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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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“In the steady state and in response to non-genotoxic injury, TRM repopulation is mainly independent of circulating monocytes 4 .”
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“This is akin to other innate cells, such as tissue-resident macrophages that are seeded in early life and self-renew in the adult, independent of circulating monocytes (Schulz et al. 2012; Hashimoto et al. 2013).”
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“Macrophages, acting as sentinel cells that patrol different tissues or organs, provide the first lines of defense against pathogenic infections or toxic stresses to maintain tissue homeostasis [14–18].”
BackgroundNanoparticle uptake by macrophages in vulnerable plaques for atherosclerosis diagnosis
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“Previously reported Tissue-resident macrophages (TRMs) are diverse cell families, which generally pre-sent long-lived and self-renewing [196, 197].”
BackgroundCentral Nervous System Macrophages in Health and Disease
Hove, H. V., Feo, D. D., Greter, M., & Becher, B. (2025) · Annual Review of Immunology · doi:10.1146/annurev-immunol-082423-041334 · Cited by 53
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Self-citationMonocyte depletion increases local proliferation of macrophage subsets after skeletal muscle injury
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“Although mechanisms of macrophage replenishment were described in other tissues [34-36], the intrinsic mechanisms supporting their accumulation in the specific context of muscle injury are still a matter of debate and how these mechanisms are modulated under various anti-inflammatory strategies remains unknown.”
BackgroundTranscriptional Regulation of Mononuclear Phagocyte Development
Tussiwand, R., & Gautier, E. L. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00533 · Cited by 50
“Lineagetracing studies recently revisited their origin and revealed how their maintenance in adult tissues is mostly independent from monocytes and adult definitive hematopoiesis (10).”
Lagassé, H. A. D., Anidi, I. U., Craig, J. M., Limjunyawong, N., Poupore, A. K., Mitzner, W., & Scott, A. L. (2015) · Journal of Leukocyte Biology · doi:10.1189/jlb.4hi0315-130rrr · Cited by 51
“Recent studies have revealed that tissue-resident macrophages are seeded before birth [45–48] and have a capacity for in situ self-renewal to maintain steady-state levels [47, 48], for replacement after depletion [49], and in response to infections [50, 51].”
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Dong, Y., Poon, G. F. T., Arif, A. A., Lee‐Sayer, S. S. M., Dosanjh, M., & Johnson, P. (2017) · Mucosal Immunology · doi:10.1038/mi.2017.83 · Cited by 51
“AM^ develop from fetal monocytes and do not depend on adult monocytes for self-maintenance at homeostasis.(6,7) Here, we show that the self-renewal of AM^ contributes to the rapid AM^ repopulation 7 days after LPS-induced inflammation and AM^ depletion.”
BackgroundHuman macrophage responses to metal-oxide nanoparticles: a review
Borgognoni, C. F., Kim, J. H., Zucolotto, V., Fuchs, H., & Riehemann, K. (2018) · Artificial Cells Nanomedicine and Biotechnology · doi:10.1080/21691401.2018.1468767 · Cited by 48
Current tools to interrogate microglial biology
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An Eye on Kupffer Cells: Development, Phenotype and the Macrophage Niche
Elchaninov, A. V., Vishnyakova, P., Menyailo, E., Sukhikh, G. T., & Fatkhudinov, T. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23179868 · Cited by 48
“However, with depletion of KCs from the liver, the niche is filled by immigrating monocytic macrophages which successfully engage in the long-term maintenance by proliferation [61,80], although in other organs recolonization proceeds differently for reasons as yet unexplained [70].”
BackgroundMethodThe role of lung macrophages in chronic obstructive pulmonary disease
Wu, J., Zhao, X., Xiao, C., Xiong, G., Ye, X., Li, L., Yan, F., Chen, H., Yang, W., & Du, X. (2022) · Respiratory Medicine · doi:10.1016/j.rmed.2022.107035 · Cited by 47
“that LMs are embryonic derived and originate from the yolk sac, the fetal liver and the bone marrow (23-25).”
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PGE2-treated macrophages inhibit development of allergic lung inflammation in mice
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Digesting the role of bone marrow macrophages on hematopoiesis
Heideveld, E., & van den Akker, E. (2016) · Immunobiology · doi:10.1016/j.imbio.2016.11.007 · Cited by 46
Isolation and In Vitro Culture of Murine and Human Alveolar Macrophages
Nayak, D. K., Mendez, O. A., Bowen, S. K., & Mohanakumar, T. (2018) · Journal of Visualized Experiments · doi:10.3791/57287 · Cited by 51
Kawanishi, S., Takata, K., Itezono, S., Nagayama, H., Konoya, S., Chisaki, Y., Toda, Y., Nakata, S., Yano, Y., Kitamura, Y., et al. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-170994 · Cited by 47
Prolactin promotes fibrosis and pancreatic cancer progression
Tandon, M., Coudriet, G. M., Criscimanna, A., Socorro, M., Eliliwi, M., Singhi, A., Cruz-Monserrate, Z., Bailey, P., Lotze, M., Zeh, H., et al. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-3064 · Cited by 43
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Macrophage‐fibroblast circuits in the spleen
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Cumming, B. M., Rahman, M. A., Lamprecht, D. A., Rohde, K. H., Saini, V., Adamson, J., Russell, D. G., & Steyn, A. J. C. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006389 · Cited by 47
“In the lung, which is the site of infection in pulmonary tuberculosis (TB), it was found that when the lung macrophages were depleted as a result of acute infection, the majority of repopulation occurred by stochastic cellular proliferation in situ in a macrophage colony-stimulating factor (CSF) and granulocyte macrop…”
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ILC-You in the Thymus: A Fresh Look at Innate Lymphoid Cell Development
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Development of an Optimized Culture System for Generating Mouse Alveolar Macrophage–like Cells
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“Bone marrow-derived and resident macrophages proliferate independently from one another with limited proliferative activity shown in resident macrophages during IA [109,134].”
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“Several lines of evidence indicate that tissue-resident macrophages in general, and alveolar macrophages in particular, self-renew independent of bone marrow progenitors under steady state and Th2-inflammatory conditions (16, 20).”
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Alveolar-like Stem Cell–derived Myb − Macrophages Promote Recovery and Survival in Airway Disease
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Microglia: A Unique Versatile Cell in the Central Nervous System
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Mitsi, E., Carniel, B. F., Reiné, J., Rylance, J., Zaidi, S. R., Schanoski, A. S., Connor, V., Collins, A. M., Schlitzer, A., Nikolaou, E., et al. (2019) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201903-0607oc · Cited by 44
Unique Phenotypes of Heart Resident Type 2 Innate Lymphoid Cells
Deng, Y., Wu, S., Yao, Y., Meng, M., Chen, X., Chen, S., Li, L., Gao, Y., Cai, Y., İmani, S., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00802 · Cited by 46
The Role of TRPV4 in Regulating Innate Immune Cell Function in Lung Inflammation
Scheraga, R. G., Southern, B. D., Grove, L. M., & Olman, M. A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01211 · Cited by 48
Salmonid Antibacterial Immunity: An Aquaculture Perspective
Semple, S. L., & Dixon, B. (2020) · Biology · doi:10.3390/biology9100331 · Cited by 52
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“Under healthy and normal conditions, microglia are self-maintained with no considerable contribution of peripheral myeloid cells [4].”
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Adipose tissue immune cells in obesity, type 2 diabetes mellitus and cardiovascular diseases
Cinkajzlová, A., Mráz, M., & Haluzík, M. (2021) · Journal of Endocrinology · doi:10.1530/joe-21-0159 · Cited by 47
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“5) in Cx3cr1;R26R-EYFP (31, 46, 61) mice (Figure 3E), the vast majority of YFP cells were still found in TIM4CD163 subpopulation, both in 5- and 10-weekold mice (Figure 3F and Supplementary Figure 6B).”
BackgroundMethodPerinatal development of innate immune topology
Henneke, P., Kierdorf, K., Hall, L. J., Sperandio, M., & Hornef, M. W. (2021) · RWTH Publications (RWTH Aachen) · Cited by 45
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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