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Efferocytosis Fuels Requirements of Fatty Acid Oxidation and the Electron Transport Chain to Polarize Macrophages for Tissue Repair
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During wound injury, efferocytosis fills the macrophage with a metabolite load nearly equal to the phagocyte itself. A timely question pertains to how metabolic phagocytic signaling regulates the signature anti-inflammatory macrophage response. Here we report the metabolome of activated macrophages during efferocytosis to reveal an interleukin-10 (IL-10) cytokine escalation that was independent of glycolysis yet bolstered by apoptotic cell fatty acids and mitochondrial β-oxidation, the electron transport chain, and heightened coenzyme NAD+. Loss of IL-10 due to mitochondrial complex III defects was remarkably rescued by adding NAD+ precursors. This activated a SIRTUIN1 signaling cascade, largely independent of ATP, that culminated in activation of IL-10 transcription factor PBX1. Il-10 activation by the respiratory chain was also important in vivo, as efferocyte mitochondrial dysfunction led to cardiac rupture after myocardial injury. These findings highlight a new paradigm whereby macrophages leverage efferocytic metabolites and electron transport for anti-inflammatory reprogramming that culminates in organ repair.
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“Efferocytosis leads to IL-10 induction in macrophages through signaling pathways activated by apoptotic cell cargo, including fatty acids and tryptophan (30, 40).”
From Impaired TIM4-mediated efferocytosis by liver macrophages contributes to fibrosis in metabolic dysfunction–associated steatohepatitis (2025) · cites this paper as [40]
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“Among the proresolving molecules known to be induced by efferocytosis is interleukin-10 (IL-10) (30, 40)”
From Impaired TIM4-mediated efferocytosis by liver macrophages contributes to fibrosis in metabolic dysfunction–associated steatohepatitis (2025) · cites this paper as [40]
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Metadata
- Authors
- Zhang, S., Weinberg, S., DeBerge, M., Gainullina, A., Schipma, M., Kinchen, J. M., Ben-Sahra, I., Gius, D. R., Yvan-Charvet, L., Chandel, N. S., Schumacker, P. T., & Thorp, E. B.
- Affiliations
- Northwestern University (US)
- ITMO University (RU)
- Metabolon (United States) (US)
- Corresponding author
- Thorp, Edward B.
- ORCID
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2019-02
- Volume
- 29
- Issue
- 2
- Pages
- 443-456.e5
- ISSN
- 1550-4131 (ISSN-L)
- PMC
- PMC6471613
- OpenAlex
- W2907223756
- Cited by
- 485
- References
- 65
- Citations by year
- 2026: 82 · 2025: 90 · 2024: 84 · 2023: 71 · 2022: 45 · 2021: 62 · 2020: 31 · 2019: 20
- FWCI
- 12.06
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NHLBI (F32HL127958, HL122309, HL139812)
- Chicago Biomedical Consortium
- Sidney Bess Memorial Fund (2R01CA152601-A1, 1R01CA152799-01A1, 1R01CA168292-01A1, 1R01CA214025-01)
- Avon Foundation
- Lynn Sage Cancer Research Foundation
- Chicago Community Trust
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Health Sciences › Medicine › Geriatrics and Gerontology › Sirtuins and Resveratrol in Medicine
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Keywords
- efferocytosis, macrophage polarization, IL-10, mitochondrial beta-oxidation, electron transport chain, NAD+, SIRT1, PBX1, mitochondrial complex III, wound healing, myocardial injury, cardiac rupture, anti-inflammatory macrophages, tissue repair
- MeSH terms
- Animals, Electron Transport, Fatty Acids, Humans, Inflammation, Macrophages, Mice, Inbred C57BL, Mitochondria, NAD, Oxidation-Reduction, Wound Healing, Interleukin-10, Jurkat Cells, Mice, Cytophagocytosis
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