MicroRNA-223 coordinates cholesterol homeostasis

MicroRNAs (miRNAs) regulate a wide variety of biological processes and contribute to metabolic homeostasis. Here, we demonstrate that microRNA-223 (miR-223), an miRNA previously associated with inflammation, also controls multiple mechanisms associated with cholesterol metabolism. miR-223 promoter a...

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Veröffentlicht in:	Proceedings of the National Academy of Sciences - PNAS Jg. 111; H. 40; S. 14518
Hauptverfasser:	Vickers, Kasey C, Landstreet, Stuart R, Levin, Michael G, Shoucri, Bassem M, Toth, Cynthia L, Taylor, Robert C, Palmisano, Brian T, Tabet, Fatiha, Cui, Huanhuan L, Rye, Kerry-Anne, Sethupathy, Praveen, Remaley, Alan T
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States 07.10.2014
Schlagworte:	Animals Cell Line, Tumor Cells, Cultured Cholesterol - metabolism Cholesterol, HDL - metabolism HEK293 Cells Homeostasis Humans Liver - metabolism Mice, Knockout MicroRNAs - genetics Models, Genetic Oligonucleotide Array Sequence Analysis Reverse Transcriptase Polymerase Chain Reaction Transcriptome - genetics atherosclerosis reverse cholesterol transport posttranscriptional gene regulation
ISSN:	1091-6490, 1091-6490
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Abstract	MicroRNAs (miRNAs) regulate a wide variety of biological processes and contribute to metabolic homeostasis. Here, we demonstrate that microRNA-223 (miR-223), an miRNA previously associated with inflammation, also controls multiple mechanisms associated with cholesterol metabolism. miR-223 promoter activity and mature levels were found to be linked to cellular cholesterol states in hepatoma cells. Moreover, hypercholesterolemia was associated with increased hepatic miR-223 levels in athero-prone mice. miR-223 was found to regulate high-density lipoprotein-cholesterol (HDL-C) uptake, through direct targeting and repression of scavenger receptor BI, and to inhibit cholesterol biosynthesis through the direct repression of sterol enzymes 3-hydroxy-3-methylglutaryl-CoA synthase 1 and methylsterol monooxygenase 1 in humans. Additionally, miR-223 was found to indirectly promote ATP-binding cassette transporter A1 expression (mRNA and protein) through Sp3, thereby enhancing cellular cholesterol efflux. Finally, genetic ablation of miR-223 in mice resulted in increased HDL-C levels and particle size, as well as increased hepatic and plasma total cholesterol levels. In summary, we identified a critical role for miR-223 in systemic cholesterol regulation by coordinated posttranscriptional control of multiple genes in lipoprotein and cholesterol metabolism.
AbstractList	MicroRNAs (miRNAs) regulate a wide variety of biological processes and contribute to metabolic homeostasis. Here, we demonstrate that microRNA-223 (miR-223), an miRNA previously associated with inflammation, also controls multiple mechanisms associated with cholesterol metabolism. miR-223 promoter activity and mature levels were found to be linked to cellular cholesterol states in hepatoma cells. Moreover, hypercholesterolemia was associated with increased hepatic miR-223 levels in athero-prone mice. miR-223 was found to regulate high-density lipoprotein-cholesterol (HDL-C) uptake, through direct targeting and repression of scavenger receptor BI, and to inhibit cholesterol biosynthesis through the direct repression of sterol enzymes 3-hydroxy-3-methylglutaryl-CoA synthase 1 and methylsterol monooxygenase 1 in humans. Additionally, miR-223 was found to indirectly promote ATP-binding cassette transporter A1 expression (mRNA and protein) through Sp3, thereby enhancing cellular cholesterol efflux. Finally, genetic ablation of miR-223 in mice resulted in increased HDL-C levels and particle size, as well as increased hepatic and plasma total cholesterol levels. In summary, we identified a critical role for miR-223 in systemic cholesterol regulation by coordinated posttranscriptional control of multiple genes in lipoprotein and cholesterol metabolism. MicroRNAs (miRNAs) regulate a wide variety of biological processes and contribute to metabolic homeostasis. Here, we demonstrate that microRNA-223 (miR-223), an miRNA previously associated with inflammation, also controls multiple mechanisms associated with cholesterol metabolism. miR-223 promoter activity and mature levels were found to be linked to cellular cholesterol states in hepatoma cells. Moreover, hypercholesterolemia was associated with increased hepatic miR-223 levels in athero-prone mice. miR-223 was found to regulate high-density lipoprotein-cholesterol (HDL-C) uptake, through direct targeting and repression of scavenger receptor BI, and to inhibit cholesterol biosynthesis through the direct repression of sterol enzymes 3-hydroxy-3-methylglutaryl-CoA synthase 1 and methylsterol monooxygenase 1 in humans. Additionally, miR-223 was found to indirectly promote ATP-binding cassette transporter A1 expression (mRNA and protein) through Sp3, thereby enhancing cellular cholesterol efflux. Finally, genetic ablation of miR-223 in mice resulted in increased HDL-C levels and particle size, as well as increased hepatic and plasma total cholesterol levels. In summary, we identified a critical role for miR-223 in systemic cholesterol regulation by coordinated posttranscriptional control of multiple genes in lipoprotein and cholesterol metabolism.MicroRNAs (miRNAs) regulate a wide variety of biological processes and contribute to metabolic homeostasis. Here, we demonstrate that microRNA-223 (miR-223), an miRNA previously associated with inflammation, also controls multiple mechanisms associated with cholesterol metabolism. miR-223 promoter activity and mature levels were found to be linked to cellular cholesterol states in hepatoma cells. Moreover, hypercholesterolemia was associated with increased hepatic miR-223 levels in athero-prone mice. miR-223 was found to regulate high-density lipoprotein-cholesterol (HDL-C) uptake, through direct targeting and repression of scavenger receptor BI, and to inhibit cholesterol biosynthesis through the direct repression of sterol enzymes 3-hydroxy-3-methylglutaryl-CoA synthase 1 and methylsterol monooxygenase 1 in humans. Additionally, miR-223 was found to indirectly promote ATP-binding cassette transporter A1 expression (mRNA and protein) through Sp3, thereby enhancing cellular cholesterol efflux. Finally, genetic ablation of miR-223 in mice resulted in increased HDL-C levels and particle size, as well as increased hepatic and plasma total cholesterol levels. In summary, we identified a critical role for miR-223 in systemic cholesterol regulation by coordinated posttranscriptional control of multiple genes in lipoprotein and cholesterol metabolism.
Author	Tabet, Fatiha Cui, Huanhuan L Rye, Kerry-Anne Shoucri, Bassem M Sethupathy, Praveen Taylor, Robert C Levin, Michael G Landstreet, Stuart R Palmisano, Brian T Vickers, Kasey C Toth, Cynthia L Remaley, Alan T
Author_xml	– sequence: 1 givenname: Kasey C surname: Vickers fullname: Vickers, Kasey C email: kasey.c.vickers@Vanderbilt.edu organization: National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892; Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN 37232; kasey.c.vickers@Vanderbilt.edu – sequence: 2 givenname: Stuart R surname: Landstreet fullname: Landstreet, Stuart R organization: Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN 37232 – sequence: 3 givenname: Michael G surname: Levin fullname: Levin, Michael G organization: National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 – sequence: 4 givenname: Bassem M surname: Shoucri fullname: Shoucri, Bassem M organization: National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 – sequence: 5 givenname: Cynthia L surname: Toth fullname: Toth, Cynthia L organization: Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN 37232 – sequence: 6 givenname: Robert C surname: Taylor fullname: Taylor, Robert C organization: Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN 37232 – sequence: 7 givenname: Brian T surname: Palmisano fullname: Palmisano, Brian T organization: National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 – sequence: 8 givenname: Fatiha surname: Tabet fullname: Tabet, Fatiha organization: Lipid Research Group, The Heart Research Institute, Newtown, NSW 2042, Australia – sequence: 9 givenname: Huanhuan L surname: Cui fullname: Cui, Huanhuan L organization: Lipoproteins and Atherosclerosis, Baker IDI Heart and Diabetes Institute, Melbourne, VIC 3004, Australia; and – sequence: 10 givenname: Kerry-Anne surname: Rye fullname: Rye, Kerry-Anne organization: Lipid Research Group, The Heart Research Institute, Newtown, NSW 2042, Australia – sequence: 11 givenname: Praveen surname: Sethupathy fullname: Sethupathy, Praveen organization: Department of Genetics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599 – sequence: 12 givenname: Alan T surname: Remaley fullname: Remaley, Alan T organization: National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892
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Snippet	MicroRNAs (miRNAs) regulate a wide variety of biological processes and contribute to metabolic homeostasis. Here, we demonstrate that microRNA-223 (miR-223),...
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SubjectTerms	Animals Cell Line, Tumor Cells, Cultured Cholesterol - metabolism Cholesterol, HDL - metabolism HEK293 Cells Homeostasis Humans Liver - metabolism Mice, Knockout MicroRNAs - genetics Models, Genetic Oligonucleotide Array Sequence Analysis Reverse Transcriptase Polymerase Chain Reaction Transcriptome - genetics
Title	MicroRNA-223 coordinates cholesterol homeostasis
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