MicroRNAs in Cardiometabolic Diseases

Anna Meiliana, Andi Wijaya

Abstract


BACKGROUND: MicroRNAs (miRNAs) are ~22-nucleotide noncoding RNAs with critical functions in multiple physiological and pathological processes. An explosion of reports on the discovery and characterization of different miRNA species and their involvement in almost every aspect of cardiac biology and diseases has established an exciting new dimension in gene regulation networks for cardiac development and pathogenesis.

CONTENT: Alterations in the metabolic control of lipid and glucose homeostasis predispose an individual to develop cardiometabolic diseases, such as type 2 diabetes mellitus and atherosclerosis. Work over the last years has suggested that miRNAs play an important role in regulating these physiological processes. Besides a cell-specific transcription factor profile, cell-specific miRNA-regulated gene expression is integral to cell fate and activation decisions. Thus, the cell types involved in atherosclerosis, vascular disease, and its myocardial sequelae may be differentially regulated by distinct miRNAs, thereby controlling highly complex processes, for example, smooth muscle cell phenotype and inflammatory responses of endothelial cells or macrophages. The recent advancements in using miRNAs as circulating biomarkers or therapeutic modalities, will hopefully be able to provide a strong basis for future research to further expand our insights into miRNA function in cardiovascular biology.

SUMMARY: MiRNAs are small, noncoding RNAs that function as post-transcriptional regulators of gene expression. They are potent modulators of diverse biological processes and pathologies. Recent findings demonstrated the importance of miRNAs in the vasculature and the orchestration of lipid metabolism and glucose homeostasis. MiRNA networks represent an additional layer of regulation for gene expression that absorbs perturbations and ensures the robustness of biological systems. A detailed understanding of the molecular and cellular mechanisms of miRNA-mediated effects on metabolism and vascular pathophysiology could pave the way for the development of novel diagnostic markers and therapeutic approaches.

KEYWORDS: microRNA, lipid metabolism, glucose homeostasis, vascular endothelium, vascular smooth muscle, atherosclerosis


Full Text:

PDF

References


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.

Van Rooij E. Introduction to the series on MicroRNAs in the cardiovascular system. Circ Res. 2012; 110: 481-2, CrossRef.

Fernandez-Hernando C, Ramirez CM, Goedeke L, Suarez Y. MicroRNAs in metabolic disease. Arterioscler Thromb Vasc Biol. 2013; 33: 178-85, CrossRef.

Weber C. MicroRNAs from basic mechanisms to clinical application in cardiovascular medicine. Arterioscler Thromb Vasc Biol. 2013; 33: 168-9, CrossRef.

Fiedler J, Thum T. MicroRNAs in myocardial infarction. Arterioscler Thromb Vasc Biol. 2013; 33: 201-5, 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.

Abdellatif M. Differential expression of microRNAs in different disease state. Circ Res. 2012; 110: 638-50, CrossRef.

Rana TM. Illuminating the silence: understanding the structure and function of small RNAs. Nat Rev Mol Cell Biol. 2007; 8: 23-36, CrossRef.

Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of posttranscriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet. 2008; 9: 102-14, CrossRef.

Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005; 120: 15-20, CrossRef.

Faraoni I, Antonetti FR, Cardone J. Bonmassar E. miR-155 gene: a typical multifunctional microRNA. Biochim Biophys Acta. 2009; 1792: 497-505, CrossRef.

Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008; 36: D154-8, CrossRef.

Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, et al. A uniform system for microRNA annotation. RNA. 2003; 9: 277-9, CrossRef.

Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature. 2008; 455: 58-63, CrossRef.

Baek D. The impact of microRNAs on protein output. Nature. 2008; 455: 64 -71, CrossRef.

Mukherji S, Ebert MS, Zheng GX, Tsang JS, Sharp PA, van Oudenaarden A. MicroRNAs can generate thresholds in target gene expression. Nat Genet. 2011; 43: 854-9, CrossRef.

Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM. Animal microRNAs confer robustness to gene expression and have a significant impact on 3’UTR evolution. Cell. 2005; 123: 1133-6, CrossRef.

Bartel DP, Chen CZ. Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat Rev Genet. 2004; 5: 396-400, CrossRef.

Farh KK, Grimson A, Jan C, Lewis BP, Johnston WK, Lim LP, et al. The widespread impact of mammalian microRNAs on mRNA repression and evolution. Science. 2005; 310: 1817-21, CrossRef.

Ambros V. The functions of animal microRNAs. Nature. 2004; 431: 350-5, CrossRef.

Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136: 215-33, CrossRef.

Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, et al. The nuclear RNase III drosha initiates microRNA processing. Nature. 2003; 425: 415-9, CrossRef.

Bauersachs J, Thum T. Biogenesis and regulation of cardiovascular MicroRNAs. Circ Res. 2011; 109: 334-47, 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(11): e3694, 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.

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.

Zile MR, Mehurg SM, Arroyo JE, Stroud RE, DeSantis SM, Spinale FG. Relationship between the temporal profile of plasma microRNA and left ventricular remodeling in patients after myocardial infarction. Circ Cardiovasc Genet. 2011; 4: 614-9, 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.

Li S, Zhu J, Zhang W, Chen Y, Zhang K, Popescu LM, et al. Signature microRNA expression profile of essential hypertension and its novel link to human cytomegalovirus infection. Circulation. 2011; 124: 175-84, 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.

Mayr M, Zampetaki A, Willeit P, Willeit J, Kiechl S. MicroRNAs within the continuum of postgenomics biomarker discovery. Arterioscler Thromb Vasc Biol. 2013; 33: 206-14, CrossRef.

Zampetaki A, Mayr M. MicroRNAs in vascular and metabolic disease. Circ Res. 2012; 110: 508-22, CrossRef.

Ouimet M, Moore KJ. A big role for small RNAs in HDL homeostasis. J Lipid Res. 2013; 54: 1161-7, CrossRef.

Ouimet M, Marcel YL. Regulation of lipid droplet cholesterol efflux from macrophage foam cells. Arterioscler Thromb Vasc Biol. 2012; 32: 575-81, CrossRef.

Krimbou L, Marcil M, Genest J. New insights into the biogenesis of human high-density lipoproteins. Curr Opin Lipidol. 2006; 17: 258-67, CrossRef.

Beltowski J. Liver X receptors (LXR) as therapeutic targets in dyslipidemia. Cardiovasc Ther. 2008; 26: 297-316, CrossRef.

Khera AV, Rader DJ. Future therapeutic directions in reverse cholesterol transport. Curr Atheroscler Rep. 2010; 12: 73-81, CrossRef.

Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr Biol. 2002; 12: 735-9, CrossRef.

Esau C, Davis S, Murray SF, Yu XX, Pandey SK, Pear M, et al. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab. 2006; 3: 87-98, CrossRef.

Hsu SH, Wang B, Kota J, Yu J, Costinean S, Kutay H, et al. Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver. J Clin Invest. 2012; 122: 2871-83, CrossRef.

Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, Munk ME, et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science. 2010; 327: 198-201, CrossRef.

Tsai WC, Hsu SD, Hsu CS, Lai TC, Chen SJ, Shen R, et al. MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. J Clin Invest. 2012; 122: 2884-97, CrossRef.

Gatfield D, Le Martelot G, Vejnar CE, Gerlach D, Schaad O, Fleury-Olela F, et al. Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev. 2009; 23: 1313-26, CrossRef.

Kojima S, Gatfield D, Esau CC, Green CB. MicroRNA-122 modulates the rhythmic expression profile of the circadian deadenylase Nocturnin in mouse liver. PLoS ONE. 2010; 5: e11264, CrossRef.

Krützfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, et al. Silencing of microRNAs in vivo with ‘antagomirs’. Nature. 2005; 438: 685-9, CrossRef.

Marquart TJ, Allen RM, Ory DS, Baldá A. miR-33 links SREBP-2 induction to repression of sterol transporters. Proc Natl Acad Sci USA. 2010; 107: 12228-32, 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.

Rayner KJ, Suárez Y, Dávalos A, Parathath S, Fitzgerald ML, Tamehiro N, et al. MiR-33 contributes to the regulation of cholesterol homeostasis. Science. 2010; 328: 1570-3, CrossRef.

Dávalos A, Goedeke L, Smibert P, Ramírez CM, Warrier NP, Andreo U, et al. miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling. Proc Natl Acad Sci USA. 2011; 108: 9232-7, CrossRef.

Gerin I, Clerbaux LA, Haumont O, Lanthier N, Das AK, Burant CF, et al. Expression of miR-33 from an SREBP2 intron inhibits cholesterol export and fatty acid oxidation. J Biol Chem. 2010; 285: 33652-61, CrossRef.

Fernandez-Hernando C, Suarez Y, Rayner KJ, Moore KJ. MicroRNAs in lipid metabolism. Curr Opin Lipidol. 2011; 22: 86-92, CrossRef.

Kim J, Yoon H, Ramírez CM, Lee SM, Hoe HS, Fernández-Hernando C, et al. MiR-106b impairs cholesterol efflux and increases Aß levels by repressing ABCA1 expression. Exp Neurol. 2012; 235: 476-83, 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.

Iliopoulos D, Drosatos K, Hiyama Y, Goldberg IJ, Zannis VI. MicroRNA-370 controls the expression of microRNA-122 and Cpt1alpha and affects lipid metabolism. J Lipid Res. 2010; 51: 1513-23, CrossRef.

Lynn FC, Skewes-Cox P, Kosaka Y, McManus MT, Harfe BD, German MS. MicroRNA expression is required for pancreatic islet cell genesis in the mouse. Diabetes. 2007; 56: 2938-45, CrossRef.

Melkman-Zehavi T, Oren R, Kredo-Russo S, Shapira T, Mandelbaum AD, Rivkin N, et al. miRNAs control insulin content in pancreatic ß-cells via downregulation of transcriptional repressors. EMBO J. 2011; 30: 835-45, CrossRef.

Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, Macdonald PE, et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature. 2004; 432: 226-30, CrossRef.

Poy MN, Hausser J, Trajkovski M, Braun M, Collins S, Rorsman P, et al. miR-375 maintains normal pancreatic alpha- and beta-cell mass. Proc Natl Acad Sci USA. 2009; 106: 5813-8, CrossRef.

Lovis P, Gattesco S, Regazzi R. Regulation of the expression of components of the exocytotic machinery of insulin-secreting cells by microRNAs. Biol Chem. 2008; 389: 305-12, CrossRef.

Plaisance V, Abderrahmani A, Perret-Menoud V, Jacquemin P, Lemaigre F, Regazzi R. MicroRNA-9 controls the expression of Granuphilin/Slp4 and the secretory response of insulin-producing cells. J Biol Chem. 2006; 281: 26932-42, CrossRef.

Ramachandran D, Roy U, Garg S, Ghosh S, Pathak S, Kolthur-Seetharam U. Sirt1 and mir-9 expression is regulated during glucose-stimulated insulin secretion in pancreatic ß-islets. FEBS J. 2011; 278: 1167-74, CrossRef.

Wijesekara N, Zhang LH, Kang MH, Abraham T, Bhattacharjee A, Warnock GL, et al. miR-33a modulates ABCA1 expression, cholesterol accumulation, and insulin secretion in pancreatic islets. Diabetes. 2012; 61: 653-8, CrossRef.

Lovis P, Roggli E, Laybutt DR, Gattesco S, Yang JY, Widmann C, et al. Alterations in microRNA expression contribute to fatty acidinduced pancreatic beta-cell dysfunction. Diabetes. 2008; 57: 2728-36, CrossRef.

Brunham LR, Kruit JK, Pape TD, Timmins JM, Reuwer AQ, Vasanji Z, et al. Beta-cell ABCA1 influences insulin secretion, glucose homeostasis and response to thiazolidinedione treatment. Nat Med. 2007; 13: 340-7, CrossRef.

Frost RJ, Olson EN. Control of glucose homeostasis and insulin sensitivity by the Let-7 family of microRNAs. Proc Natl Acad Sci USA. 2011; 108: 21075-80, CrossRef.

Zhu H, Shyh-Chang N, Segrè AV, Shinoda G, Shah SP, Einhorn WS, et al. The Lin28/let-7 axis regulates glucose metabolism. Cell. 2011; 147: 81-94, CrossRef.

Pullen TJ, da Silva Xavier G, Kelsey G, Rutter GA. miR-29a and miR-29b contribute to pancreatic beta-cell-specific silencing of monocarboxylate transporter 1 (Mct1). Mol Cell Biol. 2011; 31: 3182-94, CrossRef.

He A, Zhu L, Gupta N, Chang Y, Fang F. Overexpression of micro ribonucleic acid 29, highly up-regulated in diabetic rats, leads to insulin resistance in 3T3-L1 adipocytes. Mol Endocrinol. 2007; 21: 2785-94, CrossRef.

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.

Fernandez–Hernando C, Moore KJ. MicroRNA modulation of cholesterol homeostasis. Arterioscler Thromb Vasc Biol. 2011; 31: 2378-82, CrossRef.

Baker AH. MicroRNA 21 “shapes” vascular smooth muscle behavior through regulating tropomyosin 1. Arterioscler Thromb Vasc Biol. 2011; 31: 1941-2, CrossRef.

Davis-Dusenbery BN, Wu C, Hata A. Micromanaging vascular smooth muscle cell differentiation and phenotypic modulation. Arterioscler Thromb Vasc Biol. 2011; 31: 2370-7, CrossRef.

Epstein FH, Ross R. Atherosclerosis - An inflammatory disease. N Engl J Med. 1999; 340: 115-26, CrossRef.

Clowes AW, Clowes MM. Kinetics of cellular proliferation after arterial injury. IV. Heparin inhibits rat smooth muscle mitogenesis and migration. Circ Res. 1986; 58: 839-45, 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.

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.

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.

Chen J, Yin H, Jiang Y, Radhakrishnan SK, Huang ZP, Li J, et al. Induction of microRNA-1 by myocardin in smooth muscle cells inhibits cell proliferation. Arterioscler Thromb Vasc Biol. 2011; 31: 368-75, 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.

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.

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.

Quintavalle M, Elia L, Condorelli G, Courtneidge SA. MicroRNA control of podosome formation in vascular smooth muscle cells in vivo and in vitro. J Cell Biol. 2010; 189: 13-22, 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.

Miano JM, Long X, Fujiwara K. Serum response factor: master regulator of the actin cytoskeleton and contractile apparatus. Am J Physiol Cell Physiol. 2007; 292: C70-81, CrossRef.

Davis-Dusenbery BN, Chan MC, Reno KE, Weisman AS, Layne MD, Lagna G, et al. Down-regulation of Kruppellike factor-4 (KLF4) by microRNA-143/145 is critical for modulation of vascular smooth muscle cell phenotype by transforming growth factor-beta and bone morphogenetic protein 4. J Biol Chem. 2011; 286: 28097-110, CrossRef.

Horita HN, Simpson PA, Ostriker A, Furgeson S, Van Putten V, Weiser-Evans MC, et al. Serum response factor regulates expression of phosphatase and tensin homolog through a micro-RNA network in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2011; 31: 2909-19, CrossRef.

Nemenoff RA, Horita H, Ostriker AC, Furgeson SB, Simpson PA, VanPutten V, et al. SDF-1a induction in mature smooth muscle cells by inactivation of PTEN is a critical mediator of exacerbated injury induced neointima formation. Arterioscler Thromb Vasc Biol. 2011; 31: 1300-8, CrossRef.

Kang H, Davis-Dusenbery BN, Nguyen PH, Lal A, Lieberman J, Van Aelst L, et al. Bone morphogenetic protein 4 promotes vascular smooth muscle contractility by activating microRNA-21 (miR-21), which down-regulates expression of family of dedicator of cytokinesis (DOCK) proteins. J Biol Chem. 2012; 287: 3976-86, CrossRef.

Wang M, Li W, Chang GQ, Ye CS, Ou JS, Li XX, et al. MicroRNA-21 regulates vascular smooth muscle cell function via targeting tropomyosin 1 in arteriosclerosis obliterans of lower extremities. Arterioscler Thromb Vasc Biol. 2011; 31: 2044-53, CrossRef.

Yang S, Banerjee S, Freitas Ad, Cui H, Xie N, Abraham E, et al. miR-21 regulates chronic hypoxiainduced pulmonary vascular remodeling. Am J Physiol Lung Cell Mol Physiol. 2012; 302: L521-9, CrossRef.

Caruso P, MacLean MR, Khanin R, McClure J, Soon E, Southgate M, et al. Dynamic changes in lung microRNA profiles during the development of pulmonary hypertension due to chronic hypoxia and monocrotaline. Arterioscler Thromb Vasc Biol. 2010; 30: 716-23, CrossRef.

Robinson HC, Baker AH. How do microRNAs affect vascular smooth muscle cell biology? Curr Opin Lipidol. 2012; 23: 405-11, CrossRef.

Bonauer A, Boon RA, Dimmeler S. Vascular microRNAs. Curr Drug Targets. 2010; 11: 943-9, CrossRef.

Small EM, Olson EN. Pervasive roles of microRNAs in cardiovascular biology. Nature. 2011; 469: 336-42, CrossRef.

Dang LTH, Lawson ND, Fish JE. MicroRNA control of vascular endothelial growth factor signaling output during vascular development. Arterioscler Thromb Vasc Biol. 2013; 33: 193-200, CrossRef.

Ferrara N. Vascular endothelial growth factor. Arterioscler Thromb Vasc Biol. 2009; 29: 789-91, CrossRef.

Ambati BK, Nozaki M, Singh N, Takeda A, Jani PD, Suthar T, et al. Corneal avascularity is due to soluble VEGF receptor-1. Nature. 2006; 443: 993-7, CrossRef.

Boon RA. MicroRNAs control vascular endothelial growth factor signaling. Circ Res. 2012; 111: 1388-90, 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.

Doebele C, Bonauer A, Fischer A, Scholz A, Reiss Y, Urbich C, et al. Members of the microRNA-17-92 cluster exhibit a cell-intrinsic antiangiogenic function in endothelial cells. Blood. 2010; 115: 4944-50, CrossRef.

Zhou Q, Gallagher R, Ufret-Vincenty R, Li X, Olson EN, Wang S. Regulation of angiogenesis and choroidal neovascularization by members of microRNA-23~27~24 clusters. Proc Natl Acad Sci USA. 2011; 108: 8287-92, CrossRef.

Urbich C, Kaluza D, Frömel T, Knau A, Bennewitz K, Boon RA, et al. MicroRNA-27a/b controls endothelial cell repulsion and angiogenesis by targeting semaphorin 6A. Blood. 2012; 119: 1607-16, CrossRef.

Fiedler J, Jazbutyte V, Kirchmaier BC, Gupta SK, Lorenzen J, Hartmann D, et al. MicroRNA-24 regulates vascularity after myocardial infarction. Circulation. 2011; 124: 720-30, CrossRef.

Schulz R, Rassaf T, Massion PB, Kelm M, Balligand JL. Recent advances in the understanding of the role of nitric oxide in cardiovascular homeostasis. Pharmacol Ther. 2005; 108: 225-56, CrossRef.

Balligand JL, Feron O, Dessy C. eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev. 2009; 89: 481-534, CrossRef.

Förstermann U, Münzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation. 2006; 113: 1708-14, CrossRef.

Sun HX, Zen DY, Li RT, Pang RP, Yang H, Hu YL, et al. Essential role of microRNA-155 in regulating endothelium-dependent vasorelaxation by targeting endothelial nitric oxide synthase. Hypertension. 2012; 60: 1407-14, CrossRef.

Fish JE, Cybulsky MI. Taming endothelial dysfunction activation with a microRNA. J Clin Invest. 2012; 122: 1967-70, CrossRef.

Grundmann S, Hans FP, Kinniry S, Heinke J, Helbing T, Bluhm F, et al. MicroRNA-100 regulates neovascularization by suppression of mammalian target of rapamycin in endothelial and vascular smooth muscle cells. Circulation. 2011; 123: 999-1009, CrossRef.

Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med. 2000; 6: 389-95, 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.

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.

Dimmeler S, Aicher A, Vasa M, Mildner-Rihm C, Adler K, Tiemann M, et al. HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/Akt pathway. J Clin Invest. 2001; 108: 391-7, CrossRef.

Vasa M, Fichtlscherer S, Adler K, Aicher A, Martin H, Zeiher AM, et al. Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation. 2001; 103: 2885-90, CrossRef.

Vickers KC, Remaley AT. MicroRNAs in atherosclerosis ad lipoprotein metabolism. Curr Opin Endocrinol Diabetes Obes. 2010; 17: 150-5, CrossRef.

Wei Y, Nazari–Jahantigh M, Neth P, Weber C, Schober A. MicroRNA-126, -145, and -155: A therapeutic triad in atherosclerosis? Arterioscler Thromb Vasc Biol. 2013; 33: 449-54, 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.

Fichtlscherer S, Zeiher A, Dimmeler S. Circulating microRNAs: Biomarkers or mediators of cardiovascular diseases?. Arterioscler Thromb Vasc Biol. 2011; 31: 2383-90, CrossRef.

Trang P, Wiggins JF, Daige CL, Cho C, Omotola M, Brown D, et al. Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol Ther. 2011; 19: 1116-22, CrossRef.

Ferdinandy P, Schulz R. Nitric oxide, superoxide, and peroxynitrite in myocardial ischaemia-reperfusion injury and preconditioning. Br J Pharmacol. 2003; 138: 532-43, CrossRef.

Frangogiannis NG, Smith CW, Entman ML. The inflammatory response in myocardial infarction. Cardiovasc Res. 2002; 53: 31-47, CrossRef.

Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 2007; 87: 315-424, CrossRef.

Wang J, Huang W, Xu R, Nie Y, Cao X, Meng J, et al. MicroRNA-24 regulates cardiac fibrosis after myocardial infarction. J Cell Mol Med. 2012; 16: 2150-60, CrossRef.

Qian L, Van Laake LW, Huang Y, Liu S, Wendland MF, Srivastava D. miR-24 inhibits apoptosis and represses Bim in mouse cardiomyocytes. J Exp Med. 2011; 208: 549-60, 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.

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.

Ji X, Takahashi R, Hiura Y, Hirokawa G, Fukushima Y, Iwai N. Plasma miR-208 as a biomarker of myocardial injury. Clin Chem. 2009; 55: 1944-9, CrossRef.

D’Alessandra Y, Devanna P, Limana F, Straino S, Di Carlo A, Brambilla PG, et al. Circulating microRNAs are new and sensitive biomarkers of myocardial infarction. Eur Heart J. 2010; 31: 2765-73, CrossRef.

Bostjancic E, Zidar N, Stajer D, Glavac D. MicroRNAs miR-1, miR-133a, miR-133b and miR-208 are dysregulated in human myocardial infarction. Cardiology. 2010; 115: 163-9, CrossRef.

Kuwabara Y, Ono K, Horie T, Nishi H, Nagao K, Kinoshita M, et al. Increased microRNA-1 and microRNA-133a levels in serum of patients with cardiovascular disease indicate myocardial damage. Circ Cardiovasc Genet. 2011; 4: 446-54, CrossRef.

Adachi T, Nakanishi M, Otsuka Y, Nishimura K, Hirokawa G, Goto Y, et al. Plasma microRNA 499 as a biomarker of acute myocardial infarction. Clin Chem. 2010; 56: 1183-5, CrossRef.

Ai J, Zhang R, Li Y, Pu J, Lu Y, Jiao J, et al. Circulating microRNA-1 as a potential novel biomarker for acute myocardial infarction. Biochem Biophys Res Commun. 2010; 391: 73-7, CrossRef.

Cheng Y, Tan N, Yang J, Liu X, Cao X, He P, et al. A translational study of circulating cell-free microRNA-1 in acute myocardial infarction. Clin Sci (Lond). 2010; 119: 87-95, CrossRef.

van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J, Olson EN. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science. 2007; 316: 575-9, CrossRef.

van Rooij E, Quiat D, Johnson BA, Sutherland LB, Qi X, Richardson JA, et al. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell. 2009; 17: 662-73, CrossRef.

Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet. 2006; 38: 228-33, CrossRef.

Wang X, Zhang X, Ren XP, Chen J, Liu H, Yang J, et al. MicroRNA-494 targeting both proapoptotic and antiapoptotic proteins protects against ischemia/reperfusion-induced cardiac injury. Circulation. 2010; 122: 1308-18, CrossRef.

Ren XP, Wu J, Wang X, Sartor MA, Qian J, Jones K, et al. MicroRNA-320 is involved in the regulation of cardiac ischemia/reperfusion injury by targeting heat-shock protein 20. Circulation. 2009; 119: 2357-66, CrossRef.




DOI: https://doi.org/10.18585/inabj.v5i2.55

Indexed by:

                 

                  

               

     

 

The Prodia Education and Research Institute