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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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Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890
Chen, Y., Wang, L., Kang, Q., Zhang, X., Yu, G., Wan, X., Wang, J., & Zhu, K. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000477308 · Cited by 10,730
Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., & Henson, P. M. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1112 · Cited by 3,166 · cited 1×
“Moreover, signaling through certain efferocytosis receptors can inhibit inflammatory signaling pathways and promote the secretion of resolution mediators (Fadok et al., 1998; Freire-de-Lima et al., 2006; Cai et al., 2016).”
Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity
Neill, D. R., Wong, S. H., Bellosi, A., Flynn, R. J., Daly, M. G., Langford, T. K. A., Bucks, C. M., Kane, C. M., Fallon, P. G., Pannell, R., et al. (2010) · Nature · doi:10.1038/nature08900 · Cited by 2,079
Matute‐Bello, G., Downey, G. P., Moore, B. B., Groshong, S. D., Matthay, M. A., Slutsky, A. S., & Kuebler, W. M. (2011) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2009-0210st · Cited by 2,016
Anti-inflammatory effect of IL-10 mediated by metabolic reprogramming of macrophages
Ip, W., Hoshi, N., Shouval, D. S., Snapper, S. B., & Medzhitov, R. M. (2017) · Science · doi:10.1126/science.aal3535 · Cited by 1,382
Natural regulatory T cells control the development of atherosclerosis in mice
Ait‐Oufella, H., Salomon, B. L., Potteaux, S., Robertson, A.-K. L., Gourdy, P., Zoll, J., Merval, R., Esposito, B., Cohen, J. L., Fisson, S., et al. (2006) · Nature Medicine · doi:10.1038/nm1343 · Cited by 1,126
Stattic: a small-molecule inhibitor of STAT3 activation and dimerization
Schust, J., Sperl, B., Hollis, A., Mayer, T. U., & Berg, T. (2006) · Chemistry & Biology · doi:10.1016/j.chembiol.2006.09.018 · Cited by 1,105
Sutmuller, R. P. M., van Duivenvoorde, L. M., van Elsas, A., Schumacher, T. N. M., Wildenberg, M. E., Allison, J. P., Toes, R. E. M., Offringa, R., & Melief, C. J. M. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.194.6.823 · Cited by 1,008
A Distinct Function of Regulatory T Cells in Tissue Protection
Arpaia, N., Green, J. A., Moltedo, B., Arvey, A., Hemmers, S., Yuan, S., Treuting, P. M., & Rudensky, A. Y. (2015) · Cell · doi:10.1016/j.cell.2015.08.021 · Cited by 991
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Zhou, H.-S., Cui, Z., Wang, H., Gao, T.-T., Wang, L., Wu, J., Xiong, Z., Hao, J., & Zhao, M.-H. (2022) · Figshare · doi:10.6084/m9.figshare.20025766
Ma, X., Qin, C., Chen, M. L., Yu, H.-H., Chu, Y., Chen, T.-J., Bosco, D. B., Wu, L.-J., Bu, B.-T., Wang, W., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16625432
Liao, Z., Lan, H., Jian, X., Huang, J., Wang, H., Hu, J., & Liao, H. (2024) · Figshare · doi:10.6084/m9.figshare.26601811
Broeckhoven, J. V., Erens, C., Sommer, D., Scheijen, E. E. M., Sanchez, S., Vidal, P. M., Dooley, D., Breedam, E. V., Quarta, A., Ponsaerts, P., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19687225
Broeckhoven, J. V., Erens, C., Sommer, D., Scheijen, E. E. M., Sanchez, S., Vidal, P. M., Dooley, D., Breedam, E. V., Quarta, A., Ponsaerts, P., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19687222
Broeckhoven, J. V., Erens, C., Sommer, D., Scheijen, E. E. M., Sanchez, S., Vidal, P. M., Dooley, D., Breedam, E. V., Quarta, A., Ponsaerts, P., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19687234
Qin, Y., & Gou, L. (2025) · medRxiv · doi:10.64898/2025.12.10.25342023
Immune imbalance and autoimmune mechanisms in plasma cell mastitis: current perspectives
Xue, B., Jiang, Y., Yan, L., Liu, X., Li, J., Li, Y., Zhang, B., Wang, Y., & Jia, H. (2026) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1727675 · Cited by 2
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Prasad, N. R., Ganesh, B. B., Dudek, S. M., Tiruppathì, C., & Malik, A. B. (2026) · Research Square · doi:10.21203/rs.3.rs-9396111/v1
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Lu, Y. N., Li, B., Mbabazi, N., Abbas, K. M., Lin, P., Pei, H., Bao, Y. N., Zou, L., Gao, F., Yang, F., et al. (2026) · Cardiovascular Innovations and Applications · doi:10.15212/cvia.2025.0032
Liu, T., Xia, L., Zhang, Y., Zhou, E., & Wang, H. (2026) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2026.1774825
“In particular, impaired clearance of apoptotic cells (efferocytosis) is recognized as a contributor to necrotic core expansion and plaque vulnerability; “find-me” signaling and phagocyte recruitment are critical components of effective efferocytosis biology (27–29).”
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Merlin, J. (2020) · theses.fr (ABES) · doi:10.70675/68e10f28zf840z48bfz9bacz5511a3a2b208
Burke, S. D. A. (2026) · American Journal of Human Biology · doi:10.1002/ajhb.70258
“Macrophages secreting IL-10 and TGF-β (also inflammation controlling) collaborate with regulatory T cells (Tregs) to suppress inflammation and produce tissue repairing proteins (Proto et al. 2018).”
Lan, H., Jian, X., Liao, Z., Li, Y., Wang, Q., Huang, J.-W., Hu, J., & Liao, H. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1810106
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“The receptors produced by the significant expression of HAVCR1 and STAB2 bind to the “eat me” signal of phosphatidylserine (PS), coupled with the destruction of tight junctions, thus promoting the rapid development of tumor [11, 12, 14].”
Ngai, D., Chowdhury, S., Sukka, S. R., Kuriakose, G., Havens, B. T., Yalçınkaya, M., Frey, J. M., Doviak, H., Bradford, J. W., Dorweiler, B., et al. (2026) · Nature Communications · doi:10.64898/2026.04.27.720940
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InfluentialSelf-citationYe, S.-Y., Qu, Y., Zhang, J.-H., Wang, X.-H., Wang, J., Xue, Y., & Liu, J.-D. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1835168
Illingworth, E. J., Sanchez, S. S., Rychlik, K. A., Kleensang, A., Laird, J., Lopez-Cecetaite, G., Steube, M. C. R., Mathur, A., Sadhukhan, P., Medina-Cleghorn, D., et al. (2026) · Environmental Research · doi:10.1016/j.envres.2026.124699
Sekiya, T., Hidano, S., & Takaki, S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.07.723421
Bao, J., Wu, L., Zhao, W., Li, B., Li, Z., Bai, Z., Ma, P., Gao, B., & Qiao, C. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1777038
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“39 Neutrophil dysfunction may cause prolonged inflammation and autoimmune diseases.”
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Chen, Y., Luo, X., Xu, B., Zhu, X., Mou, J., Wang, M., Gu, Q., Wang, Y., Bai, X., Zhang, S., et al. (2026) · BMC Medicine · doi:10.1186/s12916-026-04975-w
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Liu, C., Yang, M., Wang, Y., Zheng, Z., Lu, B., 周盛松, Xu, L., & Huang, H. (2026) · Orthopaedic Journal of Sports Medicine · doi:10.1177/23259671261440807
“Proto et al 23 demonstrated that Treg cells enhanced the capacity of macrophages to phagocytose apoptotic cells and thereby facilitated the resolution of inflammation.”
Zhang, M., Shi, L., Dong, Y., Sun, Y., Zhu, S., & Jin, Q. (2026) · Molecular Biology Reports · doi:10.1007/s11033-026-12088-z
“Under homeostatic conditions, splenic Tregs contribute to peripheral immune tolerance, restrain excessive activation of splenic myeloid cells, and support an immune milieu favorable for inflammation resolution and phagocytic clearance [43, 52 ].”
Khademi, M., Kazemifard, N., Ghavami, S. B., Farmani, M., & Shahrokh, S. (2026) · Molecular Biology Reports · doi:10.1007/s11033-026-12291-y
“The process by which neutrophils undergo cell death plays a crucial role in the resolution of inflammation [ 49].”
Legere, S. A., Nanjundappa, R. H., Meghnem, D., Haidl, I. D., Edgar, A., Hu, Q., Légaré, J., & Marshall, J. S. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1802300
Haile, S. A., Gatta, A., Colon, N., Philpott, D. J., Kufer, T. A., Ying, L., Tong, D., & Ferrero, R. L. (2026) · The FASEB Journal · doi:10.1096/fj.202504879r
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Tang, W., Zhang, S. J., Qi, Y., Li, B., Gao, Z., Pan, Z., Qiu, J., Xue, H., Li, G., & Wang, S. (2026) · Cellular and Molecular Immunology · doi:10.1038/s41423-026-01458-z
Sahebi, K., Bordbar, M., Eslamzadeh, S., Hosseinpour-Soleimani, F., Tajbakhsh, A., Savardashtaki, A., & Attar, A. (2026) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2026.119872
de Castro, I. S., Rahman, M. A., Bissa, M., Goldfarbmuren, K. C., Schifanella, L., Sarkis, S., N’Guessan, K. F., Ma, Z.-M., Gutowska, A., Stamos, J. D., et al. (2026) · Cell Reports Medicine · doi:10.1016/j.xcrm.2026.103022
“41,42 No other cell subset differences were detected between vaccine groups (Figures S8A–S8F).”
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Yalçınkaya, M., Hsu, C.-C., Li, L., Wang, R., Ngai, D., Vela, P. S., Fernández-Maestre, I., Olszewska, M., Liu, W., Chen, M., et al. (2026) · Circulation · doi:10.1161/circulationaha.126.080527
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Qin, Z., Chen, S., Lyu, Z., Zhou, F., Liu, L., Ai, Q., & Zeng, Z. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1923083
CD47-mediated efferocytosis in diseases: A comprehensive review
Wang, C., Yu, S., Kang, J., Yang, S., Pan, Z., Zhao, Y., Li, C., & Zhu, W. (2026) · Molecular Biology Reports · doi:10.1007/s11033-026-12854-z
Xu, W., Wang, X., Dai, J., Wang, G., Yang, X., Wang, Q., 李学选, Huang, Q., Li, Y., Lina, Z., et al. (2026) · Pharmacological Research · doi:10.1016/j.phrs.2026.108475
Subramanian, M. (2026) · Current topics in microbiology and immunology · doi:10.1007/82_2026_361
Self-citationWang, X., Mei, J., Li, R., Zhang, Y., Zhao, G., Hu, Y., Yan, G., Sun, H., & Lv, H. (2026) · Human Reproduction · doi:10.1093/humrep/deag160
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Proskurina, A. S., Kirikovich, S. S., Ivanov, N. A., Levites, E. V., Ritter, G. S., Ruzanova, V. S., Долгова, Е. В., Chernykh, E. R., Kolchanov, N. A., & Bogachev, S. S. (2026) · The Open Rheumatology Journal · doi:10.2174/0118743129512761261007054624
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kumar, D., Pandit, R., Frausto, L., Governale, T.-A., Yuan, S. S., Fieira, J. N., Quaye, A., McGee, K., Das, S. R., Anand, S. K., et al. (2026) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.126.325444
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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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