Macrophages are critical to the maintenance of IL-13-dependent lung inflammation and fibrosis
Open accessAbstract
The roles of macrophages in type 2-driven inflammation and fibrosis remain unclear. Here, using CD11b-diphtheria toxin receptor (DTR) transgenic mice and three models of interleukin 13 (IL-13)-dependent inflammation, fibrosis, and immunity, we show that CD11b(+) F4/80(+) Ly6C(+) macrophages are required for the maintenance of type 2 immunity within affected tissues but not secondary lymphoid organs. Direct depletion of macrophages during the maintenance or resolution phases of secondary Schistosoma mansoni egg-induced granuloma formation caused a profound decrease in inflammation, fibrosis, and type 2 gene expression. Additional studies with CD11c-DTR and CD11b/CD11c-DTR double-transgenic mice suggested that macrophages but not dendritic cells were critical. Mechanistically, macrophage depletion impaired effector CD4(+) T helper type 2 (Th2) cell homing and activation within the inflamed lung. Depletion of CD11b(+) F4/80(+) Ly6C(+) macrophages similarly reduced house dust mite-induced allergic lung inflammation and suppressed IL-13-dependent immunity to the nematode parasite Nippostrongylus brasiliensis. Consequently, therapeutic strategies targeting macrophages offer a novel approach to ameliorate established type 2 inflammatory diseases.
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TGF-β1 activity is believed to control tissue homeostasis in all mucosal surfaces, especially the intestine.
“This has relevance to all mucosal surfaces, especially the intestine, where TGF-β1 activity is believed to control tissue homeostasis83–85.”
From Fibrosis: from mechanisms to medicines (2020) · cites this paper as [83]
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“By using the CD11b-diphtheria toxin receptor (DTR) in transgenic mice to establish an IL-13-depend-ent model, Borthwick et al. [19] demonstrated that lung fibrosis and inflammation crucially rely on monocyte-derived AMs to maintain type-2 immunity, and AMs may harness this role by regulating…”
MethodMacrophage and Innate Lymphoid Cell Interplay in the Genesis of Fibrosis
Hams, E., Bermingham, R., & Fallon, P. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00597 · Cited by 68 · see citing works
“Conversely, IL-13-elicited macrophages are also implicated in the pathogenesis of fibrosis (102).”
BackgroundMethodRolot, M., & Dewals, B. G. (2018) · Journal of Immunology Research · doi:10.1155/2018/2790627 · Cited by 63 · see citing works
“The role of Arg1 further seems to depend on the tissue, as attested by the observation that although lung macrophages are essential to maintain IL-13dependent inflammation and fibrosis [145], macrophagespecific Arg1 is largely dispensable to control helminthdriven lung inflammation [146].”
BackgroundIL-17 Promotes Scar Formation by Inducing Macrophage Infiltration.
Zhang, J.-L., Qiao, Q., Liu, M.-D., He, T., Shi, J.-H., Bai, X.-Z., Zhang, Y.-J., Li, Y., Cai, W., Han, S.-C., et al. (2018) · American Journal of Pathology · doi:10.1016/j.ajpath.2018.04.005 · Cited by 56 · see citing works
T-bet deficiency attenuates cardiac remodelling in rats
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Therapeutic pro-fibrogenic signaling pathways in fibroblasts
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“orchestrating local inflammatory reactions that maintain fibrotic responses or by blocking the emergence of pro-resolution pathways [13,28,41,42].”
BackgroundInfectious Triggers of Chronic Lung Allograft Dysfunction
Gregson, A. L. (2016) · Current Infectious Disease Reports · doi:10.1007/s11908-016-0529-6 · Cited by 60 · see citing works
“These pathways suggest potential mechanistic links between ACR and fibrotic CLAD [86] .”
BackgroundLambrecht, B., Ahmed, E., & Hammad, H. (2025) · Nature Immunology · doi:10.1038/s41590-025-02212-9 · Cited by 54 · see citing works
Enhanced protection from fibrosis and inflammation in the combined absence of IL‐13 and IFN ‐γ
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Self-citationIL-13 is a driver of COVID-19 severity
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“is a significant driver of goblet cell responses (14), and our data provide evidence that IL-13 signaling is active in COVID-19 but less dramatic, histologically, than in other models of type 2 immunity (26, 27).”
BackgroundSenescence in Pulmonary Fibrosis: Between Aging and Exposure
Venosa, A. (2020) · Frontiers in Medicine · doi:10.3389/fmed.2020.606462 · Cited by 48 · see citing works
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“Parasite killing In vitro Bind to larvae (18); immobilize larvae (17); kill larvae (43–45) Bind and damage larvae (71, 75, 76); kill larvae (16, 70, 76, 78, 79); damage eggs (77) Used bone marrow-derived and/or peritoneal cells (16–18, 70, 78); chemical-induced yield of peritoneal cells may alter cell physiology (133)…”
BackgroundClonorchis sinensis antigens alter hepatic macrophage polarization in vitro and in vivo
Kim, E.-M., Kwak, Y. S., Yi, M.-H., Kim, J., Sohn, W., & Yong, T. (2017) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0005614 · Cited by 46
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Epitranscriptomic 5-Methylcytosine Profile in PM2.5-induced Mouse Pulmonary Fibrosis
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“Inflammatory responses [8,9], immune cell activation [9– 11], and oxidative stress [12,13] are highly associated with pulmonary fibrosis pathogenesis.”
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Roles of Macrophages and Endothelial Cells and Their Crosstalk in Acute Lung Injury
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“These molecules are crucial for monocyte recruitment and their differentiation into macrophages, highlighting the role of ECs as gatekeepers in modulating the immune cell population within the lung microenvironment [9,41,89,107].”
BackgroundFaz-Lopez, B., Morales-Montor, J., & Terrazas, L. (2016) · BioMed Research International · doi:10.1155/2016/8634603 · Cited by 37 · see citing works
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“After activation by pathogen exposure, the cells can be recruited into inflamed tissues and express many proinflammatory cytokines, such as TNF-alpha and other cytokines, responsible for tissue damage [25, 26].”
BackgroundWithaferin A attenuates ovalbumin induced airway inflammation.
Zhao, H.-M., Gao, Z.-W., Xie, S.-X., Han, X., & Sun, Q.-S. (2019) · Frontiers in Bioscience · doi:10.2741/4737 · Cited by 32
“Fibrosis formation is associated with an inflammatory response (56,57).”
BackgroundIntestinal Macrophages at the Crossroad between Diet, Inflammation, and Cancer
Caprara, G., Allavena, P., & Erreni, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21144825 · Cited by 38 · see citing works
Immune-mediated inflammation in the pathogenesis of emphysema: insights from mouse models
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“…regulated response , these M2 cells can also receive additional signals from the local environment that transition them towards a phenotype capable of remodeling newly deposited extracellular matrix components through the production of tissue proteases (Borthwick et al. 2016; Novak and Koh 2013).”
Coleman, S. L., & Shaw, O. M. (2017) · Food & Function · doi:10.1039/c7fo00789b · Cited by 41 · see citing works
TRPM7 modulates macrophage polarization by STAT1/STAT6 pathways in RAW264.7 cells.
Li, L., Wei, C., Cai, S., & Fang, L. (2020) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1016/j.bbrc.2020.10.062 · Cited by 29 · see citing works
Impact of chronic schistosomiasis and HBV/HCV co-infection on the liver: current perspectives
Omar, H. (2019) · Hepatic Medicine : Evidence and Research · doi:10.2147/hmer.s155962 · Cited by 29
“Also, many different cells were activated as macrophages, hepatic stellate cells and regulatory T cells.(15,16)”
Moledina, D., Mansour, S., Jia, Y.-Q., Obeid, W., Thiessen-Philbrook, H., Koyner, J. L., McArthur, E., Garg, A. X., Wilson, F. P., Shlipak, M. G., et al. (2019) · Kidney International Reports · doi:10.1016/j.ekir.2019.09.003 · Cited by 28 · see citing works
Negative Regulation of Type 2 Immunity
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“brasiliensis infected mice, researchers have shown that macrophages do not affect the initiation of the immune response but rather play a role in parasite expulsion and subsequent tissue repair [60, 61].”
BackgroundAnti-fibrotic effects of valproic acid: role of HDAC inhibition and associated mechanisms.
Khan, S., Ahirwar, K., & Jena, G. (2016) · Epigenomics · doi:10.2217/epi-2016-0034 · Cited by 25 · see citing works
Facts and promises on lung biomarkers in interstitial lung diseases
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“IL-13 is a Th2-type cytokine produced by numerous immune cell types, including T lymphocytes and alternatively activated macrophages [102,103].”
BackgroundPlasticity towards Rigidity: A Macrophage Conundrum in Pulmonary Fibrosis
Sari, E., He, C., & Margaroli, C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231911443 · Cited by 26 · see citing works
“showed that depletion of M2 macrophages decreased collagen levels and attenuated fibrosis even in the presence of TGF-β [101], suggesting an important role for macrophage-derived IL-13, as highlighted by Borthwick and colleagues [102].”
BackgroundThe Role of Ninjurin1 and Its Impact beyond the Nervous System
Liu, K., Wang, Y., & Li, H.-G. (2021) · Developmental Neuroscience · doi:10.1159/000512222 · Cited by 24 · see citing works
Monocyte Transmodulation: The Next Novel Therapeutic Approach in Overcoming Ischemic Stroke?
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“On the contrary, the alternative non-classical monocytes (Ly6C−CCR2lowCX3CR1high) play a crucial role in reparative processes, producing anti-inflammatory cytokines, such as IL-4, IL-10 (39), and IL-13 (40), in inflammatory environments.”
BackgroundHematopoietic cell-derived RELMα regulates hookworm immunity through effects on macrophages
Batugedara, H., Li, J., Chen, G., Lu, D., Patel, J. J., Jang, J. C., Radecki, K. C., Burr, A. C., Lo, D. D., Dillman, A. R., et al. (2018) · Journal of Leukocyte Biology · doi:10.1002/jlb.4a0917-369rr · Cited by 24 · see citing works
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IL-13 promotes functional recovery after myocardial infarction via direct signaling to macrophages
Alvarez‐Argote, S., Paddock, S. J., Flinn, M. A., Moreno, C. W., Knas, M. C., Almeida, V. A., Buday, S. L., Nik, A. B., Patterson, M., Chen, Y., et al. (2023) · JCI Insight · doi:10.1172/jci.insight.172702 · Cited by 26 · see citing works
“While IL-13 is known to directly polarize macrophages, the phenotypic consequence of macrophage IL-13 signaling is variable across tissue types and disease conditions; it can be proreparative in some cases (22, 49) and, in other cases, can drive inflammation and fibrosis (50, 51).”
BackgroundReview: Research progress of adipose-derived stem cells in the treatment of chronic wounds
Hao, Z.-L., Qi, W.-L., Sun, J.-M., Zhou, M., & Guo, N.-Q. (2023) · Frontiers in Chemistry · doi:10.3389/fchem.2023.1094693 · Cited by 21 · see citing works
“, and the balance between pro-inflammatory and anti-inflammatory is broken, resulting in a long-term inflammatory state of the wound and the formation of chronic wounds (Borthwick et al., 2016).”
BackgroundInsights from Transcriptomics: CD163+ Profibrotic Lung Macrophages in COVID-19
Bhattacharya, M. (2022) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2022-0107tr · Cited by 23 · see citing works
You Say You Want a Resolution (of Fibrosis)
Atabai, K., Yang, C. D., & Podolsky, M. J. (2020) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2020-0182tr · Cited by 30 · see citing works
Therapeutic and diagnostic targeting of fibrosis in metabolic, proliferative and viral disorders
Sofias, A. M., Lorenzi, F. D., Peña, Q., Shalmani, A. A., Vucur, M., Wang, J., Kiessling, F. M., Shi, Y., Consolino, L., Storm, G., et al. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.113831 · Cited by 27 · see citing works
“Macrophages are critical to the maintenance of IL-13 Adv Drug Deliv Rev. Author manuscript; available in PMC 2021 October 27.”
BackgroundInfluentialInnate immune memory: The evolving role of macrophages in therapy
Damani‐Yokota, P., & Khanna, K. M. (2025) · eLife · doi:10.7554/elife.108276 · Cited by 21 · see citing works
“…crossed to CX3CR1- flox-DTR) mice have been used to deplete lung interstitial macrophages and broader tissue-resident macrophage populations ( Ural et al., 2020 ; Hua et al., 2018 ; Yu et al., 2023 ; Gaertner et al., 2024 ; Borthwick et al., 2016 ; Duffield et al., 2005 ; Miyake et al., 2007 ).”
Iron overload and mitochondrial dysfunction orchestrate pulmonary fibrosis
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Monocyte and Macrophage-Mediated Pathology and Protective Immunity During Schistosomiasis
Souza, C. O. S., Gardinassi, L. G., Rodrigues, V., & Faccioli, L. H. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01973 · Cited by 24 · see citing works
“mansoni eggs reduced the size of granulomas, downregulated the expression of IL-13ra2 (IL-13Rα2), Retnla and Chi3l3 and affected CD4 Th2 cell responses in the lung (Borthwick et al., 2016).”
BackgroundInfluentialHermansyah, D., Putra, A., Muhar, A., Retnaningsih, Wirastuti, K., & Dirja, B. T. (2020) · Medical archives · doi:10.5455/medarh.2021.75.16-22 · Cited by 19 · see citing works
“Prolonged inflammation is a common hallmark of fibrosis, represented by the release of a wide range of growth factors and inflammatory mediators, such as TGF-β, IL-17, and IL-13, to stimulate organ fibrosis, including LF [13].”
The role of ILC 2 in hookworm infection
Filbey, K. J., Bouchery, T., & Gros, G. S. L. (2017) · Parasite Immunology · doi:10.1111/pim.12429 · Cited by 17 · see citing works
Kim, R. Y., Bang, J., Kim, J., Mo, Y., Kim, Y., Lee, C., Elias, J., Kim, H. Y., & Kang, H.-R. (2022) · Scientific Reports · doi:10.1038/s41598-022-14027-x · Cited by 18 · see citing works
Phillippi, D., Daniel, S., Pusadkar, V., Youngblood, V., Nguyen, K. N., Azad, R. K., McFarlin, B. K., & Lund, A. K. (2022) · Particle and Fibre Toxicology · doi:10.1186/s12989-022-00452-3 · Cited by 27 · see citing works
“It has been studied in obesity, metabolic syndrome, and colitis, and its activity in the lung and air pollution has been established [65, 66].”
Liang, Y., Tang, Y., Ren, C., Liu, M., Shen, J., & Hou, X. (2019) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0007474 · Cited by 21 · see citing works
Blockade of RGMb inhibits allergen-induced airways disease
Yu, S., Leung, K. M., Kim, H. Y., Umetsu, S. E., Xiao, Y., Albacker, L. A., Lee, H., Umetsu, D. T., Freeman, G. J., & DeKruyff, R. H. (2019) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2018.12.1022 · Cited by 18 · see citing works
Macrophage polarization and function: new prospects for fibrotic disease
Zhou, D., Yang, K., Chen, L., Wang, Y., Zhang, W., Xu, Z., Zuo, J., Jiang, H., & Luan, J. (2017) · Immunology and Cell Biology · doi:10.1038/icb.2017.64 · Cited by 31 · see citing works
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Properties and Immune Function of Cardiac Fibroblasts
Furtado, M. B., & Hasham, M. G. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-57613-8_3 · Cited by 15 · see citing works
Antecedent Nippostrongylus infection alters the lung immune response to Plasmodium berghei
Craig, J. M., & Scott, A. L. (2017) · Parasite immunology (Print) · doi:10.1111/pim.12441 · Cited by 13 · see citing works
Involvement of ion channels in allergy.
Pelletier, L., & Savignac, M. (2018) · Current Opinion in Immunology · doi:10.1016/j.coi.2018.04.006 · Cited by 12
Dietary NaCl affects bleomycin-induced lung fibrosis in mice
Chen, W., Pilling, D., & Gomer, R. H. (2017) · Experimental Lung Research · doi:10.1080/01902148.2017.1385110 · Cited by 14 · see citing works
Lung Immune Cell Niches and the Discovery of New Cell Subtypes
Shan, Q., Qiu, J., Dong, Z., Xu, X., Zhang, S., Ma, J., & Liu, S. (2024) · Advanced Science · doi:10.1002/advs.202405490 · Cited by 10 · see citing works
Itaconate suppresses house dust mite-induced allergic airways disease and Th2 cell differentiation
Li, Y., Singh, S., Breckenridge, H. A., Cui, T. X., Vigil, T. M., Kreger, J. E., Lei, J., Wong, H. K. A., Sajjakulnukit, P., Zhou, X., et al. (2024) · Mucosal Immunology · doi:10.1016/j.mucimm.2024.08.001 · Cited by 12 · see citing works
“33 Macrophage depletion impaired effector CD4 + T helper type 2 (Th2) cell homing and activation within the inflamed lung, consistent with the notion that after allergen exposure, macrophages promote Th2 effector functions.”
Soliman, S. S. M., El-labbad, E. M., Abu-Qiyas, A., Fayed, B., Hamoda, A. M., Al-Rawi, A. M., Dakalbab, S., El-Shorbagi, A., Hamad, M., Ibrahim, A., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.863133 · Cited by 11 · see citing works
β-Ionone-Derived Curcumin Analogs as Potent Anti-Inflammatory Agents
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IL-13 and TGF-β1: Core Mediators of Fibrosis
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“mansoni egg-driven pulmonary fibrosis, macrophages are important for maintaining T cell responses in the tissue, but not the dLNs (46), while ILC2s, basophils and cDCs have been implicated to play a role in promoting the maintenance of Th2 cells and Tregs at sites of inflammation and at mucosal barriers (47–50).”
Xiu, W.-B., Chen, Y., Chen, Q., Deng, B., Su, J., & Guo, Z.-Z. (2020) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1016/j.bbrc.2020.05.022 · Cited by 9 · see citing works
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Shades of white: new insights into tissue‐resident leukocyte heterogeneity
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Qu, Y., Wang, Y., Wu, T., Liu, X., Wang, H., & Ma, D.-F. (2023) · Lipids in Health and Disease · doi:10.1186/s12944-023-01967-0 · Cited by 7 · see citing works
“The activation of myofibroblasts, tissue injury, and fibrosis are increased in chronic inflammatory conditions due to the influx of infiltrating macrophages [21, 52, 53].”
BackgroundRen, C.-P., Liu, F.-C., Xing, C., Zhao, R., Tang, X., Liu, M., Gao, W.-D., & Shen, J.-J. (2022) · Parasites & Vectors · doi:10.1186/s13071-022-05420-6 · Cited by 7 · see citing works
“They play a key role in the formation and development of egg granulomas and hepatic fibrosis [3, 4].”
Background
- Authors
- Borthwick, L. A., Barron, L., Hart, K. M., Vannella, K. M., Thompson, R. W., Oland, S., Cheever, A., Sciurba, J., Ramalingam, T. R., Fisher, A. J., & Wynn, T. A.
- Affiliations
- National Institutes of Health (US)
- Freeman Hospital (GB)
- Corresponding author
- Wynn, T A
- Venue
- Mucosal Immunology
- Publisher
- Elsevier BV
- Published
- 2016-01
- Volume
- 9
- Issue
- 1
- Pages
- 38-55
- ISSN
- 1933-0219 (ISSN-L)
- PMC
- PMC4626445
- OpenAlex
- W1989021802
- Cited by
- 138
- References
- 54
- Citations by year
- 2026: 8 · 2025: 5 · 2024: 14 · 2023: 10 · 2022: 11 · 2021: 15 · 2020: 15 · 2019: 11 · 2018: 15 · 2017: 18 · 2016: 11 · 2015: 5
- FWCI
- 12.03
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Mucosal Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Newcastle University ePrints (Newcastle Univesity) (cc-by-nc)
- Funders
- European Commission
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (Z01AI000829)
- Topics
- Health Sciences › Medicine › Physiology › Asthma and respiratory diseases
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
- Keywords
- macrophages, IL-13, Th2 immune response, pulmonary fibrosis, lung inflammation, house dust mite allergy, Nippostrongylus brasiliensis, macrophage depletion, CD11b, F4/80, Ly6C, dendritic cells, macrophage-targeted therapy
- MeSH terms
- Animals, Antigens, Differentiation, Antigens, Ly, Fibrosis, Gene Expression Regulation, Lung, Mice, Transgenic, Nippostrongylus, Pneumonia, Schistosoma mansoni, Schistosomiasis mansoni, Signal Transduction, Macrophages, Alveolar, Strongylida Infections, Th2 Cells, Interleukin-13, CD11b Antigen, Pyroglyphidae, Mice, Heparin-binding EGF-like Growth Factor
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