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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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BackgroundInfluentialCigarette smoke exposure and alveolar macrophages: mechanisms for lung disease
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ResultMacrophages: friend or foe in idiopathic pulmonary fibrosis?
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BackgroundMacrophage polarization and meta-inflammation
Li, C., Xu, M. M., Wang, K., Adler, A. J., Vella, A. T., & Zhou, B. (2017) · Translational research · doi:10.1016/j.trsl.2017.10.004 · Cited by 376
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Tissue macrophages: origin, heterogenity, biological functions, diseases and therapeutic targets
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Tumor-Associated Macrophages: Implications in Cancer Immunotherapy
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Self-citationEfferocytosis induces macrophage proliferation to help resolve tissue injury
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InfluentialMacrophages: An Inflammatory Link Between Angiogenesis and Lymphangiogenesis
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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 367
“The Development of Monocyte-Derived ‘‘AMs’’ after Irradiation Requires TGF-bR Signaling AMs self-maintain in the steady-state independently of circulating precursors (Hashimoto et al., 2013).”
BackgroundResultInfluentialSelf-citationHematological methods in fish – Not only for beginners
Witeska, M., Kondera, E., Ługowska, K., & Bojarski, B. (2021) · Aquaculture · doi:10.1016/j.aquaculture.2021.737498 · Cited by 384
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“Indeed, there is accumulating evidence that tissue-resident macrophages undergo in situ proliferation with minimal contribution from circulating monocytes in several patho-physiological conditions (Hashimoto et al., 2013; Jenkins et al., 2011; Robbins et al., 2013).”
BackgroundMacrophages in Kidney Injury, Inflammation, and Fibrosis
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“Recent studies have emphasized the importance of tissue-resident macrophages and demonstrated that they selfmaintain locally without need for input from circulating monocytes (1, 47).”
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“derived from fetal monocyte-derived macrophages that enter the tissue during neonatal periods.(14) In addition, Langerhans”
Nonclassical Ly6C− Monocytes Drive the Development of Inflammatory Arthritis in Mice
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“Here, we generated bone marrow chimeric mice with selective shielding of the joint during irradiation to demonstrate that the naive mouse joint contains a heterogeneous population of macrophages, namely tissue-resident and bone-marrow-derived macrophages (Ginhoux and Jung, 2014; Hashimoto et al., 2013; Yona et al., 20…”
InfluentialOsteoMacs: Key players around bone biomaterials
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Genetic Tracing via DNGR-1 Expression History Defines Dendritic Cells as a Hematopoietic Lineage
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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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