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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Tregs contribute to the control and termination of the inflammatory response by producing anti-inflammatory cytokines such as IL-10, TGF-β, and IL-35.
“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]
The Introduction says Tregs can secrete IL-10, and the Discussion links them to inflammation resolution. However, the Results say the pathway studied here depends on Treg-derived IL-13 inducing IL-10 production in macrophages, not on Tregs producing all three listed cytokines. Our copy does not establish Treg production of TGF-β or IL-35 in this response. (LLM, conf=0.89)
Experimental — accuracy not yet measuredA regulatory T cell-mediated pathway of the inflammation resolution response promotes efferocytosis.
“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]
The regulatory T cell mechanism involves IL-13 secretion, which stimulates macrophages to secrete and then be activated by IL-10.
“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]
Impaired macrophage efferocytosis enhances atherogenesis and atherosclerotic plaque instability.
“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]
Elevated IL-10 signaling upregulates macrophage STAT3-mediated VAV1, which activates GTPase Rac1 to enhance apoptotic cell engulfment by macrophages.
“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]
Activated Treg cells secrete IL-13 to stimulate IL-10 production in macrophages via binding to the IL-13 receptor.
“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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“Efferocytosis is a well-conserved process as evident from the observation that IL-13 secreted by Treg cells resolves lung inflammation through activating M V -mediated efferocytosis (5).”
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“During inflammation resolution, Regulatory T (Treg) cells secreted IL13 to promote macrophage efferocytosis and enhanced apoptotic cell internalization (24).”
BackgroundCD8+ T cell–derived IL-13 increases macrophage IL-10 to resolve neuropathic pain
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“However, the beneficial effects of macrophages and regulatory T cell interactions during inflammation resolution and tissue regeneration have been reported (Panduro et al., 2018; Proto et al., 2018).”
BackgroundIL-33–mediated IL-13 secretion by ST2+ Tregs controls inflammation after lung injury
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The Src-family Kinase Lyn in Immunoreceptor Signaling
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Efferocytosis drives a tryptophan metabolism pathway in macrophages to promote tissue resolution
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“We next examined the effect of IDO1 KO or inhibition on Rac1 GTPase activity, because Rac1-mediated actin remodelling around the forming phagosome is a key step in the engulfment of ACs and other large substrates 27,28 .”
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Revisiting regulatory T cells as modulators of innate immune response and inflammatory diseases
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Dysregulated cellular metabolism in atherosclerosis: mediators and therapeutic opportunities
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“It was recently shown by Proto et al. (2018) that IL-10 signaling can increase the phagocytic capacity of lung macrophages by stimulating the STAT3- VAV1-RAC1 axis ( 50 ).”
BackgroundImmunomodulation for Tissue Repair and Regeneration
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Mechanisms of exTreg induction
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Self-citationDeficiency of macrophage PHACTR1 impairs efferocytosis and promotes atherosclerotic plaque necrosis
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Sterile inflammation and the NLRP3 inflammasome in cardiometabolic disease
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- 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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