Tissue-resident macrophages are locally programmed for silent clearance of apoptotic cells
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Abstract
Although apoptotic cells (ACs) contain nucleic acids that can be recognized by Toll-like receptors (TLRs), engulfment of ACs does not initiate inflammation in healthy organisms. Here we identified macrophage populations that continually engulf ACs in distinct tissues and found that these macrophages share characteristics compatible with immunologically silent clearance of ACs; such characteristics include high expression of AC recognition receptors, low expression of TLR9, and reduced TLR responsiveness to nucleic acids. Removal of the macrophages from tissues resulted in loss of many of these characteristics and the ability to generate inflammatory responses to AC-derived nucleic acids, suggesting that cues from the tissue microenvironment program macrophages for silent AC clearance. The transcription factors KLF2 and KLF4 control the expression of many genes within this AC clearance program. The coordinated expression of AC receptors with genes that limit responses to nucleic acids might ensure maintenance of homeostasis and thus represent a central feature of tissue macrophages.
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Macrophages take up apoptotic cells in particular tissues (efferocytosis), preventing apoptotic cells from becoming necrotic or pro-inflammatory.
“Specific populations of innate immune effector macrophages take up apoptotic cells in particular tissues, known as efferocytosis, which prevents apoptotic cells from being necrotic or pro-inflammatory [138].”
From Immune Clearance of Senescent Cells to Combat Ageing and Chronic Diseases (2020) · cites this paper as [138]
Macrophage transcription factors KLF2 and KLF4 are crucial controllers inducing gene expression necessary to silently eradicate apoptotic cells.
“Macrophage transcription factors Kruppel-like factors 2 (KLF2) and 4 (KLF4) are crucial controllers inducing gene expression necessary to silently eradicate apoptotic cells [138].”
From Immune Clearance of Senescent Cells to Combat Ageing and Chronic Diseases (2020) · cites this paper as [138]
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Song, P., An, J., & Zou, M.-H. (2020) · Cells · doi:10.3390/cells9030671 · Cited by 198 · see citing works
“Specific populations of innate immune effector macrophages take up apoptotic cells in particular tissues, known as efferocytosis, which prevents apoptotic cells from being necrotic or proinflammatory [138].”
Background<i>Cx3cr1-</i> deficient microglia exhibit a premature aging transcriptome
Gyoneva, S., Hosur, R., Gosselin, D., Zhang, B., Ouyang, Z., Cotleur, A. C., Peterson, M., Allaire, N., Challa, R., Cullen, P., et al. (2019) · Life Science Alliance · doi:10.26508/lsa.201900453 · Cited by 103 · see citing works
“Only genes with FDR < 0.05, fold change > 30%, and average expression > 4 TPM were included in the enrichment analysis. augmented up-regulation of Klf2 , among other genes, could mediate durable functional responses by microglia (Das et al, 2006; de Bruin et al, 2016; Roberts et al, 2017).”
Influential
- Authors
- Roberts, A. W., Lee, B. L., Deguine, J., John, S., Shlomchik, M. J., & Barton, G. M.
- Affiliations
- University of California, Berkeley (US)
- Yale University (US)
- University of Pittsburgh (US)
- Corresponding author
- Barton, Gregory M.
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2017-11
- Volume
- 47
- Issue
- 5
- Pages
- 913-927.e6
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC5728676
- OpenAlex
- W2672444148
- Cited by
- 261
- References
- 77
- Citations by year
- 2026: 14 · 2025: 23 · 2024: 36 · 2023: 29 · 2022: 41 · 2021: 43 · 2020: 33 · 2019: 29 · 2018: 12 · 2017: 1
- FWCI
- 9.28
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- NIH (AI072429, AI105184, AI063302, AI118841, AR050256)
- Lupus Research Institute (Distinguished Innovator Award)
- Long-Term Human Frontier Science Program Fellowship (LT-000081-2013L)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- efferocytosis, tissue-resident macrophages, Toll-like receptors, TLR9, tissue microenvironment, KLF2, KLF4, inflammation, macrophage homeostasis
- MeSH terms
- Kruppel-Like Factor 4, Animals, Female, Macrophage Activation, Macrophages, Male, Mice, Inbred C57BL, Apoptosis, Toll-Like Receptor 7, Toll-Like Receptor 9, Mice, Kruppel-Like Transcription Factors
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