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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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“including microglia, originate from similar progenitor pools during embryogenesis (Ginhoux et al., 2010; Hashimoto et al., 2013; Kierdorf et al., 2013; Schulz et al., 2012; Yona et al., 2013), and might therefore share pathologies in the context of Mecp2-deficiency.”
BackgroundDeletion of c-FLIP from CD11bhi Macrophages Prevents Development of Bleomycin-induced Lung Fibrosis
McCubbrey, A. L., Barthel, L., Mohning, M. P., Redente, E. F., Mould, K. J., Thomas, S. M., Leach, S. M., Danhorn, T., Gibbings, S. L., Jakubzick, C. V., et al. (2018) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2017-0154oc · Cited by 195
Cell Origin Dictates Programming of Resident versus Recruited Macrophages during Acute Lung Injury
Mould, K. J., Barthel, L., Mohning, M. P., Thomas, S. M., McCubbrey, A. L., Danhorn, T., Leach, S. M., Fingerlin, T. E., O’Connor, B. P., Reisz, J. A., et al. (2017) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2017-0061oc · Cited by 204
“Resident AMs populate the lung during embryogenesis and self-renew throughout life, with little or no contribution from circulating monocytes (12, 13).”
Malainou, C., Abdin, S. M., Lachmann, N., Matt, U., & Herold, S. (2023) · Journal of Clinical Investigation · doi:10.1172/jci170501 · Cited by 215
“Nevertheless, single-cell RNA-Seq experiments strongly indicate that the lung AM populations are heterogeneous (6, 140).”
BackgroundDendritic Cells and Macrophages in the Pathogenesis of Psoriasis
Kamata, M., & Tada, Y. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.941071 · Cited by 204
Splenic Macrophage Subsets and Their Function during Blood-Borne Infections
da Silva, H. B., Fonseca, R., Pereira, R. M., Cassado, A. D. A., Álvarez, J. M., & Lima, M. R. D. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00480 · Cited by 201
“As stated previously, RpMΦs form a vast network inside the Rp, and although there is no consensus about the origin of RpMΦs, recent data indicate that these MΦs are maintained by local proliferation during physiological conditions (31).”
Cai, Y., Sugimoto, C., Araínga, M., Alvarez, X. A., Didier, E. S., & Kuroda, M. J. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302269 · Cited by 201
Patel, A. A., Ginhoux, F., & Yona, S. (2021) · Immunology · doi:10.1111/imm.13320 · Cited by 228
Self-citationDendritic cells and macrophages in the kidney: a spectrum of good and evil
Rogers, N. M., Ferenbach, D. A., Isenberg, J. S., Thomson, A. W., & Hughes, J. (2014) · Nature Reviews Nephrology · doi:10.1038/nrneph.2014.170 · Cited by 206
Zayyad, Z., & Spudich, S. (2015) · Current HIV/AIDS Reports · doi:10.1007/s11904-014-0255-3 · Cited by 198
Myeloid Colony-Stimulating Factors as Regulators of Macrophage Polarization
Hamilton, T. A., Zhao, C., Pavicic, P. G., & Datta, S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00554 · Cited by 200
“It is noteworthy that most resident tissue macrophages are capable of self-replenishment and generally do not derive from circulating monocytes (9, 11).”
BackgroundThe Myeloid Cell Compartment—Cell by Cell
Bassler, K. E., Schulte-Schrepping, J., Warnat‐Herresthal, S., Aschenbrenner, A. C., & Schultze, J. L. (2019) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042718-041728 · Cited by 200
The Role of Macrophages in HIV-1 Persistence and Pathogenesis
Kruize, Z., & Kootstra, N. A. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02828 · Cited by 205
Williams, J. W., Zaitsev, K., Kim, K.-W., Ivanov, S., Saunders, B. T., Schrank, P. R., Kim, K., Elvington, A., Kim, S. H., Tucker, C., et al. (2020) · Nature Immunology · doi:10.1038/s41590-020-0768-4 · Cited by 205
“We next examined macrophage proliferation 32,33 using parabiosis, a surgical method to connect the microvasculature of animal pairs, examining parabionts at two weeks or five months after pairing.”
Wang, T., Zhang, J., Wang, Y., Li, Y., Wang, L., Yu, Y., & Yao, Y. (2023) · Nature Immunology · doi:10.1038/s41590-023-01428-x · Cited by 196
Macrophages Are Key Regulators of Stem Cells during Skeletal Muscle Regeneration and Diseases
Dort, J., Fabre, P., Molina, T., & Dumont, N. A. (2019) · Stem Cells International · doi:10.1155/2019/4761427 · Cited by 211
Vascular Wall Progenitor Cells in Health and Disease
Psaltis, P. J., & Simari, R. D. (2015) · Circulation Research · doi:10.1161/circresaha.116.305368 · Cited by 198
“are maintained by local renewal, independently of BM hematopoiesis and monocyte trafficking.(74,76) Although recent studies of microglia(77)and Langerhans cells(78) have proposed”
BackgroundSchraml, B. U., & Reis e Sousa, C. (2015) · Current Opinion in Immunology · doi:10.1016/j.coi.2014.11.001 · Cited by 197
Macrophages Contribute to the Cyclic Activation of Adult Hair Follicle Stem Cells
Castellana, D., Paus, R., & Pérez‐Moreno, M. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1002002 · Cited by 189
Yoshida, K., Maekawa, T., Zhu, Y., Renard-Guillet, C., Chatton, B., Inoue, K., Uchiyama, T., Ishibashi, K., Yamada, T., Ohno, N., et al. (2015) · Nature Immunology · doi:10.1038/ni.3257 · Cited by 198
Human Dendritic Cell Functional Specialization in Steady-State and Inflammation
Boltjes, A., & van Wijk, F. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00131 · Cited by 216
Osteoimmunology: A Current Update of the Interplay Between Bone and the Immune System
Guder, C., Gravius, S., Burger, C., Wirtz, D. C., & Schildberg, F. A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00058 · Cited by 199
Contribution of adipose tissue to development of cancer
Cozzo, A. J., Fuller, A. M., & Makowski, L. (2017) · Comprehensive Physiology · doi:10.1002/cphy.c170008 · Cited by 188
Mitochondrial quality control in pulmonary fibrosis
Larson‐Casey, J. L., He, C., & Carter, A. B. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101426 · Cited by 192
Roles of Macrophages in the Development and Treatment of Gut Inflammation
Han, X., Ding, S., Jiang, H., & Liu, G. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.625423 · Cited by 196
Youssef, L. A., Rebbaa, A., Pampou, S., Weisberg, S. P., Stockwell, B. R., Hod, E. A., & Spitalnik, S. L. (2018) · Blood · doi:10.1182/blood-2017-12-822619 · Cited by 186
Transcriptional and functional profiling defines human small intestinal macrophage subsets
Bujko, A., Atlasy, N., Landsverk, O. J. B., Richter, L., Yaqub, S., Horneland, R., Øyen, O. M., Aandahl, E. M., Aabakken, L., Stunnenberg, H. G., et al. (2017) · The Journal of Experimental Medicine · doi:10.1084/jem.20170057 · Cited by 188
“However, recent studies in mice have demonstrated that in many organs Mfs are populations of self-renewing cells, established before birth from yolk sac– or fetal liver–derived precursors and independent of bone marrow–derived PBMos (Schulz et al., 2012; Hashimoto et al., 2013; Sieweke and Allen, 2013; Hoeffel et al.,…”
BackgroundMacrophage: A Cell With Many Faces and Functions in Tuberculosis
Ahmad, F., Rani, A., Alam, A., Zarin, S., Pandey, S., Singh, H., Hasnain, S. E., & Ehtesham, N. Z. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.747799 · Cited by 207
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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