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Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis
Open accessAbstract
Plasma HDL levels have a protective role in atherosclerosis, yet clinical therapies to raise HDL levels have remained elusive. Recent advances in the understanding of lipid metabolism have revealed that miR-33, an intronic microRNA located within the SREBF2 gene, suppresses expression of the cholesterol transporter ABC transporter A1 (ABCA1) and lowers HDL levels. Conversely, mechanisms that inhibit miR-33 increase ABCA1 and circulating HDL levels, suggesting that antagonism of miR-33 may be atheroprotective. As the regression of atherosclerosis is clinically desirable, we assessed the impact of miR-33 inhibition in mice deficient for the LDL receptor (Ldlr-/- mice), with established atherosclerotic plaques. Mice treated with anti-miR33 for 4 weeks showed an increase in circulating HDL levels and enhanced reverse cholesterol transport to the plasma, liver, and feces. Consistent with this, anti-miR33-treated mice showed reductions in plaque size and lipid content, increased markers of plaque stability, and decreased inflammatory gene expression. Notably, in addition to raising ABCA1 levels in the liver, anti-miR33 oligonucleotides directly targeted the plaque macrophages, in which they enhanced ABCA1 expression and cholesterol removal. These studies establish that raising HDL levels by anti-miR33 oligonucleotide treatment promotes reverse cholesterol transport and atherosclerosis regression and suggest that it may be a promising strategy to treat atherosclerotic vascular disease.
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“In any case, the effect of miR-33 deletion in macrophages is not as simple as a shift from the M1 to the M2 phenotype, as described in a previous report.19”
From MicroRNA‐33 Deficiency Reduces the Progression of Atherosclerotic Plaque in ApoE −/− Mice (2012) · cites this paper as [19]
In the citing paper
“Furthermore, macrophages within the atherosclerotic lesions of these mice exhibit an anti-inflammatory phenotype characterized by enhanced cholesterol efflux, which leads to a reduction in foam cell formation.”
From Critical Role of microRNA-33a/b in Cardiovascular and Metabolic Disease: Molecular Mechanisms and Therapeutic Perspectives (2026) · cites this paper as [21]
In the citing paper
“Inhibition or genetic ablation of miR-33a has been shown to either promote the regression of atherosclerosis or prevent its formation in mouse models, such as LDL receptor-deficient or apoprotein E (ApoE)-deficient mice, conferring resistance to the disease 21 - 23) .”
From Critical Role of microRNA-33a/b in Cardiovascular and Metabolic Disease: Molecular Mechanisms and Therapeutic Perspectives (2026) · cites this paper as [21]
In the citing paper
“Moreover, the effect of miR-33 deletion in macrophages is not as simple as the shift from the M1 to M2 phenotype reported previously.19”
From MicroRNA‐33 Deficiency Reduces the Progression of Atherosclerotic Plaque in ApoE −/− Mice (2012) · cites this paper as [19]
In the citing paper
“Moreover, antisense inhibition of miR-33 resulted in a regression of the atherosclerotic plaque volume in LDL-receptor-deficient mice.19”
From MicroRNA‐33 Deficiency Reduces the Progression of Atherosclerotic Plaque in ApoE −/− Mice (2012) · cites this paper as [19]
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MicroRNAs and Energy Metabolism in Cancer Cells
Sun, L., He, X., Cao, Y., Gao, P., & Zhang, H. (2014) · Springer eBooks · doi:10.1007/978-3-319-03725-7_4 · Cited by 3
MicroRNAs in Lipid Metabolism and Atherosclerosis
Meiliana, A., & Wijaya, A. (2014) · The Indonesian Biomedical Journal · doi:10.18585/inabj.v6i1.39 · Cited by 3
Recent insights into the pathophysiology and implications for surgery in atherosclerosis
Liu, L., Wang, Z., Ma, L., & Wu, S. (2025) · Journal of Cardiothoracic Surgery · doi:10.1186/s13019-025-03655-9 · Cited by 4
“Recent preclinical studies have demonstrated that miRNA-based therapies, particularly those targeting miR-33 and miR-122, can effectively reduce lipid accumulation while mitigating inflammatory responses in atherosclerotic lesions [60].”
Innovative molecular intervention and precision therapy for atherosclerosis
Wang, Z., Peng, W., Huang, L., Zhang, Y., Yang, J., Chen, X., Liu, X., Li, F., & Zhang, Q. (2025) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2025.1652933 · Cited by 4
Huang, K., Pokhrel, A., Echesabal-Chen, J., Scott, J., Bruce, T., Jo, H., & Stamatikos, A. D. (2025) · Medicina · doi:10.3390/medicina61020329 · Cited by 5
“While earlier studies showed promise that inhibiting miR-33a-(5p) systemically may have atheroprotective benefits [40,46,84], other data suggests that the systemic inhibition of this microRNA may actually exhibit pro-atherogenic properties [85,86].”
Roles of extracellular vesicles derived from immune cells in atherosclerosis
Qiao, K., Cui, X., Gao, J., Yu, F., Liu, H., Dai, Y., Liu, J., Yang, Y., Xian, X., Hu, J.-M., et al. (2023) · Extracellular Vesicle · doi:10.1016/j.vesic.2023.100028 · Cited by 4
Lee, M.-S., & Kim, Y. (2023) · Preventive Nutrition and Food Science · doi:10.3746/pnf.2023.28.3.271 · Cited by 5
“Particularly, miR-33 suppresses ABCA1 expression and reduces HDL-C levels (Rayner et al., 2011). miR-34a directly binds to the 3’ untranslated region of ABCA1 and ABCG1, and miR-34a inhibition promotes macrophage cholesterol efflux by inducing ABCA1 and ABCG1 expression (Xu et al., 2020).”
BackgroundInvestigational therapies for hypercholesterolemia
TOMKIN, G. H., & Owens, D. (2017) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2017.1315407 · Cited by 4
“Evacetrapib, yet another CETP inhibitor, was shown in healthy adults to elevate HDL-C, lower LDL-C and to have no effect on blood pressure [115].”
BackgroundRNA Binding Proteins and Non-coding RNA’s in Cardiovascular Diseases
Bansal, P., & Arora, M. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-981-15-1671-9_5 · Cited by 5
Cardiovascular Disease and Transgenerational Epigenetic Effects
Zullo, A., Casamassimi, A., Mancini, F. P., & Claudio Napoli, A. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405944-3.00023-4 · Cited by 4
MicroRNA-33 inhibition ameliorates muscular dystrophy by enhancing skeletal muscle regeneration
Sowa, N., Horie, T., Ide, Y., Baba, O., Kora, K., Yoshida, T., Nakamura, Y., Matsumura, S., Matsushita, K., Imanaka, M., et al. (2025) · EMBO Molecular Medicine · doi:10.1038/s44321-025-00273-9 · Cited by 4
“…al, 2010; Rayner et al, 2010). miR-33a-knockout (miR-33a-KO) mice or mice in which miR-33a is inhibited show reduced atherosclerosis with an improved serum cholesterol pro fi le, enhanced reverse cholesterol transport, and ameliorated vascular in fl ammation (Horie et al, 2012; Rayner et al, 2011).”
Zhang, Y., Chai, Z., Chen, M., Li, S., Zhuang, W., Hu, W. W., & Chen, M. (2025) · Precision medicine and engineering. · doi:10.1016/j.preme.2025.100046 · Cited by 5
Dong, J., Sun, M., Li, Y., & Xie, Z. (2025) · Journal of drug targeting · doi:10.1080/1061186x.2025.2544786 · Cited by 4
“[109] rna therapeutics Delivering rna/ oligonucleotides to modulate gene expression.”
Mahdizadeh, F., Sobhi, P., & Banaei, S. (2025) · Clinics And Research in Hepatology and Gastroenterology · doi:10.1016/j.clinre.2025.102547 · Cited by 3
Aranda, J. F., Pérez-García, A., Torrecilla-Parra, M., Frutos, M. F.-D., Martín-Martín, Y., Mateos-Gómez, P. A., Pardo-Marqués, V., Busto, R., & Ramírez, C. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.994080 · Cited by 3
“In the last 10 years, numerous studies have shown that ABCA1 expression is beyond its classic transcriptional regulation, being extensively regulated at the posttranscriptional level by miRNAs including miR-33 (46, 47), miR-758 (26), miR-144 (27), miR-27b (28), miR-148a (29), miR-106b (30), and some RBPs (48).”
BackgroundPatel, S., Mastrogiacomo, L., Fulmer, M., Shi, Y.-Y., & Werstuck, G. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23169293 · Cited by 3
“Previous studies have shown that atherosclerotic regression is associated with an upregulation of ABCA1 expression and enhanced RCT in lesional macrophages of Ldlr−/− mice treated with an antisense to micro-RNA-33 [40].”
BackgroundLu, R., Lin, M., Yang, F., Jia, S., Zhang, Y., Qin, C., Meng, X., & Nie, G.-X. (2021) · Fish Physiology and Biochemistry · doi:10.1007/s10695-021-00956-3 · Cited by 6
Belyaeva, V. S., Stepenko, Y. V., Lyubimov, I. I., Kulikov, A. L., Tietze, A. A., Kochkarova, I. S., Martynova, O. V., Pokopeyko, O. N., Крупенькина, Л. А., Nagikh, A. S., et al. (2020) · Research Results in Pharmacology · doi:10.3897/rrpharmacology.6.58891 · Cited by 4
“MiR33a and MiR-33b contribute to atherosclerosis by disrupting cholesterol outflow and promoting inflammatory macrophage conversion (Rayner et al. 2011; Horie et al. 2012; Nishino et al. 2018).”
BackgroundNiu, R., Xiao, X.-P., Liu, B., Li, Y.-Q., Zhong, Y., & Ma, L.-J. (2017) · Scientific Reports · doi:10.1038/s41598-019-53536-0 · Cited by 3
RetractedChen, S.-T., Huang, C., Kok, V. C., Huang, C. F., Ciou, J.-S., Tsai, J. J. P., Kurubanjerdjit, N., & Ng, K. (2016) · Journal of Bioinformatics and Computational Biology · doi:10.1142/s0219720016500438 · Cited by 6
Hoda, E. M., Dina, M. A., Same, M. S., & Amr, T. S. (2016) · African Journal of Pharmacy and Pharmacology · doi:10.5897/ajpp2016.4655 · Cited by 5
“…transfer protein (MTTP) expression, thereby decreasing very low density lipoprotein (VLDL) secretion from liver Furthermore, the silencing of miR-33a by knockout or antisense techniques in mice results in an improvement in plasma lipid profile with increasing (HDLc) level (Rayner et al., 2011).”
BackgroundEpigenetic factors in atherogenesis: MicroRNA
Smirnova, A. V., Sukhorukov, V. N., Карагодин, В. П., & Orekhov, A. N. (2016) · Biochemistry (Moscow) Supplement Series B Biomedical Chemistry · doi:10.1134/s199075081603015x
Nikpour, P., Mahabadi, H. M., Emadi‐Baygi, M., & Kelishadi, R. (2016) · International Journal of Preventive Medicine · doi:10.4103/2008-7802.177314 · Cited by 1
“Previous studies have shown a reverse correlation between miR‐33a and miR‐33b expressions and HDL‐C levels and a direct association with TC.[18,39,40] Thus, we may hypothesize that having two copies of G allele in the ‐1099 location, may have a negative regulatory effect on miR‐33b transcription and consequently incre…”
BackgroundVázquez, G. (2015) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2015.08.009 · Cited by 2
Therapeutic Potential of Modulating microRNAs in Atherosclerotic Vascular Disease
Araldi, E., Chamorro-Jorganes, A., Solingen, C. V., Fernandez-Hernando, C. F., & Suárez, Y. (2015) · Current Vascular Pharmacology · doi:10.2174/15701611113119990012 · Cited by 47
Gordeladze, J. O., Stakkestad, Ø., Haugen, S., Reseland, J. E., Syversen, U., Johnsen, G. F., Haugen, H. J., Lyngstadaas, S. P., Møller, M. E., & Valtieri, M. (2014) · InTech eBooks · doi:10.5772/59149 · Cited by 2
“The microRNA species 33b and 33a, respectively, have been shown to target the ATPbinding cassette A1 cholesterol transporter [21], which mediates intracellular cholesterol efflux from cells to form HDL that is protective against atherosclerosis [22, 23].”
BackgroundExpanding the Therapeutic Frontier in Atherosclerosis
Major, A. S. (2013) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0b013e3182a18bea · Cited by 3
MicroRNA-Linked Heart Disease and Therapeutic Potential
Ono, K. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-800553-8.00010-x · Cited by 3
Prakash, B., Chang, Z., Rajan, S., Scarberry, S. R., Gangula, B., Hossain, M. M., Prakashmurthy, C., Valmiki, S., Pulatov, O., Yadav, P. K., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-72276-0 · Cited by 2
Self-citationVélez-Slimani, H., & Salazar, L. A. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27083582 · Cited by 2
Fert-Bober, J. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262110492 · Cited by 2
“These findings complement those of prior studies showing the regulatory roles of miR-33, miR-27b, miR-148a, and miR-223 in cholesterol transport, lipoprotein metabolism, and atherogenesis [21–24].”
Saha, D., Dutta, P., Hussain, T., & Chakraborty, A. (2025) · ExRNA · doi:10.55092/exrna20250011 · Cited by 2
“In contrast, miRNA therapeutics such as anti-miR-33 and anti-miR-92a regulate broader gene networks and impact multiple pathways, including cholesterol efflux, vascular inflammation, and endothelial repair [26].”
InfluentialMontaño-Samaniego, M., Sánchez-Cedillo, J., Lucas-González, A., Bravo‐Estupiñan, D. M., Alarcón-Hernández, E., Rivera-Gutiérrez, S., Balderas-López, J. A., & Ibáñez-Hernández, M. Á. (2023) · Current Issues in Molecular Biology · doi:10.3390/cimb45090445 · Cited by 3
“However, although these strategies have been effective in reducing miR-33 levels, given the route of administration [16,43], this remains a non-specific option, since targeting to specific cells is still deficient, in addition, there may be a low uptake efficiency and, therefore, high doses and continuous administrati…”
BackgroundWu, L., Li, Y., Zhang, D., Huang, Z., Du, B., Wang, Z., Yang, L., & Zhang, Y. (2019) · RSC Advances · doi:10.1039/c9ra06282c · Cited by 4
RetractedLoss of MLKL Decreases Necrotic Core but Increases Macrophage Lipid Accumulation In AtherosclerosisPreprint
Rasheed, A., Robichaud, S., Nguyen, M.-A., Geoffrion, M., Cottee, M. L., Dennison, T., Pietrangelo, A., Lee, R. G., Ouimet, M., & Rayner, K. J. (2019) · bioRxiv · doi:10.1101/746644 · Cited by 2
Self-citationNesan, D., & Ng, D. S. (2014) · Critical Reviews in Clinical Laboratory Sciences · doi:10.3109/10408363.2014.937523 · Cited by 2
MicroRNAs and Cardiovascular Diseases
Ono, K. (2013) · Wiley eBooks · doi:10.1002/9781118300312.ch29 · Cited by 3
Therapeutic modulation of microRNAs
Chau, B. N., Esau, C., MacKenna, D. A., Neben, S., & Gibson, N. W. (2013) · Drug Discovery Today Therapeutic Strategies · doi:10.1016/j.ddstr.2013.12.002 · Cited by 2
Self-citationAtherosclerosis: beyond cholesterol.
Getz, G., & Reardon, C. (2011) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e32834d179e · Cited by 2
Noncoding RNAs in Platelet Biology
Edelstein, L. C., & Bray, P. F. (2017) · Springer eBooks · doi:10.1007/978-3-319-47462-5_18 · Cited by 3
Paasch, D., Haake, K., Kan, C., Ulpiano, C., Nikolouli, E., Jang, M.-S., Klassen, M.-C., Epstein, M., Sugimura, R., & Lachmann, N. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-026-02907-x · Cited by 1
“120 Additional approaches include miRNA-33 inhibition to enhance cholesterol ef fl ux and limit lipid accumulation, 121 cytokine modulation such as IL-19 to suppresses M Φ in fl ammation and maintain cholesterol homeostasis in atherosclerotic lesions.”
RNA-Targeted Therapeutics for Lipid Metabolic Disorders: From Bench to Bedside
Ali, I., Qiu, J., Cheang, W. S., Wang, G., & Xu, S. (2026) · Research · doi:10.34133/research.1288 · Cited by 1
She, J.-H., Yu, Y., Gao, B.-Y., Song, J.-Y., Cao, L., Wang, M., Yan, X.-L., Chang, L.-P., & Shi, G.-J. (2026) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2026.1770481 · Cited by 1
“Carlos Fernández-Hernando, an internationally recognized medical scientist, specializes in CVDs, miRNA regulation, and (12, 29).”
Jha, P., Chelvanambi, S., Nakamura, Y., Itto, L. Y., Vijay, A., Lupieri, A., Barbeiro, M., Le, T.-D., Nascimento, C. B., Kasai, T., et al. (2025) · JCI Insight · doi:10.1172/jci.insight.191274 · Cited by 1
“Multiple lines of evidence associated altered expression of lncRNAs and miRNAs with diseases. miRNAs in particular has been studied for its role in macrophage and atherosclerosis (10, 11).”
miRNAs activate mitochondrial energy metabolism: a narrative view
Nascimento, O. V., Cavalcante, K. S., da Silva, W. K. B., Nascimento, W., & Astolfi, S. (2023) · Concilium · doi:10.53660/clm-1475-23g02a · Cited by 1
Mechanism of Immune Response Through mRNA/miRNA Effect in Vascular Dysfunctions
Jiang, H. F., Ali, H., & Iftikhar, H. B. (2018) · Cardiology and Cardiovascular Medicine · doi:10.26502/fccm.92920045
“The opposing transcriptional process of fatty acid oxidation 80% of macrophages enhance the transportation to plasma retaining anti-inflammation, excreting bile and endothelial cells protection from induced cytokines [19].”
BackgroundMicroRNA-146a & hematopoiesis: friend or foe in atherosclerosis
Raffai, R. (2018) · Non-coding RNA Investigation · doi:10.21037/ncri.2018.06.08 · Cited by 1
“These investigators also demonstrated benefits of miR-33 antagonism in suppressing and even reversing atherosclerosis in rodents and primates (7).”
Background
Metadata
- Authors
- Rayner, K. J., Sheedy, F. J., Esau, C. C., Hussain, F. N., Temel, R. E., Parathath, S., van Gils, J. M., Rayner, A. J., Chang, A. N., Suarez, Y., Fernandez-Hernando, C., Fisher, E. A., & Moore, K. J.
- Affiliations
- New York University (US)
- Regulus Therapeutics (United States) (US)
- Wake Forest University Health Sciences (US)
- Corresponding author
- Moore, Kathryn J.
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2011-07-01
- Volume
- 121
- Issue
- 7
- Pages
- 2921-2931
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC3223840
- OpenAlex
- W2168964544
- Cited by
- 690
- References
- 0
- Citations by year
- 2026: 14 · 2025: 27 · 2024: 21 · 2023: 35 · 2022: 41 · 2021: 36 · 2020: 38 · 2019: 43 · 2018: 45 · 2017: 48 · 2016: 63 · 2015: 62 · 2014: 82 · 2013: 71 · 2012: 50
- FWCI
- 70.78
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- Funders
- National Institutes of Health (5r00hl088528-05)
- Canadian Institutes of Health Research
- National Institute on Aging (R01AG020255)
- National Heart, Lung, and Blood Institute (R01HL084312, R00-HL088528, K99HL088528, P01HL098055, R01HL108182, R01HL107953)
- 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, reverse cholesterol transport, HDL cholesterol, atherosclerosis regression, ABCA1, SREBF2, LDL receptor-deficient mice, atherosclerotic plaque, plaque macrophages, cholesterol efflux, plaque stability, inflammation
- MeSH terms
- Animals, Humans, Cholesterol, HDL, Liver, Macrophages, Mice, Inbred C57BL, Random Allocation, Receptors, LDL, Gene Expression, Mice, Knockout, ATP-Binding Cassette Transporters, MicroRNAs, Atherosclerosis, Lipid Metabolism, Mice, ATP Binding Cassette Transporter 1
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