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      Ontogeny of Tissue-Resident Macrophages

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          Abstract

          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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          Most cited references77

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          Local self-renewal can sustain CNS microglia maintenance and function throughout adult life.

          Microgliosis is a common response to multiple types of damage in the CNS. However, the origin of the cells involved in this process is still controversial and the relative importance of local expansion versus recruitment of microglia progenitors from the bloodstream is unclear. Here, we investigated the origin of microglia using chimeric animals obtained by parabiosis. We found no evidence of microglia progenitor recruitment from the circulation in denervation or CNS neurodegenerative disease, suggesting that maintenance and local expansion of microglia are solely dependent on the self-renewal of CNS resident cells in these models.
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            Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation.

            A defining feature of inflammation is the accumulation of innate immune cells in the tissue that are thought to be recruited from the blood. We reveal that a distinct process exists in which tissue macrophages undergo rapid in situ proliferation in order to increase population density. This inflammatory mechanism occurred during T helper 2 (T(H)2)-related pathologies under the control of the archetypal T(H)2 cytokine interleukin-4 (IL-4) and was a fundamental component of T(H)2 inflammation because exogenous IL-4 was sufficient to drive accumulation of tissue macrophages through self-renewal. Thus, expansion of innate cells necessary for pathogen control or wound repair can occur without recruitment of potentially tissue-destructive inflammatory cells.
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              In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium.

              Haematopoietic stem cells (HSCs), responsible for blood production in the adult mouse, are first detected in the dorsal aorta starting at embryonic day 10.5 (E10.5). Immunohistological analysis of fixed embryo sections has revealed the presence of haematopoietic cell clusters attached to the aortic endothelium where HSCs might localize. The origin of HSCs has long been controversial and several candidates of the direct HSC precursors have been proposed (for review see ref. 7), including a specialized endothelial cell population with a haemogenic potential. Such cells have been described both in vitro in the embryonic stem cell (ESC) culture system and retrospectively in vivo by endothelial lineage tracing and conditional deletion experiments. Whether the transition from haemogenic endothelium to HSC actually occurs in the mouse embryonic aorta is still unclear and requires direct and real-time in vivo observation. To address this issue we used time-lapse confocal imaging and a new dissection procedure to visualize the deeply located aorta. Here we show the dynamic de novo emergence of phenotypically defined HSCs (Sca1(+), c-kit(+), CD41(+)) directly from ventral aortic haemogenic endothelial cells.
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                Author and article information

                Contributors
                URI : http://frontiersin.org/people/u/81961
                URI : http://frontiersin.org/people/u/34775
                Journal
                Front Immunol
                Front Immunol
                Front. Immunol.
                Frontiers in Immunology
                Frontiers Media S.A.
                1664-3224
                22 September 2015
                2015
                : 6
                : 486
                Affiliations
                [1] 1Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A*STAR) , Singapore, Singapore
                Author notes

                Edited by: Peter M. Van Endert, Université Paris Descartes, France

                Reviewed by: Meredith O’Keeffe, Burnet Institute for Medical Research, Australia; Jean M. Davoust, Institut National de la Santé et la Recherche Médicale, France

                *Correspondence: Guillaume Hoeffel and Florent Ginhoux, Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A*STAR), 8A Biomedical Grove, IMMUNOS Building #3-4, Biopolis, 138648 Singapore, guillaumehoeffel1@ 123456gmail.com ; florent_ginhoux@ 123456immunol.a-star.edu.sg

                Specialty section: This article was submitted to Antigen Presenting Cell Biology, a section of the journal Frontiers in Immunology

                Article
                10.3389/fimmu.2015.00486
                4585135
                26441990
                18f98eef-20fb-47a5-ab37-df27680f5236
                Copyright © 2015 Hoeffel and Ginhoux.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 22 July 2015
                : 07 September 2015
                Page count
                Figures: 6, Tables: 0, Equations: 0, References: 116, Pages: 14, Words: 11223
                Funding
                Funded by: Singapore Immunology Network (SIgN) Core Grant
                Categories
                Immunology
                Review

                Immunology
                macrophages,monocytes,fetal liver,yolk sac,c-myb,erythro-myeloid progenitors,hematopoiesis,hematopoietic stem cells

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