MicroRNAs in Lipid Metabolism and Atherosclerosis
Abstract
BACKGROUND: MicroRNAs (miRNA) are mediators of post-transcriptional gene expression that likely regulate most biological pathways and networks. The study of miRNAs is a rapidly emerging field; recent findings have revealed a significant role for miRNAs in atherosclerosis and lipoprotein metabolism.
CONTENT: Results from recent studies demonstrated a role for miRNAs in endothelial integrity, macrophage inflammatory response to oxidized low-density lipoprotein, vascular smooth muscle cell proliferation and cholesterol synthesis. These mechanisms are all vital to the initiation and proliferation of atherosclerosis and cardiovascular disease. The importance of miRNAs has recently been recognized in cardiovascular sciences and miRNAs will likely become an integral part of our fundamental comprehension of atherosclerosis and lipoprotein metabolism. The extensive impact of miRNA mediated gene regulation and the relative ease of in vivo applicable modifications highlight the enormous potential of miRNA-based therapeutics in cardiovascular diseases.
SUMMARY: miRNA studies in the field of lipid metabolism and atherosclerosis are in their infancy, and thus there is tremendous opportunity for discovery in this understudied area. The ability to target miRNAs in vivo through delivery of miRNA-mimics to enhance miRNA function, or antimiRNAs which inhibit miRNAs, has opened new avenues for the development of therapeutics for dyslipidemias and atherosclerosis, offers a unique approach to treating disease by modulating entire biological pathways. These exciting findings support the development of miRNA antagonists as potential therapeutics for the treatment of dyslipidaemia, atherosclerosis and related metabolic diseases.
KEYWORDS: atherosclerosis, lipoprotein, HDL, miRNA
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Voight BF, Peloso GM, Orho-Melander M, Frikke-Schmidt R, Barbalic M, Jensen MK, et al. Plasma HDL cholesterol and risk of myocardial infarction: A Mendelian randomisation study. Lancet. 2012; 380: 572-80, CrossRef.
Boden WE, Probstfield JL, Anderson T, Chaitman BR, Desvignes-Nickens P, Koprowicz K, et al. Niacin in patients with low HDL cholesterol levels receiving intensive statin therapy. N Engl J Med. 2011; 365: 2255-67, CrossRef.
Schwartz GG, Olsson AG, Abt M, Ballantyne CM, Barter PJ, Brumm J, et al. Effects of dalcetrapib in patients with a recent acute coronary syndrome. N Engl J Med. 2012; 367: 2089-99, CrossRef.
Vickers KC, Remaley AT. Lipid-based carriers of MicroRNAs and intercellular communication. Cur Opin Lipidol. 2012; 23: 91-7, CrossRef.
Rayner KJ, Moore KJ. MicroRNA control of high density lipoprotein metabolism and function. Circ Res. 2014; 114: 183-92, CrossRef.
ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012; 489: 57-74, PMID.
Trajkovski M, Hausser J, Soutschek J, Bhat B, Akin A, Zavolan M, et al. MicroRNAs 103 and 107 regulate insulin sensitivity. Nature. 2011; 474: 649-53, CrossRef.
Schroen B, Heymans S. Small but smart: microRNAs in the centre of inflammatory processes during cardiovascular diseases, the metabolic syndrome, and ageing. Cardiovasc Res. 2011; 93: 605-13, CrossRef.
Hulsmans M, De Keyzer D, Holvoet P. MicroRNAs regulating oxidative stress and inflammation in relation to obesity and atherosclerosis. FASEB J. 2011; 25: 2515-27, CrossRef.
De Rosa S, Fichtlscherer S, Lehmann R, Assmus B, Dimmeler S, Zeiher AM. Transcoronary concentration gradients of circulating MicroRNAs. Circulation. 2011; 124: 1936-44, CrossRef.
Vickers KC, Remaley AT. MicroRNAs in atherosclerosis and lipoprotein metabolism. Curr Opin Endocrinol Diabetes Obes. 2010; 17: 150-5, CrossRef.
Rayner KJ, Esau CC, Hussain FN, McDaniel AL, Marshall SM, van Gils JM, et al. Inhibition of miR-33a/b in nonhuman primates raises plasma HDL and lowers VLDL triglycerides. Nature. 2011; 478: 404-7, CrossRef.
Cheung O, Puri P, Eicken C, Contos MJ, Mirshahi F, Maher JW, et al. Nonalcoholic steatohepatitis is associated with altered hepatic MicroRNA expression. Hepatology. 2008; 48: 1810-20, CrossRef.
Fichtlscherer S, Zeiher AM, Dimmeler S. Circulating microRNAs: biomarkers or mediators of cardiovascular diseases? Arterioscler Thromb Vasc Biol. 2011; 31: 2383-90, CrossRef.
McManus DD, Ambros V. Circulating MicroRNAs in cardiovascular disease. Circulation. 2011; 124: 1908-10, CrossRef.
Zhu H, Fan GC. Extracellular/circulating microRNAs and their potential role in cardiovascular disease. Am J Cardiovasc Dis. 2011; 1: 138-49, PMID.
Friel AM, Corcoran C, Crown J, O’Driscoll L. Relevance of circulating tumor cells, extracellular nucleic acids, and exosomes in breast cancer. Breast Cancer Res Treat. 2010; 123: 613-25, CrossRef.
Kosaka N, Iguchi H, Ochiya T. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 2010; 101: 2087-92, CrossRef.
Rabinowits G, Gerçl-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer. 2009; 10: 42-6, CrossRef.
Rosell R, Wei J, Taron M. Circulating MicroRNA signatures of tumor-derived exosomes for early diagnosis of non-small-cell lung cancer. Clin Lung Cancer. 2009; 10: 8-9, CrossRef.
Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol. 2008; 110: 13-21, CrossRef.
Ji R, Cheng Y, Yue J, Yang J, Liu X, Chen H, et al. MicroRNA expression signature and antisense mediated depletion reveal an essential role of microRNA in vascular neointimal lesion formation. Circ Res. 2007; 100: 1579-88, CrossRef.
Chen T, Huang Z, Wang L, Wang Y, Wu F, Meng S, et al. MicroRNA-125a-5p partly regulates the inflammatory response, lipid uptake, and ORP9 expression in oxLDL-stimulated monocyte/macrophages. Cardiovasc Res. 2009; 83: 131-9, CrossRef.
Sacco LD, Masotti A. Recent insights and novel bioinformatics tools to understand the role of microRNAs binding to 5′ untranslated region. Int J Mol Sci. 2012; 14: 480-95, CrossRef.
Reczko M, Maragkakis M, Alexiou P, Grosse I, Hatzigeorgiou AG. Functional microRNA targets in protein coding sequences. Bioinformatics. 2012; 28: 771-6, CrossRef.
He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet. 2004; 5: 522-31, CrossRef.
Lee Y, Jeon K, Lee JT, Kim S, Kim VN. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 2002; 21: 4663-70, CrossRef.
Baek D, Villé J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature. 2008; 455: 64-71, CrossRef.
Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature. 2005; 433: 769-73, CrossRef.
Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature. 2008; 455: 58-63, CrossRef.
Meiliana A, Wijaya A. MicroRNAs in obesity, metabolic syndrome, and diabetes mellitus. Indones Biomed J. 2011; 3: 4-17, CrossRef.
Carleton M, Cleary MA, Linsley PS. MicroRNAs and cell cycle regulation. Cell Cycle. 2007; 6: 2127-32, CrossRef.
Bueno MJ, de Castro IP, Malumbres M. Control of cell proliferation pathways by microRNAs. Cell Cycle. 2008; 7: 3143-8, CrossRef.
Schickel R, Boyerinas B, Park SM, Peter ME. MicroRNAs: key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene. 2008; 27: 5959-74, CrossRef.
Jovanovic M, Hengartner MO. miRNAs and apoptosis: RNAs to die for. Oncogene. 2006; 25: 6176-87, CrossRef.
Schratt G. microRNAs at the synapse. Nat Rev Neurosci. 2009; 10: 842-9, CrossRef.
Xiao C, Rajewsky K. MicroRNA control in the immune system: basic principles. Cell. 2009; 136: 26-36, CrossRef.
Liu N, Olson EN. MicroRNA regulatory networks in cardiovascular development. Dev Cell. 2010; 18: 510-25, CrossRef.
Garzon R, Calin GA, Croce CM. MicroRNAs in cancer. Annu Rev Med. 2009; 60: 167-79, CrossRef.
Small EM, Frost RJ, Olson EN. MicroRNAs add a new dimension to cardiovascular disease. Circulation. 2010; 121: 1022-32, CrossRef.
Latronico MV, Condorelli G. MicroRNAs and cardiac pathology. Nat Rev Cardiol. 2009; 6: 418-29, CrossRef.
Bagga S, Bracht J, Hunter S, Massirer K, Holtz J, Eachus R, et al. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell. 2005; 122: 553-63, CrossRef.
Elmén J, Lindow M, Schütz S, Lawrence M, Petri A, Obad S, et al. LNA-mediated microRNA silencing in non-human primates. Nature. 2008; 452: 896-900, CrossRef.
Simons M, Raposo G. Exosomes vesicular carriers for intercellular communication. Curr Opin Cell Biol. 2009; 21: 575-881, CrossRef.
Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007; 9: 654-9, CrossRef.
Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One. 2008; 3: e3694, CrossRef.
Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia. 2006; 20: 1487-95, CrossRef.
Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116: 281-97, CrossRef.
Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, et al. Circulating microRNAs as stable bloodbased markers for cancer detection. Proc Natl Acad Sci USA. 2008; 105: 10513-8, CrossRef.
Rayner KJ, Hennessy EJ. Exrtacellular communication via microRNA: lipid particles have a new message. J Lipid Res. 2013; 54: 1174-81, CrossRef.
Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008; 18: 997-1006, CrossRef.
Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem. 2010; 285: 17442-52, CrossRef.
Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011; 39: 7223-33, CrossRef.
Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova- Agadjanyan EL, et al. Circulating microRNAs as stable bloodbased markers for cancer detection. Proc Natl Acad Sci USA. 2008; 105: 10513-8, CrossRef.
Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA. 2011; 108: 5003-8, CrossRef.
Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 2010; 39: 133-44, CrossRef.
Muller G, Schneider M, Biemer-Daub G, Wied S. Microvesicles released from rat adipocytes and harboring glycosylphosphatidylinositolanchored proteins transfer RNA stimulating lipid synthesis. Cell Signal. 2011; 23: 1207-23, CrossRef.
Ohshima K, Inoue K, Fujiwara A, Hatakeyama K, Kanto K, Watanabe Y, et al. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One. 2010; 5: e13247, CrossRef.
Thery C. Exosomes: secreted vesicles and intercellular communications. F1000 Biol Rep. 2011; 3: 15, CrossRef.
Mause SF, Weber C. Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ Res. 2010; 107: 1047-57, CrossRef.
Muralidharan-Chari V, Clancy JW, Sedgwick A, D'Souza-Schorey C. Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci. 2010; 123: 1603-11, CrossRef.
Freyssinet JM. Cellular microparticles: what are they bad or good for? J Thromb Haemost. 2003; 1: 1655-62, CrossRef.
Huber J, Vales A, Mitulovic G, Blumer M, Schmid R, Witztum JL, et al. Oxidized membrane vesicles and blebs from apoptotic cells contain biologically active oxidized phospholipids that induce monocyte-endothelial interactions. Arterioscler Thromb Vasc Biol. 2002; 22: 101-7, CrossRef.
Brown WV. High-density lipoprotein and transport of cholesterol and triglyceride in blood. J Clin Lipidol. 2007; 1: 7-19, CrossRef.
Babin PJ, Gibbons GF. The evolution of plasma cholesterol: direct utility or a “spandrel” of hepatic lipid metabolism? Prog Lipid Res. 2009; 48: 73-91, CrossRef.
Ferracin M, Veronese A, Negrini M. Micromarkers: miRNAs in cancer diagnosis and prognosis. Expert Rev Mol Diagn. 2010; 10: 297-308, CrossRef.
Wang GK, Zhu JQ, Zhang JT, Li Q, Li Y, He J, et al. Circulating microRNA: a novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J. 2010; 31: 659-66, CrossRef.
Wang JF, Yu ML, Yu G, Bian JJ, Deng XM, Wan XJ, et al. Serum miR-146a and miR-223 as potential new biomarkers for sepsis. Biochem Biophys Res Commun. 2010; 394: 184-8, CrossRef.
Heneghan HM, Miller N, Lowery AJ, Sweeney KJ, Kerin MJ. MicroRNAs as novel biomarkers for breast cancer. J Oncol. 2009; 2009: 950201, CrossRef.
Gilad S, Meiri E, Yogev Y, Benjamin S, Lebanony D, Yerushalmi N, et al. Serum microRNAs are promising novel biomarkers. PLoS One. 2008; 3: e3148, CrossRef.
Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 2011; 13: 423-33, CrossRef.
Turchinovich A, Burwinkel B. Distinct AGO1 and AGO2 associated miRNA profiles in human cells and blood plasma. RNA Biol. 2012; 9: 1066-75, CrossRef.
Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008; 319: 1244-7, CrossRef.
Wang K, Zhang S, Weber J, Baxter D, Galas DJ. Export of microRNAs and microRNAprotective protein by mammalian cells. Nucleic Acids Res. 2010; 38: 7248-59, CrossRef.
Morelli AE, Larregina AT, Shufesky WJ, Sullivan ML, Stolz DB, Papworth GD, et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood. 2004; 104: 3257-66, CrossRef.
Tian T, Wang Y, Wang H, Zhu Z, Xiao Z. Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy. J Cell Biochem. 2010; 111: 488-96, CrossRef.
Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood. 2012; 119: 756-66, CrossRef.
Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem. 2009; 284: 34211-22, CrossRef.
Acton S, Rigotti A, Landschulz KT, Xu S, Hobbs HH, Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science. 1996; 271: 518-20, CrossRef.
Connelly MA, Williams DL. Scavenger receptor BI: a scavenger receptor with a mission to transport high density lipoprotein lipids. Curr Opin Lipidol. 2004; 15: 287-95, CrossRef.
Grange C, Tapparo M, Collino F, Vitillo L, Damasco C, Deregibus MC, et al. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res. 2011; 71: 5346-56, CrossRef.
Zhang L, Hou D, Chen X, Li D, Zhu L, Zhang Y, et al. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res. 2012; 22: 107-26, CrossRef.
Yang M, Chen J, Su F, Yu B, Su F, Lin L, et al. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer. 2011; 10: 117, CrossRef.
Dietschy JM, Turley SD. Control of cholesterol turnover in the mouse. J Biol Chem. 2002; 277: 3801-4, CrossRef.
Girard M, Jacquemin E, Munnich A, Lyonnet S, Henrion-Caude A. miR-122, a paradigm for the role of microRNAs in the liver. J Hepatol. 2008; 48: 648-56, CrossRef.
Lynn FC. Meta-regulation: microRNA regulation of glucose and lipid metabolism. Trends Endocrinol Metab. 2009; 20: 452-9, CrossRef.
Chen XM. MicroRNA signatures in liver diseases. World J Gastroenterol. 2009; 15: 1665-72, CrossRef.
Alberti KG, Zimmet P, Shaw J. Metabolic syndrome: a new worldwide definition. A Consensus Statement from the International Diabetes Federation. Diabet Med. 2006; 23: 469-80, CrossRef.
Glass CK, Witztum JL. Atherosclerosis. The road ahead. Cell. 2001; 104: 503-16, CrossRef.
Lusis AJ. Atherosclerosis. Nature. 2000; 407: 233-41, CrossRef.
Teran-Garcia M, Bouchard C. Genetics of the metabolic syndrome. Appl Physiol Nutr Metab. 2007; 32: 89-114, CrossRef.
Fernandez-Hernando C, Suarez Y, Rayner KJ, Moore KJ. MicroRNAs in lipid metabolism. Curr Opin Lipidol. 2011; 22: 86-92, CrossRef.
Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006; 444: 860-7, CrossRef.
Brown MS, Goldstein JL. The SREBP pathway: Regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell. 1997; 89: 331-40, CrossRef.
Horton JD, Goldstein JL, Brown MS. SREBPs: Activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest. 2002; 109: 1125-31, CrossRef.
Osborne TF. Sterol regulatory element-binding proteins (SREBPs): Key regulators of nutritional homeostasis and insulin action. J Biol Chem. 2000; 275: 32379-82, CrossRef.
Brooks-Wilson A, Marcil M, Clee SM, Zhang LH, Roomp K, van Dam M, et al. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat Genet. 1999; 22: 336-45, CrossRef.
Bodzioch M1, Orsó E, Klucken J, Langmann T, Böttcher A, Diederich W, et al. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat Genet. 1999; 22: 347-51, CrossRef.
Lawn RM, Wade DP, Garvin MR, Wang X, Schwartz K, Porter JG, et al. The Tangier disease gene product ABC1 controls the cellular apolipoprotein-mediated lipid removal pathway. J Clin Invest. 1999; 104: R25-31, CrossRef.
Rust S, Rosier M, Funke H, Real J, Amoura Z, Piette JC, et al. Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat Genet. 1999; 22: 352-5, CrossRef.
Timmins JM, Lee JY, Boudyguina E, Kluckman KD, Brunham LR, Mulya A, et al. Targeted inactivation of hepatic Abca1 causes profound hypoalphalipoproteinemia and kidney hypercatabolism of apoA-I. J Clin Invest. 2005; 115: 1333-42, CrossRef.
Chung S, Sawyer JK, Gebre AK, Maeda N, Parks JS. Adipose tissue ATP binding cassette transporter A1 contributes to high-density lipoprotein biogenesis in vivo. Circulation. 2011; 124: 1663-72, CrossRef.
McGillicuddy FC, Reilly MP, Rader DJ. Adipose modulation of high-density lipoprotein cholesterol: implications for obesity, high-density lipoprotein metabolism, and cardiovascular disease. Circulation. 2011; 124: 1602-5, CrossRef.
Brunham LR, Kruit JK, Iqbal J, Fievet C, Timmins JM, Pape TD, et al. Intestinal ABCA1 directly contributes to HDL biogenesis in vivo. J Clin Invest. 2006; 116: 1052-62, CrossRef.
Brunham LR, Kruit JK, Pape TD, Parks JS, Kuipers F, Hayden MR. Tissue-specific induction of intestinal ABCA1 expression with a liver X receptor agonist raises plasma HDL cholesterol levels. Circ Res. 2006; 99: 672-4, CrossRef.
Rayner KJ, Suárez Y, Dávalos A, Parathath S, Fitzgerald ML, Tamehiro, et al. MiR-33 contributes to the regulation of cholesterol homeostasis. Science. 2010; 328: 1570-3, CrossRef.
Najafi-Shoushtari SH, Kristo F, Li Y, Shioda T, Cohen DE, Gerszten RE, et al. MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science. 2010; 328: 1566-9, CrossRef.
Horie T, Ono K, Horiguchi M, Nishi H, Nakamura T, Nagao K, et al. MicroRNA-33 encoded by an intron of sterol regulatory elementbinding protein 2 (SREBP2) regulates HDL in vivo. Proc Natl Acad Sci USA. 2010; 107: 17321-6, CrossRef.
Ramirez CM, Dávalos A, Goedeke L, Salerno AG, Warrier N, Cirera-Salinas D, et al. MicroRNA-758 regulates cholesterol efflux through posttranscriptional repression of ATP-binding cassette transporter A1. Arterioscler Thromb Vasc Biol. 2011; 31: 2707-14, CrossRef.
Sun D, Zhang J, Xie J, Wei W, Chen M, Zhao X. MiR-26 controls LXRdependent cholesterol efflux by targeting ABCA1 and ARL7. FEBS Lett. 2012; 586: 1472-9, CrossRef.
Kim J, Yoon H, Ramirez CM, Lee SM, Hoe HS, Fernandez-Hernando C. Mir-106b impairs cholesterol efflux and increases abeta levels by repressing abca1 expression. Exp Neurol. 2012; 235: 476-83, CrossRef.
Ramírez CM, Rotllan N, Vlassov AV, Dávalos A, Li M, Goedeke L, et al. Control of cholesterol metabolism and plasma high-density lipoprotein levels by microRNA-144. Circ Res. 2013; 112: 1592-601, CrossRef.
de Aguiar Vallim TQ, Tarling EJ, Kim T, Civelek M, Baldán Á, Esau C, et al. MicroRNA-144 regulates hepatic ATP binding cassette transporter A1 and plasma high-density lipoprotein after activation of the nuclear receptor farnesoid X receptor. Circ Res. 2013; 112: 1602-12, CrossRef.
Ouimet M. Autophagy in obesity and atherosclerosis: Interrelationships between cholesterol homeostasis, lipoprotein metabolism and autophagy in macrophages and other systems. Biochim Biophys Acta. 2013; 1831: 1124-33, CrossRef.
Le Guezennec X, Brichkina A, Huang YF, Kostromina E, Han W, Bulavin DV. Wip1-dependent regulation of autophagy, obesity, and atherosclerosis. Cell Metab. 2012; 16: 68-80, CrossRef.
Ouimet M, Franklin V, Mak E, Liao X, Tabas I, Marcel YL. Autophagy regulates cholesterol efflux from macrophage foam cells via lysosomal acid lipase. Cell Metab. 2011; 13: 655-67, CrossRef.
Razani B, Feng C, Coleman T, Emanuel R, Wen H, Hwang S, et al. Autophagy links inflammasomes to atherosclerotic progression. Cell Metab. 2012; 15: 534-44, CrossRef.
Robinet P, Ritchey B, Smith JD. Physiological difference in autophagic flux in macrophages from 2 mouse strains regulates cholesterol ester metabolism. Arterioscler Thromb Vasc Biol. 2013; 33: 903-10, CrossRef.
Chen WX, Hu Q, Qiu MT, Zhong SL, Xu JJ, Tang JH, et al. miR-221/222: promising biomarkers for breast cancer. Tumour Biol. 2013; 34: 1361-70, CrossRef.
Chen Y, Liersch R, Detmar M. The mir-290-295 cluster suppresses autophagic cell death of melanoma cells. Sci Rep. 2012; 2: 808, CrossRef.
Frankel LB, Wen J, Lees M, Høyer-Hansen M, Farkas T, Krogh A, et al. microRNA-101 is a potent inhibitor of autophagy. EMBO J. 2011; 30: 4628-41, CrossRef.
Korkmaz G, le Sage C, Tekirdag KA, Agami R, Gozuacik D. miR-376b controls starvation and mTOR inhibition-related autophagy by targeting ATG4C and BECN1. Autophagy. 2012; 8: 165-76, CrossRef.
Qased AB, Yi H, Liang N, Ma S, Qiao S, Liu X. MicroRNA-18a upregulates autophagy and ataxia telangiectasia mutated gene expression in HCT116 colon cancer cells. Mol Med Rep. 2012; 7: 559-64, CrossRef.
Tekirdag KA, Korkmaz G, Ozturk DG, Agami R, Gozuacik D. MIR181A regulates starvation- and rapamycin-induced autophagy through targeting of ATG5. Autophagy. 2013; 9: 374-85, CrossRef.
Wu H, Wang F, Hu S, Yin C, Li X, Zhao S, et al. MiR-20a and miR-106b negatively regulate autophagy induced by leucine deprivation via suppression of ULK1 expression in C2C12 myoblasts. Cell Signal. 2012; 24: 2179-86, CrossRef.
Xu Y, An Y, Wang Y, Zhang C, Zhang H, Huang C, et al. miR-101 inhibits autophagy and enhances cisplatin-induced apoptosis in hepatocellular carcinoma cells. Oncol Rep. 2013; 29: 2019-24, CrossRef.
Yang X, Zhong X, Tanyi JL, Shen J, Xu C, Gao P, et al. mir-30d regulates multiple genes in the autophagy pathway and impairs autophagy process in human cancer cells. Biochem Biophys Res Commun. 2013; 431: 617-22, CrossRef.
Wolf A, Bauer B, Hartz AM. ABC Transporters and the Alzheimer’s Disease Enigma. Front Psychiatry. 2012; 3: 54, CrossRef.
Wang L, Jia XJ, Jiang HJ, Du Y, Yang F, Si SY, et al. MicroRNAs 185, 96, and 223 repress selective high-density lipoprotein cholesterol uptake through posttranscriptional inhibition. Mol Cell Biol. 2013; 33: 1956-64, CrossRef.
Hair P, Cameron F, McKeage K. Mipomersen sodium: first global approval. Drugs. 2013; 73: 487-93, CrossRef.
Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med. 1999; 340: 115-26, CrossRef.
Widlansky ME, Gokce N, Keaney JF Jr, Vita JA. The clinical implications of endothelial dysfunction. J Am Coll Cardiol. 2003; 42: 1149-60, CrossRef.
Endemann DH, Schiffrin EL. Endothelial dysfunction. J Am Soc Nephrol. 2004; 15: 1983-92, CrossRef.
Sua´rez Y, Ferna´ndez-Hernando C, Pober JS, Sessa WC. Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res. 2007; 100: 1164-73, CrossRef.
Suárez Y, Fernádez-Hernando C, Yu J, Gerber SA, Harrison KD, Pober JS, et al. Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc Natl Acad Sci USA. 2008; 105: 14082-7, CrossRef.
Kuehbacher A, Urbich C, Zeiher AM, Dimmeler S. Role of dicer and drosha for endothelial microRNA expression and angiogenesis. Circ Res 2007; 101: 59-68, CrossRef.
Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, et al. MicroRNAs modulate the angiogenic properties of HUVECs. Blood. 2006; 108: 3068-71, CrossRef.
Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, et al. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science. 2009; 324: 1710-3, CrossRef.
Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, et al. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008; 15: 261-71, CrossRef.
Hergenreider E, Heydt S, Tréguer K, Boettger T, Horrevoets AJ, Zeiher AM, et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol. 2012; 14: 249-56, CrossRef.
Zampetaki A, Kirton JP, Xu Q. Vascular repair by endothelial progenitor cells. Cardiovasc Res. 2008; 78: 413-21, CrossRef.
Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997; 275: 964-7, CrossRef.
Minami Y, Satoh M, Maesawa C, Takahashi Y, Tabuchi T, Itoh T, et al. Effect of atorvastatin on microRNA 221/222 expression in endothelial progenitor cells obtained from patients with coronary artery disease. Eur J Clin Invest. 2009; 39: 359-67, CrossRef.
Zernecke A, Bidzhekov K, Noels H, Shagdarsuren E, Gan L, Denecke B, et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal. 2009; 2: ra81, CrossRef.
Nicoli S, Standley C, Walker P, Hurlstone A, Fogarty KE, Lawson ND. MicroRNA-mediated integration of haemodynamics and Vegf signalling during angiogenesis. Nature 2010; 64: 1196-2000, CrossRef.
Qin X, Wang X, Wang Y, Tang Z, Cui Q, Xi J, et al. MicroRNA-19a mediates the suppressive effect of laminar flow on cyclin D1 expression in human umbilical vein endothelial cells. Proc Natl Acad Sci USA. 2010; 107: 3240-4, CrossRef.
Fang Y, Shi C, Manduchi E, Civelek M, Davies PF. MicroRNA-10a regulation of proinflammatory phenotype in athero-susceptible endothelium in vivo and in vitro. Proc Natl Acad Sci USA. 2010; 107: 13450-5, CrossRef.
Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, et al. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature. 2009; 460: 705-10, CrossRef.
Elia L, Quintavalle M, Zhang J, Contu R, Cossu L, Latronico MV, et al. The knockout of miR-143 and -145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ. 2009; 16: 1590-8, CrossRef.
Boettger T, Beetz N, Kostin S, Schneider J, Krüger M, Hein L, et al. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J Clin Invest. 2009; 119: 2634-47, CrossRef.
Lin Y, Liu X, Cheng Y, Yang J, Huo Y, Zhang C. Involvement of MicroRNAs in hydrogen peroxidemediated gene regulation and cellular injury response in vascular smooth muscle cells. J Biol Chem 2009; 284: 7903-13, CrossRef.
Zhang C. MicroRNA-145 in vascular smooth muscle cell biology: a new therapeutic target for vascular disease. Cell Cycle 2009; 8: 3469-73, CrossRef.
Cheng Y, Liu X, Yang J, Lin Y, Xu DZ, Lu Q, et al. MicroRNA-145, a novel smooth muscle cell phenotypic marker and modulator, controls vascular neointimal lesion formation. Circ Res. 2009; 105: 158-66, CrossRef.
Liu X, Cheng Y, Zhang S, Lin Y, Yang J, Zhang C. A necessary role of miR-221 and miR-222 in vascular smooth muscle cell proliferation and neointimal hyperplasia. Circ Res. 2009; 104: 476-87, CrossRef.
Zhang C. MicroRNA and vascular smooth muscle cell phenotype: new therapy for atherosclerosis? Genome Med. 2009; 1: 85, CrossRef.
Xin M, Small EM, Sutherland LB, Qi X, McAnally J, Plato CF, et al. MicroRNAs miR-143 and miR-145 modulate cytoskeletal dynamics and responsiveness of smooth muscle cells to injury. Genes Dev. 2009; 23: 2166-78, CrossRef.
De Winther MPJ, Lutgens E. MiR-92a: at the heart of lipid-driven endothelial dysfunction. Circ Res 2014; 114: 399-401, CrossRef.
Loyer X, Potteaux S, Vion A-C, Guerin CL, Boulkroun S, Rautou P-E, et al. Inhibition of microRNA-92a prevents endothelial dysfunction and atherosclerosis in mice. Circ Res. 2014; 114: 434-43, CrossRef.
Raitoharju E, Oksala N, Lehtimaki T. MicroRNAs in the atherosclerotic plaque. Clin Chem. 2013; 59: 1708-21, CrossRef.
Widera C, Gupta SK, Lorenzen JM, Bang C, Bauersachs J, Bethmann K, et al. Diagnostic and prognostic impact of six circulating microRNAs in acute coronary syndrome. J Mol Cell Cardiol. 2011; 51: 872-5, CrossRef.
Zampetaki A, Willeit P, Tilling L, Drozdov I, Prokopi M, Renard JM, et al. Prospective study on circulating MicroRNAs and risk of myocardial infarction. J Am Coll Cardiol. 2012; 60: 290-9, CrossRef.
Devaux Y, Vausort M, Goretti E, Nazarov PV, Azuaje F, Gilson G, et al. Use of circulating microRNAs to diagnose acute myocardial infarction. Clin Chem. 2012; 58: 559-67, CrossRef.
Corsten MF, Dennert R, Jochems S, Kuznetsova T, Devaux Y, Hofstra L, et al. Circulating microRNA-208b and microRNA-499 reflect myocardial damage in cardiovascular disease. Circ Cardiovasc Genet. 2010; 3: 499-506, CrossRef.
Ono K, Kuwabara Y, Han J. MicroRNAs and cardiovascular diseases. FEBS J. 2011; 278: 1619-33, CrossRef.
Olivieri F, Antonicelli R, Capogrossi MC, Procopio AD. Circulating microRNAs (miRs) for diagnosing acute myocardial infarction: An exciting challenge. Int J Cardiol. 2013; 167: 3028-9, CrossRef.
Cermelli S, Ruggieri A, Marrero JA, Ioannou GN, Beretta L. Circulating microRNAs in patients with chronic hepatitis C and non-alcoholic fatty liver disease. PLoS One. 2011; 6: e23937, CrossRef.
Gao W, He HW, Wang ZM, Zhao H, Lian XQ, Wang YS, et al. Plasma levels of lipometabolism-related miR-122 and miR-370 are increased in patients with hyperlipidemia and associated with coronary artery disease. Lipids Health Dis. 2012; 11: 55, CrossRef.
Kuwabara Y, Ono K, Horie T, Nishi H, Nagao K, kinoshita M, et al. Increased microRNA-1 and microRNA-3 levels in serum of patients with cardiovascular disease indicate myocardial damage. Circ Cardiovasc Genet. 2011; 4: 446-54, CrossRef.
Zampetaki A, Kiechl S, Drozdov I, Willeit P, Mayr U, Prokopi M, et al. Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res. 2010; 107: 810-7, CrossRef.
Fish JE, Santoro MM, Morton SU, Yu S, Yeh RF. miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell. 2008; 15: 272-84, CrossRef.
Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C, et al. Circulating microRNAs in patients with coronary artery disease. Circ Res. 2010; 107: 677-84, CrossRef.
Sun X, Zhang M, Sanagawa A, Mori C, Ito S, Iwaki S, et al. Circulating microRNA-126 in patients with coronary artery disease: correlation with LDL cholesterol. Thromb. J. 2010; 10: 16, CrossRef.
Russo F, Di Bella S, Nigita G, Macca V, Laganà A, Giugno R, et al. miRandola: extracellular circulating microRNAs database. PLoS One. 2012; 7: e47786, CrossRef.
Rayner KJ, Sheedy FJ, Esau CC, Hussain FN, Temel RE, et al. Antagonism of mir-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J Clin Invest 2011; 121: 2921-31, CrossRef.
DOI: https://doi.org/10.18585/inabj.v6i1.39
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