ERV1/ChemR23 Signaling Protects Against Atherosclerosis by Modifying Oxidized Low-Density Lipoprotein Uptake and Phagocytosis in Macrophages
Open accessAbstract
Background: In addition to enhanced proinflammatory signaling, impaired resolution of vascular inflammation plays a key role in atherosclerosis. Proresolving lipid mediators formed through the 12/15 lipoxygenase pathways exert protective effects against murine atherosclerosis. n-3 Polyunsaturated fatty acids, including eicosapentaenoic acid (EPA), serve as the substrate for the formation of lipid mediators, which transduce potent anti-inflammatory and proresolving actions through their cognate G-protein–coupled receptors. The aim of this study was to identify signaling pathways associated with EPA supplementation and lipid mediator formation that mediate atherosclerotic disease progression. Methods: Lipidomic plasma analysis were performed after EPA supplementation in Apoe −/− mice. Erv1/Chemr23 −/− xApoe −/− mice were generated for the evaluation of atherosclerosis, phagocytosis, and oxidized low-density lipoprotein uptake. Histological and mRNA analyses were done on human atherosclerotic lesions. Results: Here, we show that EPA supplementation significantly attenuated atherosclerotic lesion growth induced by Western diet in Apoe −/− mice and was associated with local cardiovascular n-3 enrichment and altered lipoprotein metabolism. Our systematic plasma lipidomic analysis identified the resolvin E1 precursor 18-monohydroxy EPA as a central molecule formed during EPA supplementation. Targeted deletion of the resolvin E1 receptor Erv1/Chemr23 in 2 independent hyperlipidemic murine models was associated with proatherogenic signaling in macrophages, increased oxidized low-density lipoprotein uptake, reduced phagocytosis, and increased atherosclerotic plaque size and necrotic core formation. We also demonstrate that in macrophages the resolvin E1–mediated effects in oxidized low-density lipoprotein uptake and phagocytosis were dependent on Erv1/Chemr23. When analyzing human atherosclerotic specimens, we identified ERV1/ChemR23 expression in a population of macrophages located in the proximity of the necrotic core and demonstrated augmented ERV1/ChemR23 mRNA levels in plaques derived from statin users. Conclusions: This study identifies 18-monohydroxy EPA as a major plasma marker after EPA supplementation and demonstrates that the ERV1/ChemR23 receptor for its downstream mediator resolvin E1 transduces protective effects in atherosclerosis. ERV1/ChemR23 signaling may represent a previously unrecognized therapeutic pathway to reduce atherosclerotic cardiovascular disease.
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ALX/FPR2 and ChemR23 are expressed in human aortic, coronary, and carotid atherosclerotic lesions, indicating that their pro-resolving ligands act locally within the vascular wall.
“These receptors are expressed in human aortic, coronary and carotid atherosclerotic lesions104–106, indicating that their pro-resolving ligands exert local effects within the vascular wall (TABLE 1).”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [105]
Transcriptomic profiling of human atherosclerotic lesions revealed that CMKLR1 expression was positively associated with phagocytosis markers and negatively associated with VLDLR and SORT1 expression.
“transcriptomic profiling of human atherosclerotic lesions revealing that the expression levels of CMKLR1, which encodes ChemR23, were positively associated with markers of phagocytosis (which is consistent with pro-resolving signalling) and negatively associated with VLDLR and SORT1 expression levels105.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [105]
Murine macrophages derived from ChemR23-deficient mice have increased production of pro-inflammatory cytokines and lack RvE1-induced effects on phagocytosis compared with wild-type macrophages.
“murine macrophages derived from ChemR23-deficient mice have increased production of pro-inflammatory cytokines105,117 and a lack of RvE1-induced effects on phagocytosis compared with wild-type macrophages105.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [105]
ChemR23 deficiency in Apoe-knockout mice increases atherosclerotic lesion size and macrophage content.
“ChemR23 deficiency in Apoe-knockout mice increases atherosclerotic lesion size and macrophage content105.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [105]
Chimeric animals receiving ChemR23-deficient bone marrow transplantation show increased atherosclerotic lesion size, macrophage content, and necrotic core size.
“Similar findings along with an increased necrotic core size were also observed in chimeric animals receiving ChemR23-deficient bone marrow transplantation105.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [105]
Macrophages from ChemR23-deficient mice show a prolonged and continuous increase in oxLDL uptake in vitro, and atherosclerotic aortas of ChemR23-deficient mice show increased expression of genes related to lipid metabolism and lipoprotein uptake compared with wild-type.
“macrophages from ChemR23-deficient mice show a prolonged and continuous increase in oxLDL uptake in vitro, and when compared with aortas of wild-type mice, the atherosclerotic aortas of the ChemR23-deficient mice showed increased expression of genes related to lipid metabolism and lipoprotein uptake105.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [105]
ChemR23 localizes to a subset of lesional macrophages near the necrotic core, pointing to a specific role for RvE1-ChemR23 signalling in macrophages to limit necrotic core formation.
“These findings, together with observations that ChemR23 localizes to a subset of lesional macrophages near the necrotic core105, point to a specific role for RvE1-ChemR23 signalling in macrophages to limit necrotic core formation.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [105]
18-HEPE was identified as a major metabolite after EPA supplementation to hyperlipidaemic mice, suggesting that SPM levels can be restored by increasing substrate availability.
“the RvE1 precursor 18-hydroxyeicosa-pentaenoic acid (18-HEPE) was identified as a major metabolite after EPA supplementation to hyperlipidae-mic mice105, suggesting that SPM levels can be restored by increasing substrate availability.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [105]
RvE1 directly decreases the uptake of oxLDL by macrophages in vitro.
“RvE1 directly decreases the uptake of oxLDL by macrophages in vitro105.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [105]
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- Authors
- Laguna-Fernandez, A., Checa, A., Carracedo, M., Artiach, G., Petri, M. H., Baumgartner, R., Forteza, M. J., Jiang, X., Andonova, T., Walker, M. E., Dalli, J., Arnardottir, H., Gisterå, A., Thul, S., Wheelock, C. E., Paulsson-Berne, G., Ketelhuth, D. F. J., Hansson, G. K., & Bäck, M.
- Affiliations
- Experimental Cardiovascular Research, Department of Medicine (A.L.-F., M.C., G.A., M.H.P., R.B., M.J.F., X.J., T.A.., H.A., A.G., S.T., G.P.-B., D.F.J.K., G.K.H., M.B.), Karolinska Institutet, Stockholm, Sweden
- Karolinska Institutet (SE)
- Queen Mary University of London (GB)
- Corresponding author
- Bäck, Magnus
- ORCID
- Venue
- Circulation
- Published
- 2018-10-16
- Volume
- 138
- Issue
- 16
- Pages
- 1693-1705
- ISSN
- 0009-7322 (ISSN-L)
- 1524-4539
- PMC
- PMC6200387
- OpenAlex
- W2896260097
- Cited by
- 141
- References
- 36
- Citations by year
- 2026: 12 · 2025: 11 · 2024: 13 · 2023: 11 · 2022: 24 · 2021: 20 · 2020: 18 · 2019: 21 · 2018: 11
- FWCI
- 14.48
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-nd
- Locations
- Circulation (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Queen Mary Research Online (Queen Mary University of London) (submittedVersion, cc-by)
- Funders
- Wellcome Trust (107613/Z/15/Z)
- Barts Charity (MGU0343)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
- Keywords
- atherosclerosis, resolvin E1, macrophage phagocytosis, omega-3 fatty acids, specialized pro-resolving mediators, G protein-coupled receptor signaling, necrotic core, atherosclerotic plaque, plasma lipidomics
- MeSH terms
- Mice, Knockout, ApoE, Animals, Aorta, Aortic Diseases, Cytochrome Reductases, Disease Models, Animal, Humans, Lipoproteins, LDL, Macrophages, Male, Mice, Inbred C57BL, Necrosis, Phagocytosis, Phenotype, Receptors, LDL, Eicosapentaenoic Acid, Signal Transduction, Receptors, Chemokine, Genetic Predisposition to Disease, Receptors, G-Protein-Coupled, Atherosclerosis, Oxidoreductases Acting on Sulfur Group Donors, Plaque, Atherosclerotic, Diet, Western
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