Cited by 395Atherosclerosis and Cardiovascular DiseasesMicroRNA in disease regulationCholesterol and Lipid Metabolism

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MicroRNA-33-dependent regulation of macrophage metabolism directs immune cell polarization in atherosclerosis

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Ouimet, Mireille, Ediriweera, Hasini N., Gundra, U. Mahesh, Sheedy, Frederick J., Ramkhelawon, Bhama, Hutchison, Susan B., Rinehold, Kaitlyn, van Solingen, Coen, Fullerton, Morgan D., Cecchini, Katharine, Rayner, Katey J., Steinberg, Gregory R., Zamore, Phillip D., Fisher, Edward A., Loke, P’ng, Moore, Kathryn J.·2015·Journal of Clinical Investigation

DOI 10.1172/jci81676PMC PMC4665799

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Abstract

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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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: Ouimet, Mireille
Sheedy, Frederick J.
Ramkhelawon, Bhama
Fullerton, Morgan D.
Cecchini, Katharine
Rayner, Katey J.
Steinberg, Gregory R.
Zamore, Phillip D.
Fisher, Edward A.
Loke, P’ng
Moore, Kathryn J.
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2015-10-26
Volume: 125
Issue: 12
Pages: 4334-4348
ISSN: 0021-9738 (ISSN-L)
1558-8238
DOI: 10.1172/jci81676
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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MicroRNA-33-dependent regulation of macrophage metabolism directs immune cell polarization in atherosclerosis

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