MicroRNAs involved in the lipid metabolism and their possible implications for atherosclerosis development and treatment

Mediators of Inflammation

Volumn 2014, Issue , 2014, Pages

  Novák, Jan ^a,b   Bienertová Vašků, Julie ^b   Kára, Tomáš ^a   Novák, Miroslav ^a  

^a ST ANNE S UNIVERSITY HOSPITAL   (Czech Republic)

^b MASARYK UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ANTAGOMIR; BIOLOGICAL MARKER; FARNESOID X RECEPTOR; HIGH DENSITY LIPOPROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INSULIN RECEPTOR SUBSTRATE 2; LIPID; LIVER X RECEPTOR; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MESSENGER RNA; MICRORNA; MICRORNA 122; MICRORNA 144; MICRORNA 155; MICRORNA 27A; MICRORNA 27B; MICRORNA 29A; MICRORNA 33; MICRORNA 370; MICRORNA 9; MIRAVIRSEN; RNA; SIRTUIN 1; SMALL UNTRANSLATED RNA; STEROL REGULATORY ELEMENT BINDING PROTEIN; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; ATHEROSCLEROSIS; BIOGENESIS; BLOOD SAMPLING; CARCINOGENESIS; CELL ACTIVATION; CHLOROCEBUS AETHIOPS; DYSLIPIDEMIA; EXTRACELLULAR SPACE; FAMILIAL HYPERCHOLESTEROLEMIA; FATTY ACID OXIDATION; GENE EXPRESSION; GENE TARGETING; HEPATITIS; HISTOPATHOLOGY; HUMAN; HYPERLIPIDEMIA; INSULIN RESISTANCE; LIPID BLOOD LEVEL; LIPID METABOLISM; LIPOGENESIS; LIPOPROTEIN METABOLISM; NONHUMAN; OBESITY; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REVIEW; RODENT; SIGNAL TRANSDUCTION; SMOKING; ANIMAL; DISEASE COURSE; GENE REGULATORY NETWORK; METABOLISM; MOUSE; PATHOPHYSIOLOGY; RNA PROCESSING;

ANIMALS; ATHEROSCLEROSIS; BIOLOGICAL MARKERS; CERCOPITHECUS AETHIOPS; DISEASE PROGRESSION; GENE REGULATORY NETWORKS; HUMANS; LIPID METABOLISM; LIPOPROTEINS, HDL; MICE; MICRORNAS; RNA PROCESSING, POST-TRANSCRIPTIONAL;

EID: 84901044615     PISSN: 09629351     EISSN: 14661861     Source Type: Journal    
DOI: 10.1155/2014/275867     Document Type: Review

References (110)

1. Ross R., Atherosclerosis: an inflammatory disease. The New England Journal of Medicine 1999 340 115 126 10.1056/nejm199901143400207
2. Glueck C. J., Role of risk factor management in progression and regression of coronary and femoral artery atherosclerosis. The American Journal of Cardiology 1986 57 14 35G 41G 2-s2.0-0022516938
3. Al Montasir A., Sadik M. H., Acute myocardial infarction in a 28 year man with familial hypercholesterolemia. Indian Journal of Medical Sciences 2012 66 78 81 10.4103/0019-5359.110914
4. Goldberg A. C., Hopkins P. N., Toth P. P., Ballantyne C. M., Rader D. J., Robinson J. G., Daniels S. R., Gidding S. S., De Ferranti S. D., Ito M. K., McGowan M. P., Moriarty P. M., Cromwell W. C., Ross J. L., Ziajka P. E., Familial hypercholesterolemia: screening, diagnosis and management of pediatric and adult patients: clinical guidance from the National Lipid Association expert panel on familial hypercholesterolemia. Journal of Clinical Lipidology 2011 5 3 S1 S8 2-s2.0-79956267846 10.1016/j.jacl.2011.04.003
5. Rader D. J., Cohen J., Hobbs H. H., Monogenic hypercholesterolemia: new insights in pathogenesis and treatment. Journal of Clinical Investigation 2003 111 12 1795 1803 2-s2.0-0041743167 10.1172/JCI200318925
6. Rayner K. J., Suárez Y., Dávalos A., Parathath S., Fitzgerald M. L., Tamehiro N., Fisher E. A., Moore K. J., Fernández- Hernando C., MiR-33 contributes to the regulation of cholesterol homeostasis. Science 2010 328 5985 1570 1573 2-s2.0-77953787211 10.1126/science.1189862
7. Najafi-Shoushtari S. H., Kristo F., Li Y., Shioda T., Cohen D. E., Gerszten R. E., Näär A. M., MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 2010 328 5985 1566 1569 2-s2.0-77953780835 10.1126/science.1189123
8. Gerin I., Clerbaux L.-A., Haumont O., Lanthier N., Das A. K., Burant C. F., Leclercq I. A., MacDougald O. A., Bommer G. T., Expression of miR-33 from an SREBP2 intron inhibits cholesterol export and fatty acid oxidation. Journal of Biological Chemistry 2010 285 44 33652 33661 2-s2.0-77958553499 10.1074/jbc.M110.152090
9. Goedeke L., Vales-Lara F. M., Fenstermaker M., A regulatory role for microRNA 33 in controlling lipid metabolism gene expression. Molecular and Cellular Biology 2013 33 2339 2352 10.1128/mcb.01714-12
10. Marquart T. J., Allen R. M., Ory D. S., Baldán Á., MiR-33 links SREBP-2 induction to repression of sterol transporters. Proceedings of the National Academy of Sciences of the United States of America 2010 107 27 12228 12232 2-s2.0-77955456415 10.1073/pnas.1005191107
11. Allen R. M., Marquart T. J., Albert C. J., MiR-33 controls the expression of biliary transporters, and mediates statin- and diet-induced hepatotoxicity. The EMBO Molecular Medicine 2012 4 882 895 10.1002/emmm.201201228
12. Krützfeldt J., Rajewsky N., Braich R., Rajeev K. G., Tuschl T., Manoharan M., Stoffel M., Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005 438 7068 685 689 2-s2.0-28444469246 10.1038/nature04303
13. Esau C., Davis S., Murray S. F., Yu X. X., Pandey S. K., Pear M., Watts L., Booten S. L., Graham M., McKay R., Subramaniam A., Propp S., Lollo B. A., Freier S., Bennett C. F., Bhanot S., Monia B. P., MiR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metabolism 2006 3 2 87 98 2-s2.0-33645075443 10.1016/j.cmet.2006.01.005
14. Hsu S. H., Wang B., Kota J., Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver. The Journal of Clinical Investigation 2012 122 2871 2883 10.1172/jci63539
15. Tsai W. C., Hsu S. D., Hsu C. S., MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. The Journal of Clinical Investigation 2012 122 2884 2897 10.1172/jci63455
16. Shirasaki T., Honda M., Shimakami T., MicroRNA-27a regulates lipid metabolism and inhibits hepatitis C virus replication in human hepatoma cells. Journal of Virology 2013 87 5270 5286
17. Kida K., Nakajima M., Mohri T., Oda Y., Takagi S., Fukami T., Yokoi T., PPAR α is regulated by miR-21 and miR-27b in human liver. Pharmaceutical Research 2011 28 10 2467 2476 2-s2.0-80054764011 10.1007/s11095-011-0473-y
18. Vickers K. C., Shoucri B. M., Levin M. G., MicroRNA-27b is a regulatory hub in lipid metabolism and is altered in dyslipidemia. Hepatology 2013 57 533 542 10.1002/hep.25846
19. Lin Q., Gao Z., Alarcon R. M., Ye J., Yun Z., A role of miR-27 in the regulation of adipogenesis. FEBS Journal 2009 276 8 2348 2358 2-s2.0-63049108381 10.1111/j.1742-4658.2009.06967.x
20. Kim S. Y., Kim A. Y., Lee H. W., Son Y. H., Lee G. Y., Lee J.-W., Lee Y. S., Kim J. B., MiR-27a is a negative regulator of adipocyte differentiation via suppressing PPAR γ expression. Biochemical and Biophysical Research Communications 2010 392 3 323 328 2-s2.0-76349089521 10.1016/j.bbrc.2010.01.012
21. Iliopoulos D., Drosatos K., Hiyama Y., Goldberg I. J., Zannis V. I., MicroRNA-370 controls the expression of MicroRNA-122 and Cpt1 α and affects lipid metabolism. Journal of Lipid Research 2010 51 6 1513 1523 2-s2.0-77952707662 10.1194/jlr.M004812
22. de Aguiar Vallim T. Q., Tarling E. J., Kim T., MicroRNA-144 regulates hepatic ATP binding cassette transporter A1 and plasma high-density lipoprotein after activation of the nuclear receptor farnesoid X receptor. Circulation Research 2013 112 1602 1612 10.1161/circresaha.112.300648
23. Ramirez C. M., Rotllan N., Vlassov A. V., Control of cholesterol metabolism and plasma high-density lipoprotein levels by microRNA-144. Circulation Research 2013 112 1592 1601 10.1161/circresaha.112.300626
24. Zhong D., Huang G., Zhang Y., MicroRNA-1 and microRNA-206 suppress LXRalpha-induced lipogenesis in hepatocytes. Cellular Signalling 2013 25 1429 137 10.1016/j.cellsig.2013.03.003
25. Xu J., Hu G., Lu M., MiR-9 reduces human acyl-coenzyme A:cholesterol acyltransferase-1 to decrease THP-1 macrophage-derived foam cell formation. Acta Biochimica et Biophysica Sinica 2013 45 953 962 10.1093/abbs/gmt096
26. Thulin P., Wei T., Werngren O., MicroRNA-9 regulates the expression of peroxisome proliferator-activated receptor delta in human monocytes during the inflammatory response. International Journal of Molecular Medicine 2013 31 1003 1010 10.3892/ijmm.2013.1311
27. Ahn J., Lee H., Jung C. H., Ha T., Lycopene inhibits hepatic steatosis via microRNA-21-induced downregulation of fatty acid-binding protein 7 in mice fed a high-fat diet. Molecular nutrition and Food Research 2012 56 1665 1674 10.1002/mnfr.201200182
28. Chen T., Li Z., Tu J., Zhu W., Ge J., Zheng X., Yang L., Pan X., Yan H., Zhu J., MicroRNA-29a regulates pro-inflammatory cytokine secretion and scavenger receptor expression by targeting LPL in oxLDL-stimulated dendritic cells. FEBS Letters 2011 585 4 657 663 2-s2.0-79951579619 10.1016/j.febslet.2011.01.027
29. Soh J., Iqbal J., Queiroz J., Fernandez-Hernando C., Hussain M. M., MicroRNA-30c reduces hyperlipidemia and atherosclerosis in mice by decreasing lipid synthesis and lipoprotein secretion. Nature Medicine 2013 19 892 900 10.1038/nm.3200
30. Chen T., Huang Z., Wang L., Wang Y., Wu F., Meng S., Wang C., MicroRNA-125a-5p partly regulates the inflammatory response, lipid uptake, and ORP9 expression in oxLDL-stimulated monocyte/macrophages. Cardiovascular Research 2009 83 1 131 139 2-s2.0-67649349865 10.1093/cvr/cvp121
31. Chen T., Li Z., Jing T., Zhu W., Ge J., Zheng X., Pan X., Yan H., Zhu J., MicroRNA-155 regulates lipid uptake, adhesion/chemokine marker secretion and SCG2 expression in oxLDL-stimulated dendritic cells/macrophages. International Journal of Cardiology 2011 147 3 446 447 2-s2.0-79952485681 10.1016/j.ijcard. 2010.10.133
32. Miller A. M., Gilchrist D. S., Nijjar J., MiR-155 has a protective role in the development of non-alcoholic hepatosteatosis in mice. PLoS ONE 2013 8 0072324 10.1371/journal.pone.0072324
33. Zhu G. F., Yang L. X., Guo R. W., MiR-155 inhibits oxidized low-density lipoprotein-induced apoptosis of RAW264. 7 cells. Molecular and Cellular Biochemistry 2013 382 253 261 10.1007/s11010-013-1741-4
34. Sun X., He S., Wara A. K., Systemic delivery of MicroRNA-181b inhibits NF-kappaB activation, vascular inflammation, and atherosclerosis in Apoe-/- Mice. Circulation Research 2014 114 1 32 40 10.1161/circresaha.113.302089
35. Li X., Chen Y. T., Josson S., MicroRNA-185 and 342 inhibit tumorigenicity and induce apoptosis through blockade of the SREBP metabolic pathway in prostate cancer cells. PLoS ONE 2013 8 e70987 10.1371/journal.pone.0070987
36. Yin H., Hu M., Zhang R., Shen Z., Flatow L., You M., MicroRNA-217 promotes ethanol-induced fat accumulation in hepatocytes by down-regulating SIRT1. Journal of Biological Chemistry 2012 287 13 9817 9826 2-s2.0-84858968923 10.1074/jbc.M111.333534
37. Nakanishi N., Nakagawa Y., Tokushige N., Aoki N., Matsuzaka T., Ishii K., Yahagi N., Kobayashi K., Yatoh S., Takahashi A., Suzuki H., Urayama O., Yamada N., Shimano H., The up-regulation of microRNA-335 is associated with lipid metabolism in liver and white adipose tissue of genetically obese mice. Biochemical and Biophysical Research Communications 2009 385 4 492 496 2-s2.0-67349179168 10.1016/j.bbrc.2009.05.058
38. Carrer M., Liu N., Grueter C. E., Control of mitochondrial metabolism and systemic energy homeostasis by microRNAs 378 and 378 Proceedings of the National Academy of Sciences of the United States of America 2012 109 15330 15335 10.1073/pnas.1207605109
39. Gerin I., Bommer G. T., McCoin C. S., Sousa K. M., Krishnan V., MacDougald O. A., Roles for miRNA-378/378 in adipocyte gene expression and lipogenesis. The American Journal of Physiology: Endocrinology and Metabolism 2010 299 2 E198 E206 2-s2.0-77954932826 10.1152/ajpendo.00179.2010
40. Ahn J., Lee H., Chung C. H., Ha T., High fat diet induced downregulation of microRNA-467b increased lipoprotein lipase in hepatic steatosis. Biochemical and Biophysical Research Communications 2011 414 4 664 669 2-s2.0-80555150535 10.1016/j.bbrc.2011.09.120
41. Tian G. P., Chen W. J., He P. P., MicroRNA-467b targets LPL gene in RAW 264. 7 macrophages and attenuates lipid accumulation and proinflammatory cytokine secretion. Biochimie 2012 94 2749 2755 10.1016/j.biochi.2012.08.018
42. Zhong D., Zhang Y., Zeng Y. J., MicroRNA-613 represses lipogenesis in HepG2 cells by downregulating LXRalpha. Lipids in Health and Disease 2013 12, article 32 10.1186/1476-511x-12-32
43. Ginter E., Simko V., New promising potential in fighting atherosclerosis: HDL and reverse cholesterol transport. Bratislavske Lekarske Listy 2013 114 172 176
44. Peluso I., Morabito G., Urban L., Ioannone F., Serafini M., Oxidative stress in atherosclerosis development: the central role of LDL and oxidative burst. Endocrine, Metabolic and Immune Disorders Drug Targets 2012 12 351 360
45. McGill H. C. Jr., McMahan C. A., Kruski A. W., Mott G. E., Relationship of lipoprotein cholesterol concentrations to experimental atherosclerosis in baboons. Arteriosclerosis 1981 1 1 3 12 2-s2.0-0019518390
46. Shimano H., Aburatani H., Mori N., Ishibashi S., Gotohda T., Mokuno H., Kawakami M., Akanuma Y., Takaku F., Murase T., Yamada N., Down-regulation of hepatic LDL receptor protein and messenger RNA in fasted rabbits. Journal of Biochemistry 1988 104 5 712 716 2-s2.0-0023734720
47. Kzhyshkowska J., Neyen C., Gordon S., Role of macrophage scavenger receptors in atherosclerosis. Immunobiology 2012 217 5 492 502 2-s2.0-84858793002 10.1016/j.imbio.2012.02.015
48. Lee Y., Jeon K., Lee J.-T., Kim S., Kim V. N., MicroRNA maturation: stepwise processing and subcellular localization. The EMBO Journal 2002 21 17 4663 4670 2-s2.0-0037009364 10.1093/emboj/cdf476
49. He L., Hannon G. J., MicroRNAs: small RNAs with a big role in gene regulation. Nature Reviews Genetics 2004 5 522 531 2-s2.0-3442889162 10.1038/nrg1379
50. Madrigal-Matute J., Rotllan N., Aranda J. F., Fernandez-Hernando C., MicroRNAs and atherosclerosis. Current Atherosclerosis Reports 2013 15 5, article 322 10.1007/s11883-013-0322-z
51. Yang J.-S., Lai E. C., Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Molecular Cell 2011 43 6 892 903 2-s2.0-80052996141 10.1016/j.molcel.2011.07.024
52. Mitchell P. S., Parkin R. K., Kroh E. M., Fritz B. R., Wyman S. K., Pogosova-Agadjanyan E. L., Peterson A., Noteboom J., O'Briant K. C., Allen A., Lin D. W., Urban N., Drescher C. W., Knudsen B. S., Stirewalt D. L., Gentleman R., Vessella R. L., Nelson P. S., Martin D. B., Tewari M., Circulating microRNAs as stable blood-based markers for cancer detection. Proceedings of the National Academy of Sciences of the United States of America 2008 105 30 10513 10518 2-s2.0-48749122914 10.1073/pnas.0804549105
53. Vickers K. C., Palmisano B. T., Shoucri B. M., Shamburek R. D., Remaley A. T., MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nature Cell Biology 2011 13 4 423 435 2-s2.0-79953301730 10.1038/ncb2210
54. Redova M., Sana J., Slaby O., Circulating miRNAs as new blood-based biomarkers for solid cancers. Future Oncology 2013 9 387 402 10.2217/fon.12.192
55. Musso G., Gambino R., Cassader M., Cholesterol metabolism and the pathogenesis of non-alcoholic steatohepatitis. Progress in Lipid Research 2013 52 175 91 10.1016/j.plipres.2012.11.002
56. Rodriguez A., Griffiths-Jones S., Ashurst J. L., Bradley A., Identification of mammalian microRNA host genes and transcription units. Genome Research 2004 14 1902 1910 2-s2.0-6344281172 10.1101/gr.2722704
57. Kozomara A., Griffiths-Jones S., MiRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Research 2011 39 1 D152 D157 2-s2.0-78651293534 10.1093/nar/gkq1027
58. Dávalos A., Goedeke L., Smibert P., Ramírez C. M., Warrier N. P., Andreo U., Cirera-Salinas D., Rayner K., Suresh U., Pastor-Pareja J. C., Esplugues E., Fisher E. A., Penalva L. O. F., Moore K. J., Suárez Y., Lai E. C., Fernández-Hernando C., MiR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling. Proceedings of the National Academy of Sciences of the United States of America 2011 108 22 9232 9237 2-s2.0-79959326172 10.1073/pnas.1102281108
59. Ramirez C. M., Goedeke L., Rotllan N., MicroRNA 33 regulates glucose metabolism. Molecular and Cellular Biology 2013 33 2891 2902 10.1128/mcb.00016-13
60. Lagos-Quintana M., Rauhut R., Yalcin A., Meyer J., Lendeckel W., Tuschl T., Identification of tissue-specific MicroRNAs from mouse. Current Biology 2002 12 9 735 739 2-s2.0-0037197803 10.1016/S0960-9822(02)00809-6
61. Chang J., Nicolas E., Marks D., Sander C., Lerro A., Buendia M. A., Xu C., Mason W. S., Moloshok T., Bort R., Zaret K. S., Taylor J. M., MiR-122, a mammalian liver-specific microRNA, is processed from hcr mRNA and may downregulate the high affinity cationic amino acid transporter CAT-1. RNA Biology 2004 1 2 106 113 2-s2.0-23844523406
62. Conrad K. D., Niepmann M., Role of microRNAs in hepatitis C virus RNA replication. Archives of Virology 2013 10.1007/s00705-013-1883-4
63. Hu J., Xu Y., Hao J., Wang S., Li C., Meng S., MiR-122 in hepatic function and liver diseases. Protein and Cell 2012 3 364 371 10.1007/s13238-012-2036-3
64. Elmén J., Lindow M., Silahtaroglu A., Bak M., Christensen M., Lind-Thomsen A., Hedtjärn M., Hansen J. B., Hansen H. F., Straarup E. M., McCullagh K., Kearney P., Kauppinen S., Antagonism of microRNA-122 in mice by systemically administered LNA-antimiR leads to up-regulation of a large set of predicted target mRNAs in the liver. Nucleic Acids Research 2008 36 4 1153 1162 2-s2.0-40249106014 10.1093/nar/gkm1113
65. Moore K. J., Rayner K. J., Suárez Y., Fernández-Hernando C., MicroRNAs and cholesterol metabolism. Trends in Endocrinology and Metabolism 2010 21 12 699 706 2-s2.0-78650262887 10.1016/j.tem.2010.08.008
66. Gao W., He H. W., Wang Z. M., Plasma levels of lipometabolism-related miR-122 and miR-370 are increased in patients with hyperlipidemia and associated with coronary artery disease. Lipids in Health and Disease 2012 11, artricle 55 10.1186/1476-511x-11-55
67. Vickers K. C., Rader D. J., Nuclear receptors and microRNA-144 coordinately regulate cholesterol efflux. Circulation Research 2013 112 1529 1531 10.1161/circresaha.113.301422
68. Wang D., Xia M., Yan X., Gut microbiota metabolism of anthocyanin promotes reverse cholesterol transport in mice via repressing miRNA-10b. Circulation Research 2012 111 967 981 266502
69. Sun D., Zhang J., Xie J., Wei W., Chen M., Zhao X., MiR-26 controls LXR-dependent cholesterol efflux by targeting ABCA1 and ARL7. FEBS Letters 2012 586 1472 1479 2-s2.0-84860197637 10.1016/j.febslet.2012.03.068
70. Kang M. H., Zhang L., Wijesekara N., Regulation of ABCA1 protein expression and function in hepatic and pancreatic islet cells by miR-145. Arteriosclerosis, Thrombosis, and Vascular Biology 2013 33 12 2724 2732 10.1161/atvbaha.113.302004
71. Kim J., Yoon H., Ramírez C. M., Lee S.-M., Hoe H.-S., Fernández-Hernando C., Kim J., MiR-106b impairs cholesterol efflux and increases A β levels by repressing ABCA1 expression. Experimental Neurology 2012 235 2 476 483 2-s2.0-84860377430 10.1016/j.expneurol.2011.11.010
72. Ramirez C. M., Dávalos A., Goedeke L., Salerno A. G., Warrier N., Cirera-Salinas D., Suárez Y., Fernández-Hernando C., MicroRNA-758 regulates cholesterol efflux through posttranscriptional repression of ATP-binding cassette transporter A1. Arteriosclerosis, Thrombosis, and Vascular Biology 2011 31 11 2707 2714 2-s2.0-80054900644 10.1161/ATVBAHA.111.232066
73. Fish J. E., Santoro M. M., Morton S. U., Yu S., Yeh R.-F., Wythe J. D., Ivey K. N., Bruneau B. G., Stainier D. Y. R., Srivastava D., MiR-126 regulates angiogenic signaling and vascular integrity. Developmental Cell 2008 15 2 272 284 2-s2.0-48749130187 10.1016/j.devcel.2008.07.008
74. Wang S., Aurora A. B., Johnson B. A., Qi X., McAnally J., Hill J. A., Richardson J. A., Bassel-Duby R., Olson E. N., The endothelial-specific MicroRNA miR-126 governs vascular integrity and angiogenesis. Developmental Cell 2008 15 2 261 271 2-s2.0-48549106378 10.1016/j.devcel.2008.07.002
75. Li J., Zhang Y., Liu Y., Microvesicle-mediated transfer of microRNA-150 from monocytes to endothelial cells promotes angiogenesis. The Journal of Biological Chemistry 2013 288 23586 23596 10.1074/jbc.M113.489302
76. Zhang Y., Liu D., Chen X., Secreted monocytic miR-150 enhances targeted endothelial cell migration. Molecular cell. 2010 39 133 144 10.1016/j.molcel. 2010.06.010
77. Wagner J., Riwanto M., Besler C., Characterization of levels and cellular transfer of circulating lipoprotein-bound microRNAs. Arteriosclerosis, Thrombosis, and Vascular Biology 2013 33 1392 1400 300741
78. Weber J. A., Baxter D. H., Zhang S., Huang D. Y., Huang K. H., Lee M. J., Galas D. J., Wang K., The microRNA spectrum in 12 body fluids. Clinical Chemistry 2010 56 11 1733 1741 2-s2.0-78149484489 10.1373/clinchem.2010.147405
79. Valadi H., Ekström K., Bossios A., Sjöstrand M., Lee J. J., Lötvall J. O., Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biology 2007 9 6 654 659 2-s2.0-34249302620 10.1038/ncb1596
80. Hunter M. P., Ismail N., Zhang X., Aguda B. D., Lee E. J., Yu L., Xiao T., Schafer J., Lee M.-L. T., Schmittgen T. D., Nana-Sinkam S. P., Jarjoura D., Marsh C. B., Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE 2008 3 11 2-s2.0-57849130395 10.1371/journal.pone. 0003694 e3694
81. Zernecke A., Bidzhekov K., Noels H., Shagdarsuren E., Gan L., Denecke B., Hristov M., Köppel T., Jahantigh M. N., Lutgens E., Wang S., Olson E. N., Schober A., Weber C., Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Science Signaling 2009 2 100 ra81 2-s2.0-77449127999 10.1126/scisignal.2000610
82. Turchinovich A., Weiz L., Langheinz A., Burwinkel B., Characterization of extracellular circulating microRNA. Nucleic Acids Research 2011 39 16 7223 7233 2-s2.0-80052381608 10.1093/nar/gkr254
83. Ji X., Takahashi R., Hiura Y., Hirokawa G., Fukushima Y., Iwai N., Plasma miR-208 as a biomarker of myocardial injury. Clinical Chemistry 2009 55 11 1944 1949 2-s2.0-70449709345 10.1373/clinchem.2009.125310
84. Kosaka N., Iguchi H., Yoshioka Y., Takeshita F., Matsuki Y., Ochiya T., Secretory mechanisms and intercellular transfer of microRNAs in living cells. Journal of Biological Chemistry 2010 285 23 17442 17452 2-s2.0-77952920881 10.1074/jbc.M110.107821
85. Diehl P., Fricke A., Sander L., Stamm J., Bassler N., Htun N., Ziemann M., Helbing T., El-Osta A., Jowett J. B. M., Peter K., Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovascular Research 2012 93 4 633 644 2-s2.0-84857975438 10.1093/cvr/cvs007
86. Fichtlscherer S., De Rosa S., Fox H., Schwietz T., Fischer A., Liebetrau C., Weber M., Hamm C. W., Röxe T., Müller-Ardogan M., Bonauer A., Zeiher A. M., Dimmeler S., Circulating microRNAs in patients with coronary artery disease. Circulation Research 2010 107 5 677 684 2-s2.0-77957028990 10.1161/CIRCRESAHA.109.215566
87. Karolina D. S., Tavintharan S., Armugam A., Circulating miRNA profiles in patients with metabolic syndrome. The Journal of Clinical Endocrinology and Metabolism 2012 97 2271 2276 10.1210/jc.2012-1996
88. Finn N. A., Eapen D., Manocha P., Coronary heart disease alters intercellular communication by modifying microparticle-mediated microRNA transport. FEBS Letters 2013 587 3456 3463 10.1016/j.febslet.2013.08.034
89. Zhou J., Li Y. S., Nguyen P., Regulation of vascular smooth muscle cell turnover by endothelial cell-secreted microRNA-126: role of shear stress. Circulation Research 2013 113 40 51 10.1161/circresaha.113.280883
90. Sun X., Zhang M., Sanagawa A., Circulating microRNA-126 in patients with coronary artery disease: correlation with LDL cholesterol. Thrombosis Journal 2012 10, article 16 10.1186/1477-9560-10-16
91. Harris T. A., Yamakuchi M., Ferlito M., Mendell J. T., Lowenstein C. J., MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proceedings of the National Academy of Sciences of the United States of America 2008 105 5 1516 1521 2-s2.0-40349103409 10.1073/pnas.0707493105
92. Zampetaki A., Willeit P., Tilling L., Prospective study on circulating MicroRNAs and risk of myocardial infarction. Journal of the American College of Cardiology 2012 60 290 299 10.1016/j.jacc.2012.03.056
93. Lu H. Q., Liang C., He Z. Q., Fan M., Wu Z. G., Circulating miR-214 is associated with the severity of coronary artery disease. Journal of Geriatric Cardiology 2013 10 34 38 10.3969/j.issn.1671-5411.2013.01.007
94. Tsai P. C., Liao Y. C., Wang Y. S., Lin H. F., Lin R. T., Juo S. H., Serum microRNA-21 and microRNA-221 as potential biomarkers for cerebrovascular disease. Journal of Vascular Research 2013 50 346 354 10.1159/000351767
95. Lu H., Buchan R. J., Cook S. A., MicroRNA-223 regulates Glut4 expression and cardiomyocyte glucose metabolism. Cardiovascular Research 2010 86 3 410 420 2-s2.0-77952346716 10.1093/cvr/cvq010
96. Wang L., Jia X. J., Jiang H. J., MicroRNAs 185, 96, and 223 repress selective high-density lipoprotein cholesterol uptake through posttranscriptional inhibition. Molecular and Cellular Biology 2013 33 1956 1964 10.1128/mcb. 01580-12
97. Bauernfeind F., Rieger A., Schildberg F. A., Knolle P. A., Schmid-Burgk J. L., Hornung V., NLRP3 inflammasome activity is negatively controlled by miR-223. Journal of Immunology 2012 189 4175 4181 10.4049/jimmunol.1201516
98. Tabet F., Vickers K. C., Cuesta Torres L. F., HDL-transferred microRNA-223 regulates ICAM-1 expression in endothelial cells. Nature Communications 2014 5 3292 10.1038/ncomms4292
99. Duffy D., Rader D. J., Update on strategies to increase HDL quantity and function. Nature Reviews Cardiology 2009 6 455 463 10.1038/nrcardio.2009.94
100. Haneklaus M., Gerlic M., 'Neill LA O., Masters S. L., MiR-223: infection, inflammation and cancer. Journal of Internal Medicine 2013 274 215 226 10.1111/joim. 12099
101. Ma X., Ma C., zheng X., MicroRNA-155 in the pathogenesis of atherosclerosis: a conflicting role? Heart, Lung and Circulation 2013 22 811 818 10.1016/j.hlc.2013.05.651
102. Pedersen T. R., Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease: the Scandinavian Simvastatin Survival Study (4S). The Lancet 1994 344 8934 1383 1389 2-s2.0-0027987849
103. Soriano A., Jubierre L., Almazan-Moga A., MicroRNAs as pharmacological targets in cancer. Pharmacological Research 2013 75 3 14 10.1016/j.phrs.2013.03. 006
104. Marquart T. J., Wu J., Lusis A. J., Baldan A., Anti-miR-33 therapy does not alter the progression of atherosclerosis in low-density lipoprotein receptor-deficient mice. Arteriosclerosis, Thrombosis, and Vascular Biology 2013 33 455 458 10.1161/atvbaha.112.300639
105. Rotllan N., Ramirez C. M., Aryal B., Esau C. C., Fernandez-Hernando C., Therapeutic silencing of microRNA-33 inhibits the progression of atherosclerosis in Ldlr-/- mice: brief report. Arteriosclerosis, Thrombosis, and Vascular Biology 2013 33 1973 1977 10.1161/atvbaha.113.301732
106. Horie T., Baba O., Kuwabara Y., MicroRNA-33 deficiency reduces the progression of atherosclerotic plaque in ApoE-/- mice. Journal of the American Heart Association 2012 1 e003376 10.1161/jaha.112.003376
107. Rayner K. J., Esau C. C., Hussain F. N., McDaniel A. L., Marshall S. M., Van Gils J. M., Ray T. D., Sheedy F. J., Goedeke L., Liu X., Khatsenko O. G., Kaimal V., Lees C. J., Fernandez-Hernando C., Fisher E. A., Temel R. E., Moore K. J., Inhibition of miR-33a/b in non-human primates raises plasma HDL and lowers VLDL triglycerides. Nature 2011 478 7369 404 407 2-s2.0-80054971110 10.1038/nature10486
108. Rayner K. J., Sheedy F. J., Esau C. C., Hussain F. N., Temel R. E., Parathath S., Van Gils J. M., Rayner A. J., Chang A. N., Suarez Y., Fernandez-Hernando C., Fisher E. A., Moore K. J., Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. Journal of Clinical Investigation 2011 121 7 2921 2931 2-s2.0-79960015327 10.1172/JCI57275
109. http://www.regulusrx.com/therapeutic-areas/#Atherosclerosis
110. Hildebrandt-Eriksen E.S.,Aarup V.,Persson R.,Hansen H.F.,Munk M.E.,Orum H.,A locked nucleic acid oligonucleotide targeting microRNA 122 is well-tolerated in cynomolgus monkeys, Nucleic Acid Therapeutics. 2012.