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Tissue-Resident Macrophages Self-Maintain Locally throughout Adult Life with Minimal Contribution from Circulating Monocytes
Open accessAbstract
Despite accumulating evidence suggesting local self-maintenance of tissue macrophages in the steady state, the dogma remains that tissue macrophages derive from monocytes. Using parabiosis and fate-mapping approaches, we confirmed that monocytes do not show significant contribution to tissue macrophages in the steady state. Similarly, we found that after depletion of lung macrophages, the majority of repopulation occurred by stochastic cellular proliferation in situ in a macrophage colony-stimulating factor (M-Csf)- and granulocyte macrophage (GM)-CSF-dependent manner but independently of interleukin-4. We also found that after bone marrow transplantation, host macrophages retained the capacity to expand when the development of donor macrophages was compromised. Expansion of host macrophages was functional and prevented the development of alveolar proteinosis in mice transplanted with GM-Csf-receptor-deficient progenitors. Collectively, these results indicate that tissue-resident macrophages and circulating monocytes should be classified as mononuclear phagocyte lineages that are independently maintained in the steady state.
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“Our findings are consistent with reports that macrophage progenitors develop from the primitive ectoderm of the yolk sac4 and give rise to tissue macrophages that do not have a monocytic progenitor16,17.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [16]
In the citing paper
“In addition, the normal arterial intima of mice and humans, like any tissue of the mammalian body, contains tissue-resident macrophages, which arise from embryonic precursors and from bone-marrow-derived circulating monocytes immediately after birth144.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [144]
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“These macrophages self-renew and fulfil homeostatic and physiological functions in the tissue concerned144.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [144]
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Metadata
- Authors
- Hashimoto, D., Chow, A., Noizat, C., Teo, P., Beasley, M. B., Leboeuf, M., Becker, C. D., See, P., Price, J., Lucas, D., Greter, M., Mortha, A., Boyer, S. W., Forsberg, E. C., Tanaka, M., van Rooijen, N., García-Sastre, A., Stanley, E. R., Ginhoux, F., Frenette, P. S., & Merad, M.
- Affiliations
- Tisch Cancer Institute (US)
- Albert Einstein College of Medicine (US)
- Agency for Science, Technology and Research (SG)
- Icahn School of Medicine at Mount Sinai (US)
- University of Zurich (CH)
- University of California, Santa Cruz (US)
- Tokyo University of Pharmacy and Life Sciences (JP)
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2013-04
- Volume
- 38
- Issue
- 4
- Pages
- 792-804
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC3853406
- OpenAlex
- W1973433801
- Cited by
- 2,311
- References
- 49
- Citations by year
- 2026: 132 · 2025: 151 · 2024: 158 · 2023: 168 · 2022: 204 · 2021: 211 · 2020: 219 · 2019: 185 · 2018: 179 · 2017: 188 · 2016: 152 · 2015: 155 · 2014: 148 · 2013: 47
- FWCI
- 92.47
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- California Institute for Regenerative Medicine
- California Institute of Regenerative Medicine
- National Institutes of Health
- Japan Society for the Promotion of Science (23390095)
- National Heart, Lung, and Blood Institute (HL097700, HL069438, R01HL116340, R01HL086899, R01HL097700, F30HL099028, R01HL069438, HL116340)
- National Cancer Institute (CA154947A, R01CA173861, R01CA154947)
- National Institute of General Medical Sciences (T32GM008646)
- National Institute of Allergy and Infectious Diseases (AI 089987, U19AI089987, AI10008)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK056638, DK056638)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Keywords
- tissue-resident macrophages, macrophage self-renewal, monocytes, lung macrophages, macrophage colony-stimulating factor, GM-CSF, IL-4, pulmonary alveolar proteinosis, bone marrow transplantation, parabiosis, fate mapping
- MeSH terms
- Adult, Animals, Cell Survival, Cells, Cultured, Homeostasis, Humans, Lung, Macrophages, Mice, Mutant Strains, Parabiosis, Interleukin-4, Bone Marrow Transplantation, Macrophage Colony-Stimulating Factor, Granulocyte-Macrophage Colony-Stimulating Factor, Receptors, Granulocyte-Macrophage Colony-Stimulating Factor, Mice, Knockout, Cell Proliferation, Mice
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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.
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