) · The Anatomical Record · doi:10.1002/ar.1092320411 · Cited by 18 · see citing works
Godin, I. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.23.10815b · Cited by 2 · see citing works
Enzan (1997) · doi:10.1002/(sici)1097-0029(19971115)39:4
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Tissue-Resident Macrophage Ontogeny and Homeostasis
Ginhoux, F., & Guilliams, M. (2016) · Immunity · doi:10.1016/j.immuni.2016.02.024 · Cited by 1,884 · see citing works
Self-citationMicroglia in physiology and disease
Wolf, S. A., Boddeke, H. W. G. M., & Kettenmann, H. (2017) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022516-034406 · Cited by 1,426 · see citing works
Monocyte differentiation and antigen-presenting functions
Jakubzick, C. V., Randolph, G. J., & Henson, P. M. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.28 · Cited by 910 · see citing works
Efficient derivation of microglia-like cells from human pluripotent stem cells
Muffat, J., Li, Y., Yuan, B., Mitalipova, M., Omer, A., Corcoran, S., Bakiasi, G., Tsai, L.-H., Aubourg, P., Ransohoff, R. M., et al. (2016) · Nature Medicine · doi:10.1038/nm.4189 · Cited by 651 · see citing works
Haenseler, W., Sansom, S. N., Buchrieser, J., Newey, S. E., Moore, C. S., Nicholls, F. J., Chintawar, S., Schnell, C., Antel, J. P., Allen, N. D., et al. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.05.017 · Cited by 593 · see citing works
Control of innate immune response by biomaterial surface topography, energy, and stiffness
Abaricia, J. O., Farzad, N., Heath, T. J., Simmons, J., Morandini, L., & Olivares-Navarrete, R. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.04.021 · Cited by 199 · see citing works
The endocytic pathway in microglia during health, aging and Alzheimer’s disease
Solé-Domènech, S., Cruz, D. L., Capetillo-Zarate, E., & Maxfield, F. R. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.07.002 · Cited by 133 · see citing works
Lopez‐Atalaya, J. P., Askew, K. E., Sierra, A., & Gomez‐Nicola, D. (2018) · Developmental Neurobiology · doi:10.1002/dneu.22545 · Cited by 49 · see citing works
Microglia and Sensitive Periods in Brain Development
Dziabis, J. E., & Bilbo, S. D. (2021) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2021_242 · Cited by 42 · see citing works
Tumor-associated macrophages: Prognostic and therapeutic targets for cancer in humans and dogs
Brady, R. V., & Thamm, D. H. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1176807 · Cited by 35 · see citing works
- Authors
- Hoeffel, G., & Ginhoux, F.
- Affiliations
- Agency for Science, Technology and Research (SG)
- Corresponding author
- Hoeffel, Guillaume
- Ginhoux, Florent
- Venue
- Frontiers in Immunology
- Publisher
- Frontiers Media SA
- Published
- 2015-09-22
- Volume
- 6
- Pages
- 486-486
- ISSN
- 1664-3224 (ISSN-L)
- PMC
- PMC4585135
- OpenAlex
- W1859780204
- Cited by
- 364
- References
- 116
- Citations by year
- 2026: 18 · 2025: 28 · 2024: 34 · 2023: 24 · 2022: 40 · 2021: 35 · 2020: 41 · 2019: 38 · 2018: 32 · 2017: 33 · 2016: 23 · 2015: 4 · 2014: 1 · 2012: 1
- FWCI
- 2.89
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Immunology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- National University of Singapore (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Singapore Immunology Network (SIgN) Core Grant
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Keywords
- tissue-resident macrophages, macrophage ontogeny, yolk sac macrophages, erythro-myeloid progenitors, MYB, microglia
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 ›
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