Cited by 486Phagocytosis and Immune RegulationSirtuins and Resveratrol in MedicineImmune cells in cancer

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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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Zhang, Shuang, Weinberg, Samuel, DeBerge, Matthew, Gainullina, Anastasiia, Schipma, Matthew, Kinchen, Jason M., Ben-Sahra, Issam, Gius, David R., Yvan-Charvet, Laurent, Chandel, Navdeep S., Schumacker, Paul T., Thorp, Edward B.·2019·Cell Metabolism

DOI 10.1016/j.cmet.2018.12.004PMC PMC6471613

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Abstract

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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Additional file 5 of Cystathionine gamma-lyase (Cth) induces efferocytosis in macrophages via ERK1/2 to modulate intestinal barrier repair
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Additional file 9 of Cystathionine gamma-lyase (Cth) induces efferocytosis in macrophages via ERK1/2 to modulate intestinal barrier repair
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Additional file 4 of Cystathionine gamma-lyase (Cth) induces efferocytosis in macrophages via ERK1/2 to modulate intestinal barrier repair
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Additional file 7 of Cystathionine gamma-lyase (Cth) induces efferocytosis in macrophages via ERK1/2 to modulate intestinal barrier repair
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Additional file 11 of Cystathionine gamma-lyase (Cth) induces efferocytosis in macrophages via ERK1/2 to modulate intestinal barrier repair
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Additional file 8 of Cystathionine gamma-lyase (Cth) induces efferocytosis in macrophages via ERK1/2 to modulate intestinal barrier repair
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Additional file 3 of Cystathionine gamma-lyase (Cth) induces efferocytosis in macrophages via ERK1/2 to modulate intestinal barrier repair
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Additional file 6 of Cystathionine gamma-lyase (Cth) induces efferocytosis in macrophages via ERK1/2 to modulate intestinal barrier repair
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Additional file 3 of Low-dose adropin stimulates inflammasome activation of macrophage via mitochondrial ROS involved in colorectal cancer progression
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Additional file 10 of Cystathionine gamma-lyase (Cth) induces efferocytosis in macrophages via ERK1/2 to modulate intestinal barrier repair
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Self-citation
Novel Mechanometabolic Signaling Cascade Linking Efferocytosis to Inflammation Resolution
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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: Zhang, Shuang
Weinberg, Samuel
DeBerge, Matthew
Gainullina, Anastasiia
Schipma, Matthew
Kinchen, Jason M.
Gius, David R.
Chandel, Navdeep S.
Schumacker, Paul T.
Thorp, Edward B.
Venue: Cell Metabolism
Publisher: Elsevier BV
Published: 2019-02
Volume: 29
Issue: 2
Pages: 443-456.e5
ISSN: 1550-4131 (ISSN-L)
DOI: 10.1016/j.cmet.2018.12.004
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 369 d)
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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Efferocytosis Fuels Requirements of Fatty Acid Oxidation and the Electron Transport Chain to Polarize Macrophages for Tissue Repair

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