HDL-transferred microRNA-223 regulates ICAM-1 expression in endothelial cells

Tabet, Fatiha; Vickers, Kasey C.; Cuesta Torres, Luisa F.; Wiese, Carrie B.; Shoucri, Bassem M.; Lambert, Gilles; Catherinet, Claire; Prado-Lourenco, Leonel; Levin, Michael G.; Thacker, Seth; Sethupathy, Praveen; Barter, Philip J.; Remaley, Alan T.; Rye, Kerry-Anne

doi:10.1038/ncomms4292

Cited by 428MicroRNA in disease regulationCholesterol and Lipid MetabolismExtracellular vesicles in disease

HDL-transferred microRNA-223 regulates ICAM-1 expression in endothelial cells

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Tabet, Fatiha, Vickers, Kasey C., Cuesta Torres, Luisa F., Wiese, Carrie B., Shoucri, Bassem M., Lambert, Gilles, Catherinet, Claire, Prado-Lourenco, Leonel +6 more·2014·Nature Communications

DOI 10.1038/ncomms4292PMC PMC4189962

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Abstract

High-density lipoproteins (HDL) have many biological functions, including reducing endothelial activation and adhesion molecule expression. We recently reported that HDL transport and deliver functional microRNAs (miRNA). Here we show that HDL suppresses expression of intercellular adhesion molecule 1 (ICAM-1) through the transfer of miR-223 to endothelial cells. After incubation of endothelial cells with HDL, mature miR-223 levels are significantly increased in endothelial cells and decreased on HDL. However, miR-223 is not transcribed in endothelial cells and is not increased in cells treated with HDL from miR-223(-/-) mice. HDL inhibit ICAM-1 protein levels, but not in cells pretreated with miR-223 inhibitors. ICAM-1 is a direct target of HDL-transferred miR-223 and this is the first example of an extracellular miRNA regulating gene expression in cells where it is not transcribed. Collectively, we demonstrate that HDL's anti-inflammatory properties are conferred, in part, through HDL-miR-223 delivery and translational repression of ICAM-1 in endothelial cells.

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Other proteins found to bind extracellular miRNAs include high-density lipoprotein and nucleophosmin 1.
“Other proteins found to bind extracellular miRNAs include high-density lipoprotein (HDL) (126, 127) and nucleophosmin 1 (NPM1) (110, 118, 128).”
From Overview of MicroRNA Biogenesis, Mechanisms of Actions, and Circulation (2018) · cites this paper as [127]
Vesicle-free miRNAs associated with HDL are taken up by HDL receptor and scavenger receptor BI (SR-BI) in the plasma membrane of target cells.
“Furthermore, vesicle-free miRNAs associated with HDL are taken up by HDL receptor and scavenger receptor BI (SR-BI) receptor in the plasma membrane of the target cells (126, 127).”
From Overview of MicroRNA Biogenesis, Mechanisms of Actions, and Circulation (2018) · cites this paper as [127]

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HDL转运的miR-223调控内皮细胞ICAM-1的表达
罗雨虹 (2014) · 生理科学进展
Abstract 31: Functional Impact of Inflammatory Cell-Originating HDL-miR-223 Communication in vivo
Wiese, C. B., Roteta, L. A., Zhu, W., Landstreet, S. R., & Vickers, K. C. (2015) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvb.35.suppl_1.31
Self-citation
Abstract 47: High-Density Lipoproteins Induce Neutrophil-miRNA Transcription and Export: Contribution to HDL-miRNA Cell to Cell Communication
Tabet, F., Torres, L., Wiese, C. B., Öhrling, G., Larsson, R., Barter, P. J., Vickers, K. C., & Rye, K. (2015) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvb.35.suppl_1.47
Self-citation
Additional file 3: of High-density lipoproteins suppress Aβ-induced PBMC adhesion to human endothelial cells in bioengineered vessels and in monoculture
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MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins
Vickers, K. C., Palmisano, B. T., Shoucri, B. M., Shamburek, R. D., & Remaley, A. T. (2011) · Nature Cell Biology · doi:10.1038/ncb2210 · Cited by 2,741 · see citing works
Self-citation

Authors: Tabet, F., Vickers, K. C., Cuesta Torres, L. F., Wiese, C. B., Shoucri, B. M., Lambert, G., Catherinet, C., Prado-Lourenco, L., Levin, M. G., Thacker, S., Sethupathy, P., Barter, P. J., Remaley, A. T., & Rye, K.-A.
Affiliations: The University of Sydney (AU)
National Institutes of Health (US)
Vanderbilt University (US)
Inserm (FR)
The Heart Research Institute (AU)
University of North Carolina at Chapel Hill (US)
Corresponding author: Tabet, Fatiha
ORCID: Vickers, Kasey C.
Wiese, Carrie B.
Lambert, Gilles
Levin, Michael G.
Thacker, Seth
Sethupathy, Praveen
Remaley, Alan T.
Venue: Nature Communications
Publisher: Springer Science and Business Media LLC
Published: 2014-02-28
Volume: 5
Issue: 1
Pages: 3292-3292
ISSN: 2041-1723 (ISSN-L)
DOI: 10.1038/ncomms4292
PMC: PMC4189962
OpenAlex: W2049702012
Cited by: 428
References: 73
Citations by year: 2026: 19 · 2025: 28 · 2024: 17 · 2023: 34 · 2022: 37 · 2021: 45 · 2020: 47 · 2019: 34 · 2018: 40 · 2017: 31 · 2016: 43 · 2015: 34 · 2014: 18
FWCI: 13.45
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Communications (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
RePEc: Research Papers in Economics (submittedVersion)
UNC Libraries
Funders: Massachusetts Institute of Technology
National Institutes of Health (5r00dk091318-03)
Canadian Institutes of Health Research
National Health and Medical Research Council (1037903)
National Heart, Lung, and Blood Institute (K22HL113039, P01HL116263)
National Institute of Diabetes and Digestive and Kidney Diseases (R00-DK091318, 5R00DK091318, P30DK056350)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
Keywords: high-density lipoprotein, miR-223, ICAM-1, endothelial cells, protein synthesis inhibition, adhesion molecules, endothelial activation
MeSH terms: Adult, Animals, Coronary Vessels, Female, Gene Expression Regulation, Humans, Lipoproteins, HDL, Male, Mice, Inbred C57BL, Gene Expression, Intercellular Adhesion Molecule-1, MicroRNAs, Endothelial Cells, Human Umbilical Vein Endothelial Cells, Healthy Volunteers

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HDL-transferred microRNA-223 regulates ICAM-1 expression in endothelial cells

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