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Epigenetic factors in atherogenesis: MicroRNA

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Abstract

MicroRNAs (miRNAs) are small (~22 nucleotides in length) noncoding RNA sequences regulating gene expression at the posttranscriptional level. MicroRNAs bind complementarily to certain mRNA and cause gene silencing. miRNAs are involved in plaque formation and rapture, regulation of cholesterol metabolism, inflammatory response, cell cycle progression and proliferation, platelet activation; they also influence functions of endothelial and vascular smooth muscle cells (VSMC). This suggests their important roles in initiation and progression of atherosclerosis. MicroRNAs play a key role in the development of cardiovascular diseases (CVDs), including atherosclerosis. The use of antisense oligonucleotides is considered as promising technique for targeted changes in gene expression both in vitro and in vivo. In this review, we consider the role of miRNAs in progression of atherosclerosis, their use as potential biomarkers and targets in the treatment of CVDs, as well as possible application of antisense oligonucleotides.

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References

  1. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E., and Mello, C.C., Nature, 1998, vol. 391, no. 6669, pp. 806–811.

    Article  CAS  Google Scholar 

  2. Karbiener, M., Glnoantschnig, C., and Scheideler, M., Int. J. Mol. Sci., 2014, vol. 15, no. 11, pp. 20266–20289.

    Article  Google Scholar 

  3. Lewis, B.P., Burge, C.B., and Bartel, D.P., Cell, 2005, vol. 120, pp. 15–20.

    Article  CAS  Google Scholar 

  4. Inukai, S. and Slack, F.J., Cell Cycle, 2012, vol. 11, no. 6, pp. 1060–1061.

    Article  CAS  Google Scholar 

  5. Kloosterman, W.P., Wienholds, E., de Bruijn, E., Kauppinen, S., and Plasterk, R.H., Nat. Methods, 2006, vol. 3, no. 1, pp. 27–29.

    Article  CAS  Google Scholar 

  6. Ho, J.J., Metcalf, J.L., Yan, M.S., Turgeon, P.J., Wang, J.J., Chalsev, M., Petruzziello-Pellegrini, T.N., Tsui, A.K., He, J.Z., Dhamko, H., Man, H.S., Robb, G.B., Teh, B.T., Ohh, M., and Marsden, P.A., J. Biol. Chem., 2012, vol. 287, no. 34, pp. 29003–29020.

    Article  CAS  Google Scholar 

  7. Moore, K.J., Rayner, K.J., Suárez, Y., and Fernández-Hernando, C., Annu. Rev. Nutr., 2011, vol. 31, pp. 49–63.

    Article  CAS  Google Scholar 

  8. Hwang, H.W., Wentzel, E.A., and Mendell, J.T., Proc. Natl. Acad. Sci. USA, 2009, vol. 106, no. 17, pp. 7016–7021.

    Article  CAS  Google Scholar 

  9. Hergenreider, E., Heydt, S., Tréguer, K., Boettger, T., Horrevoets, A.J., Zeiher, A.M., Scheffer, M.P., Frangakis, A.S., Yin, X., Mayr, M., Braun, T., Urbich, C., Boon, R.A., and Dimmeler, S., Nat. Cell Biol., 2012, vol. 14, pp. 249–256.

    Article  CAS  Google Scholar 

  10. Boon, R.A. and Vickers, K.C., Arterioscler. Thromb. Vasc. Biol., 2013, vol. 33, no. 2, pp. 186–192.

    Article  CAS  Google Scholar 

  11. Ross, R., N. Engl. J. Med., 1998, vol. 340, no. 2, pp. 115–126.

    Google Scholar 

  12. Borodachev, E.N., Sobenin, I.A., Karagodin, V.P., Bobryshev, Yu.V., and Orekhov, A.N., Patogenez, 2013, vol. 11, no. 4, pp. 16–21.

    Google Scholar 

  13. Fang, Y., Shi, C., Manduchi, E., Civelek, M., and Davies, P.F., Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 13450–13455.

    Article  CAS  Google Scholar 

  14. Sun, X., He, S., Wara, A.K., Icli, B., Shvartz, E., Tesmenitsky, Y., Belkin, N., Li, D., Blackwell, T.S., Sukhova, G.K., Croce, K., and Feinberg, M.W., Circ. Res., 2014, vol. 114, no. 1, pp. 32–40.

    Article  CAS  Google Scholar 

  15. Suarez, Y., Wang, C., Manes, T.D., and Pober, J.S., J. Immunol., 2010, vol. 184, pp. 21–25.

    Article  CAS  Google Scholar 

  16. Asgeirsdottir, S.A., van Solingen, C., Kurniati, N.F., Zwiers, P.J., Heeringa, P., Van Meurs, M., Satchell, S.C., Saleem, M.A., Mathieson, P.W., Banas, B., Kamps, J.A., Rabelink, T.J., Van Zonneveld, A.J., and Molema, G., Am. J. Physiol. Renal. Physiol., 2012, vol. 302, pp. F1630–F1639.

    Article  CAS  Google Scholar 

  17. 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., Garcia-Cardena, G., and Shyy, J.Y., Circulation, 2011, vol. 124, pp. 633–641.

    Article  CAS  Google Scholar 

  18. Fang, Y. and Davies, P.F., Arterioscler. Thromb. Vasc. Biol., 2012, vol. 32, pp. 979–987.

    Article  CAS  Google Scholar 

  19. Olivieri, F., Lazzarini, R., Recchioni, R., Marcheselli, F., Rippo, M.R., Di Nuzzo, S., Albertini, M.C., Graciotti, L., Babini, L., Mariotti, S., Spada, G., Abbatecola, A.M., Antonicelli, R., Franceschi, C., and Procopio, A.D., Age (Dordr), 2013, vol. 35, no. 4, pp. 1157–1172.

    Article  CAS  Google Scholar 

  20. Menghini, R., Stöhr, R., and Federici, M., Ageing Res. Rev., 2014, vol. 17, pp. 68–78.

    Article  CAS  Google Scholar 

  21. Glass, C.K. and Witztum, J.L., Cell, 2001, vol. 104, pp. 503–516.

    Article  CAS  Google Scholar 

  22. Brown, M.S. and Goldstein, J.L., Cell, 1997, vol. 89, pp. 331–340.

    Article  CAS  Google Scholar 

  23. Sudhof, T.C., Russell, D.W., Brown, M.S., and Goldstein, J.L., Cell, 1987, vol. 48, pp. 1061–1069.

    Article  CAS  Google Scholar 

  24. Lee, Y.S., Lee, H.H., Park, J., Yoo, E.J., Glackin, C.A., Choi, Y.I., Jeon, S.H., Seong, R.H., Park, S.D., and Kim, J.B., Nucleic Acids Res., 2003, vol. 31, no. 24, pp. 7165–7174.

    Article  CAS  Google Scholar 

  25. Gong, Y., Lee, J.N., Lee, P.C., Goldstein, J.L., Brown, M.S., and Ye, J., Cell Metab., 2006, vol. 3, no. 1, pp. 15–24.

    Article  CAS  Google Scholar 

  26. Marquart, T.J., Allen, R.M., Ory, D.S., and Baldan, A., Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 12228–12232.

    Article  CAS  Google Scholar 

  27. Lindholm, M.W., Elmén, J., Fisker, N., Hansen, H.F., Persson, R., Moller, M.R., Rosenbohm, C., Orum, H., Straarup, E.M., and Koch, T., Mol. Ther., 2012, vol. 20, no. 2, pp. 376–381.

    Article  CAS  Google Scholar 

  28. Nie, Y.Q., Cao, J., Zhou, Y.J., Liang, X., Du, Y.L., Wan, Y.J., and Li, Y.Y., J. Cell. Biochem., 2014, vol. 115, no. 5, pp. 839–846.

    Article  CAS  Google Scholar 

  29. Brown, M.S. and Goldstein, J.L., Ciba Foundation Symp., 1982, vol. 92, pp. 77–95.

    Google Scholar 

  30. Brown, M.S. and Goldstein, J.L., N. Engl. J. Med., 1976, vol. 294, pp. 1386–1390.

    Article  CAS  Google Scholar 

  31. Tailleux, A., Duriez, P., Fruchart, J.C., and Clavey, V., Atherosclerosis, 2002, vol. 164, no. 1, pp. 1–13.

    Article  CAS  Google Scholar 

  32. Horie, T., Baba, O., Kuwabara, Y., Chujo, Y., Watanabe, S., Kinoshita, M., Horiguchi, M., Nakamura, T., Chonabayashi, K., Hishizawa, M., Hasegawa, K., Kume, N., Yokode, M., Kita, T., Kimura, T., and Ono, K., J. Am. Heart Assoc., 2012, doi 10.1161/JAHA.112.003376

    Google Scholar 

  33. Hayden, M.R., Clee, S.M., Brooks-Wilson, A., Genest, J., Attie, A., and Kastelein, J.J., Curr. Opin. Lipidol., 2000, vol. 11, no. 2, pp. 117–122.

    Article  CAS  Google Scholar 

  34. Rotllan, N., Ramírez, C.M., Aryal, B., Esau, C.C., and Fernández-Hernando C., Arterioscler. Thromb. Vasc. Biol., 2013, vol. 33, no. 8, pp. 1973–1977.

    Article  CAS  Google Scholar 

  35. Horie, T., Nishino, T., Baba, O., Kuwabara, Y., Nakao, T., Nishiga, M., Usami, S., Izuhara, M., Nakazeki, F., Ide, Y., Koyama, S., Sowa, N., Yahagi, N., Shimano, H., Nakamura, T., Hasegawa, K., Kume, N., Yokode, M., Kita, T., Kimura, T., and Ono, K., Sci. Rep., 2014, vol. 4, p. 5312.

    Article  CAS  Google Scholar 

  36. Ramírez, C.M., Dávalos, A., Goedeke, L., Salerno, A.G., Warrier, N., Cirera-Salinas, D., Suárez, Y., and Fernández-Hernando, C., Arterioscler. Thromb. Vasc. Biol., 2011, vol. 31, pp. 2707–2714.

    Article  Google Scholar 

  37. Sun, D., Zhang, J., Xie, J., Wei, W., Chen, M., and Zhao, X., FEBS Lett., 2010, vol. 586, pp. 1472–1479.

    Article  Google Scholar 

  38. Kim, J., Yoon, H., Ramírez, C.M., Lee, S.M., Hoe, H.S., Fernández-Hernando, C., and Kim, J., Exp. Neurol., 2012, vol. 235, pp. 476–483.

    Article  CAS  Google Scholar 

  39. Huang, R.S., Hu, G.Q., Lin, B., Lin, Z.Y., and Sun, C.C., J. Investig. Med., 2010, vol. 58, pp. 961–967.

    Article  CAS  Google Scholar 

  40. Chen, T., Huang, Z., Wang, L., Wang, Y., Wu, F., Meng, S., and Wang, C., Cardiovasc. Res., 2009, vol. 83, pp. 131–139.

    Article  CAS  Google Scholar 

  41. Wei, Y., Zhu, M., Corbalán-Campos, J., Heyll, K., Weber, C., and Schober, A., Arterioscler. Thromb. Vasc. Biol., 2015, vol. 35, no. 4, pp. 796–803.

    Article  CAS  Google Scholar 

  42. Leeper, N.J., Raiesdana, A., Kojima, Y., Chun, H.J., Azuma, J., Maegdefessel, L., Kundu, R.K., Quertermous, T., Tsao, P.S., and Spin, J.M., J. Cell Physiol., 2011, vol. 226, pp. 1035–1043.

    Article  CAS  Google Scholar 

  43. Kushlinskii, N.E. and Gershtein, T.S., Pathogenesis, 2013, vol. 11, no. 2, pp. 3–10.

    Google Scholar 

  44. Chen, K.C., Liao, Y.C., Hsieh, I.C., Wang, Y.S., Hu, C.Y., and Juo, S.H., J. Mol. Cell. Cardiol., 2012, vol. 52, no. 3, pp. 587–595.

    Article  CAS  Google Scholar 

  45. Lovren, F., Pan, Y., Quan, A., Singh, K.K., Shukla, P.C., Gupta, N., Steer, B.M., Ingram, A.J., Gupta, M., Al-Omran, M., Teoh, H., Marsden, P.A., and Verma, S., Circulation, 2012, vol. 126, pp. S81–S90.

    Article  CAS  Google Scholar 

  46. Goettsch, C., Rauner, M., Pacyna, N., Hempel, U., Bornstein, S.R., and Hofbauer, L.C., Am. J. Pathol., 2011, vol. 179, pp. 1594–1600.

    Article  CAS  Google Scholar 

  47. Chistiakov, D.A., Orekhov, A.N., and Bobryshev, Y.V., Acta Physiol. (Oxf)., 2015, vol. 213, no. 3, pp. 539–553.

    Article  CAS  Google Scholar 

  48. Chistiakov, D.A., Sobenin, I.A., Orekhov, A.N., and Bobryshev, Y.V., Biomed. Res. Int., 2015, doi 10.1155/2015/354517

    Google Scholar 

  49. 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., and Zhou, J.G., Hypertension, 2012, vol. 60, pp. 1407–1414.

    Article  CAS  Google Scholar 

  50. Kuehbacher, A., Urbich, C., and Dimmeler, S., Trends Pharmacol. Sci., 2008, vol. 29, pp. 12–15.

    Article  CAS  Google Scholar 

  51. Urbich, C., Kaluza, D., Frömel, T., Knau, A., Bennewitz, K., Boon, R.A., Bonauer, A., Doebele, C., Boeckel, J.N., Hergenreider, E., Zeiher, A.M., Kroll, J., Fleming, I., and Dimmeler, S., Blood, 2012, vol. 119, pp. 1607–1616.

    Article  CAS  Google Scholar 

  52. Guo, M., Mao, X., Ji, Q., Lang, M., Li, S., Peng, Y., Zhou, W., Xiong, B., and Zeng, Q., Immunol. Cell Biol., 2010, vol. 88, pp. 555–564.

    Article  CAS  Google Scholar 

  53. Li, Z., Hassan, M.Q., Jafferji, M., Aqeilan, R.I., Garzon, R., Croce, C.M., Van Wijnen, A.J., Stein, J.L., Stein, G.S., and Lian, J.B., J. Biol. Chem., 2009, vol. 284, pp. 15676–15684.

    Article  CAS  Google Scholar 

  54. Qin, B., Xiao, B., Liang, D., Xia, J., Li, Y., and Yang, H., Biochem. Biophys. Res. Commun., 2011, vol. 410, pp. 127–133.

    Article  CAS  Google Scholar 

  55. Lin, Y., Liu, X., Cheng, Y., Yang, J., Huo, Y., and Zhang, C., J. Biol. Chem., 2009, vol. 284, pp. 7903–7913.

    Article  CAS  Google Scholar 

  56. Yeom, K.H., Lee, Y., Han, J., Suh, M.R., and Kim, V.N., Nucl. Acids Res., 2006, vol. 34, no. 16, pp. 4622–4629.

    Article  CAS  Google Scholar 

  57. Davis, N., Mor, E., and Ashery-Padan, R., Development, 2011, vol. 138, pp. 127–138.

    Article  CAS  Google Scholar 

  58. Siomi, H. and Siomi, M.C., Nat. Cell Biol., 2009, vol. 11, no. 9, pp. 1049–1051.

    Article  CAS  Google Scholar 

  59. Faehnle, C.R., Elkayam, E., Haase, A.D., Hannon, G.J., and Joshua-Tor, L., Cell Rep., 2013, vol. 3, no. 6, pp. 1901–1909.

    Article  CAS  Google Scholar 

  60. Wang, W., Zhao, L.J., Tan, Y.X., Ren, H., and Qi, Z.T., World J. Gastroenterol., 2012, vol. 18, no. 38, pp. 5442–5453.

  61. Filipowicz, W., Bhattacharyya, S.N., and Sonenberg, N., Nat. Rev. Genet., 2008, vol. 9, no. 2, pp. 102–114.

    Article  CAS  Google Scholar 

  62. Forman, J.J. and Coller, H.A., Cell Cycle, 2010, vol. 9, pp. 1533–1541.

    Article  CAS  Google Scholar 

  63. Zhou, H. and Rigoutsos, I., RNA, 2014, vol. 20, no. 9, pp. 1431–1439.

    Article  Google Scholar 

  64. Madrigal-Matute, J., Martin-Ventura, J.L., Blanco-Colio, L.M., Egido, J., Michel, J.B., and Meilhac, O., Adv. Clin. Chem., 2011, vol. 54, pp. 1–43.

    Article  CAS  Google Scholar 

  65. Pirola, C.J., Fernández Gianotti, T., Castaño, G.O., Mallardi, P., San Martino, J., Mora Gonzalez Lopez Ledesma, M., Flichman, D., Mirshahi, F., Sanyal, A.J., and Sookoian, S., Gut, 2015, vol. 64, no. 5, pp. 800–812.

    Article  CAS  Google Scholar 

  66. Wagner, J., Riwanto, M., Besler, C., Knau, A., Fichtlscherer, S., Röxe, T., Zeiher, A.M., Landmesser, U., and Dimmeler, S., Arterioscler. Thromb. Vasc. Biol., 2013, vol. 33, no. 6, pp. 1392–1400.

    Article  CAS  Google Scholar 

  67. Yamamoto, Y., Yoshioka, Y., Minoura, K., Takahashi, R.U., Takeshita, F., Taya, T., Horii, R., Fukuoka, Y., Kato, T., Kosaka, N., and Ochiya, T., Mol. Cancer, 2011, vol. 10, p. 135.

    Article  CAS  Google Scholar 

  68. Tijsen, A.J., Pinto, Y.M., and Creemers, E.E., Am. J. Physiol. Heart Circ. Physiol., 2012, vol. 303, no. 9, pp. H1085–H1095.

    Article  CAS  Google Scholar 

  69. Arroyo, J.D., Chevillet, J.R., Kroh, E.M., Ruf, I.K., Pritchard, C.C., Gibson, D.F., Mitchell, P.S., Bennett, C.F., Pogosova-Agadjanyan, E.L., Stirewalt, D.L., Tait, J.F., and Tewari, M., Proc. Natl. Acad. Sci. USA, 2011, vol. 108, pp. 5003–5008.

    Article  CAS  Google Scholar 

  70. Kosaka, N., Iguchi, H., Yoshioka, Y., Hagiwara, K., Takeshita, F., and Ochiya, T., J. Biol. Chem., 2012, vol. 287, no. 2, pp. 1397–1405.

    Article  CAS  Google Scholar 

  71. Li, J., Zhang, Y., Liu, Y., Dai, X., Li, W., Cai, X., Yin, Y., Wang, Q., Xue, Y., Wang, C., Li, D., Hou, D., Jiang, X., Zhang, J., Zen, K., Chen, X., and Zhang, C.Y., J. Biol. Chem., 2013, vol. 288, no. 32, pp. 23586–23596.

    Article  CAS  Google Scholar 

  72. Schober, A., Nazari-Jahantigh, M., Wei, Y., Bidzhekov, K., Gremse, F., Grommes, J., Megens, R.T., Heyll, K., Noels, H., Hristov, M., Wang, S., Kiessling, F., Olson, E.N., and Weber, C., Nat. Med., 2014, vol. 20, no. 4, pp. 368–376.

    Article  CAS  Google Scholar 

  73. Davis, S., Propp, S., Freier, S.M., Jones, L.E., Serra, M.J., Kinberger, G., Bhat, B., Swayze, E.E., Bennett, C.F., and Esau, C., Nucleic Acids Res., 2009, vol. 37, pp. 70–77.

    Article  CAS  Google Scholar 

  74. Krutzfeldt, J., Rajewsky, N., Braich, R., Rajeev, K.G., Tuschl, T., Manoharan, M., and Stoffel, M., Nature, 2005, vol. 438, pp. 685–689.

    Article  Google Scholar 

  75. 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., and Moore, K.J., Nature, 2011, vol. 478, pp. 404–407.

    Article  CAS  Google Scholar 

  76. 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., and Moore, K.J., J. Clin. Invest., 2011, vol. 121, pp. 2921–2931.

    Article  CAS  Google Scholar 

  77. Marquart, T.J., Wu, J., Lusis, A.J., and Baldan, A., Arterioscl. Thromb., Vasc. Biol., 2013, vol. 33, no. 3, pp. 455–458.

    Article  CAS  Google Scholar 

  78. Tao, J., Ji, J., Li, X., Ding, N., Wu, H., Liu, Y., Wang, X.W., Calvisi, D.F., Song, G., and Chen, X., Oncotarget, 2015, vol. 6, no. 9, pp. 6977–6988.

    Article  Google Scholar 

  79. Ma, J., Wu, Q., Zhang, Y., Li, J., Yu, Y., Pan, Q., and Sun, F., Oncol. Rep., 2014, vol. 32, no. 6, pp. 2744–2752.

    CAS  Google Scholar 

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Authors and Affiliations

  1. Institute for Atherosclerosis Research, Skolkovo Innovative Center, P.O. Box 21, Moscow, 121609, Russia

    A. V. Smirnova & A. N. Orekhov

  2. Laboratory of Angiopathology, Institute of General Pathology and Pathophysiology, ul. Baltiyskaya 8, Moscow, 125315, Russia

    V. N. Sukhorukov & A. N. Orekhov

  3. Plekhanov Russian University of Economics, Stremyanny per. 36, Moscow, 117997, Russia

    V. P. Karagodin

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  1. A. V. Smirnova
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Original Russian Text © A.V. Smirnova, V.N. Sukhorukov, V.P. Karagodin, A.N. Orekhov, 2016, published in Biomeditsinskaya Khimiya.

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Smirnova, A.V., Sukhorukov, V.N., Karagodin, V.P. et al. Epigenetic factors in atherogenesis: MicroRNA. Biochem. Moscow Suppl. Ser. B 10, 269–275 (2016). https://doi.org/10.1134/S199075081603015X

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