Functional regulatory roles of microRNAs in atherosclerosis

Clinica Chimica Acta

Volumn 460, Issue , 2016, Pages 164-171

  Gao, Ya ^a   Peng, Juan ^a   Ren, Zhong ^a   He, Ni ya ^a   Li, Qing ^a   Zhao, Xue shan ^a   Wang, Mei mei ^a   Wen, Hong yan ^b   Tang, Zhi han ^a,c   Jiang, Zhi sheng ^a   Wang, Gui xue ^c   Liu, Lu shan ^a,c  

^a UNIVERSITY OF SOUTH CHINA   (China)

^b HUNAN UNIVERSITY OF CHINESE MEDICINE   (China)

^c CHONGQING UNIVERSITY   (China)

Author keywords

Atherosclerosis; Endothelial cells; Inflammation; Macrophages; microRNA; Vascular smooth muscle cells

Indexed keywords

CYCLIN D; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROGEN PEROXIDE; INTERLEUKIN 6; INTERLEUKIN 8; LRRFIP1 PROTEIN; MICRORNA; MICRORNA 143; MICRORNA 145; MICRORNA 155; MICRORNA 18A 5P; MICRORNA 199A 5P; MICRORNA 21; MICRORNA 221; MICRORNA 222; MICRORNA 424; MICRORNA 503; MICRORNA 663; MITOGEN ACTIVATED PROTEIN KINASE; MYOSIN HEAVY CHAIN; RNA DIRECTED DNA POLYMERASE; SIRTUIN 1; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; STEM CELL FACTOR; TELOMERASE; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; TRANSGELIN; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ATHEROSCLEROSIS; CELL DEATH; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENDOTHELIUM CELL; GENE FUNCTION; INFLAMMATION; MACROPHAGE; MONOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SENESCENCE; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE CELL; GENETICS; HUMAN; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PHYSIOLOGY; PROCEDURES; VASCULAR SMOOTH MUSCLE;

ATHEROSCLEROSIS; ENDOTHELIAL CELLS; HUMANS; MACROPHAGES; MICRORNAS; MOLECULAR TARGETED THERAPY; MUSCLE, SMOOTH, VASCULAR;

EID: 84977104375     PISSN: 00098981     EISSN: 18733492     Source Type: Journal    
DOI: 10.1016/j.cca.2016.06.044     Document Type: Review

References (86)

1. [1] Libby, P., Ridker, P.M., Hansson, G.K., Progress and challenges in translating the biology of atherosclerosis. Nature 473 (2011), 317–325.
2. [2] Kovacic, S., Bakran, M., Genetic susceptibility to atherosclerosis. Stroke Res. Treat., 2012, 2012, 362941.
3. [3] Zhang, C.F., Kang, K., Li, X.M., Xie, B.D., MicroRNA-136 promotes vascular muscle cell proliferation through the ERK1/2 pathway by targeting PPP2R2A in atherosclerosis. Curr. Vasc. Pharmacol. 13 (2015), 405–412.
4. [4] Yu, X., Li, Z., Chen, G., Wu, W.K., MicroRNA-10b induces vascular muscle cell proliferation through Akt pathway by targeting TIP30. Curr. Vasc. Pharmacol. 13 (2015), 679–686.
5. [5] Menghini, R., Casagrande, V., Cardellini, M., et al. MicroRNA 217 modulates endothelial cell senescence via silent information regulator 1. Circulation 120 (2009), 1524–1532.
6. [6] Di Gregoli, K., Jenkins, N., Salter, R., White, S., Newby, A.C., Johnson, J.L., MicroRNA-24 regulates macrophage behavior and retards atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 34 (2014), 1990–2000.
7. [7] Ha, M., Kim, V.N., Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15 (2014), 509–524.
8. [8] Zhang, D., Xiao, Y.F., Zhang, J.W., et al. miR-1182 attenuates gastric cancer proliferation and metastasis by targeting the open reading frame of hTERT. Cancer Lett. 360 (2015), 151–159.
9. [9] Chen, D., Farwell, M.A., Zhang, B., MicroRNA as a new player in the cell cycle. J. Cell. Physiol. 225 (2010), 296–301.
10. [10] Choe, N., Kwon, J.S., Kim, J.R., et al. The microRNA miR-132 targets Lrrfip1 to block vascular smooth muscle cell proliferation and neointimal hyperplasia. Atherosclerosis 229 (2013), 348–355.
11. [11] Ozkor, M.A., Quyyumi, A.A., Endothelium-derived hyperpolarizing factor and vascular function. Cardiol. Res. Pract., 2011, 2011, 156146.
12. [12] Gimbrone, M.A. Jr., Garcia-Cardena, G., Endothelial cell dysfunction and the pathobiology of atherosclerosis. Circ. Res. 118 (2016), 620–636.
13. [13] Brandes, R.P., Fleming, I., Busse, R., Endothelial aging. Cardiovasc. Res. 66 (2005), 286–294.
14. [14] Togliatto, G., Trombetta, A., Dentelli, P., et al. Unacylated ghrelin induces oxidative stress resistance in a glucose intolerance and peripheral artery disease mouse model by restoring endothelial cell miR-126 expression. Diabetes 64 (2015), 1370–1382.
15. [15] Yamakuchi, M., Endothelial senescence and microRNA. Biomol. Concepts 3 (2012), 213–223.
16. [16] Sun, H.X., Zeng, D.Y., Li, R.T., et al. Essential role of microRNA-155 in regulating endothelium-dependent vasorelaxation by targeting endothelial nitric oxide synthase. Hypertension 60 (2012), 1407–1414.
17. [17] Salminen, A., Kaarniranta, K., Regulation of the aging process by autophagy. Trends Mol. Med. 15 (2009), 217–224.
18. [18] Ito, T., Yagi, S., Yamakuchi, M., MicroRNA-34a regulation of endothelial senescence. Biochem. Biophys. Res. Commun. 398 (2010), 735–740.
19. [19] Zhao, T., Li, J., Chen, A.F., MicroRNA-34a induces endothelial progenitor cell senescence and impedes its angiogenesis via suppressing silent information regulator 1. Am. J. Phys. Endocrinol. Metab. 299 (2010), E110–E116.
20. [20] Chen, B., Lu, Y.R., Chen, Y.N., Kang, Y.J., Cheng, J.Q., Endothelium Aging and Oxidative Stress. Sheng Li Ke Xue Jin Zhan [Progress in Physiology], 46, 2015, 23–27.
21. [21] Vasa-Nicotera, M., Chen, H., Tucci, P., et al. miR-146a is modulated in human endothelial cell with aging. Atherosclerosis 217 (2011), 326–330.
22. [22] Sui, X.Q., Xu, Z.M., Xie, M.B., Pei, D.A., Resveratrol inhibits hydrogen peroxide-induced apoptosis in endothelial cells via the activation of PI3K/Akt by miR-126. J. Atheroscler. Thromb. 21 (2014), 108–118.
23. [23] Magenta, A., Greco, S., Gaetano, C., Martelli, F., Oxidative stress and microRNAs in vascular diseases. Int. J. Mol. Sci. 14 (2013), 17319–17346.
24. [24] Magenta, A., Cencioni, C., Fasanaro, P., et al. miR-200c is upregulated by oxidative stress and induces endothelial cell apoptosis and senescence via ZEB1 inhibition. Cell Death Differ. 18 (2011), 1628–1639.
25. [25] Huang, C., Li, G., Dong, H., et al. Arg(9)(7)(2) insulin receptor substrate-1 inhibits endothelial nitric oxide synthase expression in human endothelial cells by upregulating microRNA-155. Int. J. Mol. Med. 36 (2015), 239–248.
26. [26] Liu, Y., Pan, Q., Zhao, Y., et al. MicroRNA-155 regulates ROS production, no generation, apoptosis and multiple functions of human brain microvessel endothelial cells under physiological and pathological conditions. J. Cell. Biochem. 116 (2015), 2870–2881.
27. [27] Bi, R., Bao, C., Jiang, L., et al. MicroRNA-27b plays a role in pulmonary arterial hypertension by modulating peroxisome proliferator-activated receptor gamma dependent Hsp90-eNOS signaling and nitric oxide production. Biochem. Biophys. Res. Commun. 460 (2015), 469–475.
28. [28] Weber, M., Baker, M.B., Moore, J.P., Searles, C.D., MiR-21 is induced in endothelial cells by shear stress and modulates apoptosis and eNOS activity. Biochem. Biophys. Res. Commun. 393 (2010), 643–648.
29. [29] Bar, C., Blasco, M.A., Telomeres and Telomerase as Therapeutic Targets to Prevent and Treat Age-Related Diseases. F1000Research, 2016, 5.
30. [30] Chen, L., Lu, M.H., Zhang, D., et al. miR-1207-5p and miR-1266 suppress gastric cancer growth and invasion by targeting telomerase reverse transcriptase. Cell Death Dis., 5, 2014, e1034.
31. [31] Li, M., Chen, S.M., Chen, C., et al. microRNA2993p inhibits laryngeal cancer cell growth by targeting human telomerase reverse transcriptase mRNA. Mol. Med. Rep. 11 (2015), 4645–4649.
32. [32] Zhao, Q., Zhai, Y.X., Liu, H.Q., Shi, Y.A., Li, X.B., MicroRNA-491-5p suppresses cervical cancer cell growth by targeting hTERT. Oncol. Rep. 34 (2015), 979–986.
33. [33] Erusalimsky, J.D., Skene, C., Mechanisms of endothelial senescence. Exp. Physiol. 94 (2009), 299–304.
34. [34] Xu, Q., Meng, S., Liu, B., et al. MicroRNA-130a regulates autophagy of endothelial progenitor cells through Runx3. Clin. Exp. Pharmacol. Physiol. 41 (2014), 351–357.
35. [35] Menghini, R., Casagrande, V., Marino, A., et al. MiR-216a: a link between endothelial dysfunction and autophagy. Cell Death Dis., 5, 2014, e1029.
36. [36] Zhang, T., Tian, F., Wang, J., Jing, J., Zhou, S.S., Chen, Y.D., Endothelial cell autophagy in atherosclerosis is regulated by miR-30-mediated translational control of ATG6. Cell. Physiol. Biochem. 37 (2015), 1369–1378.
37. [37] Xu, Z., Han, Y., Liu, J., et al. MiR-135b-5p and MiR-499a-3p promote cell proliferation and migration in atherosclerosis by directly targeting MEF2C. Sci. Rep., 5, 2015, 12276.
38. [38] Liu, D., Zhang, X.L., Yan, C.H., et al. MicroRNA-495 regulates the proliferation and apoptosis of human umbilical vein endothelial cells by targeting chemokine CCL2. Thromb. Res. 135 (2015), 146–154.
39. [39] Yang, Y., Yang, J.J., Tao, H., Jin, W.S., MicroRNA-21 controls hTERT via PTEN in human colorectal cancer cell proliferation. J. Physiol. Biochem. 71 (2015), 59–68.
40. [40] Zuo, K., Li, M., Zhang, X., et al. MiR-21 suppresses endothelial progenitor cell proliferation by activating the TGFbeta signaling pathway via downregulation of WWP1. Int. J. Clin. Exp. Pathol. 8 (2015), 414–422.
41. [41] Schober, A., Nazari-Jahantigh, M., Wei, Y., et al. MicroRNA-126-5p promotes endothelial proliferation and limits atherosclerosis by suppressing Dlk1. Nat. Med. 20 (2014), 368–376.
42. [42] Zhang, X., Liu, X., Shang, H., Xu, Y., Qian, M., Monocyte chemoattractant protein-1 induces endothelial cell apoptosis in vitro through a p53-dependent mitochondrial pathway. Acta Biochim. Biophys. Sin. 43 (2011), 787–795.
43. [43] Zhu, N., Zhang, D., Chen, S., et al. Endothelial enriched microRNAs regulate angiotensin II-induced endothelial inflammation and migration. Atherosclerosis 215 (2011), 286–293.
44. [44] Zhang, Y., Liu, D., Chen, X., et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol. Cell 39 (2010), 133–144.
45. [45] Wu, Y., Huang, A., Li, T., et al. MiR-152 reduces human umbilical vein endothelial cell proliferation and migration by targeting ADAM17. FEBS Lett. 588 (2014), 2063–2069.
46. [46] Lu, H., Daugherty, A., Atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 35 (2015), 485–491.
47. [47] Yu, X., Li, Z., MicroRNAs regulate vascular smooth muscle cell functions in atherosclerosis (review). Int. J. Mol. Med. 34 (2014), 923–933.
48. [48] Xie, B., Zhang, C., Kang, K., Jiang, S., miR-599 inhibits vascular smooth muscle cells proliferation and migration by targeting TGFB2. PLoS One, 10, 2015, e0141512.
49. [49] Pardali, E., Goumans, M.J., ten Dijke, P., Signaling by members of the TGF-beta family in vascular morphogenesis and disease. Trends Cell Biol. 20 (2010), 556–567.
50. [50] Leeper, N.J., Raiesdana, A., Kojima, Y., et al. MicroRNA-26a is a novel regulator of vascular smooth muscle cell function. J. Cell. Physiol. 226 (2011), 1035–1043.
51. [51] Qi, L., Zhi, J., Zhang, T., et al. Inhibition of microRNA-25 by tumor necrosis factor alpha is critical in the modulation of vascular smooth muscle cell proliferation. Mol. Med. Rep. 11 (2015), 4353–4358.
52. [52] Kim, M.H., Ham, O., Lee, S.Y., et al. MicroRNA-365 inhibits the proliferation of vascular smooth muscle cells by targeting cyclin D1. J. Cell. Biochem. 115 (2014), 1752–1761.
53. [53] Li, T.J., Chen, Y.L., Gua, C.J., Xue, S.J., Ma, S.M., Li, X.D., MicroRNA 181b promotes vascular smooth muscle cells proliferation through activation of PI3K and MAPK pathways. Int. J. Clin. Exp. Pathol. 8 (2015), 10375–10384.
54. [54] Li, P., Liu, Y., Yi, B., et al. MicroRNA-638 is highly expressed in human vascular smooth muscle cells and inhibits PDGF-BB-induced cell proliferation and migration through targeting orphan nuclear receptor NOR1. Cardiovasc. Res. 99 (2013), 185–193.
55. [55] Mitra, S., Goyal, T., Mehta, J.L., Oxidized LDL, LOX-1 and Atherosclerosis. Cardiovascular Drugs and Therapy / Sponsored by the International Society of Cardiovascular Pharmacotherapy, 25, 2011, 419–429.
56. [56] Sun, Y., Chen, D., Cao, L., et al. MiR-490-3p modulates the proliferation of vascular smooth muscle cells induced by ox-LDL through targeting PAPP-A. Cardiovasc. Res. 100 (2013), 272–279.
57. [57] Choe, N., Kwon, J.S., Kim, Y.S., et al. The microRNA miR-34c inhibits vascular smooth muscle cell proliferation and neointimal hyperplasia by targeting stem cell factor. Cell. Signal. 27 (2015), 1056–1065.
58. [58] von der Thusen, J.H., Borensztajn, K.S., Moimas, S., et al. IGF-1 has plaque-stabilizing effects in atherosclerosis by altering vascular smooth muscle cell phenotype. Am. J. Pathol. 178 (2011), 924–934.
59. [59] Gao, S., Wassler, M., Zhang, L., et al. MicroRNA-133a regulates insulin-like growth factor-1 receptor expression and vascular smooth muscle cell proliferation in murine atherosclerosis. Atherosclerosis 232 (2014), 171–179.
60. [60] Chen, G., Fang, T., Huang, Z., et al. MicroRNA-133a inhibits osteosarcoma cells proliferation and invasion via targeting IGF-1R. Cell. Physiol. Biochem. 38 (2016), 598–608.
61. [61] Zhang, W., Liu, K., Liu, S., Ji, B., Wang, Y., Liu, Y., MicroRNA-133a functions as a tumor suppressor by targeting IGF-1R in hepatocellular carcinoma. Tumour Biol. 36 (2015), 9779–9788.
62. [62] Li, P., Zhu, N., Yi, B., et al. MicroRNA-663 regulates human vascular smooth muscle cell phenotypic switch and vascular neointimal formation. Circ. Res. 113 (2013), 1117–1127.
63. [63] Boettger, T., Beetz, N., Kostin, S., et al. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J. Clin. Investig. 119 (2009), 2634–2647.
64. [64] Kee, H.J., Kim, G.R., Cho, S.N., et al. miR-18a-5p microRNA increases vascular smooth muscle cell differentiation by downregulating Syndecan4. Korean Circ. J. 44 (2014), 255–263.
65. [65] Iaconetti, C., De Rosa, S., Polimeni, A., et al. Down-regulation of miR-23b induces phenotypic switching of vascular smooth muscle cells in vitro and in vivo. Cardiovasc. Res. 107 (2015), 522–533.
66. [66] Liao, X.B., Zhang, Z.Y., Yuan, K., et al. MiR-133a modulates osteogenic differentiation of vascular smooth muscle cells. Endocrinology 154 (2013), 3344–3352.
67. [67] De Paoli, F., Staels, B., Chinetti-Gbaguidi, G., Macrophage phenotypes and their modulation in atherosclerosis. Circ. J. 78 (2014), 1775–1781.
68. [68] Dhaliwal, B.S., Steinbrecher, U.P., Scavenger receptors and oxidized low density lipoproteins. Clin. Chim. Acta. 286 (1999), 191–205.
69. [69] Forrest, A.R., Kanamori-Katayama, M., Tomaru, Y., et al. Induction of microRNAs, mir-155, mir-222, mir-424 and mir-503, promotes monocytic differentiation through combinatorial regulation. Leukemia 24 (2010), 460–466.
70. [70] Donners, M.M., Wolfs, I.M., Stoger, L.J., et al. Hematopoietic miR155 deficiency enhances atherosclerosis and decreases plaque stability in hyperlipidemic mice. PLoS One, 7, 2012, e35877.
71. [71] Lin, H.S., Gong, J.N., Su, R., et al. miR-199a-5p inhibits monocyte/macrophage differentiation by targeting the activin a type 1B receptor gene and finally reducing C/EBPalpha expression. J. Leukoc. Biol. 96 (2014), 1023–1035.
72. [72] Ouimet, M., Ediriweera, H.N., Gundra, U.M., et al. MicroRNA-33-dependent regulation of macrophage metabolism directs immune cell polarization in atherosclerosis. J. Clin. Invest., 2015, 2015.
73. [73] Karunakaran, D., Richards, L., Geoffrion, M., et al. Therapeutic inhibition of miR-33 promotes fatty acid oxidation but does not ameliorate metabolic dysfunction in diet-induced obesity. Arterioscler. Thromb. Vasc. Biol. 35 (2015), 2536–2543.
74. [74] Banerjee, S., Cui, H., Xie, N., et al. miR-125a-5p regulates differential activation of macrophages and inflammation. J. Biol. Chem. 288 (2013), 35428–35436.
75. [75] Nazari-Jahantigh, M., Wei, Y., Noels, H., et al. MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages. J. Clin. Invest. 122 (2012), 4190–4202.
76. [76] Du, F., Yu, F., Wang, Y., et al. MicroRNA-155 deficiency results in decreased macrophage inflammation and attenuated atherogenesis in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 34 (2014), 759–767.
77. [77] Huang, R.S., Hu, G.Q., Lin, B., Lin, Z.Y., Sun, C.C., MicroRNA-155 silencing enhances inflammatory response and lipid uptake in oxidized low-density lipoprotein-stimulated human THP-1 macrophages. J. Invest. Med. 58 (2010), 961–967.
78. [78] Zhu, J., Chen, T., Yang, L., et al. Regulation of microRNA-155 in atherosclerotic inflammatory responses by targeting MAP3K10. PLoS One, 7, 2012, e46551.
79. [79] Wei, Y., Nazari-Jahantigh, M., Chan, L., et al. The microRNA-342-5p fosters inflammatory macrophage activation through an Akt1- and microRNA-155-dependent pathway during atherosclerosis. Circulation 127 (2013), 1609–1619.
80. [80] Hu, Y.W., Zhao, J.Y., Li, S.F., et al. RP5-833A20.1/miR-382-5p/NFIA-dependent signal transduction pathway contributes to the regulation of cholesterol homeostasis and inflammatory reaction. Arterioscler. Thromb. Vasc. Biol. 35 (2015), 87–101.
81. [81] Yang, K., He, Y.S., Wang, X.Q., et al. MiR-146a inhibits oxidized low-density lipoprotein-induced lipid accumulation and inflammatory response via targeting toll-like receptor 4. FEBS Lett. 585 (2011), 854–860.
82. [82] Feng, J., Li, A., Deng, J., et al. miR-21 attenuates lipopolysaccharide-induced lipid accumulation and inflammatory response: potential role in cerebrovascular disease. Lipids Health Dis., 13, 2014, 27.
83. [83] He, P.P., Ouyang, X.P., Tang, Y.Y., et al. MicroRNA-590 attenuates lipid accumulation and pro-inflammatory cytokine secretion by targeting lipoprotein lipase gene in human THP-1 macrophages. Biochimie 106 (2014), 81–90.
84. [84] Nakamachi, Y., Kawano, S., Takenokuchi, M., et al. MicroRNA-124a is a key regulator of proliferation and monocyte chemoattractant protein 1 secretion in fibroblast-like synoviocytes from patients with rheumatoid arthritis. Arthritis Rheum. 60 (2009), 1294–1304.
85. [85] Tano, N., Kim, H.W., Ashraf, M., microRNA-150 regulates mobilization and migration of bone marrow-derived mononuclear cells by targeting Cxcr4. PLoS One, 6, 2011, e23114.
86. [86] Manoharan, P., Basford, J.E., Pilcher-Roberts, R., Neumann, J., Hui, D.Y., Lingrel, J.B., Reduced levels of microRNAs miR-124a and miR-150 are associated with increased proinflammatory mediator expression in Kruppel-like factor 2 (KLF2)-deficient macrophages. J. Biol. Chem. 289 (2014), 31638–31646.