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Control of Cholesterol Metabolism and Plasma High-Density Lipoprotein Levels by microRNA-144
Open accessAbstract
Rationale: Foam cell formation because of excessive accumulation of cholesterol by macrophages is a pathological hallmark of atherosclerosis, the major cause of morbidity and mortality in Western societies. Liver X nuclear receptors (LXRs) regulate the expression of the adenosine triphosphate–binding cassette (ABC) transporters, including adenosine triphosphate–binding cassette transporter A1 (ABCA1) and adenosine triphosphate–binding cassette transporter G1 (ABCG1). ABCA1 and ABCG1 facilitate the efflux of cholesterol from macrophages and regulate high-density lipoprotein (HDL) biogenesis. Increasing evidence supports the role of microRNA (miRNAs) in regulating cholesterol metabolism through ABC transporters. Objective: We aimed to identify novel miRNAs that regulate cholesterol metabolism in macrophages stimulated with LXR agonists. Methods and Results: To map the miRNA expression signature of macrophages stimulated with LXR agonists, we performed an miRNA profiling microarray analysis in primary mouse peritoneal macrophages stimulated with LXR ligands. We report that LXR ligands increase miR-144 expression in macrophages and mouse livers. Overexpression of miR-144 reduces ABCA1 expression and attenuates cholesterol efflux to apolipoproteinA1 in macrophages. Delivery of miR-144 oligonucleotides to mice attenuates ABCA1 expression in the liver, reducing HDL levels. Conversely, silencing of miR-144 in mice increases the expression of ABCA1 and plasma HDL levels. Thus, miR-144 seems to regulate both macrophage cholesterol efflux and HDL biogenesis in the liver. Conclusions: miR-144 regulates cholesterol metabolism via suppressing ABCA1 expression and modulation of miRNAs may represent a potential therapeutical intervention for treating dyslipidemia and atherosclerotic vascular disease.
Overview
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Written from the paper’s full text.
TL;DR
miR-144 is induced by LXR ligands in macrophages and liver and directly represses ABCA1, reducing macrophage cholesterol efflux and hepatic HDL biogenesis. In mice, miR-144 overexpression lowers plasma HDL, whereas miR-144 inhibition raises ABCA1 and HDL, suggesting anti-miR-144 as a possible dyslipidemia/atherosclerosis strategy.
Key findings
- An unbiased miRNA microarray in T090-treated mouse peritoneal macrophages identified 32 differentially regulated miRNAs; miR-144 was predicted to target lipid-metabolism genes and had 7 potential binding sites in the ABCA1 3′UTR.
- miR-144 overexpression reduced ABCA1 mRNA/protein and attenuated cholesterol efflux to ApoA1 in macrophages; anti-miR-144 increased ABCA1 and efflux. In vivo, miR-144 mimic delivery produced a 250-fold increase in liver miR-144, reduced liver ABCA1, and significantly lowered total and HDL cholesterol without changing TG or other lipoprotein distributions.
- miR-144 inhibition reduced miR-144 levels and increased liver ABCA1 protein; after T090, miR-144 was induced 2.3-fold and inhibited 2.1-fold by anti-miR-144, with increased plasma HDL cholesterol.
- miR-33 and miR-144 co-transfection reduced Abca1 3′UTR luciferase activity by 60%, compared with 30–40% suppression by either miRNA alone, suggesting additive regulation of ABCA1.
Methods
- Primary mouse peritoneal macrophages were stimulated with 3 μmol/L T090 for 24 h and profiled by Illumina miRNA microarrays; differential expression used unpaired t-test with p<0.2 and fold change ≥1.5, without multiple-testing correction.
- In vitro studies used miR-144 mimics/inhibitors in mouse peritoneal macrophages, J774, THP-1, HepG2, Huh-7, Hepa, and EAhy926 cells; ABCA1/ABCG1 expression, 3′UTR luciferase reporters, and 3H-cholesterol efflux to ApoA1 were measured.
- In vivo, 8-week-old male C57BL/6 mice were randomized into 4 groups (n=24 total; n=6/group) and injected intravenously twice every three days with control or miR-144 mimic/inhibitor at 7 mg/kg; some mice also received T090 (10 mg/kg) by oral gavage. Plasma lipids and FPLC lipoprotein fractions were analyzed.
Limitations
- The paper states that detailed methods are in the supplemental material due to space limits, and that whether LXR regulates pri-miR-144/451 by direct promoter interaction remains unanswered; further experiments are warranted to understand transcriptional regulation.
- The paper notes that the lack of further cholesterol-efflux reduction with combined miR-33/miR-144 may reflect the very low 5 nM mimic dose and T090-induced endogenous miR-144 in hepatic cells but not in COS-7 cells used for 3′UTR assays.
- Evident from the text: the microarray screen used a relaxed p<0.2 threshold with no multiple-testing correction, in vivo groups were small (n=6), and the study reports lipid/HDL endpoints rather than atherosclerosis outcomes.
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Claims the paper makes
46 Own result · 15 Own interpretation · 6 Own method · 1 No full text of the sources · 1 Not checked yet
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Delivery of miR-144 oligonucleotides to mice attenuates ABCA1 expression in the liver, reducing HDL levels.”
- Also stated in: § INTRODUCTION · plain
“in vivo delivery of miR-144 to mice represses ABCA1 expression in the liver, reducing circulating HDL levels.”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > Abstract > Methods and Results
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
- Also stated in: § INTRODUCTION · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In contrast to ABCA1, ABCG1 expression was slightly reduced in miR-144 over-expressing macrophages.”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 regulates ABCA1 expression in macrophages and hepatic cells
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Moreover ABCG1 was also down-regulated at the mRNA level in macrophages transfected with miR-144 (Figure 3A, right panel).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 regulates ABCA1 expression in macrophages and hepatic cells
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Transfection of mouse peritoneal macrophages with miR-144 increased its expression 350-fold (not shown) and significantly inhibited ABCA1 mRNA levels (Figure 3A, left panel).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 regulates ABCA1 expression in macrophages and hepatic cells
plaindirect- Asserted: passes — The authors put it forward as true.
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- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Interestingly, hepatic miR-144 levels are regulated by high fat diet in vivo (Online Figure IIIC, right panel).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 is up-regulated in LXR-activated macrophages and in the liver of mice fed with high fat diet
plaindirect- Asserted: passes — The authors put it forward as true.
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- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“We report that LXR ligands increase miR-144 expression in macrophages and mouse livers.”
- Also stated in: § miR-144 is up-regulated in LXR-activated macrophages and in the liver of mice fed with high fat diet · plain
“mouse peritoneal macrophages, human monocytes (THP-1) and human hepatic (Huh-7) cells treated with T090 showed an increased expression of miR-144.”
- Also stated in: § miR-144 is up-regulated in LXR-activated macrophages and in the liver of mice fed with high fat diet · boosted
“Collectively, these data demonstrated that treatment of macrophages and hepatic cells with a LXR agonist resulted in higher expression of miR-144.”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > Abstract > Methods and Results
boosteddirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
- Also stated in: § miR-144 is up-regulated in LXR-activated macrophages and in the liver of mice fed with high fat diet · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Overexpression of miR-144 reduces ABCA1 expression and attenuates cholesterol efflux to ApoA1 in macrophages.”
- Also stated in: § INTRODUCTION · plain
“miR-144 over-expression inhibits ABCA1 expression in different cell lines including hepatocytes and monocyte/macrophages, thereby attenuating cholesterol efflux to apolipoprotein A1 (ApoA1).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > Abstract > Methods and Results
plaindirect- Asserted: passes — The authors put it forward as true.
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- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
- Also stated in: § INTRODUCTION · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“after cholesterol loading with acetylated low-density lipoproteins (Ac-LDL) in mouse peritoneal macrophages (Online Figure IIB).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 is up-regulated in LXR-activated macrophages and in the liver of mice fed with high fat diet
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Finally, we also found that the miR-144/451 promoter activity was induced in Huh-7 cells treated with T090 (Figure 2E).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 is up-regulated in LXR-activated macrophages and in the liver of mice fed with high fat diet
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Overexpression of miR-144 reduces ABCA1 expression and attenuates cholesterol efflux to ApoA1 in macrophages.”
- Also stated in: § miR-144 regulates ABCA1 expression in macrophages and hepatic cells · plain
“Transfection of mouse peritoneal macrophages with miR-144 increased its expression 350-fold (not shown) and significantly inhibited ABCA1 mRNA levels (Figure 3A, left panel).”
- Also stated in: § miR-144 regulates ABCA1 expression in macrophages and hepatic cells · boosted
“Transfection of mouse peritoneal macrophages with miR-144 mimics but not a control miRNA (Con-miR) strongly decreased the stimulation of ABCA1 (Figure 3B, left panel).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > Abstract > Methods and Results
boosteddirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
- Also stated in: § miR-144 regulates ABCA1 expression in macrophages and hepatic cells · plain
- It may state two separate claims as one. 14
- Probably not a substantial claim. 8
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“miR-144 was widely expressed in mouse tissues and is particularly abundant in the liver, spleen and aorta (Online Figure IIIA).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 is up-regulated in LXR-activated macrophages and in the liver of mice fed with high fat diet
plain- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Co-transfection of miR-33 and miR-144 resulted in a 60% decrease in luciferase activity whereas miR-144 or miR-33 alone suppressed the 3’UTR activity 30-40% (Figure 4B).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-33 and miR-144 have an additive effect on ABCA1 protein expression
plaindirect- Asserted: passes — The authors put it forward as true.
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- Load-bearing: passes — The paper’s conclusions depend on it.
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It may state two separate claims as one.
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In the paper
“miR-33 and miR-144 inhibited cholesterol efflux but the combination of both miRNAs do not further reduced the cholesterol export in this human hepatic cell line (Figure 4C).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-33 and miR-144 have an additive effect on ABCA1 protein expression
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“As expected plasma TG levels were slightly increased after T090 treatment but no differences were not affected by anti-miR-144 treatment (Figure 7D, right panel).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 expression regulates cellular cholesterol efflux and HDL levels in vivo
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Importantly, antagonism of endogenous miR-144 increased ABCA1 expression (Figure 5B, upper panel) and cellular cholesterol efflux to ApoA1 (Figure 5B, bottom panel).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 expression regulates cellular cholesterol efflux and HDL levels in vivo
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The inhibition of ABCA1 expression after 6 days of treatment with miR-144 particles leads to a significant reduction in total cholesterol and HDL cholesterol levels without changes in TG or cholesterol distribution in other lipoproteins (Figure 6C and D).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 expression regulates cellular cholesterol efflux and HDL levels in vivo
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“As expected, miR-144 over-expression inhibited ABCA1 expression (Figure 5A, upper panel) and attenuated cholesterol efflux to ApoA1 (Figure 5A, bottom panel).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 expression regulates cellular cholesterol efflux and HDL levels in vivo
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The data show that miR-144 inhibition in basal conditions resulted in a significant reduction of miR-144 levels (Figure 7A) and an increase of liver ABCA1 protein expression without changes at the mRNA level (Figure 7B and C upper panel).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 expression regulates cellular cholesterol efflux and HDL levels in vivo
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“As seen in Online Figure VIA, inhibition of miR-144 does not alter miR-33 levels and miR-33 inhibition does not change miR-144 expression.”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-33 and miR-144 have an additive effect on ABCA1 protein expression
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Under this condition, miR-144 was induced 2.3-fold and inhibited 2.1-fold after the injection of anti-miR-144 oligonucleotides (Figure 7A).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 expression regulates cellular cholesterol efflux and HDL levels in vivo
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Thus, miR-144 appears to regulate both macrophage cholesterol efflux and HDL biogenesis in the liver.”
- Also stated in: § INTRODUCTION · hedged
“Thus, miR-144 appears to regulate both macrophage cholesterol efflux and HDL biogenesis in the liver.”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > Abstract > Methods and Results
hedgedconditional- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
- Also stated in: § INTRODUCTION · hedged
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“The 1.5-fold-change threshold was chosen on the basis of its use in previously published articles employing these particular types of microarrays.”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > METHODS > miRNA microarray analysis
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
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In the paper
“Quadruplicates for each condition were used for microarray analysis.”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > METHODS > miRNA microarray analysis
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“The expression of both ABCA1 and ABCG1 are up-regulated in states of cholesterol excess by LXR 9.”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > INTRODUCTION
What the sources say
- Not checked — no full text of the sourcecites [9] Venkateswaran A Laffitte BA Joseph SB Mak PA Wilpitz DC Edwards PA Tontonoz P Control of cellular cholesterol efflux by the nuclear oxysterol receptor lxr alpha Proc Natl Acad Sci U S A 2000 97 12097 12102 11035776 PMC17300 source
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Eight-week-old male C57BL/6 mice were randomized into 4 groups (n= 24 mice): non-targeting control mimic (Con-mir, n=6), miR-144-mimic (miR-144, n=6), inhibitor negative control sequence (Con-inh, n=6) and miR-144-inhibitors (Inh-miR-144).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > METHODS > Animals
plainn = 24- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Altogether, these results establish that miR-144 overexpression or inhibition reduces and increases circulating HDL, respectively.”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-144 expression regulates cellular cholesterol efflux and HDL levels in vivo
boosteddirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“The purity and integrity of both the total RNA sample and the enriched miRNA was verified using the Agilent Bioanalyzer (Agilent Technologies, Santa Clara, CA).”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > METHODS > miRNA microarray analysis
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
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In the paper
“We have previously reported that miR-33, an intronic miRNA encoded in the Srebp genes, regulates ABCA1 expression.”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > RESULTS > miR-33 and miR-144 have an additive effect on ABCA1 protein expression
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Verification of miR-144 over-expression and knockdown was determined using qPCR, as described above.”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > METHODS > miR-144 mimic and anti-miR-144 transfection
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim.
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In the paper
“All experimental control samples were treated with an equal concentration of a non-targeting control mimic sequence (Con-miR) or inhibitor negative control sequence (Con-inh), for use as controls for non-sequence-specific effects in miRNA experiments.”
§ Control of Cholesterol Metabolism and Plasma HDL Levels by miRNA-144 > METHODS > miR-144 mimic and anti-miR-144 transfection
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim.
The paper relies on this without support.
ABCA1 and ABCG1 facilitate cholesterol efflux from macrophages and regulate HDL biogenesis.
“ABCA1 and ABCG1 facilitate the efflux of cholesterol from macrophages and regulate high-density lipoprotein (HDL) biogenesis.”
“Several ABC transporters, including ABCA1 and ABCG1, facilitate the efflux of cholesterol from macrophages.”
The paper relies on this without support.
In the liver, ABCA1 plays a critical role in HDL biogenesis and its deficiency leads to a dramatic reduction of plasma HDL levels.
“In the liver, ABCA1 also plays a critical role in the biogenesis of HDL and its deficiency leads to a dramatic reduction of plasma HDL levels.”
The paper relies on this without support.
ABCA1 plays a critical role in regulating cellular cholesterol efflux to ApoA1.
“ABCA1 plays a critical role in regulating cellular cholesterol efflux to ApoA1.”
The paper relies on this without support.
ABCA1 plays a key role in regulating HDL biogenesis in the liver.
“In addition to regulating cellular cholesterol efflux, ABCA1 plays a key role in regulating HDL biogenesis in the liver.”
The paper relies on this without support.
Hepatic ABCA1 is critical for the generation of plasma HDL.
“Finally, because hepatic ABCA1 is critical for the generation of plasma HDL, it seems likely that a combination therapy that includes both miR-144 and miR-33 antisense oligonucleotides might result in increased HDL levels, thus improving the prognosis for patients with cardiovascular disease.”
Citations
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“Macrophages cannot limit the uptake of cholesterol and, therefore, depend on cholesterol efflux pathways for preventing their transformation into foam cells.(1,2) Several ABC transporters, including adenosine triphosphate–binding cassette transporter A1 (ABCA1) and adenosine triphosphate– binding cassette transporter…”
BackgroundmiR-122 regulation of lipid metabolism revealed by in vivo antisense targeting
Esau, C., Davis, S., Murray, S. F., Yu, X. X., Pandey, S. K., Pear, M., Watts, L., Booten, S. L., Graham, M., McKay, R., et al. (2006) · Cell Metabolism · doi:10.1016/j.cmet.2006.01.005 · Cited by 2,082 · cited 2×
“Interestingly some of the miRNAs induced by T090, including miR-370 and miR-122, were previously identified as important regulators of lipid metabolism.(15,16,18,28) To determine the potential candidates involved in regulating cholesterol metabolism, we analyzed the predicted target genes using a combination of bioinf…”
BackgroundMethodMutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency
Brooks-Wilson, A., Marcil, M., Clee, S. M., Zhang, L.-H., Roomp, K., van Dam, M., Yu, L., Brewer, C., Collins, J. A., Molhuizen, H. O. F., et al. (1999) · Nature Genetics · doi:10.1038/11905 · Cited by 1,687
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Macrophage miRNAs in atherosclerosis
Karunakaran, D., & Rayner, K. J. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2016.02.006 · Cited by 29
Dietary lipids modulate the expression of miR‐107, a miRNA that regulates the circadian system
Daimiel, L., Klett‐Mingo, M., Konstantinidou, V., Micó, V., Aranda, J. F., García, B., Martı́nez-Botas, J., Dávalos, A., Fernandez-Hernando, C. F., & Ordovás, J. M. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201570094 · Cited by 30
Self-citationCoenzyme Q10 Increases Cholesterol Efflux and Inhibits Atherosclerosis Through MicroRNAs
Allen, R. M., & Vickers, K. C. (2014) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.114.303741 · Cited by 29
Analysis of miRNAs and their target genes associated with lipid metabolism in duck liver
He, J., Wang, W., Lu, L., Tian, Y., Niu, D., Ren, J., Dong, L., Sun, S., Zhao, Y., Chen, L., et al. (2016) · Scientific Reports · doi:10.1038/srep27418 · Cited by 27
Xing, K., Zhao, X., Ao, H., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-53377-x · Cited by 26
MicroRNAs in Cardiovascular Health: From Order to Disorder
Karunakaran, D., & Rayner, K. J. (2013) · Endocrinology · doi:10.1210/en.2013-1299 · Cited by 26
“(cholesterol synthesis pathways) Liver LDL, HDL 28–30 miR-27b Angptl3, Gpam Hepatocytes HDL, triglycerides 31 Hormones (eg, estrogen) miR-16, miR-125a ER gene targets Breast cancer Estrogen-responsive gene changes 39 miR-203a Abl1, p63 Vascular SMCs SMC proliferation 40 Insulin resistance and obesity miR-375 NF B, PDK…”
BackgroundInfluentialHong, X., Chen, R., Yuan, L., & Zha, J. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.08.305 · Cited by 25
Sud, N., Taher, J., & Su, Q. (2015) · Drug Development Research · doi:10.1002/ddr.21269 · Cited by 25
“These regulate cholesterol efflux and are upregulated in states of cholesterol excess [Ramirez et al., 2013].”
BackgroundInfluentialBian, Y., Qian, W., Li, H., et al. (2015) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2015.2273 · Cited by 24
MicroRNAs in Ischemic Heart Disease
Lima, J., Batty, J. A., Sinclair, H., & Kunadian, V. (2016) · Cardiology in Review · doi:10.1097/crd.0000000000000114 · Cited by 24
Role of miRNA in the Regulatory Mechanisms of Estrogens in Cardiovascular Ageing
Pérez‐Cremades, D., Mompeón, A., Vidal‐Gómez, X., Hermenegildo, C., & Novella, S. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/6082387 · Cited by 29
“Furthermore, induced LXR and ABCA1 expression has been related to an estradiol-dependent reduction of lipid accumulation in macrophages and VSMCs [58, 59] suggesting that estrogen tightly regulates lipid content via this miRNA-mediated pathway.”
BackgroundThe Role of MicroRNAs in Hyperlipidemia: From Pathogenesis to Therapeutical Application
Xiang, Y., Li, M., Zuo, M., Song, G., Tan, L.-M., & Yang, Z. (2022) · Mediators of Inflammation · doi:10.1155/2022/3101900 · Cited by 24
Self-citationPotential Therapeutic Agents That Target ATP Binding Cassette A1 (ABCA1) Gene Expression
Haas, M. J., & Mooradian, A. D. (2022) · Drugs · doi:10.1007/s40265-022-01743-x · Cited by 23
Zaiou, M., & Bakillah, A. (2018) · Diseases · doi:10.3390/diseases6020034 · Cited by 22
“Moreover, the activation of LXR has been associated with an increase in miR-144 and ABCA1 expression to fine-tune RCT by macrophages [11].”
BackgroundFrutos, M. F.-D., Pardo, V., Torrecilla-Parra, M., Rada, P., Pérez-García, A., Martín-Martín, Y., de la Peña, G., Gómez, A., Toledano‐Zaragoza, A., Gómez‐Coronado, D., et al. (2023) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2023.194938 · Cited by 21
Self-citationMoeez, S., Riaz, S. K., Masood, N., Kanwal, N., Arif, M. A., Niazi, R., & Khalid, S. (2018) · Canadian Journal of Diabetes · doi:10.1016/j.jcjd.2018.07.001 · Cited by 20
Lightbody, R. J., Taylor, J. M. W., Dempsie, Y., & Graham, A. (2020) · World Journal of Cardiology · doi:10.4330/wjc.v12.i7.303 · Cited by 20
Implications for MicroRNA involvement in the prognosis and treatment of atherosclerosis
Tabaei, S., & Tabaee, S. S. (2021) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-020-03992-4 · Cited by 21
“Various miRNAs such as miR-758 [34], miR-302a [35], miR-301b [36], miR148a [36], miR-130b [36], miR-128-1 [36], miR-26 [37], miR-106 [38], miR-33 [39–41], and miR-144 [42, 43] regulate the cholesterol efflux in macrophage through ABCA1 and, thereby, promote formation of macrophage foam cells.”
Non-coding RNA crosstalk with nuclear receptors in liver disease
Wu, J., Nagy, L. E., Liangpunsakul, S., & Wang, L. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2021.166083 · Cited by 20
Vickers, K. C., & Moore, K. J. (2013) · Circulation Research · doi:10.1161/circresaha.113.302732 · Cited by 20
Qiao, X., Zheng, T., Xie, Y., yao, X., Yuan, Z., Wu, Y., Zhou, D., & Chen, T. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04140-4 · Cited by 23
“This will reduce the outflow of cholesterol to apolipoprotein A1 (ApoA1) mediated by the ABCA1/G1 of hepatocytes and macrophages, promoting inflammatory activation and atherosclerosis [45].”
BackgroundmiR-28-5p Involved in LXR-ABCA1 Pathway is Increased in the Plasma of Unstable Angina Patients.
Liu, J., Liu, Y., Sun, Y.-N., Li, S., Liu, X.-Q., Li, J., Li, C.-M., Tian, W., Zhou, Y.-T., & Shang, X.-M. (2015) · Heart, Lung and Circulation · doi:10.1016/j.hlc.2014.12.160 · Cited by 19
Fan, A., Wang, Q., Yuan, Y., Cheng, J.-L., Chen, L., Guo, X., Li, Q., Chen, B., Huang, X., & Huang, Q. (2015) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00102.2015 · Cited by 19
Advances in miRNA research: Unraveling the complexities of gene regulation
Zheng, J., Zhang, G., & Ren, L. (2025) · Animal Models and Experimental Medicine · doi:10.1002/ame2.70076 · Cited by 23
“104 Additionally, miR-144 has been shown to con-trol cholesterol metabolism and plasma high-density lipoprotein levels, 105,106 indicating its role in lipolysis regulation.”
Harnessing the Therapeutic Potential of MicroRNAs for Cardiovascular Disease
Calway, T., & Kim, G. H. (2014) · Journal of Cardiovascular Pharmacology and Therapeutics · doi:10.1177/1074248414552902 · Cited by 17
“ABCA1 is also targeted by miR-144, which was shown to lower HDL cholesterol levels when administered as an miRNA mimic.(59) Lovren et al found that miR-145 treatment via a lentiviral vector directed toward smooth muscle cells reduced plaque size in aortic sinuses, ascending aortas, and brachiocephalic arteries and inc…”
BackgroundmiRNAs and High-Density Lipoprotein metabolism
Baldán, Á., & Vallim, T. Q. D. A. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2016.01.021 · Cited by 18
Chen, Q., Wang, S., Bao, R., Wang, D., Wu, Y., Zhang, Y., Liu, M., & Wang, T. (2024) · Chinese Medicine · doi:10.1186/s13020-023-00876-9 · Cited by 16
“Synthetic liver X receptor (LXR) agonists, such as T0901317 (T0) and GW3965, are effective regulators for AS therapy in animal models and clinical trials, due to upregulating expression of ABCA1 and ABCG1 [9].”
BackgroundExploring the Genetic Association between Obesity and Serum Lipid Levels Using Bivariate Methods
Ke, J., Gao, W., Wang, B., Cao, W., Lv, J., Yu, C., Huang, T., Sun, D., Liao, C., Pang, Y., et al. (2022) · Twin Research and Human Genetics · doi:10.1017/thg.2022.39 · Cited by 16
Inflammation related miRNAs as an important player between obesity and cancers
Gholami, M., Larijani, B. A., Zahedi, Z., Mahmoudian, F., Bahrami, S., Omran, S. P., Saadatian, Z., Hasani‐Ranjbar, S., Taslimi, R., Bastami, M., et al. (2019) · Journal of Diabetes & Metabolic Disorders · doi:10.1007/s40200-019-00459-2 · Cited by 16
From Endothelium to Lipids, Through microRNAs and PCSK9: A Fascinating Travel Across Atherosclerosis
D’Ardes, D., Santilli, F., Guagnano, M. T., Bucci, M., & Cipollone, F. (2020) · High Blood Pressure & Cardiovascular Prevention · doi:10.1007/s40292-019-00356-y · Cited by 17
MicroRNA: a connecting road between apoptosis and cholesterol metabolism
Adlakha, Y. K., & Saini, N. (2016) · Tumor Biology · doi:10.1007/s13277-016-4988-z · Cited by 16
Yang, C., Lv, K., Chen, B., Yang, Y., Ai, X., Yu, H., Yang, Y., Yi, B., & Lu, K. (2018) · Experimental Cell Research · doi:10.1016/j.yexcr.2018.02.009 · Cited by 16
Emerging roles of microRNAs in the metabolic control of immune cells
Yao, Q., Song, Z., Wang, B., & Zhang, J. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.06.024 · Cited by 17
Chalcone Derivatives Enhance ATP-Binding Cassette Transporters A1 in Human THP-1 Macrophages
Teng, I.-J., Tsai, M., Shih, S.-F., Tsuei, B.-F., Chang, H. W., Chuang, Y., Lin, C., Chern, C., & Chen, S. (2018) · Molecules · doi:10.3390/molecules23071620 · Cited by 15
Ablation of miR-144 increases vimentin expression and atherosclerotic plaque formation
He, Q., Wang, F., Honda, T., Greis, K. D., & Redington, A. N. (2020) · Scientific Reports · doi:10.1038/s41598-020-63335-7 · Cited by 14
New Insights on the Regulation of the Insulin-Degrading Enzyme: Role of microRNAs and RBPs
Martín-Martín, Y., Pérez-García, A., Torrecilla-Parra, M., Frutos, M. F.-D., Pardo, V., Casarejos, M. J., Busto, R., & Ramírez, C. M. (2022) · Cells · doi:10.3390/cells11162538 · Cited by 13
Self-citationVladimirov, S. S., Tomasevic, M., Popov, N., Munjas, J., de Gonzalo‐Calvo, D., & Sopić, M. (2025) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2025.06.005 · Cited by 14
Liu, J., Liu, X.-Q., Liu, Y., Sun, Y.-N., Li, S., Li, C.-M., Li, J., Tian, W., Shang, X.-M., & Zhou, Y.-T. (2016) · Molecular Medicine Reports · doi:10.3892/mmr.2015.4563 · Cited by 12
Mohammadi, A., Fallah, H., Shahouzehi, B., & Najafipour, H. (2017) · Europe PMC (PubMed Central) · Cited by 13
MicroRNA sensing and regulating microbiota-host crosstalk via diet motivation
Fan, Y., Qin, M., Zhu, J., Chen, X., Luo, J., Chen, T., Sun, J., Zhang, Y., & Xi, Q. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2139220 · Cited by 12
Rotllán, N., Zhang, X., Canfrán‐Duque, A., Goedeke, L., Griñán, R., Ramírez, C. M., Suárez, Y., & Fernandez-Hernando, C. F. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113419 · Cited by 14
Self-citationThe pleiotropic effects of high-density lipoproteins and apolipoprotein A-I
Thomas, S. R., Zhang, Y., & Rye, K. (2022) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2022.101689 · Cited by 12
Desgagné, V., Guérin, R., Guay, S., Boyer, M., Hutchins, E. D., Picard, S., Maréchal, A., Corbin, F., Keuren‐Jensen, K. R. V., Arsenault, B. J., et al. (2019) · Epigenomics · doi:10.2217/epi-2018-0161 · Cited by 12
Unlocking the Door to New Therapies in Cardiovascular Disease: MicroRNAs Hold the Key
Nguyen, M.-A., Karunakaran, D., & Rayner, K. J. (2014) · Current Cardiology Reports · doi:10.1007/s11886-014-0539-7 · Cited by 12
Liver X receptor: from metabolism to cancer
Venteclef, N., & Ferré, P. (2014) · Biochemical Journal · doi:10.1042/bj20140211 · Cited by 11
The Link between miRNAs and PCKS9 in Atherosclerosis
Mačvanin, M., Gluvic, Z. M., Klisic, A. N., Manojlovic, M. S., Suri, J. S., Rizzo, M., & Isenović, E. R. (2023) · Current Medicinal Chemistry · doi:10.2174/0109298673262124231102042914 · Cited by 13
Endo, Y., Sasaki, K., & Ikewaki, K. (2025) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat.rv22042 · Cited by 13
“Similarly, miR-144 has been identified as a novel regulator that targets ABCA1 and modulates cholesterol efflux 39) .”
Dlouhá, D., Bláha, M., Huckova, P., Lánská, V., Hubáček, J., & Bláha, V. (2023) · Genes · doi:10.3390/genes14081571 · Cited by 10
Investigational therapies for the treatment of atherosclerosis
TOMKIN, G. H., & Owens, D. (2014) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.2014.922950 · Cited by 10
“[46] have recently demonstrated that MiRNA-144 can regulate cholesterol metabolism by suppressing ABCA1 expression and conversely, silencing of miR-144 in mice increased ABCA1 expression and increased HDL, perhaps a future therapy for atherosclerosis.”
BackgroundAntisense Oligonucleotides, microRNAs, and Antibodies
Dávalos, A., & Chroni, A. (2014) · Handbook of experimental pharmacology · doi:10.1007/978-3-319-09665-0_22 · Cited by 10
“2013) or mirVana inhibitors (7 mg/kg) coupled with In vivo fectamine (Invitrogen) for intravenous injections twice every 3 days (Ramirez et al. 2013) increased both hepatic ABCA1 protein expression and HDL-C levels in mice.”
BackgroundInfluentialSelf-citationTorres-Paz, Y., Gamboa, R., Fuentevilla-Álvarez, G., Cardoso-Saldaña, G., Martínez-Alvarado, R., Soto, M. E., & Huesca-Gómez, C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25168605 · Cited by 7
Nishi, H., & Fisher, E. A. (2015) · Circulation Research · doi:10.1161/circresaha.115.305467 · Cited by 7
“studies in Huh7 cells, it was then shown that miR-223 (1) in-”
BackgroundTruths and controversies concerning the role of miRNAs in atherosclerosis and lipid metabolism
Baldán, Á., & Fernandez-Hernando, C. F. (2016) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000358 · Cited by 9
“Two independent reports have identified miR-144 as a regulator of ABCA1 expression in monocyte/macrophages and liver [32,35].”
Zhang, Y., Zhan, Y., Liu, D., & Yu, B. (2019) · Drug Delivery · doi:10.1080/10717544.2019.1628117 · Cited by 9
“MicroRNAs (miRNAs) are small and noncoding RNAs which post-transcriptionally modulate gene expression, and they also play a role in keeping normal cellular functions (NajafiShoushtari et al., 2010; Ramirez et al., 2013).”
BackgroundNuclear Receptors and microRNA-144 Coordinately Regulate Cholesterol Efflux
Vickers, K. C., & Rader, D. J. (2013) · Circulation Research · doi:10.1161/circresaha.113.301422 · Cited by 9
“mice; however, HDL-C levels were found to be significantly elevated in both LXR-agonist–treated and untreated mice.(27) The study of de Aguiar Vallim et al(26) was consistent with this observation, as inhibition of miR-144 in mice only affected”
BackgroundResultInfluentialIntegrative Analysis of miRNAs Involved in Fat Deposition in Different Pig Breeds
Zhang, X., Huang, W., Guo, J., & Miao, X. (2022) · Genes · doi:10.3390/genes14010094 · Cited by 8
Non-coding RNAs in lipid metabolism and their roles in atherosclerosis
Sallam, T., Solingen, C. V., & Moore, K. J. (2026) · Nature Reviews Cardiology · doi:10.1038/s41569-025-01229-9 · Cited by 8
Gonçalves, B. D. S., Meadows, A., Pereira, D. G., Puri, R., & Pillai, S. S. (2023) · Biomedicines · doi:10.3390/biomedicines11061597 · Cited by 10
MiR‐144 affects fatty acid composition by regulating ELOVL6 expression in duck hepatocytes
He, J., Tian, Y., Zhao, Y., Liu, Y., Tao, Z., Li, G., Niu, D., Lu, L., & Lu, Y. (2017) · Cell Biology International · doi:10.1002/cbin.10753 · Cited by 9
“In lipid metabolism, miR-144 was found to control cholesterol metabolism and plasma highdensity lipoprotein levels (Ramirez et al., 2013).”
BackgroundHuesca‐Gómez, C., Torres-Paz, Y. E., Martínez-Alvarado, M. R., Fuentevilla-Álvarez, G., del Valle‐Mondragón, L., Torres‐Tamayo, M., Soto, M. E., & Gamboa, R. (2019) · Molecular Biology Reports · doi:10.1007/s11033-019-05229-0 · Cited by 8
Non-coding RNA-Associated Therapeutic Strategies in Atherosclerosis
Tang, Y., Li, H., & Chen, C. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.889743 · Cited by 8
“miR-144 Two independent studies almost revealed the important role miR-144 played in cholesterol metabolism in both the liver and macrophages at the same time (79, 80).”
BackgroundEpigenética en la arteriosclerosis
Guardiola, M., Vallvé, J.-C., Zaina, S., & Ribalta, J. (2015) · Clínica e Investigación en Arteriosclerosis · doi:10.1016/j.arteri.2015.04.002 · Cited by 8
MicroRNA regulatory dynamic, emerging diagnostic and therapeutic frontier in atherosclerosis
Zaidi, S. A., Fan, Z., Chauhdari, T., & Ding, Y. (2025) · Microvascular Research · doi:10.1016/j.mvr.2025.104818 · Cited by 6
miR17-92 cluster drives white adipose tissue browning
Huang, Y., Zhang, H., Dong, M., Zhang, L., Lin, J., Ye, R., Zhou, H., Liu, X., & Jin, W. (2020) · Journal of Molecular Endocrinology · doi:10.1530/jme-20-0032 · Cited by 6
MASLD Under the Microscope: How microRNAs and Microbiota Shape Hepatic Metabolic Disease Progression
Asero, C., Franzè, M. S., Cacciola, I., & Gangemi, S. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26178633 · Cited by 6
“MiR-144 silencing via L. casei could restore ABCA1/ABCG1 activity, ameliorating cholesterol metabolism into the hepatocyte [75] (Table 1).”
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
“Supernatants were collected after 6 h, and radioactivity content was expressed as a percentage of 3Hcholesterol in the media/total cell 3H-cholesterol content (total effluxed 3H-cholesterol + cell-associated 3H-cholesterol) (27).”
BackgroundMethodSelf-citationmiRNA Biology in Pathological Processes
Zhang, X., Dong, H., & Tian, Y. (2015) · Springer briefs in molecular science · doi:10.1007/978-3-662-47293-4_2 · Cited by 5
Na, J., Huang, L., Wang, L. J., Ni, Y., Chen, Y., Luo, Q., & Li, Y. (2026) · Biomaterials · doi:10.1016/j.biomaterials.2026.124209 · Cited by 4
Gao, F., Wang, F., Lyu, R., et al. (2018) · Molecular Medicine Reports · doi:10.3892/mmr.2018.8498 · Cited by 4
“Consequently, a total of 65 miRNAs were identified, among which miR‑33 with the function of HDL synthesis and cholesterol transport, was upregulated in the CVD group.”
BackgroundInfluentialRegulation of Hepatobiliary Transporters During Liver Injury
Manautou, J. E., & Ghanem, C. I. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.95661-7 · 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
“However, miR-144 would be induced by LXR to target ABCA1 under similar conditions (112), and thus further studies of the temporal expression and abundance of these 2 miRNAs will be needed to resolve their relative contribution to cholesterol eflux control.”
BackgroundInfluentialNamous, H., Krueger, C. G., Cheng, Y., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-46762-0 · Cited by 3
“Among the DE miRNAs found in our study, miR-7, miR-144, miR-146a-5p, and miR-24-3p regulate foam cell formation. miR-7 and miR-144 were upregulated and promote foam cell formation by directly downregulating genes involved in cholesterol efflux (STK11 and TR4) 19,20 .”
BackgroundHuang, Y., Yang, Y. B., & Sun, X. H. (2016) · Gene Reports · doi:10.1016/j.genrep.2016.07.006 · Cited by 3
The role of micro-RNA in cerebrovascular disease
Раскуражев, А. А., & Tanashyan, M. M. (2019) · Annals of Clinical and Experimental Neurology · doi:10.25692/acen.2019.3.6 · Cited by 3
LncRNA H19 drives atherosclerosis progression via the miR-let-7a/ITGB3 axis
Hu, Z.-Y., Li, Y., Liu, L.-Y., Chen, X., Lin, K.-X., Chaurembo, A. I., Li, X.-S., Huang, G.-Q., Wu, X.-Q., Huang, Z.-F., et al. (2026) · Frontiers in Physiology · doi:10.3389/fphys.2026.1801950 · Cited by 2
THE ROLE OF MICRORNA IN CHOLESTEROL METABOLISM REGULATION
Gutsol, L. O., Юрьевна, К. Е., & Nepomnyaschikh, S. F. (2019) · Современные проблемы науки и образования · doi:10.17513/spno.29020 · Cited by 2
Advancements in microRNA research in dyslipidemia
Zhao, W., Li, N., & YuanMeng, L. I. (2020) · Scientia Sinica Vitae · doi:10.1360/ssv-2020-0125 · Cited by 2
Iswari, R. S., Dafip, M., & Rifai, M. T. A. (2020) · Biosaintifika Journal of Biology & Biology Education · doi:10.15294/biosaintifika.v12i3.23337 · Cited by 2
“However, high lipid consumption contributes in increases blood-cholesterol level, which is then known as hypercholesterolemic condition (Ramírez et al., 2013).”
BackgroundNesan, D., & Ng, D. S. (2014) · Critical Reviews in Clinical Laboratory Sciences · doi:10.3109/10408363.2014.937523 · Cited by 2
The 10 Most Read Articles Published in Circulation Research in 2015
Bolli, R. (2016) · Circulation Research · doi:10.1161/circresaha.116.308583 · Cited by 2
Vega‐Badillo, J. (2016) · TIP Revista Especializada en Ciencias Químico-Biológicas · doi:10.1016/j.recqb.2016.11.005 · Cited by 2
MicroRNA Regulation of HDL Homeostasis
Sun, X., & Feinberg, M. W. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-812513-7.00010-0 · Cited by 2
Noncoding RNAs in Cholesterol Metabolism and Atherosclerosis
Price, N. L., & Fernandez-Hernando, C. F. (2017) · Cardiac and vascular biology · doi:10.1007/978-3-319-52945-5_2 · Cited by 2
Huang, Y., Ren, H., Wang, Z. B., & Sun, X. H. (2015) · Russian Journal of Bioorganic Chemistry · doi:10.1134/s1068162015040147 · Cited by 2
MicroRNAs as Novel Biomarkers in Cardiovascular Medicine
Vogel, B., Katus, H. A., & Meder, B. (2014) · Wiley eBooks · doi:10.1002/9783527672165.ch02 · Cited by 2
Circulation Research “In This Issue” Anthology
Williams, R. R. E., & Editors, T. (2017) · Circulation Research · doi:10.1161/res.0000000000000152 · Cited by 2
Ngo, T. H., & Tran, S. K. (2025) · World Journal of Cardiology · doi:10.4330/wjc.v17.i10.109961 · 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
“MiR-144 directly binds to ABCA1 mRNA, reducing ABCA1 protein synthesis by destabilizing the transcript or inhibiting its translation, thereby modulating cholesterol metabolism (69).”
Modern Transcriptomics and Small RNA Diversity
Vickers, K. C. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-799961-6.00002-0 · Cited by 1
A Closer Look at Cardioprotective Function of HDL: Revise the HDL – Cholesterol Hypothesis?
Meiliana, A., & Wijaya, A. (2014) · The Indonesian Biomedical Journal · doi:10.18585/inabj.v6i1.40 · Cited by 1
Non-coding RNAs Related to Lipid Metabolism and Non-alcoholic Fatty Liver Disease
Holvoet, P. (2021) · Springer eBooks · doi:10.1007/978-3-030-68844-8_4 · Cited by 1
Editorial: Emerging roles of miRNAs in cardiovascular disease
Santovito, D., Fan, Y., Elia, L., et al. (2023) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2023.1144849 · Cited by 1
Non-coding RNA in Cardiovascular Diseases and Therapeutic Potential
Dong, Y. (2016) · Journal of Heart Health · doi:10.16966/2379-769x.e102
“A variety of miRNAs have been demonstrated to play a critical role in AS, for instance, miR-122, miR-33, miR-144, and miR-106 are reported to be related to lipoprotein metabolism [14-17].”
BackgroundRole of microRNA-21 in atherogenesis.
Hamed-Berair, R. E. (2016) · ThinkIR: The University of Louisville's Institutional Repository (University of Louisville) · doi:10.18297/etd/2431
“Similarly, miR-27 [116], miR-144 [117, 118], miR-145 [91, 119], miR-223 [120], and miR-758 [121] target ABCA1 and post-transcriptionally regulate”
Γενετική διερεύνηση ανευρύσματος κοιλιακής αορτής
Μουρμούρα, Ε. (2016) · doi:10.12681/eadd/39065
Expresión de PPAR-γ y miR-27 en el tejido adiposo de pacientes obesos
Triana, J. L. T. (2015) · doi:10.14201/gredos.127896
Estudio de selección de microRNA como posibles biomarcadores de aneurisma de aorta abdominal
Plana, E., Gálvez, L., Medina, P., et al. (2017) · Angiología · doi:10.1016/j.angio.2017.09.001
Rea, I. M., & Mills, K. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-811060-7.00006-1
Martinelli, A. E. M. (2017) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.5.2017.tde-07082017-084252
High-Density Lipoprotein: From Biological Functions to Clinical Perspectives
Liu, D. (2020) · IntechOpen eBooks · doi:10.5772/intechopen.91136 · Cited by 1
Metadata
- Authors
- Ramírez, C. M., Rotllan, N., Vlassov, A. V., Dávalos, A., Li, M., Goedeke, L., Aranda, J. F., Cirera-Salinas, D., Araldi, E., Salerno, A., Wanschel, A., Zavadil, J., Castrillo, A., Kim, J., Suárez, Y., & Fernández-Hernando, C.
- Affiliations
- Universidad de Las Palmas de Gran Canaria (ES)
- From the Leon H. Charney Division of Cardiology, Departments of Medicine and Cell Biology and the Marc and Ruti Bell Vascular Biology and Disease Program (C.M.R., N.R., A.D., L.G., J.F.A., D.C.-S., E.A., A.S., A.W., Y.S., C.F.-H.), Department of Pathology, New York University Center for Health Informatics and Bioinformatics (J.Z.), New York University School of Medicine, New York, New York; Life Technologies, Austin, Texas (A.V.V., M.L.); Instituto de Investigaciones Biomédicas “Alberto Sols,”...
- ORCID
- Venue
- Circulation Research
- Published
- 2013-06-07
- Volume
- 112
- Issue
- 12
- Pages
- 1592-1601
- ISSN
- 0009-7330 (ISSN-L)
- 1524-4571
- PMC
- PMC3929583
- OpenAlex
- W2120525672
- Semantic Scholar
- 7805b86aa3521ae15aacb68031f440532d0f4b06
- Cited by
- 217
- References
- 37
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 4 · 2023: 9 · 2022: 15 · 2021: 13 · 2020: 12 · 2019: 20 · 2018: 14 · 2017: 15 · 2016: 25 · 2015: 25 · 2014: 41 · 2013: 9
- FWCI
- 29.92
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Circulation Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (submittedVersion)
- PubMed Central (submittedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Funders
- American Heart Association
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- National Institutes of Health (5p30ns069329-02)
- National Institute on Aging (P30 AG0 28383)
- National Heart, Lung, and Blood Institute (R01HL105945, R01 HL106063, R01HL107953)
- National Institute of Neurological Disorders and Stroke (P30-NS069329)
- 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
- microRNA-144, cholesterol metabolism, high-density lipoprotein, ABCA1, ABCG1, liver X receptor, macrophage cholesterol efflux, foam cell formation, atherosclerosis, HDL biogenesis, dyslipidemia, miRNA expression profiling, apolipoprotein A-I
- MeSH terms
- Liver X Receptors, Benzenesulfonamides, Animals, Anticholesteremic Agents, Chlorocebus aethiops, Fluorocarbons, Homeostasis, Humans, Hydrocarbons, Fluorinated, Cholesterol, HDL, Macrophages, Male, Mice, Inbred C57BL, Oligonucleotides, Sulfonamides, Apolipoprotein A-I, Mice, Knockout, ATP-Binding Cassette Transporters, COS Cells, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Hepatocytes, MicroRNAs, Mice, Hep G2 Cells, Orphan Nuclear Receptors, Diet, High-Fat, ATP Binding Cassette Transporter 1
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