ArticleArteriosclerosis, thrombosis, and vascular biology2017
microRNA-33 Regulates Macrophage Autophagy in Atherosclerosis.
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Article in Arteriosclerosis, thrombosis, and vascular biology, 2017. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 133 papers, 1 of them a synthesis that pooled it.
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133citing papers in PubMed, 1 pooled it
13.8field-weighted citation impact, top 1% of its field
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Who cites it
133 citing papers in PubMed, 1 synthesis or guideline pooled it, 213 citations in OpenAlex.
- Discussion on the comparison of Raman spectroscopy and cardiovascular disease-related imaging techniques and the future applications of Raman technology: a systematic review.Lasers in medical science · 2025Pooled it
- Non-Coding RNAs from Cardiac Development to Disease: Regulatory Context, Regenerative Potential, and Translational Limits.International journal of molecular sciences · 2026Review
- S100A8/A9 and S100A12 Proteins and Macrophage Polarization: Therapeutic Targets in Atherosclerosis.Biomolecules · 2026Review
- MicroRNAs as master regulators of macrophage function in atherosclerosis: From polarization to therapeutic potential.iScience · 2026Review
- Non-coding RNAs in lipid metabolism and their roles in atherosclerosis.Nature reviews. Cardiology · 2026Review
- Molecular and Genetic Aspects of Lipid Metabolism Disorders and Potential Targets for Gene Therapy.Journal of lipid and atherosclerosis · 2026Review
- Key Molecular Events in PMCells · 2026Article
- From Storage to Signaling: Lipid Droplet Lipolysis in Cholesterol Mobilization and Foam Cell Remodeling.Current atherosclerosis reports · 2026Review
- MicroRNAs in Cardiovascular Diseases: Molecular Networks of Cellular Homeostasis, Inflammation, and Pathological Remodeling.International journal of molecular sciences · 2026Review
- Cathelicidin LL-37-ApoB-100 interaction promotes LDL clearance and attenuates cholesterol accumulation in the liver.Science China. Life sciences · 2026Article
- The transcription factor HHEX maintains glucocorticoid levels and protects adrenals from androgen-induced lipid depletion.Nature communications · 2026Article
- Molecular Mechanisms Underlying Atherosclerosis and Current Advances in Targeted Therapeutics.International journal of molecular sciences · 2026Review
- TNFSF13 Drives Atherosclerosis Progression by Targeting Macrophage Senescence.International journal of medical sciences · 2026Article
- Macrophage-associated noncoding RNAs in atherosclerosis and chronic kidney disease.Frontiers in cardiovascular medicine · 2026Review
- Bibliometric analysis of research hotspots and emerging trends in microRNAs and atherosclerosis (2007-2025).Frontiers in cardiovascular medicine · 2026Review
- Critical Role of microRNA-33a/b in Cardiovascular and Metabolic Disease: Molecular Mechanisms and Therapeutic Perspectives.Journal of atherosclerosis and thrombosis · 2026Review
- Orally deliverable biomimetic nucleic acid therapies for targeted treatment of atherosclerosis.Acta pharmaceutica Sinica. B · 2025Article
- Efferocytosis: the art of cellular clearance and novel perspectives in disease therapy.Molecular cancer · 2025Review
- Inflammasomes in Cardiovascular Diseases: Current Knowledge and Future Perspectives.International journal of molecular sciences · 2025Review
- Connecting the Dots: How MicroRNAs Link Asthma and Atherosclerosis.International journal of molecular sciences · 2025Review
73 more citing papers are in PubMed but not listed here.
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Authors and funding
13 authors at 3 institutions in 2 countries.
Mireille OuimetFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.).
Hasini EdiriweeraFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.).
Milessa Silva AfonsoFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.).
Bhama RamkhelawonFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.).
Ragunath SingaraveluFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.).
Xianghai LiaoFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.).
Rachel C BandlerFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.).
Karishma RahmanFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.).
Edward A FisherFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.).
Katey J RaynerFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.).
John P PezackiFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.).
Ira TabasFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.).
Kathryn J MooreFrom the Marc and Ruti Bell Vascular Biology and Disease Program, Leon H. Charney Division of Cardiology, Department of Medicine (M.O., H.E., M.S.A., R.C.B., K.R., E.A.F., K.J.M.) and Division of Vascular Surgery, Department of Surgery (B.R.), New York University Medical Center; Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Canada (R.S., K.J.R., J.P.P.); National Research Council of Canada, Ottawa, Ontario (R.S., J.P.P.); Departments of Medicine, Pathology and Cell Biology, Columbia University, New York (X.L., I.T.); and University of Ottawa Heart Institute, Ontario, Canada (K.J.R.). kathryn.moore@nyumc.org.
Columbia University · USNational Research Council Canada · CAUniversity of Ottawa · CA
Funding
Translational Research CoreP30DK020541 · NIDDK · ALBERT EINSTEIN COLLEGE OF MEDICINE, INC · PI JEFFREY E. PESSIN · 2015 to 2026
$27.7MNon-coding RNA regulation of cholesterol homeostasis and atherosclerosisR35HL135799 · NHLBI · NEW YORK UNIVERSITY SCHOOL OF MEDICINE · PI MOORE, KATHRYN J · 2017 to 2023
$6.7MTraining Program in Immunology and Inflammation.T32AI100853 · NIAID · NEW YORK UNIVERSITY SCHOOL OF MEDICINE · PI Susan Ruth Schwab · 2012 to 2026
$4.5MHDL and atherosclerosis regressionR01HL129433 · NHLBI · NEW YORK UNIVERSITY SCHOOL OF MEDICINE · PI FISHER, EDWARD A, MOORE, KATHRYN J · 2016 to 2019
$2.4MmiR-33 Pathway Inhibition for Improving HDL FunctionalityR01HL119047 · NHLBI · NEW YORK UNIVERSITY SCHOOL OF MEDICINE · PI MOORE, KATHRYN J, RAYNER, KATEY · 2015 to 2018
$1.9MAutophagy in Advanced AtherosclerosisR01HL106019 · NHLBI · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI TABAS, IRA A · 2011 to 2014
$1.8M"MerTK Cleavage and Signaling in Atherosclerosis"R01HL132412 · NHLBI · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI TABAS, IRA A · 2016 to 2018
$1.5MDysregulation of Neuronal Guidance Cue Netrin-1 in Accelerated AAAR00HL125667 · NHLBI · NEW YORK UNIVERSITY SCHOOL OF MEDICINE · PI RAMKHELAWON, BHAMA · 2017 to 2019
$735kDysregulation of Neuronal Guidance Cue Netrin-1 in Accelerated AAAK99HL125667 · NHLBI · NEW YORK UNIVERSITY SCHOOL OF MEDICINE · PI RAMKHELAWON, BHAMA · 2015 to 2016
$221kCIHR MOP130365CIHR MSH130157NHLBI NIH HHS K99 HL125667NHLBI NIH HHS R00 HL125667NHLBI NIH HHS R01 HL106019NHLBI NIH HHS R01 HL119047NHLBI NIH HHS R01 HL129433NHLBI NIH HHS R01 HL132412NHLBI NIH HHS R35 HL135799NIAID NIH HHS T32 AI100853NIDDK NIH HHS P30 DK020541
Abstract
objectiveDefective autophagy in macrophages leads to pathological processes that contribute to atherosclerosis, including impaired cholesterol metabolism and defective efferocytosis. Autophagy promotes the degradation of cytoplasmic components in lysosomes and plays a key role in the catabolism of stored lipids to maintain cellular homeostasis. microRNA-33 (miR-33) is a post-transcriptional regulator of genes involved in cholesterol homeostasis, yet the complete mechanisms by which miR-33 controls lipid metabolism are unknown. We investigated whether miR-33 targeting of autophagy contributes to its regulation of cholesterol homeostasis and atherogenesis. APPROACH AND
resultsUsing coherent anti-Stokes Raman scattering microscopy, we show that miR-33 drives lipid droplet accumulation in macrophages, suggesting decreased lipolysis. Inhibition of neutral and lysosomal hydrolysis pathways revealed that miR-33 reduced cholesterol mobilization by a lysosomal-dependent mechanism, implicating repression of autophagy. Indeed, we show that miR-33 targets key autophagy regulators and effectors in macrophages to reduce lipid droplet catabolism, an essential process to generate free cholesterol for efflux. Notably, miR-33 regulation of autophagy lies upstream of its known effects on ABCA1 (ATP-binding cassette transporter A1)-dependent cholesterol efflux, as miR-33 inhibitors fail to increase efflux upon genetic or chemical inhibition of autophagy. Furthermore, we find that miR-33 inhibits apoptotic cell clearance via an autophagy-dependent mechanism. Macrophages treated with anti-miR-33 show increased efferocytosis, lysosomal biogenesis, and degradation of apoptotic material. Finally, we show that treating atherosclerotic
conclusionsCollectively, these data provide insight into the mechanisms by which miR-33 regulates cellular cholesterol homeostasis and atherosclerosis.
Indexed as
AutophagyAnimalsAtherosclerosisAutophagy-Related Protein 5CholesterolGene Expression RegulationGenetic Predisposition to DiseaseHumansJurkat CellsLipid DropletsLysosomesMacrophages, PeritonealMice, Inbred C57BLMice, KnockoutMicroRNAsNecrosisAtg5 protein, mouseAutophagy-Related Protein 5CholesterolMicroRNAsMIRN33a microRNA, humanMirn33 microRNA, mouseReceptors, LDLatherosclerosisautophagyhydrolysislipid dropletsmacrophages
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