Cited by 529Phagocytosis and Immune RegulationCell death mechanisms and regulationAutophagy in Disease and Therapy

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Macrophage Metabolism of Apoptotic Cell-Derived Arginine Promotes Continual Efferocytosis and Resolution of Injury

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Yurdagul, Arif, Subramanian, Manikandan, Wang, Xiaobo, Crown, Scott B., Ilkayeva, Olga R., Darville, Lancia, Kolluru, Gopi K., Rymond, Christina C., Gerlach, Brennan D., Zheng, Ze, Kuriakose, George, Kevil, Christopher G., Koomen, John M., Cleveland, John L., Muoio, Deborah M., Tabas, Ira·2020·Cell Metabolism

DOI 10.1016/j.cmet.2020.01.001PMC PMC7173557

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Abstract

Continual efferocytic clearance of apoptotic cells (ACs) by macrophages prevents necrosis and promotes injury resolution. How continual efferocytosis is promoted is not clear. Here, we show that the process is optimized by linking the metabolism of engulfed cargo from initial efferocytic events to subsequent rounds. We found that continual efferocytosis is enhanced by the metabolism of AC-derived arginine and ornithine to putrescine by macrophage arginase 1 (Arg1) and ornithine decarboxylase (ODC). Putrescine augments HuR-mediated stabilization of the mRNA encoding the GTP-exchange factor Dbl, which activates actin-regulating Rac1 to facilitate subsequent rounds of AC internalization. Inhibition of any step along this pathway after first-AC uptake suppresses second-AC internalization, whereas putrescine addition rescues this defect. Mice lacking myeloid Arg1 or ODC have defects in efferocytosis in vivo and in atherosclerosis regression, while treatment with putrescine promotes atherosclerosis resolution. Thus, macrophage metabolism of AC-derived metabolites allows for optimal continual efferocytosis and resolution of injury.

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Authors: Yurdagul, A., Subramanian, M., Wang, X., Crown, S. B., Ilkayeva, O. R., Darville, L., Kolluru, G. K., Rymond, C. C., Gerlach, B. D., Zheng, Z., Kuriakose, G., Kevil, C. G., Koomen, J. M., Cleveland, J. L., Muoio, D. M., & Tabas, I.
Affiliations: Columbia University Irving Medical Center (US)
Institute of Genomics and Integrative Biology (IN)
Columbia University (US)
Duke University (US)
Moffitt Cancer Center (US)
Louisiana State University Health Sciences Center Shreveport (US)
Corresponding author: Yurdagul, Arif
Tabas, Ira
ORCID: Yurdagul, Arif
Subramanian, Manikandan
Wang, Xiaobo
Crown, Scott B.
Ilkayeva, Olga R.
Darville, Lancia
Kolluru, Gopi K.
Rymond, Christina C.
Gerlach, Brennan D.
Zheng, Ze
Kevil, Christopher G.
Koomen, John M.
Cleveland, John L.
Muoio, Deborah M.
Tabas, Ira
Venue: Cell Metabolism
Publisher: Elsevier BV
Published: 2020-03
Volume: 31
Issue: 3
Pages: 518-533.e10
ISSN: 1550-4131 (ISSN-L)
DOI: 10.1016/j.cmet.2020.01.001
PMC: PMC7173557
OpenAlex: W3004079464
Cited by: 525
References: 70
Citations by year: 2026: 112 · 2025: 101 · 2024: 97 · 2023: 76 · 2022: 61 · 2021: 57 · 2020: 21
FWCI: 18.48
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, 367 d)
Locations: Cell Metabolism (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
Topics: Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Keywords: efferocytosis, macrophage metabolism, arginine metabolism, ornithine, putrescine, arginase-1, ornithine decarboxylase, Rac1, actin cytoskeleton, atherosclerosis regression
MeSH terms: ELAV-Like Protein 1, Animals, Arginase, Arginine, Humans, Macrophages, Male, Mice, Inbred C57BL, Ornithine Decarboxylase, Phagocytosis, Putrescine, RNA, Messenger, Apoptosis, Gene Deletion, Jurkat Cells, Guanine Nucleotide Exchange Factors, rac1 GTP-Binding Protein, RNA Stability, Myeloid Cells

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Macrophage Metabolism of Apoptotic Cell-Derived Arginine Promotes Continual Efferocytosis and Resolution of Injury

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