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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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Alternative activation of macrophages
Gordon, S. (2003) · Nature Reviews Immunology · doi:10.1038/nri978 · Cited by 6,189
Cholesterol efflux capacity, high-density lipoprotein function, and atherosclerosis
Khera, A. V., Cuchel, M., de la Llera-Moya, M., Rodrigues, A., Burke, M. F., Jafri, K., French, B. C., Phillips, J. A., Mucksavage, M. L., Wilensky, R. L., et al. (2011) · New England Journal of Medicine · doi:10.1056/nejmoa1001689 · Cited by 1,943
HDL cholesterol, very low levels of LDL cholesterol, and cardiovascular events
Barter, P., Gotto, A. M., LaRosa, J. C., Maroni, J., Szarek, M., Grundy, S. M., Kastelein, J. J. P., Bittner, V., & Fruchart, J.-C. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa064278 · Cited by 1,610
Stewart, C. R., Stuart, L. M., Wilkinson, K., van Gils, J. M., Deng, J., Halle, A., Rayner, K. J., Boyer, L., Zhong, R., Frazier, W. A., et al. (2010) · Nature Immunology · doi:10.1038/ni.1836 · Cited by 1,513
Self-citationMicroRNA-33 and the SREBP Host Genes Cooperate to Control Cholesterol Homeostasis
Najafi-Shoushtari, S. H., Kristo, F., Li, Y., Shioda, T., Cohen, D. E., Gerszten, R. E., & Näär, A. M. (2010) · Science · doi:10.1126/science.1189123 · Cited by 957
Safety of anacetrapib in patients with or at high risk for coronary heart disease
Cannon, C. P., Shah, S., Dansky, H. M., Davidson, M., Brinton, E. A., Gotto, A. M., Stepanavage, M., Liu, S. X., Gibbons, P., Ashraf, T. B., et al. (2010) · New England Journal of Medicine · doi:10.1056/nejmoa1009744 · Cited by 749
miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling
Dávalos, A., Goedeke, L., Smibert, P., Ramírez, C. M., Warrier, N. P., Andreo, U., Cirera-Salinas, D., Rayner, K., Suresh, U., Pastor-Pareja, J. C., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102281108 · Cited by 670
Self-citationmiR-33 links SREBP-2 induction to repression of sterol transporters
Marquart, T. J., Allen, R. M., Ory, D. S., & Baldán, Á. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005191107 · Cited by 562
Increased Atherosclerosis in Hyperlipidemic Mice With Inactivation of ABCA1 in Macrophages
Aiello, R. J., Brees, D., Bourassa, P.-A., Royer, L., Lindsey, S., Coskran, T., Haghpassand, M., & Francone, O. L. (2002) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000014804.35824.da · Cited by 390
Expression of miR-33 from an SREBP2 Intron Inhibits Cholesterol Export and Fatty Acid Oxidation*
Gerin, I., Clerbaux, L.-A., Haumont, O., Lanthier, N., Das, A. K., Burant, C. F., Leclercq, I. A., MacDougald, O. A., & Bommer, G. T. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.152090 · Cited by 382
Research works printed but not linked: 63
- Castelli, 1977, Circulation., 55, 767, 10.1161/01.CIR.55.5.767 · DOI · Paper page
- 10.1016/0002-9149(90)90562-F · DOI
- 10.1038/353265a0 · DOI
- 10.1172/JCI117412 · DOI
- 10.1073/pnas.91.20.9607 · DOI
- 10.1161/01.ATV.0000142808.34602.25 · DOI
- Tangirala, 1999, Circulation., 100, 1816, 10.1161/01.CIR.100.17.1816 · DOI
- 10.1161/hc4501.098952 · DOI
- 10.1161/hc2501.092494 · DOI
- 10.1172/JCI114558 · DOI
- 10.1001/jama.290.17.2292 · DOI · Paper page
- 10.1038/11905 · DOI · Paper page
- 10.1038/11914 · DOI · Paper page
- 10.1161/01.RES.0000250171.54048.5c · DOI · Paper page
- 10.1016/j.cmet.2005.01.002 · DOI
- 10.1073/pnas.0403506101 · DOI
- 10.1016/j.cmet.2008.03.001 · DOI · Paper page
- 10.1172/JCI32057 · DOI
- 10.1161/ATVBAHA.107.156935 · DOI
- Yvan-Charvet, 2007, J Clin Invest., 117, 3900
- 10.1194/jlr.M700274-JLR200 · DOI
- 10.1210/me.2003-0061 · DOI
- 10.1073/pnas.112059299 · DOI
- 10.1194/jlr.M800374-JLR200 · DOI
- 10.1172/JCI38911 · DOI
- 10.1161/CIRCULATIONAHA.105.560177 · DOI
- 10.1172/JCI31909 · DOI
- 10.1126/science.1189862 · DOI · Paper page
- 10.1093/nar/gkn904 · DOI
- 10.1038/nature06783 · DOI · Paper page
- 10.1126/science.1178178 · DOI · Paper page
- Henry, 2000, J Pharmacol Exp Ther., 292, 468, 10.1016/S0022-3565(24)35315-7 · DOI
- 10.1172/JCI25327 · DOI · Paper page
- 10.1172/JCI32057 · DOI
- 10.1517/17425250902877680 · DOI
- 10.1073/pnas.1016086108 · DOI
- 10.1073/pnas.1008499107 · DOI · Paper page
- 10.1161/ATVBAHA.110.207142 · DOI
- 10.1172/JCI27602 · DOI
- Innerarity, 1982, Arteriosclerosis., 2, 114, 10.1161/01.ATV.2.2.114 · DOI
- Rader, 2009, J Lipid Res., 50 suppl, S189, 10.1194/jlr.R800088-JLR200 · DOI
- 10.1161/CIRCRESAHA.108.182568 · DOI
- 10.1161/CIRCULATIONAHA.110.984146 · DOI
- Mills, 2001, Crit Rev Immunol., 21, 399, 10.1615/CritRevImmunol.v21.i5.10 · DOI
- 10.1161/01.ATV.0000208364.22732.16 · DOI
- Vaisman, 2001, J Clin Invest., 108, 303, 10.1172/JCI200112517 · DOI
- 10.1074/jbc.M604526200 · DOI · Paper page
- Singaraja, 2002, J Clin Invest., 110, 35, 10.1172/JCI0215748 · DOI · Paper page
- 10.1016/j.cmet.2006.01.005 · DOI · Paper page
- 10.1093/nar/gkm1113 · DOI
- 10.1016/S0140-6736(05)67394-1 · DOI · Paper page
- 10.1016/S0140-6736(08)60104-X · DOI · Paper page
- 10.1161/01.CIR.0000034508.55617.65 · DOI
- 10.1161/01.CIR.0000148955.19792.8D · DOI
- 10.1001/jama.297.15.jpc70004 · DOI
- 10.1056/NEJMe0707210 · DOI
- 10.1056/NEJMe078029 · DOI
- 10.1161/01.ATV.0000256728.60226.77 · DOI
- 10.1172/JCI24061 · DOI
- 10.1161/ATVBAHA.108.176644 · DOI
- 10.1073/pnas.042683999 · DOI
- Trogan, 2005, Methods Mol Biol., 293, 221
- 10.1093/bioinformatics/19.2.185 · DOI
Cited by
Sorted by citations
Items 201–300 of 642
Rasheed, A., Robichaud, S., Nguyen, M.-A., Geoffrion, M., Wyatt, H., Cottee, M. L., Dennison, T., Pietrangelo, A., Lee, R. G., Lagace, T. A., et al. (2020) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.119.313640 · Cited by 76
Self-citationPosttranscriptional regulation of lipid metabolism by non-coding RNAs and RNA binding proteins
Singh, A. K., Aryal, B. K., Zhang, X., Fan, Y., Price, N. L., Suárez, Y., & Fernandez-Hernando, C. F. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.11.026 · Cited by 55
“Interestingly, the three reports that found significant reduction in atherosclerotic burden without affecting circulating HDL-C also demonstrated the efficacy of anti-miR-33 therapy in targeting atherosclerotic plaque macrophages and the whole aorta [36, 63, 64, 66, 67].”
BackgroundKostopoulou, F., Malizos, Κ. Ν., Papathanasiou, I. V., & Tsezou, A. (2015) · Arthritis Research & Therapy · doi:10.1186/s13075-015-0556-y · Cited by 63
“Contrarily, inhibition of endogenous miR-33a increases plasma HDL levels through positive regulation of ABCA1 expression [23,25,29-31], serving as useful tool for treating dyslipidemia, cardiovascular disorders and related metabolic diseases.”
BackgroundDesmoglein-1, differentiation, and disease
Hammers, C. M., & Stanley, J. R. (2013) · Journal of Clinical Investigation · doi:10.1172/jci69071 · Cited by 62
“…studies indicated that the autoantigen was indeed DSG1 (8), and further studies have shown that the auto-antibodies, even as monovalent cloned single chain variable fragments from patients (9), can cause loss of cell adhesion in the superficial epidermis where DSG1 is highly expressed.”
Elucidating the contributory role of microRNA to cardiovascular diseases (a review)
Johnson, J. L. (2018) · Vascular Pharmacology · doi:10.1016/j.vph.2018.10.010 · Cited by 60
2014 Jeffrey M. Hoeg Award Lecture
Zhu, Y. P., Thomas, G. D., & Hedrick, C. C. (2016) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.116.304054 · Cited by 77
Micro-RNAs and High-Density Lipoprotein Metabolism
Canfrán‐Duque, A., Lin, C., Goedeke, L., Suárez, Y., & Fernandez-Hernando, C. F. (2016) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.116.307028 · Cited by 64
“such, inhibition of miR-33 lead to increased sterol accumulation in the bile and enhanced RCT in vivo.(30,31) Furthermore, Li et al(32) reported that cholesterol 7α-hydroxylase, the rate-”
Circulating miR-33a and miR-33b are up-regulated in familial hypercholesterolaemia in paediatric age
Martino, F., Carlomosti, F., Avitabile, D., Persico, L., Picozza, M., Barillà, F., Arca, M., Montali, A., Martino, E., Zanoni, C., et al. (2015) · Clinical Science · doi:10.1042/cs20150235 · Cited by 60
Canfrán‐Duque, A., Ramírez, C. M., Goedeke, L., Lin, C., & Fernandez-Hernando, C. F. (2014) · Cardiovascular Research · doi:10.1093/cvr/cvu140 · Cited by 59
Efferocytosis and Atherosclerosis: Regulation of Phagocyte Function by MicroRNAs
Tajbakhsh, A., Bianconi, V., Pirro, M., Hayat, S. M. G., Johnston, T. P., & Sahebkar, A. (2019) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2019.07.006 · Cited by 57
Deciphering Non-coding RNAs in Cardiovascular Health and Disease
Das, A., Samidurai, A., & Salloum, F. N. (2018) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2018.00073 · Cited by 56
“Anti-atherosclerotic effects of anti-miR-33 therapy have been attributed to increasing circulating levels of HDL or improving macrophage cholesterol efflux via ABCA1 and ABCG1, two of the well-established targets of miR-33 (155, 162, 164).”
BackgroundA MicroRNA Perspective on Cardiovascular Development and Diseases: An Update
Islas, J. F., & Moreno-Cuevas, J. E. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19072075 · Cited by 63
“Hence, their control can be a useful tool in potential therapies for dyslipidemia and atherosclerosis [75,76].”
BackgroundmicroRNAs in lipoprotein and lipid metabolism: from biological function to clinical application
Desgagné, V., Bouchard, L., & Guérin, R. (2016) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm-2016-0575 · Cited by 57
Fisher, E. A. A. (2015) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.115.301926 · Cited by 59
Self-citationMiR-181a regulates lipid metabolism via IDH1
Chu, B., Wu, T. H., Miao, L., Mei, Y., & Wu, M. (2015) · Scientific Reports · doi:10.1038/srep08801 · Cited by 68
Lin, J. B., Moolani, H. V., Sene, A., Sidhu, R., Kell, P., Lin, J. B., Dong, Z., Ban, N., Ory, D. S., & Apte, R. S. (2018) · JCI Insight · doi:10.1172/jci.insight.120157 · Cited by 54
Role of miRNAs on the Pathophysiology of Cardiovascular Diseases
Pereira‐Silva, D. C., Carneiro, F. D., Almeida, K. C. D., & Fernandes‐Santos, C. (2018) · Arquivos Brasileiros de Cardiologia · doi:10.5935/abc.20180215 · Cited by 59
Huang, K., Bao, H., Yan, Z., Wang, L., Zhang, P., Yao, Q., Shi, Q., Chen, X., Wang, K., Shen, B., et al. (2017) · Cardiovascular Research · doi:10.1093/cvr/cvw257 · Cited by 52
Vergnes, L., Chin, R. G., de Aguiar Vallim, T., Fong, L. G., Osborne, T. F., Young, S. G., & Reue, K. (2016) · Journal of Lipid Research · doi:10.1194/jlr.m064022 · Cited by 72
SREBP-1c/MicroRNA 33b Genomic Loci Control Adipocyte Differentiation
Price, N. L., Holtrup, B., Kwei, S. L., Wabitsch, M., Rodeheffer, M. S., Bianchini, L., Suárez, Y., & Fernandez-Hernando, C. F. (2016) · Molecular and Cellular Biology · doi:10.1128/mcb.00745-15 · Cited by 61
Anti–miR-148a regulates platelet FcγRIIA signaling and decreases thrombosis in vivo in mice
Zhou, Y., Abraham, S., André, P., Edelstein, L. C., Shaw, C. A., Dangelmaier, C., Tsygankov, A. Y., Kunapuli, S. P., Bray, P. F., & McKenzie, S. E. (2015) · Blood · doi:10.1182/blood-2015-02-631135 · Cited by 59
Potential Mechanisms and Effects of Efferocytosis in Atherosclerosis
Wang, L., Li, H., Tang, Y., & Yao, P. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.585285 · Cited by 67
“Increasing HDL levels with anti-miR33 oligonucleotide treatment promotes reverse cholesterol transport and regression of AS (98).”
BackgroundmiR-33 Silencing Reprograms the Immune Cell Landscape in Atherosclerotic Plaques
Afonso, M. S., Sharma, M., Schlegel, M., van Solingen, C., Koelwyn, G. J., Shanley, L. C., Beckett, L., Peled, D., Rahman, K., Giannarelli, C., et al. (2021) · Circulation Research · doi:10.1161/circresaha.120.317914 · Cited by 53
Self-citationJiang, T., Xu, L., Zhao, M., Kong, F., Lu, X., Tang, C., & Yin, C. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.121324 · Cited by 57
Wiese, C. B., Zhong, J., Xu, Z., Zhang, Y., Solano, M. A. R., Zhu, W., Linton, M. F., Sheng, Q., Kon, V., & Vickers, K. C. (2019) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2019.01.023 · Cited by 64
Non-coding RNAs in lipid metabolism
Zhang, X., Price, N. L., & Fernandez-Hernando, C. F. (2018) · Vascular Pharmacology · doi:10.1016/j.vph.2018.06.011 · Cited by 54
Human genetics of HDL: Insight into particle metabolism and function
Brunham, L. R., & Hayden, M. R. (2015) · Progress in Lipid Research · doi:10.1016/j.plipres.2015.01.001 · Cited by 54
Relevance of microRNA in metabolic diseases
Price, N. L., Ramírez, C. M., & Fernandez-Hernando, C. F. (2014) · Critical Reviews in Clinical Laboratory Sciences · doi:10.3109/10408363.2014.937522 · Cited by 55
Functions of microRNA-33a/b and microRNA therapeutics
Ono, K. (2015) · Journal of Cardiology · doi:10.1016/j.jjcc.2015.10.017 · Cited by 52
“This promotion of RCT was shown to be achieved in two ways: by directly increasing HDL-C biogenesis in the liver, and by increasing cellular cholesterol efflux from plaque macrophages.”
BackgroundInfluentialDyslipidemia management update
Chang, Y., & Robidoux, J. (2017) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2017.04.005 · Cited by 50
Current concept of reverse cholesterol transport and novel strategy for atheroprotection
Ono, K. (2012) · Journal of Cardiology · doi:10.1016/j.jjcc.2012.07.014 · Cited by 49
“It has already reported that silencing miR-33a resulted in a reduction of atherosclerosis in mice [49].”
BackgroundLópez‐Pastor, A. R., Infante‐Menéndez, J., Escribano, Ó., & Gómez‐Hernández, A. (2020) · Frontiers in Medicine · doi:10.3389/fmed.2020.527059 · Cited by 53
“Moreover, it has been demonstrated that miR-33 inhibition attenuates atherosclerosis progression (57, 58).”
BackgroundLee, L. K., Medzikovic, L., Eghbali, M., Eltzschig, H. K., & Yuan, X. (2020) · Anesthesia & Analgesia · doi:10.1213/ane.0000000000005146 · Cited by 60
Price, N. L., Zhang, X., Fernández-Tussy, P., Singh, A. K., Burnap, S. A., Rotllan, N., Goedeke, L., Sun, J., Canfrán-Duque, A., Aryal, B., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2006478118 · Cited by 50
Horie, T., Nishino, T., Baba, O., Kuwabara, Y., Nakao, T., Nishiga, M., Usami, S., Izuhara, M., Nakazeki, F., Ide, Y., et al. (2014) · Scientific Reports · doi:10.1038/srep05312 · Cited by 49
Zhong, C., Lin, Z., Ke, L., Shi, P., Li, S.-G., Huang, L.-Y., Lin, X.-H., & Yao, H. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.778847 · Cited by 49
Hou, J., Deng, Q., Deng, X., Zhong, W., Liu, S., & Zhong, Z. (2021) · Annals of Translational Medicine · doi:10.21037/atm-21-3903 · Cited by 57
“MiR-33 has been shown to target the cholesterol transporter ABC transporter A1 (ABCA1) to repress cholesterol efflux and promote the progress of AS (53) .”
Liang, B., Wang, X., Song, X., Bai, R., Yang, H., Yang, Z., Xiao, C., & Bian, Y. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2017.06.002 · Cited by 45
Tontonoz, P., Wu, X.-H., Jones, M. C., Zhang, Z.-Y., Salisbury, D. A., & Sallam, T. (2017) · Circulation · doi:10.1161/circulationaha.117.029002 · Cited by 49
MicroRNAs in lipid metabolism and atherosclerosis
Giral, H., Kratzer, A., & Landmesser, U. (2016) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2016.11.010 · Cited by 56
microRNA-33 maintains adaptive thermogenesis via enhanced sympathetic nerve activity
Horie, T., Nakao, T., Miyasaka, Y., Nishino, T., Matsumura, S., Nakazeki, F., Ide, Y., Kimura, M., Tsuji, S., Rodriguez, R. R., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21107-5 · Cited by 49
The Immunomodulatory Effects of Statins on Macrophages
Sheridan, A., Wheeler-Jones, C. P. D., & Gage, M. C. (2022) · Immuno · doi:10.3390/immuno2020021 · Cited by 48
Introduction to the Series on MicroRNAs in the Cardiovascular System
van Rooij, E. (2012) · Circulation Research · doi:10.1161/circresaha.111.257311 · Cited by 54
Atherosclerotic plaque instability in carotid arteries: miR-200c as a promising biomarker.
Magenta, A., Sileno, S., D'Agostino, M., Persiani, F., Beji, S., Paolini, A., Camilli, D., Platone, A., Capogrossi, M., & Furgiuele, S. (2018) · Clinical science · doi:10.1042/cs20180684 · Cited by 47
Sun, Y., Zhang, D., Liu, X.-L., Li, X., Liu, F., Yu, Y., Jia, S., Zhou, Y., & Zhao, Y.-X. (2018) · Cellular Physiology and Biochemistry · doi:10.1159/000492522 · Cited by 47
Diet, gonadal sex, and sex chromosome complement influence white adipose tissue miRNA expression
Link, J. C., Hasin-Brumshtein, Y., Cantor, R. M., Chen, X., Arnold, A. P., Lusis, A. J., & Reue, K. (2017) · BMC Genomics · doi:10.1186/s12864-017-3484-1 · Cited by 52
“Indeed, studies in mice and non-human primates have shown that antagonism of miR-33a/b reduces plasma lipid levels and atherosclerosis [16, 17].”
BackgroundDávalos, A., & Fernandez-Hernando, C. F. (2013) · Pharmacological Research · doi:10.1016/j.phrs.2013.02.005 · Cited by 52
MicroRNA-98 regulates foam cell formation and lipid accumulation through repression of LOX-1
Dai, Y., Wu, X.-Q., Dai, D.-S., Li, J., & Mehta, J. (2018) · Redox Biology · doi:10.1016/j.redox.2018.03.003 · Cited by 46
Novák, J., Vašků, J. B., Kára, T., & Novák, M. (2014) · Mediators of Inflammation · doi:10.1155/2014/275867 · Cited by 53
Targeting and delivery of microRNA-targeting antisense oligonucleotides in cardiovascular diseases
Saenz-Pipaon, G., & Dichek, D. (2022) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2022.12.003 · Cited by 45
HDL and microRNA therapeutics in cardiovascular disease
Michell, D. L., & Vickers, K. C. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.09.001 · Cited by 45
Zhu, T., Corraze, G., Plagnes-Juan, E., Quillet, E., Dupont-Nivet, M., & Skiba-Cassy, S. (2018) · American Journal of Physiology. Regulatory Integrative and Comparative Physiology · doi:10.1152/ajpregu.00179.2017 · Cited by 45
Mathematical Modelling and Simulation of Atherosclerosis Formation and Progress: A Review
Avgerinos, N. A., & Neofytou, P. (2019) · Annals of Biomedical Engineering · doi:10.1007/s10439-019-02268-3 · Cited by 44
Christian, P., & Su, Q. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00194.2014 · Cited by 42
miR-206 controls LXRα expression and promotes LXR-mediated cholesterol efflux in macrophages
Vinod, M., Chennamsetty, I., Colin, S., Belloy, L., De Paoli, F., Schaider, H., Graier, W. F., Frank, S., Kratky, D., Staels, B., et al. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2014.02.006 · Cited by 44
Diverse Epigenetic Regulations of Macrophages in Atherosclerosis
Yang, H., Sun, Y., Li, Q., Jin, F., & Dai, Y. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.868788 · Cited by 46
“For example, increasing HDL levels by targeting miR-33 (an intronic microRNA located within the SREBF2 gene that encodes sterol regulatory element binding transcription factor 2) leads to the regression of established plaques in Ldlr−/− mice (23).”
BackgroundLi, X., Yang, Y., Wang, Z., Jiang, S., Meng, Y., Song, X., Zhao, L., Zou, L., Li, M., & Yu, T. (2021) · International Journal of Biological Sciences · doi:10.7150/ijbs.62506 · Cited by 49
“miR-33 down regulation promotes the expression of ABCA1 and the clearance of cholesterol increase [174]”
BackgroundSmall but smart: MicroRNAs orchestrate atherosclerosis development and progression
Santovito, D., Egea, V., & Weber, C. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2015.12.013 · Cited by 45
miRNA regulation of LDL-cholesterol metabolism
Goedeke, L., Wagschal, A., Fernández-Hernando, C., & Näär, A. M. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2016.03.007 · Cited by 39
MicroRNAs and lipoproteins: A connection beyond atherosclerosis?
Norata, G. D., Sala, F., Catapano, A. L., & Fernandez-Hernando, C. F. (2012) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2012.11.019 · Cited by 40
“Interestingly, anti-miR-33 therapy promotes RCT and regresses atherosclerosis in LDLr knockout mice [26].”
BackgroundChistiakov, D. A., Sobenin, I. A., & Orekhov, A. N. (2012) · Drug Delivery · doi:10.3109/10717544.2012.738436 · Cited by 43
A cross-tissue transcriptome-wide association study reveals novel susceptibility genes for migraine
Gui, J., Yang, X., Tan, C., Wang, L., Meng, L., Han, Z., Liu, J., & Jiang, L. (2024) · The Journal of Headache and Pain · doi:10.1186/s10194-024-01802-6 · Cited by 43
“Diseases associated with SREBF2 include atherosclerosis [42] and adrenoleuko-dystrophy [43].”
BackgroundMicroRNAs as the actors in the atherosclerosis scenario
Hajibabaie, F., Kouhpayeh, S., Mirian, M., Rahimmanesh, I., Boshtam, M., Sadeghian, L., Gheibi, A., Khanahmad, H., & Shariati, L. (2019) · Journal of physiology and biochemistry · doi:10.1007/s13105-019-00710-7 · Cited by 42
Advances in Glycolysis Metabolism of Atherosclerosis
Xu, R., Yuan, W., & Wang, Z. (2022) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-022-10311-3 · Cited by 41
“Previous studies have shown that miR-33 inhibitors are promising for the treatment of atherosclerosis because they increase the expression of the cholesterol transporter ABCA1 in the liver and macrophages, which in turn increases plasma HDL levels and macrophage cholesterol efflux [29].”
BackgroundMa, C., Zhang, J., Yang, S., Hua, Y., Su, J., Shang, Y., Wang, Z., Feng, K., Zhang, J., Yang, X., et al. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.610550 · Cited by 41
MicroRNAs as therapeutic targets in atherosclerosis
Loyer, X., Mallat, Z., Boulanger, C. M., & Tedgui, A. (2014) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2014.989835 · Cited by 43
“Specific antagomiR-33 treatment promotes reverse cholesterol transport, increases circulating high density lipoprotein and contributes to atherosclerosis diminution in nonhuman primates [43], as well as in ApoE/ [42] and Ldlr/ mice [44].”
BackgroundMicroRNA-33 in atherosclerosis etiology and pathophysiology
Chen, W., Zhang, M., Zhao, G., Fu, Y., Zhang, D., Zhu, H., & Tang, C. (2012) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2012.11.025 · Cited by 39
“Silencing miR-33 with antisense oligonucleotides also resulted in a substantial increase in plasma HDL levels [6,14].”
BackgroundInfluentialOrtega, R., Liu, B., & Persaud, S. J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241310777 · Cited by 45
“All of these effects were also accompanied by an increase in plasma HDL levels in these mice [19].”
BackgroundRNA Biology Provides New Therapeutic Targets for Human Disease
Harries, L. W. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00205 · Cited by 53
de Gaetano, M., McEvoy, C. M., Andrews, D. C., Cacace, A., Hunter, J., Brennan, E. P., & Godson, C. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.01488 · Cited by 38
“…including the “transplantation mouse,” a transplant model in which plaque-bearing aortic segments are transferred into normolipidemic mice (Reis et al., 2001); the “reversa mouse,” a genetic “switch” model in which LDL production can be conditionally reduced in LDL-R−/− mice (Feig et…”
BackgroundRahman, K., & Fisher, E. A. A. (2018) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2018.00032 · Cited by 48
“In addition, there are still other regression models that are based on non-LDL lowering strategies, such as raising HDL particles either transgenetically, by infusion of HDL, and treatment with anti-miR-33 (43, 106, 123, 129, 130).”
BackgroundSelf-citationShao, D., Lian, Z., Di, Y., Zhang, L., Rajoka, M. S. R., Zhang, Y., Kong, J., Jiang, C., & Shi, J. (2018) · npj Science of Food · doi:10.1038/s41538-018-0022-8 · Cited by 49
Control of very low-density lipoprotein secretion by N-ethylmaleimide-sensitive factor and miR-33
Allen, R. M., Marquart, T. J., Jesse, J. J., & Baldán, Á. (2014) · Circulation Research · doi:10.1161/circresaha.115.303100 · Cited by 38
“However, we and others have reported conflicting results after therapeutic silencing of miR-33 in Ldlr mice.(14,18,19) Herein, we show that prolonged silencing of miR-33 results in a sustained raise in hepatic secretion, leading to increased plasma levels of VLDL-TAG and other liver-secreted proteins in chow-fed C57BL…”
Li, C., Liu, C., Zhang, J., Lu, Y., Jiang, B., Xiong, H., & Li, C. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1296687 · Cited by 42
Diagnostic and theranostic microRNAs in the pathogenesis of atherosclerosis
Shoeibi, S. (2019) · Acta Physiologica · doi:10.1111/apha.13353 · Cited by 40
Regulatory RNAs and Cardiovascular Disease – With a Special Focus on Circulating MicroRNAs
Dlouhá, D., & Hubacek, J. A. (2017) · Physiological Research · doi:10.33549/physiolres.933588 · Cited by 40
“Inhibition of miR-33 using modified antisense or locked nucleic acid oligonucleotides increases hepatic ABCA1 expression and plasma HDL-C levels in both mice and monkeys by 40-50 % and enhanced cholesterol transport from macrophages to the plasma, liver, and feces by >80 % (Rayner et al. 2011).”
miRNA and cholesterol homeostasis
Jeon, T.-I., & Osborne, T. F. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2016.01.005 · Cited by 43
Mandolini, C., Santovito, D., Marcantonio, P., Buttitta, F., Bucci, M., Ucchino, S., Mezzetti, A., & Cipollone, F. (2015) · NMCD. Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2014.09.005 · Cited by 38
“Interestingly, inhibition of miR-33 raises plasma HDL in nonhuman primates and promotes atherosclerosis regression in mice [18,19].”
BackgroundHuang, A., Young, T. L., Dang, V. T., Shi, Y., McAlpine, C. S., & Werstuck, G. H. (2017) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2017.09.034 · Cited by 40
Hou, W., & Bonkovsky, H. (2013) · World Journal of Gastroenterology · doi:10.3748/wjg.v19.i44.7836 · Cited by 37
Targeting High Density Lipoproteins in the Prevention of Cardiovascular Disease?
Larach, D. B., deGoma, E. M., & Rader, D. J. (2012) · Current Cardiology Reports · doi:10.1007/s11886-012-0317-3 · Cited by 33
Hepatic ABC transporters and triglyceride metabolism
Parks, J. S., Chung, S., & Shelness, G. S. (2012) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e328352dd1a · Cited by 38
Use of Mouse Models in Atherosclerosis Research
Getz, G. S., & Reardon, C. A. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2929-0_1 · Cited by 38
miR‐33 in cardiometabolic diseases: lessons learned from novel animal models and approaches
Price, N. L., Goedeke, L., Suárez, Y., & Fernández‐Hernando, C. (2021) · EMBO Molecular Medicine · doi:10.15252/emmm.202012606 · Cited by 36
Self-citationImmune-based therapies in cardiovascular and metabolic diseases: past, present and future
Murphy, A. J., & Febbraio, M. A. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-021-00580-5 · Cited by 35
MicroRNAs and Circular RNAs in Lipoprotein Metabolism
Fernández‐Tussy, P., Ruz‐Maldonado, I., & Fernandez-Hernando, C. F. (2021) · Current Atherosclerosis Reports · doi:10.1007/s11883-021-00934-3 · Cited by 44
Zhang, J., Zhao, W.-S., Xu, L., Wang, X., Li, X.-L., & Yang, X.-C. (2020) · Experimental Cell Research · doi:10.1016/j.yexcr.2020.112443 · Cited by 36
MicroRNA regulated macrophage activation in obesity
Li, C., Qu, L., Farragher, C., Vella, A. T., & Zhou, B. (2019) · Journal of Translational Internal Medicine · doi:10.2478/jtim-2019-0011 · Cited by 38
“MicroRNA-33a and microRNA-33b target genes are related to metabolism [45,46] and microRNA-103 and microRNA-107 regulate insulin sensitivity and glucose homeostasis by modulating the abundance of caveolin-1 in adipocytes [47,48].”
BackgroundInduction of MiR133a expression by IL-19 targets LDLRAP1 and reduces oxLDL uptake in VSMC
Gabunia, K., Herman, A. B., Ray, M., Kelemen, S. E., England, R. N., Cadena, R. D., Foster, W. J., Elliott, K. J., Eguchi, S., & Autieri, M. V. (2017) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2017.02.005 · Cited by 35
“For example, circulating levels miR-33a and miR-33b, which have been found to play a role in cholesterol transport and regression of atherosclerosis, were found to be increased in plasma of hypercholesteremic children [17,41].”
BackgroundJia, L., Song, N., Yang, G.-L., Ma, Y.-X., Li, X.-T., Lu, R., Cao, H., Zhang, N., Zhu, M.-L., Wang, J., et al. (2016) · Molecular Medicine Reports · doi:10.3892/mmr.2016.5133 · Cited by 36
“Previous studies have demonstrated that miR-33 is able to regulate cholesterol efflux and HDL biogenesis by suppressing expression of the ABC transporters, ABCA1 and ABCG1 (39,26).”
Adeno-Associated Virus-Mediated MicroRNA Delivery and Therapeutics
Xie, J., Burt, D. R., & Gao, G. (2015) · Seminars in Liver Disease · doi:10.1055/s-0034-1397352 · Cited by 40
Novel Therapies Focused on the High-Density Lipoprotein Particle
van Capelleveen, J. C., Brewer, H. B., Kastelein, J. J. P., & Hovingh, G. K. (2014) · Circulation Research · doi:10.1161/circresaha.114.301804 · Cited by 34
“enhanced cholesterol efflux, induced regression of atherosclerotic plaques in LDLr mice.(80) Subsequent studies in nonhuman primates showed that 12-week administration of antisense”
BackgroundMicroRNA-144 Silencing Protects Against Atherosclerosis in Male, but Not Female Mice
Cheng, J., Cheng, A., Clifford, B. L., Wu, X., Hedin, U., Mäegdefessel, L., Pamir, N., Sallam, T., Tarling, E. J., & Vallim, T. Q. D. A. (2019) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.119.313633 · Cited by 43
Role of MicroRNAs in Obesity-Induced Metabolic Disorder and Immune Response
Zhong, H., Ma, M., Liang, T., & Guo, L. (2018) · Journal of Immunology Research · doi:10.1155/2018/2835761 · Cited by 36
“Further, numerous studies have regarded miR-33 as the therapy target of obesity and induced metabolic disorder [68].”
BackgroundAdvances in understanding the regulatory mechanism of cholesterol 7α-hydroxylase
Ge, M., Shao, R., & He, H. (2019) · Biochemical Pharmacology · doi:10.1016/j.bcp.2019.04.008 · Cited by 38
Circulating miRNA-33: a potential biomarker in patients with coronary artery disease
Reddy, L. L., Shah, S. A. V., Ponde, C. K., Rajani, R. M., & Ashavaid, T. F. (2018) · Biomarkers · doi:10.1080/1354750x.2018.1501760 · Cited by 37
“Table 6 (Rayner et al. 2011, Horie et al. 2012, Wijesekara et al. 2012, Mao et al. 2014, Kim et al. 2016) shows in vivo and in vitro studies to support the role of miR-33 in progression of atherosclerosis and its regulatory function in cholesterol metabolism.”
BackgroundGadde, S., & Rayner, K. J. (2016) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.116.307481 · Cited by 44
Self-citationChen, W., Sheu, W. H., Tseng, P., Lee, T., Lee, W., Chang, P., & Chiang, A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0154672 · Cited by 37
“Several reports show that miR-33 contributes to regulation of cholesterol homeostasis, which may promote the progress of atherosclerosis [42,43].”
BackgroundSon, S., Goo, Y., Choi, M., Saha, P., Oka, K., Chan, L., & Paul, A. (2015) · Cardiovascular Research · doi:10.1093/cvr/cvv241 · Cited by 39
Novel concepts in HDL pharmacology
Remaley, A. T., Norata, G. D., & Catapano, A. L. (2014) · Cardiovascular Research · doi:10.1093/cvr/cvu141 · Cited by 36
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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