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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 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]
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“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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Metadata
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › 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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