Pivotal Advance: Macrophages become resistant to cholesterol-induced death after phagocytosis of apoptotic cells
Abstract
One of the most important functions of macrophages is the phagocytosis of apoptotic cells (ACs). ACs deliver large amounts membrane-derived cholesterol to phagocytes, which, if not handled properly, can be cytotoxic. In atherosclerosis, where the ACs are cholesterol-loaded, this situation is exaggerated, because the ACs deliver both endogenous membrane cholesterol and stored lipoprotein-derived cholesterol. To examine how phagocytes handle this very large amount of cholesterol, we incubated macrophage phagocytes with cholesterol-loaded ACs. Our results show that the phagocytes call into play a number of cellular responses to protect them from cholesterol-induced cytotoxicity. First, through efficient trafficking of the internalized AC-derived cholesterol to acyl-CoA:cholesterol acyltransferase (ACAT) in the endoplasmic reticulum, phagocytes efficiently esterify the cholesterol and thus prevent its toxic effects. However, the phagocytes show no signs of cytotoxicity even when ACAT is rendered dysfunctional, as might occur in advanced atherosclerotic lesions. Under these conditions, the phagocytes remain viable through massive efflux of AC-derived cholesterol. Remarkably, these phagocytes still show a survival response even when high cholesterol levels are maintained in the post-phagocytosis period by subsequent incubation with atherogenic lipoproteins, as also may occur in atheromata. In this case, death in phagocytes is prevented by activation of survival pathways involving PI-3 kinase/Akt and NF-κB. Thus, macrophages that have ingested ACs successfully employ three survival mechanisms—cholesterol esterification, massive cholesterol efflux, and cell-survival signaling. These findings have implications for macrophage physiology in both AC clearance and atherosclerotic plaque progression.
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Efferocytosis enhances cholesterol efflux via the ATP-binding cassette transporters ABCA-1 and ABCG1 upon apoptosis (but not necrotic cell uptake), which protects efferocytes from cholesterol-induced ER stress and apoptosis upon massive uptake of dead cells.
“Efferocytosis enhances cholesterol efflux via the ATP-binding cassette transporters A1 and G1 (ABCA-1, ABCG1) upon apoptosis (but not necrotic cell uptake), which protects efferocytes from cholesterol-induced ER stress and apoptosis upon massive uptake of dead cells (152, 153).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [153]
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- Authors
- Cui, D., Thorp, E., Li, Y., Wang, N., Yvan-Charvet, L., Tall, A. R., & Tabas, I.
- Affiliations
- Columbia University (US)
- Department of Medicine, Columbia University , New York, New York , USA
- Corresponding author
- Tabas, Ira
- Venue
- Journal of Leukocyte Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2007-06-18
- Volume
- 82
- Issue
- 5
- Pages
- 1040-1050
- ISSN
- 0741-5400 (ISSN-L)
- 1938-3673
- OpenAlex
- W2148735069
- Cited by
- 73
- References
- 57
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 3 · 2023: 3 · 2022: 5 · 2021: 3 · 2020: 3 · 2019: 3 · 2018: 2 · 2017: 6 · 2016: 2 · 2015: 4 · 2014: 1 · 2013: 2 · 2012: 5
- FWCI
- 7.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Leukocyte Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (HL-54591, HL-75662)
- American Heart Association Scientist Development
- NIH Postdoctoral Atherosclerosis Training
- Topics
- Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Keywords
- macrophages, phagocytosis of apoptotic cells, atherosclerosis, cholesterol esterification, acyl-CoA:cholesterol acyltransferase, cholesterol efflux, NF-κB, cell survival signaling, atherogenic lipoproteins, foam cells
- MeSH terms
- Acetyl-CoA C-Acetyltransferase, Animals, Cell Communication, Cells, Cultured, Cholesterol, Endoplasmic Reticulum, Esterification, Female, Mice, Inbred C57BL, Phagocytes, Phagocytosis, Ultraviolet Rays, Blotting, Western, NF-kappa B, Apoptosis, Macrophages, Peritoneal, Mice, Knockout, Phosphatidylinositol 3-Kinases, Proto-Oncogene Proteins c-akt, Mice
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