Macrophage mitochondrial energy status regulates cholesterol efflux and is enhanced by anti-miR33 in atherosclerosis
Open accessAbstract
RATIONALE: Therapeutically targeting macrophage reverse cholesterol transport is a promising approach to treat atherosclerosis. Macrophage energy metabolism can significantly influence macrophage phenotype, but how this is controlled in foam cells is not known. Bioinformatic pathway analysis predicts that miR-33 represses a cluster of genes controlling cellular energy metabolism that may be important in macrophage cholesterol efflux. OBJECTIVE: We hypothesized that cellular energy status can influence cholesterol efflux from macrophages, and that miR-33 reduces cholesterol efflux via repression of mitochondrial energy metabolism pathways. METHODS AND RESULTS: In this study, we demonstrated that macrophage cholesterol efflux is regulated by mitochondrial ATP production, and that miR-33 controls a network of genes that synchronize mitochondrial function. Inhibition of mitochondrial ATP synthase markedly reduces macrophage cholesterol efflux capacity, and anti-miR33 required fully functional mitochondria to enhance ABCA1-mediated cholesterol efflux. Specifically, anti-miR33 derepressed the novel target genes PGC-1α, PDK4, and SLC25A25 and boosted mitochondrial respiration and production of ATP. Treatment of atherosclerotic Apoe(-/-) mice with anti-miR33 oligonucleotides reduced aortic sinus lesion area compared with controls, despite no changes in high-density lipoprotein cholesterol or other circulating lipids. Expression of miR-33a/b was markedly increased in human carotid atherosclerotic plaques compared with normal arteries, and there was a concomitant decrease in mitochondrial regulatory genes PGC-1α, SLC25A25, NRF1, and TFAM, suggesting these genes are associated with advanced atherosclerosis in humans. CONCLUSIONS: This study demonstrates that anti-miR33 therapy derepresses genes that enhance mitochondrial respiration and ATP production, which in conjunction with increased ABCA1 expression, works to promote macrophage cholesterol efflux and reduce atherosclerosis.
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Inhibition of miR-33a or miR-33a deletion in macrophages affects myeloid cell differentiation, induces M2 macrophage polarization with mitochondrial respiratory and metabolic changes, and enhances autophagy.
“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 [27]
The Results section ('Anti-miR33 treatment increases mitochondrial respiration and ATP production'; page not provided) reports increased respiration and ATP production after miR-33 inhibition in macrophages. The cited paper does not establish that this treatment induces M2 macrophage polarization. The sentence assigns myeloid differentiation and autophagy to other citations, so those claims are not judged here. (LLM, conf=0.88)
Experimental — accuracy not yet measuredSeveral studies have found that antagonism of miR-33 can reduce atherosclerotic plaque burden.
“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 Karunakaran et al., 2015
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- Authors
- Karunakaran, D., Thrush, A. B., Nguyen, M.-A., Richards, L., Geoffrion, M., Singaravelu, R., Ramphos, E., Shangari, P., Ouimet, M., Pezacki, J. P., Moore, K. J., Perisic, L., Maegdefessel, L., Hedin, U., Harper, M.-E., & Rayner, K. J.
- Affiliations
- University of Ottawa (CA)
- From the University of Ottawa Heart Institute, Ottawa, Ontario, Canada (D.K., M.-A.N., L.R., M.G., E.R., P.S., K.J.R.); Department of Biochemistry, Microbiology, and Immunology, University of Ottawa, Ottawa, Ontario, Canada (A.B.T., M.-A.N., R.S., J.P.P., M.-E.H., K.J.R.); National Research Council of Canada, Ottawa, Ontario, Canada (R.S., J.P.P.); Marc and Ruti Bell Program for Vascular Biology and Disease, The Leon H. Charney Division of Cardiology, New York University School of Medicine (M.O., K...
- ORCID
- Venue
- Circulation Research
- Published
- 2015-07-17
- Volume
- 117
- Issue
- 3
- Pages
- 266-278
- ISSN
- 0009-7330 (ISSN-L)
- 1524-4571
- PMC
- PMC4578799
- OpenAlex
- W2171031572
- Cited by
- 188
- References
- 46
- Citations by year
- 2026: 12 · 2025: 9 · 2024: 14 · 2023: 17 · 2022: 19 · 2021: 21 · 2020: 13 · 2019: 18 · 2018: 18 · 2017: 15 · 2016: 26 · 2015: 6
- FWCI
- 21.84
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Circulation Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- NPARC (submittedVersion)
- Funders
- University of Ottawa
- Hjärt-Lungfonden
- Canadian Institutes of Health Research (30365_1, OCN126572)
- National Heart, Lung, and Blood Institute (R01HL119047, R01HL108182)
- Topics
- Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Keywords
- miR-33, macrophage cholesterol efflux, atherosclerosis, mitochondrial bioenergetics, ATP synthase, ABCA1, PGC-1α, mitochondrial respiration, foam cells, ApoE-deficient mice, carotid plaque, reverse cholesterol transport
- MeSH terms
- Adenosine Triphosphate, Animals, Apolipoproteins E, Base Sequence, Calcium-Binding Proteins, Cell Line, Cholesterol, Gene Expression Regulation, Humans, Macrophages, Mice, Inbred C57BL, Mitochondria, Sequence Homology, Nucleic Acid, Transcription Factors, Genetic Therapy, Oligonucleotides, Antisense, Sequence Alignment, Protein Serine-Threonine Kinases, Macrophages, Peritoneal, Amino Acid Transport Systems, Acidic, Mitochondrial Membrane Transport Proteins, MicroRNAs, Atherosclerosis, Mice, HEK293 Cells
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