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MicroRNA-33 and the SREBP Host Genes Cooperate to Control Cholesterol Homeostasis
Open accessAbstract
miR-33 in Cholesterol Control: With the well-established link between serum cholesterol levels and cardiovascular disease and the availability of effective cholesterol-lowering drugs, cholesterol screening has rapidly become a routine part of health care. Yet, much remains to be learned about how cholesterol levels are regulated at the cellular level (see the Perspective by Brown et al. ). Now, Najafi-Shoushtari et al. (p. 1566 , published online 13 May) and Rayner et al. (p. 1570 , published online 13 May) have discovered a new molecular player in cholesterol control—a small noncoding RNA that, intriguingly, is embedded within the genes coding for sterol regulatory element-binding proteins (SREBPs), transcription factors already known to regulate cholesterol levels. This microRNA, called miR-33, represses expression of the adenosine triphosphate–binding cassette transporter A1, a protein that regulates synthesis of high-density lipoprotein (HDL, or “good” cholesterol) and that helps to remove “bad” cholesterol from the blood. Reducing the levels of miR-33 in mice boosted serum HDL levels, suggesting that manipulation of this regulatory circuit might be therapeutically useful.
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“Pharmacological inhibition of miR-33 increased plasma high-density lipoprotein cholesterol levels in mice (Horie et al., 2010;Najafi-Shoushtari et al., 2010;Rayner et al., 2011a) and primates (Rayner et al., 2011b;Rottiers et al., 2013), leading to a marked reduction of atherosclerosis phenotypes.”
From microRNA-33 Regulates ApoE Lipidation and Amyloid-β Metabolism in the Brain (2015) · cites this paper as Najafi-Shoushtari et al., 2010
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In the citing paper
“in vivo antagonism or genetic deletion of miR-33 enhances hepatic ABCA1 expression and increases circulating HDL-cholesterol (HDL-C) (Marquart et al., 2010; Najafi-Shoushtari et al., 2010; Rayner et al., 2010).”
From Genetic dissection of the impact of miR-33a and miR-33b during the progression of atherosclerosis (2017) · cites this paper as Najafi-Shoushtari et al., 2010
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“These differences in miRNA expression vary between cell types suggesting that the role of miR-33b in the liver, where miR-33 is most highly expressed both in our mouse model and in human tissues (Najafi-Shoushtari et al., 2010), and other tissues may be considerably more important.”
From Genetic dissection of the impact of miR-33a and miR-33b during the progression of atherosclerosis (2017) · cites this paper as Najafi-Shoushtari et al., 2010
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“In miR-33a knockout mice or when miR-33a is suppressed by synthetic nucleic acids such as antagomirs, the expression of ABCA1 in macrophages and the liver is increased 11 - 15) .”
From Critical Role of microRNA-33a/b in Cardiovascular and Metabolic Disease: Molecular Mechanisms and Therapeutic Perspectives (2026) · cites this paper as [11]
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In the citing paper
“MicroRNA (miR)-33 is known to target ABCA1 and ABCG1 in vivo.”
From MicroRNA‐33 Deficiency Reduces the Progression of Atherosclerotic Plaque in ApoE −/− Mice (2012) · cites this paper as [17]
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“Two miR-33 genes are present in humans: miR-33b, which is present in intron 17 of the Srebp-1 gene on chromosome 17, and miR-33a, which is located in intron 16 of the Srebp-2 gene on chromosome 22.”
From miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling (2011) · cites this paper as [13]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“We and others have recently established that, during sterol-limited states, miR-33a is coincidentally generated with Srebp-2 transcription and works to increase cellular cholesterol levels by limiting cholesterol export through the down-regulation of ABC transporters, ABCA1 and ABCG1 (12–14).”
From miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling (2011) · cites this paper as [13]
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In the citing paper
“miR-33a and miR-33b are intronic miRNAs encoded within the SREBP-2 and SREBP-1 genes respectively (Marquart et al., 2010; Najafi-Shoushtari et al., 2010; Rayner et al., 2010).”
From Genetic dissection of the impact of miR-33a and miR-33b during the progression of atherosclerosis (2017) · cites this paper as Najafi-Shoushtari et al., 2010
The cited source says what the claim attributes to it.
In the citing paper
“This work led to the demonstration that miR-33a and miR-33b are co-transcribed along with SREBP-2 and SREBP-1, and work in concert with their host genes to help maintain proper lipid levels within the cell (Davalos et al., 2011; Marquart et al., 2010; Najafi-Shoushtari et al., 2010; Rayner et al., 2010).”
From Genetic dissection of the impact of miR-33a and miR-33b during the progression of atherosclerosis (2017) · cites this paper as Najafi-Shoushtari et al., 2010
The cited source says what the claim attributes to it.
In the citing paper
“The most well-known target gene of miR-33a/b is ATP-binding cassette subfamily A member 1 (ABCA1).”
From Critical Role of microRNA-33a/b in Cardiovascular and Metabolic Disease: Molecular Mechanisms and Therapeutic Perspectives (2026) · cites this paper as [11]
The cited source says what the claim attributes to it.
In the citing paper
“Recent reports, including ours, have indicated that miR-33 controls cholesterol homeostasis based on knockdown experiments using antisense technology.16–18”
From MicroRNA‐33 Deficiency Reduces the Progression of Atherosclerotic Plaque in ApoE −/− Mice (2012) · cites this paper as [17]
The cited source says what the claim attributes to it.
In the citing paper
“We and others provided identification of a highly conserved miRNA family, miR-33, within the intronic sequences of the Srebp genes in organisms ranging from Drosophila to humans (11–14).”
From miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling (2011) · cites this paper as [13]
The cited source says what the claim attributes to it.
In the citing paper
“In mice, however, there is only one miR-33 gene, which is conserved with human miR-33a and located within intron 15 of the mouse Srebp-2 gene.”
From miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling (2011) · cites this paper as [13]
The cited source says what the claim attributes to it.
In the citing paper
“Importantly, these pathways regulate circulating HDL levels through their roles in HDL biogenesis and cellular cholesterol efflux (12–14).”
From miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling (2011) · cites this paper as [13]
In the citing paper
“These microRNAs participate in the regulation of cholesterol synthesis, fatty acid metabolism, and insulin signaling.”
From The Vasculature in Prediabetes (2018) · cites this paper as [143]
In the citing paper
“They are co-transcribed and act in conjunction with their host genes, Srebp1 and Srebp2, to regulate cholesterol synthesis.”
From The Vasculature in Prediabetes (2018) · cites this paper as [143]
In the citing paper
“Furthermore, an intronic microRNA located within Srebf2 gene, miR-33, inhibits the expression of Abca1 (Najafi-Shoushtari et al., 2010; Rayner et al., 2010).”
From Inhibition of cholesterol biosynthesis through RNF145-dependent ubiquitination of SCAP (2017) · cites this paper as Najafi-Shoushtari et al., 2010
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“MiR-33, encoded by an intron of the sterol regulatory element binding protein gene, has been shown to collaborate with sterol regulatory element binding protein to regulate intracellular cholesterol levels and lipid homeostasis by targeting the adenosine triphosphatebinding cassette transporter A1, a regulator of cell…”
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“After 7 additional days of eye drops treatment, CNV volume was quantified, and mRNA levels of ABCA1 and ABCG1 were analyzed in mouse tissues.”
InfluentialCell-free 3D scaffold with two-stage delivery of miRNA-26a to regenerate critical-sized bone defects
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Self-citationGenome-wide identification of microRNAs regulating cholesterol and triglyceride homeostasis
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Self-citationTranscriptional and Epigenomic Regulation of Adipogenesis
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“Another important intronic miRNA is miR-33, which is embedded within the SREBP-2 gene and targets ABCA1 to control cholesterol homeostasis (157, 158).”
BackgroundMicroRNA-148a regulates LDL receptor and ABCA1 expression to control circulating lipoprotein levels
Goedeke, L., Rotllan, N., Canfrán-Duque, A., Aranda, J. F., Ramírez, C. M., Araldi, E., Lin, C.-S., Anderson, N. N., Wagschal, A., de Cabo, R., et al. (2015) · Nature Medicine · doi:10.1038/nm.3949 · Cited by 238
“…including ours, have demonstrated that miRNAs are a critical component of the cholesterol regulatory circuitry (e.g. the SREBP/miR-33 loci 16,17 and the SREBP-responsive miR-96/182/183 operon 18 ) and have identified a number of miRNAs (miR-122, miR-30c, miR-33a/b, miR-144, miR-223) that…”
Self-citationRole of microRNAs in diabetes and its cardiovascular complications
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“miR-33a and miR-33b have been shown to regulate cholesterol homeostasis through interaction with sterol regulatory elementbinding proteins.(48) Davalos et al.”
BackgroundXiao, H., Lu, M., Lin, T. Y., Chen, Z., Chen, G., Wang, W.-C., Marin, T., Shentu, T.-P., Wen, L., Gongol, B., et al. (2013) · Circulation · doi:10.1161/circulationaha.113.002714 · Cited by 257
“In macrophages, the SREBP2-coinduced miR-33a targets ABCA1, which impairs reverse cholesterol transport.(5,6) An antigomir against miR-33 decreases atherosclerosis in LDL receptor–null mice, with a concomitant increase in the level of high-density lipoprotein.”
BackgroundATP-Binding Cassette Transporters, Atherosclerosis, and Inflammation
Westerterp, M., Bochem, A. E., Yvan‐Charvet, L., Murphy, A. J., Wang, N., & Tall, A. R. (2014) · Circulation Research · doi:10.1161/circresaha.114.300738 · Cited by 261
MicroRNAs in Metabolic Disease
Fernández-Hernando, C., Ramírez, C. M., Goedeke, L., & Suárez, Y. (2013) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.112.300144 · Cited by 257
Vollmers, C., Schmitz, R. J., Nathanson, J. L., Yeo, G. W.-M., Ecker, J. R., & Panda, S. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.11.004 · Cited by 260
“Mapping of the sequence reads from small RNA-seq to annotated miRNAs identified 258 expressed miRNAs, including several miRNAs expressed in the mouse liver, such as miR-33, miR-122, miR-103, miR-107, miR-221, and the Let-7 family of miRNAs (Fornari et al., 2008; Frost and Olson, 2011; Jopling et al., 2005; Najafi-Shou…”
Deep sequencing of small RNAs from human skin reveals major alterations in the psoriasis miRNAome
Joyce, C. E., Zhou, X., Xia, J., Ryan, C., Thrash, B., Menter, A., Zhang, W., & Bowcock, A. M. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr331 · Cited by 240
“Likewise, miR-33, which lies in an intron of the sterolresponse-element-binding protein gene (SREBP), regulates cholesterol homeostasis (44).”
BackgroundThe carnitine system and cancer metabolic plasticity
Melone, M. A. B., Valentino, A., Margarucci, S., Galderisi, U., Giordano, A., & Peluso, G. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0313-7 · Cited by 260
MicroRNAs in Vascular and Metabolic Disease
Zampetaki, A., & Mayr, M. (2012) · Circulation Research · doi:10.1161/circresaha.111.247445 · Cited by 247
Ramirez, C. M., Dávalos, A., Goedeke, L., Salerno, A. G., Warrier, N., Cirera-Salinas, D., Suárez, Y., & Fernández-Hernando, C. (2011) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.111.232066 · Cited by 242
Microrna-27b Is a Regulatory Hub in Lipid Metabolism and Is Altered in Dyslipidemia
Vickers, K. C., Shoucri, B. M., Levin, M. G., Wu, H., Pearson, D. S., Osei-Hwedieh, D. O., Collins, F. S., Remaley, A. T., & Sethupathy, P. (2012) · Hepatology · doi:10.1002/hep.25846 · Cited by 239
The Spectrum of Achalasia: Lessons From Studies of Pathophysiology and High-Resolution Manometry
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MicroRNA-33 regulates sterol regulatory element-binding protein 1 expression in mice
Horie, T., Nishino, T., Baba, O., Kuwabara, Y., Nakao, T., Nishiga, M., Usami, S., Izuhara, M., Sowa, N., Yahagi, N., et al. (2013) · Nature Communications · doi:10.1038/ncomms3883 · Cited by 230
microRNA-33 regulates macrophage autophagy in atherosclerosis
Ouimet, M., Ediriweera, H., Afonso, M. S., Ramkhelawon, B., Singaravelu, R., Liao, X., Bandler, R. C., Rahman, K., Fisher, E. A., Rayner, K. J., et al. (2017) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.116.308916 · Cited by 221
Alsaweed, M., Hartmann, P. E., Geddes, D. T., & Kakulas, F. (2015) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph121113981 · Cited by 229
MicroRNA‐33 Deficiency Reduces the Progression of Atherosclerotic Plaque in ApoE −/− Mice
Horie, T., Baba, O., Kuwabara, Y., Chujo, Y., Watanabe, S., Kinoshita, M., Horiguchi, M., Nakamura, T., Chonabayashi, K., Hishizawa, M., et al. (2012) · Journal of the American Heart Association · doi:10.1161/jaha.112.003376 · Cited by 220
Control of Cholesterol Metabolism and Plasma High-Density Lipoprotein Levels by microRNA-144
Ramírez, C. M., Rotllan, N., Vlassov, A. V., Dávalos, A., Li, M., Goedeke, L., Aranda, J. F., Cirera-Salinas, D., Araldi, E., Salerno, A., et al. (2013) · Circulation Research · doi:10.1161/circresaha.112.300626 · Cited by 217
“We and others provided identification of a highly conserved miRNA family, miR-33a/b, within the intronic sequences of the Srebp genes in organisms ranging from Drosophila to humans.(20,21,23) The 3′UTR of Abca1 contains 3 highly conserved binding sites for miR-33a/b, and the expression of ABCA1 mRNA and protein is str…”
BackgroundRegulation of cholesterol homeostasis
Goedeke, L., & Fernandez-Hernando, C. F. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0857-5 · Cited by 232
MicroRNAs and Metabolism Crosstalk in Energy Homeostasis
Dumortier, O., Hinault, C., & OBBERGHEN, E. V. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.06.004 · Cited by 220
Zhu, Y., Yang, L., Zhang, Q., Liu, J., Li, T.-J., Yang, J., Zeng, C., & Zhuang, S. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1278 · Cited by 212
Preclinical and Clinical Development of Noncoding RNA Therapeutics for Cardiovascular Disease
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Disorders in the initial steps of steroid hormone synthesis
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Roles of microRNA on cancer cell metabolism
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MicroRNAs and lipid metabolism
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“miR-33 family of microRNAs consists of miR33a and miR-33b, which are encoded within the introns of the SREBF2 and SREBF1 genes, respectively, and are co-expressed in different stimulatory conditions [12,13,32].”
Vassiliou, E. K., & Farias‐Pereira, R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241512032 · Cited by 214
“SREBPs promote cholesterol biosynthesis, and the SREBP-2 isoform is the one associated with cholesterol metabolism in macrophages [23,24].”
BackgroundEpigenetic mechanisms in diabetic vascular complications
Reddy, M. A., & Natarajan, R. D. (2011) · Cardiovascular Research · doi:10.1093/cvr/cvr024 · Cited by 202
“inflammation, response to oxidized lipids, oxidative stress, immune function, cholesterol homeostasis, and differentiation.(109,118) –122”
BackgroundDiverse Roles of Macrophages in Atherosclerosis: From Inflammatory Biology to Biomarker Discovery
Gui, T., Shimokado, A., Sun, Y., Akasaka, T., & Muragaki, Y. (2012) · Mediators of Inflammation · doi:10.1155/2012/693083 · Cited by 209
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“Inhibition of miR-33 elevated plasma high density lipoprotein cholesterol (HDL-C) levels in both normal and high-fat-diet-fed mice [10-12].”
DNA Methylation of Lipid-Related Genes Affects Blood Lipid Levels
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MicroRNA therapeutics in cardiovascular medicine
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Metabolic and functional relevance of HDL subspecies
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Emerging role of microRNAs in lipid metabolism
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Mir-33 regulates cell proliferation and cell cycle progression
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“We and others provided the first identification of a highly conserved miRNA family, miR-33, within the intronic sequences of the Srebp genes.(20-22) Two miR-33 genes are present in humans: miR-33b, which is encoded within intron 17 of the Srebp-1 gene on chromosome 17, and miR-33a, which is expressed in intron 16 of t…”
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“miR-33a, miR-33b Regulate fatty acids, triglyceride, and cholesterol homeostasis, cooperate with the SREBP2 to upregulate intracellular cholesterol levels, have a crucial role in the posttranscriptional repression of ABCA1, which promotes the efflux of free cholesterol from within the cell to ApoA1 and is essential fo…”
BackgroundMicroRNAs and cardiovascular diseases
Ono, K., Kuwabara, Y., & Han, J. (2011) · The FEBS Journal · doi:10.1111/j.1742-4658.2011.08090.x · Cited by 169
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“In addition to its pivotal role in RCT in the liver, human SR-BI is expressed in cultured macrophages and atherosclerotic lesions (19).”
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“…that combines statins and anti-miR-33 oligonucleotides may be useful in hyperlipidemic patients by reversing statin-induced, miR-33-mediated repression of ABCA1, which ultimately would increase plasma HDL (Horie et al, 2010; Marquart et al, 2010; Najafi-Shoushtari et al, 2010; Rayner et al, 2010).”
InfluentialThe Role of the ATP-Binding Cassette A1 (ABCA1) in Human Disease
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“The physiological relevance of miR-33 targeting of ABCA1 was initially demonstrated using miR-33 inhibitors, which caused a two-fold increase of cholesterol efflux from hepatocytes to ApoA-I in vitro [47] and a 30% increase of plasma HDL-C levels in mice [48].”
BackgroundThe intricate balance between microRNA‐induced mRNA decay and translational repression
Naeli, P., Winter, T., Hackett, A. P., Alboushi, L., & Jafarnejad, S. M. (2022) · FEBS Journal · doi:10.1111/febs.16422 · Cited by 175
“Hence, the expression and activity of miRNAs are interlinked with various cellular processes including development, maintenance of homeostasis, and diseases such as cancer and metabolic disorders [5-7].”
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“Cholesterol/oxysterols might also repress miR33a levels to increase CYP7A1 expression as well as cholesterol efflux transporters.(9) Figure 6 shows a proposed mechanism for the regulation of cholesterol homeostasis by a CYP7A1/SREBP2/miR-33a axis, based on this study, and the well-recognized mechanism for maintaining…”
BackgroundInfluentialDifferential Expression of MicroRNAs in Different Disease States
Abdellatif, M. (2012) · Circulation Research · doi:10.1161/circresaha.111.247437 · Cited by 154
Role of Cholesterol and Lipid Rafts in Cancer Signaling: A Promising Therapeutic Opportunity?
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Cholesterol metabolism in Huntington disease
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Metadata
- Authors
- Najafi-Shoushtari, S. H., Kristo, F., Li, Y., Shioda, T., Cohen, D. E., Gerszten, R. E., & Näär, A. M.
- Affiliations
- Harvard University (US)
- Massachusetts General Hospital (US)
- Brigham and Women's Hospital (US)
- Corresponding author
- Näär, Anders M.
- ORCID
- Venue
- Science
- Published
- 2010-06-18
- Volume
- 328
- Issue
- 5985
- Pages
- 1566-1569
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC3840500
- OpenAlex
- W2102901373
- Semantic Scholar
- 8e1f87e5a8c468d11cb938b52c20c8e6954402ce
- Cited by
- 957
- References
- 31
- Citations by year
- 2026: 20 · 2025: 30 · 2024: 24 · 2023: 47 · 2022: 41 · 2021: 56 · 2020: 50 · 2019: 65 · 2018: 66 · 2017: 59 · 2016: 86 · 2015: 88 · 2014: 85 · 2013: 92 · 2012: 73
- FWCI
- 80.88
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of General Medical Sciences (R01GM071449)
- National Institute of Diabetes and Digestive and Kidney Diseases (R21DK084459, R01 DK48873, P30-DK34854, R01DK056626, R01 DK56626, R37DK048873, P30DK034854, R01DK048873)
- 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
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipoproteins and Cardiovascular Health
- Keywords
- miR-33, cholesterol homeostasis, ABCA1, reverse cholesterol transport, HDL synthesis, cholesterol efflux, post-transcriptional regulation, antisense oligonucleotides, locked nucleic acid, cholesterol biosynthesis, cardiometabolic disease
- MeSH terms
- Animals, Cell Line, Cholesterol, Diet, Gene Expression Regulation, Homeostasis, Humans, Introns, Cholesterol, HDL, Liver, Macrophages, Mice, Inbred C57BL, Up-Regulation, Oligonucleotides, Antisense, ATP-Binding Cassette Transporters, 3' Untranslated Regions, RNA Interference, MicroRNAs, Mice, Sterol Regulatory Element Binding Proteins, Sterol Regulatory Element Binding Protein 1, Sterol Regulatory Element Binding Protein 2, ATP Binding Cassette Transporter 1
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