Cited by 363Phagocytosis and Immune RegulationCell death mechanisms and regulationAtherosclerosis and Cardiovascular Diseases

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Efferocytosis induces macrophage proliferation to help resolve tissue injury

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Gerlach, Brennan D., Ampomah, Patrick B., Yurdagul, Arif, Liu, Chuang, Lauring, Max C., Wang, Xiaobo, Kasikara, Canan, Kong, Na, Shi, Jinjun, Tao, Wei, Tabas, Ira·2021·Cell Metabolism

DOI 10.1016/j.cmet.2021.10.015PMC PMC8665147

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Abstract

Apoptotic cell clearance by macrophages (efferocytosis) promotes resolution signaling pathways, which can be triggered by molecules derived from the phagolysosomal degradation of apoptotic cells. We show here that nucleotides derived from the hydrolysis of apoptotic cell DNA by phagolysosomal DNase2a activate a DNA-PKcs-mTORC2/Rictor pathway that increases Myc to promote non-inflammatory macrophage proliferation. Efferocytosis-induced proliferation expands the pool of resolving macrophages in vitro and in mice, including zymosan-induced peritonitis, dexamethasone-induced thymocyte apoptosis, and atherosclerosis regression. In the dexamethasone-thymus model, hematopoietic Rictor deletion blocked efferocytosing macrophage proliferation, apoptotic cell clearance, and tissue resolution. In atherosclerosis regression, silencing macrophage Rictor or DNase2a blocked efferocyte proliferation, apoptotic cell clearance, and plaque stabilization. In view of previous work showing that other types of apoptotic cell cargo can promote resolution in individual efferocytosing macrophages, the findings here suggest that signaling-triggered apoptotic cell-derived nucleotides can amplify this benefit by increasing the number of these macrophages.

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Authors: Gerlach, B. D., Ampomah, P. B., Yurdagul, A., Liu, C., Lauring, M. C., Wang, X., Kasikara, C., Kong, N., Shi, J., Tao, W., & Tabas, I.
Affiliations: Columbia University Irving Medical Center (US)
Brigham and Women's Hospital (US)
Corresponding author: Tabas, Ira
ORCID: Gerlach, Brennan D.
Ampomah, Patrick B.
Yurdagul, Arif
Wang, Xiaobo
Kong, Na
Shi, Jinjun
Tao, Wei
Tabas, Ira
Venue: Cell Metabolism
Publisher: Elsevier BV
Published: 2021-12
Volume: 33
Issue: 12
Pages: 2445-2463.e8
ISSN: 1550-4131 (ISSN-L)
DOI: 10.1016/j.cmet.2021.10.015
PMC: PMC8665147
OpenAlex: W3212263362
Cited by: 360
References: 71
Citations by year: 2026: 79 · 2025: 105 · 2024: 91 · 2023: 53 · 2022: 31 · 2021: 1
FWCI: 16.70
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, 371 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cell Metabolism (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (R35 HL145228, K99 HL145131, P20 GM121307, P30CA013696, R01 HL087123, R01 HL127464, S10OD020056, S10RR025686, S10RR027050, T32 5T32HL007343-42)
American Heart Association (20POST35210962)
Harvard Medical School (122829)
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 › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
Keywords: efferocytosis, macrophage proliferation, DNA-PKcs, mTORC2, Rictor, c-Myc, atherosclerosis regression, plaque stabilization, peritonitis, thymocyte apoptosis, phagolysosomes
MeSH terms: Animals, Macrophages, Mice, Inbred C57BL, Phagocytosis, Apoptosis, Cell Proliferation, Mice

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Efferocytosis induces macrophage proliferation to help resolve tissue injury

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