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Regulatory T Cells Promote Macrophage Efferocytosis during Inflammation Resolution
Open accessAbstract
Regulatory T (Treg) cell responses and apoptotic cell clearance (efferocytosis) represent critical arms of the inflammation resolution response. We sought to determine whether these processes might be linked through Treg-cell-mediated enhancement of efferocytosis. In zymosan-induced peritonitis and lipopolysaccharide-induced lung injury, Treg cells increased early in resolution, and Treg cell depletion decreased efferocytosis. In advanced atherosclerosis, where defective efferocytosis drives disease progression, Treg cell expansion improved efferocytosis. Mechanistic studies revealed the following sequence: (1) Treg cells secreted interleukin-13 (IL-13), which stimulated IL-10 production in macrophages; (2) autocrine-paracrine signaling by IL-10 induced Vav1 in macrophages; and (3) Vav1 activated Rac1 to promote apoptotic cell engulfment. In summary, Treg cells promote macrophage efferocytosis during inflammation resolution via a transcellular signaling pathway that enhances apoptotic cell internalization. These findings suggest an expanded role of Treg cells in inflammation resolution and provide a mechanistic basis for Treg-cell-enhancement strategies for non-resolving inflammatory diseases.
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In the citing paper
“They contribute to the control and termination of the inflammatory response by producing anti‐inflammatory cytokines such as IL‐10, TGF‐β, and IL‐35.[ 9 ]”
From Ccl2-Induced Regulatory T Cells Balance Inflammation Through Macrophage Polarization During Liver Reconstitution (2024) · cites this paper as [9]
Experimental — accuracy not yet measuredIn the citing paper
“and new work indicates that a cellular pathway of the inflammation resolution response — mediated by regulatory T cells — also promotes efferocytosis79.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [79]
In the citing paper
“The mechanism of the regulatory T cell response involves secretion of IL-13, which in turn stimulates macrophages to secrete and then be activated by the pro-efferocytic cytokine IL-10 (REF79).”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [79]
In the citing paper
“The impaired ability of macrophage efferocytosis would enhance atherogenesis [139,140,141] and atherosclerotic plaque instability [142,143,144].”
From Immune Clearance of Senescent Cells to Combat Ageing and Chronic Diseases (2020) · cites this paper as [139]
In the citing paper
“The elevated IL-10 signaling upregulates macrophage STAT3-mediated VAV1 (a guanine nucleotide exchange factor), which activates GTPase Rac1 to enhance apoptotic cell engulfment by macrophages [139].”
From Immune Clearance of Senescent Cells to Combat Ageing and Chronic Diseases (2020) · cites this paper as [139]
In the citing paper
“activated Treg cells secrete IL-13 to stimulate IL-10 production in macrophages via binding to the IL-13 receptor.”
From Immune Clearance of Senescent Cells to Combat Ageing and Chronic Diseases (2020) · cites this paper as [139]
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“The efferocytic clearance of apoptotic neutrophils, for instance, stimulates the secretion of anti-inflammatory cytokines like TGF-β and IL-10, as well as prostaglandin E2 (PGE2), while reducing the release of pro-inflammatory mediators [104, 105].”
Immune Cell Activation in Obesity and Cardiovascular Disease
Garcia, J. N., Wanjalla, C. N., Mashayekhi, M., & Hasty, A. H. (2022) · Current Hypertension Reports · doi:10.1007/s11906-022-01222-4 · Cited by 25
Resveratrol activates CD8+ T cells through IL-18 bystander activation in lung adenocarcinoma
Zhang, W., Zhang, R., Chang, Z., & Wang, X. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.1031438 · Cited by 22
Zhu, J., Fan, J., Xia, Y., Wang, H., Li, Y., Feng, Z., & Fu, C. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1219487 · Cited by 26
Zhang, J., Liu, S., Ding, W. B., Wan, J., Qin, J., & Wang, M. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102352 · Cited by 23
The dual role of tissue regulatory T cells in tissue repair: return to homeostasis or fibrosis
Zhang, P., Wang, J., Miao, J., & Zhu, P. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1560578 · Cited by 24
Anti-inflammatory and Immunomodulatory Therapies in Atherosclerosis
Deroissart, J., Porsch, F., Köller, T., & Binder, C. J. (2021) · Handbook of experimental pharmacology · doi:10.1007/164_2021_505 · Cited by 24
Macrophage efferocytosis in atherosclerosis
Baraniecki, Ł., Tokarz–Deptuła, B., Syrenicz, A., & Deptuła, W. (2022) · Scandinavian Journal of Immunology · doi:10.1111/sji.13251 · Cited by 21
Responses of hepatic sinusoidal cells to liver ischemia–reperfusion injury
Ito, Y., Hosono, K., & Amano, H. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1171317 · Cited by 22
Insights into the Role of Inflammation in the Management of Atherosclerosis
Rocha, V. Z., Rached, F. H., & Miname, M. H. (2023) · Journal of Inflammation Research · doi:10.2147/jir.s276982 · Cited by 22
Sjogren’s Syndrome and TAM Receptors: A Possible Contribution to Disease Onset
Witas, R., Peck, A. B., Ambrus, J. L., & Nguyen, C. Q. (2019) · Journal of Immunology Research · doi:10.1155/2019/4813795 · Cited by 21
“A recent paper has reported that regulatory T cells (Tregs) stimulate macrophage efferocytosis by production of IL-13 which in turn stimulates macrophages to release IL-10 which acts in an autocrine-paracrine manner to upregulate Vav1 and activate Rac1, enabling apoptotic cell engulfment [131].”
BackgroundWeathering the Storm: Harnessing the Resolution of Inflammation to Limit COVID-19 Pathogenesis
Silberberg, E., Filep, J. G., & Ariel, A. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.863449 · Cited by 22
“A key route by which pro-resolving pathways are activated include the production of specialized pro-resolving mediators (SPMs) (87), as well as the upregulation of genes involved in the generation of Treg cells, which were shown to enhance macrophage efferocytosis through the IL-13-IL-10 axis (88).”
BackgroundHong, N. E., Chaplin, A. M. L., Di, L., Ravodina, A. M., Bevan, G. H., Gao, H., Asase, C., Gangwar, R. S., Cameron, M. J., Mignery, M., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114911 · Cited by 20
Okamoto, M., Kuratani, A., Okuzaki, D., Kamiyama, N., Kobayashi, T., Sasai, M., & Yamamoto, M. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2401692121 · Cited by 20
“Previous studies have shown that macrophages cocultured with Tregs polarize into M2 - type to be anti - inflammatory ( 67 ) and increase efferocytotic capability ( 68 ), indicating that the direct effect of Tregs on mac rophages is to make them anti - inflammatory.”
Che, X., Xiao, Q., Song, W., Zhang, H., Sun, B., Geng, N., Tao, Z., Shao, Q., & Pu, J. (2021) · Journal of the American Heart Association · doi:10.1161/jaha.120.018455 · Cited by 20
Cheng, L., Weng, B., Jia, C., Zhang, L., Hu, B., Deng, L., Mou, N., Sun, F., & Hu, J. Y. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.977025 · Cited by 20
Unique Pro-Inflammatory Response of Macrophages during Apoptotic Cancer Cell Clearance
Mendoza‐Reinoso, V., Baek, D. Y., Kurutz, A., Rubin, J. R., Koh, A. J., McCauley, L. K., & Roca, H. (2020) · Cells · doi:10.3390/cells9020429 · Cited by 20
“This may be explained by the presence of M-CSF in the media, which is known for its effect in promoting M2 polarization in macrophages [20].”
BackgroundNakamoto, S., Ito, Y., Nishizawa, N., Goto, T., Kojo, K., Kumamoto, Y., Watanabe, M., Narumiya, S., & Majima, M. (2020) · The FASEB Journal · doi:10.1096/fj.201901955r · Cited by 20
Regulatory T cells and macrophages in atherosclerosis: from mechanisms to clinical significance
Ouyang, X., & Liu, Z. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1435021 · Cited by 20
Efferocytosis: The Janus‐Faced Gatekeeper of Aging and Tumor Fate
Liu, Z., Li, Y., Ren, Y., Chen, J., Weng, S., Zhou, Z., Luo, P., Cheng, Q., Xu, H., Ba, Y., et al. (2025) · Aging Cell · doi:10.1111/acel.14467 · Cited by 21
“This, in turn, promotes the efferocytosis of macrophages by starting the accumulation of Rac1-associated actin in phagosomes and the internalization of apoptotic cells (Proto et al. 2018).”
InfluentialLang, F., Li, Y., Yao, R., & Jiang, M. (2025) · Biology · doi:10.3390/biology14040428 · Cited by 25
“Macrophages are integral to both the initiation and resolution of inflammation [41].”
Reddy, N. M., Tamatam, C. M., Ankireddy, A., & Reddy, S. P. (2022) · Antioxidants · doi:10.3390/antiox11020212 · Cited by 19
“, T cells) [15] also plays a vital role in efferocytosis and inflammation resolution.”
BackgroundLigand-based adoptive T cell targeting CA125 in ovarian cancer
Zhao, H., Wu, L., Dai, J., Sun, K., Zi, Z., Guan, J., & Zhang, L. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04271-8 · Cited by 19
“IL-13 was an immunoregulatory cytokine produced primarily by Th2 cells that may improve T cell regulation and prevent T cell overreaction [40, 41].”
BackgroundIL-10 Counteracts IFN-γ to Alleviate Acute Lung Injury in a Viral-Bacterial Superinfection Model
McKelvey, M. C., Uddin, M. B., Palani, S., Shao, S., & Sun, K. (2024) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2023-0437oc · Cited by 19
Fan, P., Lai, H.-Q., Wang, H., Hu, K., Ruan, Y., Ye, J.-R., Wang, S., Peng, Y., He, W., Li, G., et al. (2025) · Cell Death and Differentiation · doi:10.1038/s41418-025-01475-x · Cited by 18
Resolution of Inflammation in Acute Graft-Versus-Host-Disease: Advances and Perspectives
Duarte, L. R. F., Pinho, V., Rezende, B. M., & Teixeira, M. M. (2022) · Biomolecules · doi:10.3390/biom12010075 · Cited by 18
The Resolution of Intestinal Inflammation: The Peace-Keeper’s Perspective
Onali, S., Favale, A., & Fantini, M. C. (2019) · Cells · doi:10.3390/cells8040344 · Cited by 19
Zhang, S., Duitman, J., Artigas, A., & Bos, L. D. J. (2024) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2024-0176tr · Cited by 18
“Extensive studies into myeloid cells in vivo have shown that cell – cell interplay exists and is important for in fl ammation modulation, immune responses, and tissue repair, in fl uencing the progression of the disease (11 – 15).”
Wara, A. K., Rawal, S., Yang, X., Pérez‐Cremades, D., Sachan, M., Chen, J., & Feinberg, M. W. (2022) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2022.08.019 · Cited by 18
Hu, W., Li, P., Zeng, N., & Tan, S. (2023) · Scientific Reports · doi:10.1038/s41598-023-27459-w · Cited by 19
Metadata
- Authors
- Proto, J. D., Doran, A. C., Gusarova, G., Yurdagul, A., Sozen, E., Subramanian, M., Islam, M. N., Rymond, C. C., Du, J., Hook, J., Kuriakose, G., Bhattacharya, J., & Tabas, I.
- Affiliations
- Columbia University (US)
- Columbia University Irving Medical Center (US)
- Corresponding author
- Tabas, Ira
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2018-10
- Volume
- 49
- Issue
- 4
- Pages
- 666-677.e6
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC6192849
- OpenAlex
- W2894606588
- Cited by
- 441
- References
- 49
- Citations by year
- 2026: 49 · 2025: 68 · 2024: 68 · 2023: 73 · 2022: 72 · 2021: 47 · 2020: 33 · 2019: 29 · 2018: 2
- FWCI
- 11.91
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Dspace Repository (Marmara Üniversitesi) (submittedVersion, other-oa)
- Funders
- NIH (HL007343, HL122730, DoD-PR150672, HL132412, HL075662, HL127464, 5P30DK063608, P30CA013696)
- American Heart Association
- Scientific and Technological Research Council of Turkey
- BIDEB 2214/A Program
- Stony Wold-Herbert Fund Inc.
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Keywords
- regulatory T cells, macrophage efferocytosis, efferocytosis, inflammation resolution, IL-13, IL-10, Vav1, Rac1, zymosan-induced peritonitis, lipopolysaccharide-induced lung injury, atherosclerosis, Treg depletion
- MeSH terms
- Animals, Cell Line, Cells, Cultured, Humans, Inflammation, Lipopolysaccharides, Lung Diseases, Macrophages, Mice, Inbred C57BL, Peritonitis, Phagocytosis, Zymosan, Interleukin-10, Apoptosis, Mice, Knockout, Interleukin-13, Jurkat Cells, T-Lymphocytes, Regulatory
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