MicroRNAs as regulators of endothelial cell functions in cardiometabolic diseases

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1861, Issue 12, 2016, Pages 2094-2103

  Araldi, Elisa ^a   Suárez, Yajaira ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Atherosclerosis; Cardiovascular disease; Endothelial cells; Metabolic syndrome; MicroRNAs; Type 2 diabetes

Indexed keywords

MICRORNA; SMALL UNTRANSLATED RNA;

ANGIOGENESIS; ARTICLE; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CELL FUNCTION; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; HUMAN; ISCHEMIA; METABOLIC DISORDER; METABOLIC SYNDROME X; NEOVASCULARIZATION (PATHOLOGY); NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; ANIMAL; GENETICS; HEART DISEASE; LIPID METABOLISM; METABOLISM; VASCULAR ENDOTHELIUM;

ANIMALS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HEART DISEASES; HUMANS; LIPID METABOLISM; METABOLIC DISEASES; MICRORNAS;

EID: 84956690733     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2016.01.013     Document Type: Article

References (117)

1. [1] W.H. Organization, Top 10 Causes of Death: Fact Sheet No. 310: WHO 2011, Ref Type: Report LU. 2011.
2. [2] W.H. Organization, Global Status Report on Noncommunicable Diseases. 2014, 2015.
3. [3] Cooper, J.A., Miller, G.J., Humphries, S.E., A comparison of the PROCAM and Framingham point-scoring systems for estimation of individual risk of coronary heart disease in the Second Northwick Park Heart Study. Atherosclerosis 181 (2005), 93–100.
4. [4] Moller, D.E., Kaufman, K.D., Metabolic syndrome: a clinical and molecular perspective. Annu. Rev. Med. 56 (2005), 45–62.
5. [5] Roberts, L.D., Gerszten, R.E., Toward new biomarkers of cardiometabolic diseases. Cell Metab. 18 (2013), 43–50.
6. [6] Stern, M.P., Diabetes and cardiovascular disease. The “common soil” hypothesis. Diabetes 44 (1995), 369–374.
7. [7] Michiels, C., Endothelial cell functions. J. Cell. Physiol. 196 (2003), 430–443.
8. [8] Pearson, J.D., Normal endothelial cell function. Lupus 9 (2000), 183–188.
9. [9] Sumpio, B.E., Riley, J.T., Dardik, A., Cells in focus: endothelial cell. Int. J. Biochem. Cell Biol. 34 (2002), 1508–1512.
10. [10] Avogaro, A., de Kreutzenberg, S.V., Mechanisms of endothelial dysfunction in obesity. Clin. Chim. Acta 360 (2005), 9–26.
11. [11] Davignon, J., Ganz, P., Role of endothelial dysfunction in atherosclerosis. Circulation 109 (2004), III27–III32.
12. [12] Fornoni, A., Raij, L., Metabolic syndrome and endothelial dysfunction. Curr. Hypertens. Rep. 7 (2005), 88–95.
13. [13] Goligorsky, M.S., Endothelial cell dysfunction: can't live with it, how to live without it. Am. J. Physiol. Ren. Physiol. 288 (2005), F871–F880.
14. [14] Hanson, M., Gluckman, P., Endothelial dysfunction and cardiovascular disease: the role of predictive adaptive responses. Heart 91 (2005), 864–866.
15. [15] O'Riordan, E., Chen, J., Brodsky, S.V., Smirnova, I., Li, H., Goligorsky, M.S., Endothelial cell dysfunction: the syndrome in making. Kidney Int. 67 (2005), 1654–1658.
16. [16] Cines, D.B., Pollak, E.S., Buck, C.A., Loscalzo, J., Zimmerman, G.A., McEver, R.P., Pober, J.S., Wick, T.M., Konkle, B.A., Schwartz, B.S., Barnathan, E.S., McCrae, K.R., Hug, B.A., Schmidt, A.M., Stern, D.M., Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 91 (1998), 3527–3561.
17. [17] Kolluru, G.K., Bir, S.C., Kevil, C.G., Endothelial dysfunction and diabetes: effects on angiogenesis, vascular remodeling, and wound healing. Int. J. Vasc. Med., 2012, 2012, 918267.
18. [18] Pober, J.S., Cotran, R.S., The role of endothelial cells in inflammation. Transplantation 50 (1990), 537–544.
19. [19] Verma, S., Buchanan, M.R., Anderson, T.J., Endothelial function testing as a biomarker of vascular disease. Circulation 108 (2003), 2054–2059.
20. [20] Davis, S., Lollo, B., Freier, S., Esau, C., Improved targeting of miRNA with antisense oligonucleotides. Nucleic Acids Res. 34 (2006), 2294–2304.
21. [21] Pushparaj, P.N., Aarthi, J.J., Manikandan, J., Kumar, S.D., siRNA, miRNA, and shRNA: in vivo applications. J. Dent. Res. 87 (2008), 992–1003.
22. [22] Soutschek, J., Akinc, A., Bramlage, B., Charisse, K., Constien, R., Donoghue, M., Elbashir, S., Geick, A., Hadwiger, P., Harborth, J., John, M., Kesavan, V., Lavine, G., Pandey, R.K., Racie, T., Rajeev, K.G., Rohl, I., Toudjarska, I., Wang, G., Wuschko, S., Bumcrot, D., Koteliansky, V., Limmer, S., Manoharan, M., Vornlocher, H.P., Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature 432 (2004), 173–178.
23. [23] Ambros, V., The functions of animal microRNAs. Nature 431 (2004), 350–355.
24. [24] Bartel, D.P., MicroRNAs: target recognition and regulatory functions. Cell 136 (2009), 215–233.
25. [25] Filipowicz, W., Bhattacharyya, S.N., Sonenberg, N., Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?. Nat. Rev. Genet. 9 (2008), 102–114.
26. [26] Araldi, E., Chamorro-Jorganes, A., van Solingen, C., Fernández-Hernando, C., Suárez, Y., Therapeutic potential of modulating microRNAs in atherosclerotic vascular disease. Curr. Vasc. Pharmacol. 13 (2015), 291–304.
27. [27] Chamorro-Jorganes, A., Araldi, E., Suárez, Y., MicroRNAs as pharmacological targets in endothelial cell function and dysfunction. Pharmacol. Res. 75 (2013), 15–27.
28. [28] Dangwal, S., Thum, T., MicroRNAs in platelet biogenesis and function. Thromb. Haemost. 108 (2012), 599–604.
29. [29] Schober, A., Thum, T., Zernecke, A., MicroRNAs in vascular biology–metabolism and atherosclerosis. Thromb. Haemost. 107 (2012), 603–604.
30. [30] Thum, T., Mayr, M., Review focus on the role of microRNA in cardiovascular biology and disease. Cardiovasc. Res. 93 (2012), 543–544.
31. [31] Glass, C.K., Witztum, J.L., Atherosclerosis. The road ahead. Cell 104 (2001), 503–516.
32. [32] Thompson, R.C., Allam, A.H., Lombardi, G.P., Wann, L.S., Sutherland, M.L., Sutherland, J.D., Soliman, M.A.-T., Frohlich, B., Mininberg, D.T., Monge, J.M., Vallodolid, C.M., Cox, S.L., Abd el-Maksoud, G., Badr, I., Miyamoto, M.I., El-Halim Nur el-din, A., Narula, J., Finch, C.E., Thomas, G.S., Atherosclerosis across 4000 years of human history: the Horus study of four ancient populations. Lancet 381 (2013), 1211–1222.
33. [33] Hilgendorf, I., Swirski, F.K., Robbins, C.S., Monocyte fate in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 35 (2015), 272–279.
34. [34] Parmar, K.M., Larman, H.B., Dai, G., Zhang, Y., Wang, E.T., Moorthy, S.N., Kratz, J.R., Lin, Z., Jain, M.K., Gimbrone, M.A. Jr., García-Cardeña, G., Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2. J. Clin. Investig. 116 (2006), 49–58.
35. [35] Atkins, G.B., Jain, M.K., Role of Krüppel-like transcription factors in endothelial biology. Circ. Res. 100 (2007), 1686–1695.
36. [36] Young, A., Wu, W., Sun, W., Benjamin Larman, H., Larman, H.B., Wang, N., Li, Y.-S., Shyy, J.Y., Chien, S., García-Cardeña, G., Flow activation of AMP-activated protein kinase in vascular endothelium leads to Krüppel-like factor 2 expression. Arterioscler. Thromb. Vasc. Biol. 29 (2009), 1902–1908.
37. [37] Dai, G., Vaughn, S., Zhang, Y., Wang, E.T., García-Cardeña, G., Gimbrone, M.A., Biomechanical forces in atherosclerosis-resistant vascular regions regulate endothelial redox balance via phosphoinositol 3-kinase/Akt-dependent activation of Nrf2. Circ. Res. 101 (2007), 723–733.
38. [38] Zakkar, M., Van der Heiden, K., Luong, L.A., Chaudhury, H., Cuhlmann, S., Hamdulay, S.S., Krams, R., Edirisinghe, I., Rahman, I., Carlsen, H., Haskard, D.O., Mason, J.C., Evans, P.C., Activation of Nrf2 in endothelial cells protects arteries from exhibiting a proinflammatory state. Arterioscler. Thromb. Vasc. Biol. 29 (2009), 1851–1857.
39. [39] Hansson, G.K., Schwartz, S.M., Evidence for cell death in the vascular endothelium in vivo and in vitro. Am. J. Pathol. 112 (1983), 278–286.
40. [40] Sakao, S., Taraseviciene-Stewart, L., Lee, J.D., Wood, K., Cool, C.D., Voelkel, N.F., Initial apoptosis is followed by increased proliferation of apoptosis-resistant endothelial cells. FASEB J. 19 (2005), 1178–1180.
41. [41] Tardy, Y., Resnick, N., Nagel, T., Gimbrone, M.A., Dewey, C.F., Shear stress gradients remodel endothelial monolayers in vitro via a cell proliferation-migration-loss cycle. Arterioscler. Thromb. Vasc. Biol. 17 (1997), 3102–3106.
42. [42] Wu, W., Xiao, H., Laguna-Fernandez, A., Villarreal, G., Wang, K.-C., Geary, G.G., Zhang, Y., Wang, W.-C., Huang, H.-D., Zhou, J., Li, Y.-S., Chien, S., García-Cardeña, G., Shyy, J.Y.J., Flow-dependent regulation of Kruppel-like factor 2 Is mediated by MicroRNA-92a. Circulation 124 (2011), 633–641.
43. [43] Fang, Y., Shi, C., Manduchi, E., Civelek, M., Davies, P.F., MicroRNA-10a regulation of proinflammatory phenotype in athero-susceptible endothelium in vivo and in vitro. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 13450–13455.
44. [44] Njock, M.S., Cheng, H.S., Dang, L.T., Nazari-Jahantigh, M., Lau, A.C., Boudreau, E., Roufaiel, M., Cybulsky, M.I., Schober, A., Fish, J.E., Endothelial cells suppress monocyte activation through secretion of extracellular vesicles containing antiinflammatory microRNAs. Blood 125 (2015), 3202–3212.
45. [45] Demolli, S., Doebele, C., Doddaballapur, A., Lang, V., Fisslthaler, B., Chavakis, E., Vinciguerra, M., Sciacca, S., Henschler, R., Hecker, M., Savant, S., Augustin, H.G., Kaluza, D., Dimmeler, S., Boon, R.A., MicroRNA-30 mediates anti-inflammatory effects of shear stress and KLF2 via repression of angiopoietin 2. J. Mol. Cell. Cardiol. 88 (2015), 111–119.
46. [46] Wang, K.-C., Garmire, L.X., Young, A., Nguyen, P., Trinh, A., Subramaniam, S., Wang, N., Shyy, J.Y.J., Li, Y.-S., Chien, S., Role of microRNA-23b in flow-regulation of Rb phosphorylation and endothelial cell growth. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 3234–3239.
47. [47] Wang, K.-C., Nguyen, P., Weiss, A., Yeh, Y.-T., Chien, H.S., Lee, A., Teng, D., Subramaniam, S., Li, Y.-S., Chien, S., MicroRNA-23b regulates cyclin-dependent kinase-activating kinase complex through cyclin H repression to modulate endothelial transcription and growth under flow. Arterioscler. Thromb. Vasc. Biol. 34 (2014), 1437–1445.
48. [48] Qin, X., Wang, X., Wang, Y., Tang, Z., Cui, Q., Xi, J., Li, Y.-S.J., Chien, S., Wang, N., MicroRNA-19a mediates the suppressive effect of laminar flow on cyclin D1 expression in human umbilical vein endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 3240–3244.
49. [49] 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., Srivastava, D., miR-126 regulates angiogenic signaling and vascular integrity. Dev. Cell 15 (2008), 272–284.
50. [50] 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. Dev. Cell 15 (2008), 261–271.
51. [51] Schober, A., Nazari-Jahantigh, M., Wei, Y., Bidzhekov, K., Gremse, F., Grommes, J., Megens, R.T.A., Heyll, K., Noels, H., Hristov, M., Wang, S., Kiessling, F., Olson, E.N., Weber, C., MicroRNA-126-5p promotes endothelial proliferation and limits atherosclerosis by suppressing Dlk1. Nat. Med. 20 (2014), 368–376.
52. [52] Zhou, J., Wang, K.-C., Wu, W., Subramaniam, S., Shyy, J.Y.J., Chiu, J.-J., Li, J.Y.-S., Chien, S., MicroRNA-21 targets peroxisome proliferators-activated receptor-alpha in an autoregulatory loop to modulate flow-induced endothelial inflammation. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 10355–10360.
53. [53] 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.
54. [54] Loyer, X., Potteaux, S., Vion, A.-C., Guérin, C.L., Boulkroun, S., Rautou, P.-E., Ramkhelawon, B., Esposito, B., Dalloz, M., Paul, J.-L., Julia, P., Maccario, J., Boulanger, C.M., Mallat, Z., Tedgui, A., Inhibition of microRNA-92a prevents endothelial dysfunction and atherosclerosis in mice. Circ. Res. 114 (2014), 434–443.
55. [55] Fang, Y., Davies, P.F., Site-specific microRNA-92a regulation of Kruppel-like factors 4 and 2 in atherosusceptible endothelium. Arterioscler. Thromb. Vasc. Biol. 32 (2012), 979–987.
56. [56] Son, D.J., Kumar, S., Takabe, W., Kim, C.W., Ni, C.-W., Alberts-Grill, N., Jang, I.-H., Kim, S., Kim, W., Kang, S.W., Baker, A.H., Seo, J.W., Ferrara, K.W., Jo, H., The atypical mechanosensitive microRNA-712 derived from pre-ribosomal RNA induces endothelial inflammation and atherosclerosis. Nat. Commun., 4, 2013, 3000.
57. [57] Ni, C.-W., Qiu, H., Jo, H., MicroRNA-663 upregulated by oscillatory shear stress plays a role in inflammatory response of endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 300 (2011), H1762–H1769.
58. [58] Warboys, C.M., de Luca, A., Amini, N., Luong, L., Duckles, H., Hsiao, S., White, A., Biswas, S., Khamis, R., Chong, C.K., Cheung, W.-M., Sherwin, S.J., Bennett, M.R., Gil, J., Mason, J.C., Haskard, D.O., Evans, P.C., Disturbed flow promotes endothelial senescence via a p53-dependent pathway. Arterioscler. Thromb. Vasc. Biol. 34 (2014), 985–995.
59. [59] Bommer, G.T., Gerin, I., Feng, Y., Kaczorowski, A.J., Kuick, R., Love, R.E., Zhai, Y., Giordano, T.J., Qin, Z.S., Moore, B.B., MacDougald, O.A., Cho, K.R., Fearon, E.R., p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr. Biol. 17 (2007), 1298–1307.
60. [60] Fan, W., Fang, R., Wu, X., Liu, J., Feng, M., Dai, G., Chen, G., Wu, G., Shear-sensitive microRNA-34a modulates flow-dependent regulation of endothelial inflammation. J. Cell Sci. 128 (2015), 70–80.
61. [61] Chen, L.-J., Chuang, L., Huang, Y.-H., Zhou, J., Lim, S.H., Lee, C.-I., Lin, W.-W., Lin, T.-E., Wang, W.-L., Chen, L., Chien, S., Chiu, J.-J., MicroRNA mediation of endothelial inflammatory response to smooth muscle cells and its inhibition by atheroprotective shear stress. Circ. Res. 116 (2015), 1157–1169.
62. [62] Hergenreider, E., Heydt, S., Tréguer, K., Boettger, T., Horrevoets, A.J.G., Zeiher, A.M., Scheffer, M.P., Frangakis, A.S., Yin, X., Mayr, M., Braun, T., Urbich, C., Boon, R.A., Dimmeler, S., Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat. Cell Biol. 14 (2012), 249–256.
63. [63] Cheng, H.S., Sivachandran, N., Lau, A., Boudreau, E., Zhao, J.L., Baltimore, D., Delgado-Olguin, P., Cybulsky, M.I., Fish, J.E., MicroRNA-146 represses endothelial activation by inhibiting pro-inflammatory pathways. EMBO Mol. Med. 5 (2013), 1017–1034.
64. [64] Sun, X., Icli, B., Wara, A.K., Belkin, N., He, S., Kobzik, L., Hunninghake, G.M., Vera, M.P., Registry, M., Blackwell, T.S., Baron, R.M., Feinberg, M.W., MicroRNA-181b regulates NF-κB-mediated vascular inflammation. J. Clin. Invest. 122 (2012), 1973–1990.
65. [65] Sun, X., He, S., Wara, A.K.M., Icli, B., Shvartz, E., Tesmenitsky, Y., Belkin, N., Li, D., Blackwell, T.S., Sukhova, G.K., Croce, K., Feinberg, M.W., Systemic delivery of microRNA-181b inhibits nuclear factor-κB activation, vascular inflammation, and atherosclerosis in apolipoprotein E-deficient mice. Circ. Res. 114 (2014), 32–40.
66. [66] Dentelli, P., Dentelli, P., Rosso, A., Rosso, A., Orso, F., Orso, F., Olgasi, C., Olgasi, C., Taverna, D., Taverna, D., Brizzi, M.F., Brizzi, M.F., microRNA-222 controls neovascularization by regulating signal transducer and activator of transcription 5 A expression. Arterioscler. Thromb. Vasc. Biol. 30 (2010), 1562–1568.
67. [67] Poliseno, L., Tuccoli, A., Mariani, L., Evangelista, M., Citti, L., Woods, K., Mercatanti, A., Hammond, S., Rainaldi, G., MicroRNAs modulate the angiogenic properties of HUVECs. Blood 108 (2006), 3068–3071.
68. [68] Suárez, Y., Wang, C., Manes, T.D., Pober, J.S., Cutting edge: TNF-induced microRNAs regulate TNF-induced expression of E-selectin and intercellular adhesion molecule-1 on human endothelial cells: feedback control of inflammation. J. Immunol. 184 (2010), 21–25.
69. [69] Qin, B., Xiao, B., Liang, D., Xia, J., Li, Y., Yang, H., MicroRNAs expression in ox-LDL treated HUVECs: MiR-365 modulates apoptosis and Bcl-2 expression. Biochem. Biophys. Res. Commun. 410 (2011), 127–133.
70. [70] Napoli, C., Quehenberger, O., De Nigris, F., Abete, P., Glass, C.K., Palinski, W., Mildly oxidized low density lipoprotein activates multiple apoptotic signaling pathways in human coronary cells. FASEB J. 14 (2000), 1996–2007.
71. [71] Chen, K.-C., Hsieh, I.-C., Hsi, E., Wang, Y.-S., Dai, C.-Y., Chou, W.-W., Juo, S.-H.H., Negative feedback regulation between microRNA let-7 g and the oxLDL receptor LOX-1. J. Cell Sci. 124 (2011), 4115–4124.
72. [72] Bao, M.-H., Zhang, Y.-W., Lou, X.-Y., Cheng, Y., Zhou, H.-H., Protective effects of let-7a and let-7b on oxidized low-density lipoprotein induced endothelial cell injuries. PLoS One, 9, 2014, e106540.
73. [73] Liao, Y.-C., Wang, Y.-S., Guo, Y.-C., Lin, W.-L., Chang, M.-H., Juo, S.-H.H., Let-7 g improves multiple endothelial functions through targeting transforming growth factor-beta and SIRT-1 signaling. J. Am. Coll. Cardiol. 63 (2014), 1685–1694.
74. [74] Kahn, B.B., Flier, J.S., Obesity and insulin resistance. J. Clin. Invest. 106 (2000), 473–481.
75. [75] Kim, J.A., Montagnani, M., Koh, K.K., Quon, M.J., Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 113 (2006), 1888–1904.
76. [76] Cersosimo, E., DeFronzo, R.A., Insulin resistance and endothelial dysfunction: the road map to cardiovascular diseases. Diabetes Metab. Res. Rev. 22 (2006), 423–436.
77. [77] Suárez, Y., Fernández-Hernando, C., Pober, J.S., Sessa, W.C., Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ. Res. 100 (2007), 1164–1173.
78. [78] Sun, H.X., Zeng, D.Y., Li, R.T., Pang, R.P., Yang, H., Hu, Y.L., Zhang, Q., Jiang, Y., Huang, L.Y., Tang, Y.B., Yan, G.J., Zhou, J.G., Essential role of microRNA-155 in regulating endothelium-dependent vasorelaxation by targeting endothelial nitric oxide synthase. Hypertension 60 (2012), 1407–1414.
79. [79] Yanagisawa, M., Kurihara, H., Kimura, S., Tomobe, Y., Kobayashi, M., Mitsui, Y., Yazaki, Y., Goto, K., Masaki, T., A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332 (1988), 411–415.
80. [80] Bohm, F., Pernow, J., The importance of endothelin-1 for vascular dysfunction in cardiovascular disease. Cardiovasc. Res. 76 (2007), 8–18.
81. [81] Li, D., Yang, P., Xiong, Q., Song, X., Yang, X., Liu, L., Yuan, W., Rui, Y.C., MicroRNA-125a/b-5p inhibits endothelin-1 expression in vascular endothelial cells. J. Hypertens. 28 (2010), 1646–1654.
82. [82] 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. Cardiovasc. Res. 83 (2009), 131–139.
83. [83] Feng, B., Cao, Y., Chen, S., Ruiz, M., Chakrabarti, S., Reprint of: miRNA-1 regulates endothelin-1 in diabetes. Life Sci. 118 (2014), 275–280.
84. [84] Brownlee, M., Biochemistry and molecular cell biology of diabetic complications. Nature 414 (2001), 813–820.
85. [85] Caporali, A., Meloni, M., Vollenkle, C., Bonci, D., Sala-Newby, G.B., Addis, R., Spinetti, G., Losa, S., Masson, R., Baker, A.H., Agami, R., le Sage, C., Condorelli, G., Madeddu, P., Martelli, F., Emanueli, C., Deregulation of microRNA-503 contributes to diabetes mellitus-induced impairment of endothelial function and reparative angiogenesis after limb ischemia. Circulation 123 (2011), 282–291.
86. [86] Khan, Z.A., Chakrabarti, S., Growth factors in proliferative diabetic retinopathy. Exp. Diabetes Res. 4 (2003), 287–301.
87. [87] Aiello, L.P., Vascular endothelial growth factor and the eye: biochemical mechanisms of action and implications for novel therapies. Ophthalmic Res. 29 (1997), 354–362.
88. [88] McArthur, K., Feng, B., Wu, Y., Chen, S., Chakrabarti, S., MicroRNA-200b regulates vascular endothelial growth factor-mediated alterations in diabetic retinopathy. Diabetes 60 (2011), 1314–1323.
89. [89] Conserva, F., Pontrelli, P., Accetturo, M., Gesualdo, L., The pathogenesis of diabetic nephropathy: focus on microRNAs and proteomics. J. Nephrol. 26 (2013), 811–820.
90. [90] Huang, Y., Liu, Y., Li, L., Su, B., Yang, L., Fan, W., Yin, Q., Chen, L., Cui, T., Zhang, J., Lu, Y., Cheng, J., Fu, P., Liu, F., Involvement of inflammation-related miR-155 and miR-146a in diabetic nephropathy: implications for glomerular endothelial injury. BMC Nephrol., 15, 2014, 142.
91. [91] Panieri, E., Santoro, M.M., ROS signaling and redox biology in endothelial cells. Cell. Mol. Life Sci. 72 (2015), 3281–3303.
92. [92] Shilo, S., Roy, S., Khanna, S., Sen, C.K., Evidence for the involvement of miRNA in redox regulated angiogenic response of human microvascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 28 (2008), 471–477.
93. [93] Magenta, A., Cencioni, C., Fasanaro, P., Zaccagnini, G., Greco, S., Sarra-Ferraris, G., Antonini, A., Martelli, F., Capogrossi, M.C., miR-200c is upregulated by oxidative stress and induces endothelial cell apoptosis and senescence via ZEB1 inhibition. Cell Death Differ. 18 (2011), 1628–1639.
94. [94] Kantharidis, P., Wang, B., Carew, R.M., Lan, H.Y., Diabetes complications: the microRNA perspective. Diabetes 60 (2011), 1832–1837.
95. [95] Carmeliet, P., Angiogenesis in life, disease and medicine. Nature 438 (2005), 932–936.
96. [96] Cross, M.J., Claesson-Welsh, L., FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol. Sci. 22 (2001), 201–207.
97. [97] Chamorro-Jorganes, A., Araldi, E., Penalva, L.O., Sandhu, D., Fernandez-Hernando, C., Suarez, Y., MicroRNA-16 and microRNA-424 regulate cell-autonomous angiogenic functions in endothelial cells via targeting vascular endothelial growth factor receptor-2 and fibroblast growth factor receptor-1. Arterioscler. Thromb. Vasc. Biol. 31 (2011), 2595–2606.
98. [98] Chamorro-Jorganes, A., Araldi, E., Rotllan, N., Cirera-Salinas, D., Suarez, Y., Autoregulation of glypican-1 by intronic microRNA-149 fine tunes the angiogenic response to FGF2 in human endothelial cells. J. Cell Sci. 127 (2014), 1169–1178.
99. [99] Chamorro-Jorganes, A., Lee, M.Y., Araldi, E., Landskroner-Eiger, S., Fernandez-Fuertes, M., Sahraei, M., Quiles Del Rey, M., van Solingen, C., Yu, J., Fernández-Hernando, C., Sessa, W.C., Suárez, Y., VEGF-Induced Expression of miR-17 ~ 92 Cluster in Endothelial Cells is Mediated by ERK/ELK1 Activation and Regulates Angiogenesis. 2015, Circulation Research (CIRCRESAHA.115.307408).
100. [100] Fasanaro, P., D'apos, Y., Alessandra, V., Stefano, Di, Melchionna, R., romani, S., Pompilio, G., Capogrossi, M.C., Martelli, F., MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J. Biol. Chem. 283 (2008), 15878–15883.
101. [101] Hu, S., Huang, M., Li, Z., Jia, F., Ghosh, Z., Lijkwan, M.A., Fasanaro, P., Sun, N., Wang, X., Martelli, F., Robbins, R.C., Wu, J.C., MicroRNA-210 as a novel therapy for treatment of ischemic heart disease. Circulation 122 (2010), S124–S131.
102. [102] Zaccagnini, G., Maimone, B., Di Stefano, V., Fasanaro, P., Greco, S., Perfetti, A., Capogrossi, M.C., Gaetano, C., Martelli, F., Hypoxia-induced miR-210 modulates tissue response to acute peripheral ischemia. Antioxid. Redox Signal. 21 (2014), 1177–1188.
103. [103] Ghosh, G., Subramanian, I.V., Adhikari, N., Zhang, X., Joshi, H.P., Basi, D., Chandrashekhar, Y.S., Hall, J.L., Roy, S., Zeng, Y., Ramakrishnan, S., Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-alpha isoforms and promotes angiogenesis. J. Clin. Invest. 120 (2010), 4141–4154.
104. [104] Suárez, Y., Fernández-Hernando, C., Yu, J., Gerber, S.A., Harrison, K.D., Pober, J.S., Iruela-Arispe, M.L., Merkenschlager, M., Sessa, W.C., Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 14082–14087.
105. [105] Kuhnert, F., Mancuso, M.R., Hampton, J., Stankunas, K., Asano, T., Chen, C.Z., Kuo, C.J., Attribution of vascular phenotypes of the murine Egfl7 locus to the microRNA miR-126. Development 135 (2008), 3989–3993.
106. [106] van Solingen, C., Bijkerk, R., de Boer, H.C., Rabelink, T.J., van Zonneveld, A.J., The Role of microRNA-126 in Vascular Homeostasis. Curr. Vasc. Pharmacol. 13 (2015), 341–351.
107. [107] van Solingen, C., Seghers, L., Bijkerk, R., Duijs, J.M., Roeten, M.K., van Oeveren-Rietdijk, A.M., Baelde, H.J., Monge, M., Vos, J.B., de Boer, H.C., Quax, P.H., Rabelink, T.J., van Zonneveld, A.J., Antagomir-mediated silencing of endothelial cell specific microRNA-126 impairs ischemia-induced angiogenesis. J. Cell. Mol. Med. 13 (2009), 1577–1585.
108. [108] van Solingen, C., de Boer, H.C., Bijkerk, R., Monge, M., van Oeveren-Rietdijk, A.M., Seghers, L., de Vries, M.R., van der Veer, E.P., Quax, P.H., Rabelink, T.J., van Zonneveld, A.J., MicroRNA-126 modulates endothelial SDF-1 expression and mobilization of Sca-1(+)/Lin(−) progenitor cells in ischaemia. Cardiovasc. Res. 92 (2011), 449–455.
109. [109] Landskroner-Eiger, S., Qiu, C., Perrotta, P., Siragusa, M., Lee, M.Y., Ulrich, V., Luciano, A.K., Zhuang, Z.W., Corti, F., Simons, M., Montgomery, R.L., Wu, D., Yu, J., Sessa, W.C., Endothelial miR-17 ∼ 92 cluster negatively regulates arteriogenesis via miRNA-19 repression of WNT signaling. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 12812–12817.
110. [110] Bonauer, A., Carmona, G., Iwasaki, M., Mione, M., Koyanagi, M., Fischer, A., Burchfield, J., Fox, H., Doebele, C., Ohtani, K., Chavakis, E., Potente, M., Tjwa, M., Urbich, C., Zeiher, A.M., Dimmeler, S., MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science (New York, N.Y.) 324 (2009), 1710–1713.
111. [111] Iaconetti, C., Polimeni, A., Sorrentino, S., Sabatino, J., Pironti, G., Esposito, G., Curcio, A., Indolfi, C., Inhibition of miR-92a increases endothelial proliferation and migration in vitro as well as reduces neointimal proliferation in vivo after vascular injury. Basic Res. Cardiol. 107 (2012), 296–309.
112. [112] Hinkel, R., Penzkofer, D., Zühlke, S., Fischer, A., Husada, W., Xu, Q.-F., Baloch, E., van Rooij, E., Zeiher, A.M., Kupatt, C., Dimmeler, S., Inhibition of microRNA-92a protects against ischemia/reperfusion injury in a large-animal model. Circulation 128 (2013), 1066–1075.
113. [113] Daniel, J.-M., Penzkofer, D., Teske, R., Dutzmann, J., Koch, A., Bielenberg, W., Bonauer, A., Boon, R.A., Fischer, A., Bauersachs, J., van Rooij, E., Dimmeler, S., Sedding, D.G., Inhibition of miR-92a improves re-endothelialization and prevents neointima formation following vascular injury. Cardiovasc. Res. 103 (2014), 564–572.
114. [114] Semo, J., Sharir, R., Afek, A., Avivi, C., Barshack, I., Maysel-Auslender, S., Krelin, Y., Kain, D., Entin-Meer, M., Keren, G., George, J., The 106b ∼ 25 microRNA cluster is essential for neovascularization after hindlimb ischaemia in mice. Eur. Heart J. 35 (2014), 3212–3223.
115. [115] Dangwal, S., Thum, T., microRNA therapeutics in cardiovascular disease models. Annu. Rev. Pharmacol. Toxicol. 54 (2014), 185–203.
116. [116] Fichtlscherer, S., Zeiher, A.M., Dimmeler, S., Circulating microRNAs: biomarkers or mediators of cardiovascular diseases?. Arterioscler. Thromb. Vasc. Biol. 31 (2011), 2383–2390.
117. [117] Ottosen, S., Parsley, T.B., Yang, L., Zeh, K., van Doorn, L.J., van der Veer, E., Raney, A.K., Hodges, M.R., Patick, A.K., In vitro antiviral activity and preclinical and clinical resistance profile of miravirsen, a novel anti-hepatitis C virus therapeutic targeting the human factor miR-122. Antimicrob. Agents Chemother. 59 (2015), 599–608.