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MicroRNA-33-dependent regulation of macrophage metabolism directs immune cell polarization in atherosclerosis
Open accessAbstract
Cellular metabolism is increasingly recognized as a controller of immune cell fate and function. MicroRNA-33 (miR-33) regulates cellular lipid metabolism and represses genes involved in cholesterol efflux, HDL biogenesis, and fatty acid oxidation. Here, we determined that miR-33-mediated disruption of the balance of aerobic glycolysis and mitochondrial oxidative phosphorylation instructs macrophage inflammatory polarization and shapes innate and adaptive immune responses. Macrophage-specific Mir33 deletion increased oxidative respiration, enhanced spare respiratory capacity, and induced an M2 macrophage polarization-associated gene profile. Furthermore, miR-33-mediated M2 polarization required miR-33 targeting of the energy sensor AMP-activated protein kinase (AMPK), but not cholesterol efflux. Notably, miR-33 inhibition increased macrophage expression of the retinoic acid-producing enzyme aldehyde dehydrogenase family 1, subfamily A2 (ALDH1A2) and retinal dehydrogenase activity both in vitro and in a mouse model. Consistent with the ability of retinoic acid to foster inducible Tregs, miR-33-depleted macrophages had an enhanced capacity to induce forkhead box P3 (FOXP3) expression in naive CD4(+) T cells. Finally, treatment of hypercholesterolemic mice with miR-33 inhibitors for 8 weeks resulted in accumulation of inflammation-suppressing M2 macrophages and FOXP3(+) Tregs in plaques and reduced atherosclerosis progression. Collectively, these results reveal that miR-33 regulates macrophage inflammation and demonstrate that miR-33 antagonism is atheroprotective, in part, by reducing plaque inflammation by promoting M2 macrophage polarization and Treg induction.
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“Inhibition of miR-33a or miR-33a deletion in macrophages has been shown to affect myeloid cell differentiation 25) , induce M2 macrophage polarization with mitochondrial respiratory and metabolic changes 26 , 27) , and enhance autophagy 28 , 29) .”
From Critical Role of microRNA-33a/b in Cardiovascular and Metabolic Disease: Molecular Mechanisms and Therapeutic Perspectives (2026) · cites this paper as [26]
In the citing paper
“several studies have found that antagonism of miR-33 can reduce atherosclerotic plaque burden (Karunakaran et al., 2015; Ouimet et al., 2015; Rayner et al., 2011b; Rotllan et al., 2013).”
From Genetic dissection of the impact of miR-33a and miR-33b during the progression of atherosclerosis (2017) · cites this paper as Ouimet et al., 2015
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“Expression of miR-33 is also overexpressed in M1, thus promoting pro-inflammatory functions [132].”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [132]
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Metadata
- Authors
- Ouimet, M., Ediriweera, H. N., Gundra, U. M., Sheedy, F. J., Ramkhelawon, B., Hutchison, S. B., Rinehold, K., van Solingen, C., Fullerton, M. D., Cecchini, K., Rayner, K. J., Steinberg, G. R., Zamore, P. D., Fisher, E. A., Loke, P., & Moore, K. J.
- Affiliations
- New York University (US)
- University of Ottawa (CA)
- Howard Hughes Medical Institute (US)
- McMaster University (CA)
- NYU Langone Health (US)
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2015-10-26
- Volume
- 125
- Issue
- 12
- Pages
- 4334-4348
- ISSN
- 0021-9738 (ISSN-L)
- 1558-8238
- PMC
- PMC4665799
- OpenAlex
- W2123366371
- Cited by
- 394
- References
- 67
- Citations by year
- 2026: 19 · 2025: 21 · 2024: 27 · 2023: 37 · 2022: 24 · 2021: 45 · 2020: 45 · 2019: 46 · 2018: 35 · 2017: 47 · 2016: 33 · 2015: 1
- FWCI
- 19.07
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Heart Association (14POST20180018, 15POST25090199)
- NYU Langone Medical Center (P30CA016087)
- Canada Research Chairs
- National Institutes of Health (UL1TR000038, TR000038)
- Canadian Institutes of Health Research
- National Heart, Lung, and Blood Institute (R01HL084312, HL-084312, HL098055, P01HL098055, R01HL119047, R01HL108182, T32HL098129)
- National Cancer Institute (P30CA016087)
- National Institute of Allergy and Infectious Diseases (R21AI094166, R01AI093811, R01AI094166, T32AI007180)
- National Center for Advancing Translational Sciences
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Cholesterol and Lipid Metabolism
- Keywords
- microRNA-33, macrophage polarization, M2 macrophages, atherosclerosis, aerobic glycolysis, mitochondrial oxidative phosphorylation, AMPK, ALDH1A2, retinoic acid, regulatory T cells, Foxp3, plaque inflammation, hypercholesterolemia, atheroprotection, lipid metabolism
- MeSH terms
- Aldehyde Dehydrogenase 1 Family, Aldehyde Dehydrogenase, Animals, Gene Expression Regulation, Glycolysis, Oxygen Consumption, Macrophages, Peritoneal, Mice, Knockout, MicroRNAs, Atherosclerosis, T-Lymphocytes, Regulatory, Retinal Dehydrogenase, Mice, Forkhead Transcription Factors, AMP-Activated Protein Kinases, Plaque, Atherosclerotic
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