Biochemistry (Moscow)

, Volume 84, Issue 11, pp 1233–1246 | Cite as

Role of MicroRNAs in the Regulation of Redox-Dependent Processes

  • E. V. KalininaEmail author
  • V. I. Ivanova-Radkevich
  • N. N. Chernov


Cellular redox homeostasis involves a combination of redox processes and corresponding regulatory systems and represents an important factor ensuring cell viability. Redox-dependent regulation of cellular processes is a multi-level system including not only proteins and enzyme complexes, but also non-coding RNAs, among which an important role belongs to microRNAs. The review focuses on the involvement of miRNAs in the redox-dependent regulation of both ROS (reactive oxygen species)-generating enzymes and antioxidant enzymes with special emphasis on the effects of miRNAs on redox-dependent processes in tumor cells. The impact of ROS on the miRNA expression and the role of the ROS/miRNA feedback regulation in the cell redox state are discussed.


reactive oxygen species cellular redox homeostasis microRNA 



antioxidant-responsive element




hypoxia-induced factor




nuclear factor κB


NF-E2-dependent factor 2


ochratoxin A


programmed cell death protein 4




reactive oxygen species


superoxide dismutase




thioredoxin reductase


untranslated region


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The publication has been prepared with the support of the “RUDN University Program 5–100”.


  1. 1.
    Singh, A., Kukreti, R., Saso, L., and Kukreti, S. (2019) Oxidative stress: a key modulator in neurodegenerative diseases, Molecules, 24, E1583, doi: Scholar
  2. 2.
    Massaro, M., Scoditti, E., Carluccio, M. A., and De Caterina, R. (2019) Oxidative stress and vascular stiffness in hypertension: a renewed interest for antioxidant therapies? Vasc. Pharmacol., 116, 45–50, doi: Scholar
  3. 3.
    Sies, H., Berndt, C., and Jones, D. P. (2017) Oxidative stress, Annu. Rev. Biochem., 86, 715–748, doi: Scholar
  4. 4.
    Ursini, F., Maiorino, M., and Forman, H. J. (2016) Redox homeostasis: the golden mean of healthy living, Redox Biol., 8, 205–215, doi: Scholar
  5. 5.
    Klotz, L. O., and Steinbrenner, H. (2017) Cellular adaptation to xenobiotics: interplay between xenosensors, reactive oxygen species and FOXO transcription factors, Redox Biol., 13, 646–654, doi: Scholar
  6. 6.
    Jones, D. P. (2006) Redefining oxidative stress, Antioxid. Redox Signal., 8, 865–1879, doi: Scholar
  7. 7.
    Hopkins, B. L., and Neumann, C. A. (2019) Redoxins as gatekeepers of the transcriptional oxidative stress response, Redox Biol., 21, 101104, doi: Scholar
  8. 8.
    Kalinina, E. V., Chernov, N. N., and Saprin, A. N. (2008) Involvement of thio-, peroxi-, and glutaredoxins in cellular redox-dependent processes, Biochemistry (Moscow), 73, 1493–1510, doi: Scholar
  9. 9.
    Leisegang, M. S., Schroder, K., and Brandes, R. P. (2018) Redox regulation and noncoding RNAs, Antioxid. Redox Signal., 29, 793–812, doi: Scholar
  10. 10.
    Uchida, S., and Bolli, R. (2018) Short and long noncoding RNAs regulate the epigenetic status of cells, Antioxid. Redox Signal., 29, 832–845, doi: Scholar
  11. 11.
    Engedal, N., Zerovnik, E., Rudov, A., Galli, F., Olivieri, F., Procopio, A. D., Rippo, M. R., Monsurro, V., Betti, M., and Albertini, M. C. (2018) From oxidative stress damage to pathways, networks, and autophagy via microRNAs, Oxid. Med. Cell. Longev., 2018, 4968321, doi: Scholar
  12. 12.
    Lan, J., Huang, Z., Han, J., Shao, J., and Huang, C. (2018) Redox regulation of microRNAs in cancer, Cancer Lett., 418, 250–259, doi: Scholar
  13. 13.
    Koroleva, I. A., Nazarenko, M. S., and Kucher, A. N. (2018) Role of microRNA in development of instability of atherosclerotic plaques, Biochemistry (Moscow), 82, 1380–1390, doi: Scholar
  14. 14.
    Vishnoi, A., and Rani, S. (2017) MiRNA biogenesis and regulation of diseases: an overview, Methods Mol. Biol., 1509, 1–10, doi: Scholar
  15. 15.
    Drusco, A., and Croce, C. M. (2017) MicroRNAs and cancer: a long story for short RNAs, Adv. Cancer Res., 135, 1–24, doi: Scholar
  16. 16.
    Wu, K., He, J., Pu, W., and Peng, Y. (2018) The role of exportin-5 in microRNA biogenesis and cancer, Genom. Proteom. Bioinform., 16, 120–126, doi: Scholar
  17. 17.
    Chendrimada, T. P., Gregory, R. I., Kumaraswamy, E., Norman, J., Cooch, N., Nishikura, K., and Shiekhattar, R. (2005) TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing, Nature, 436, 740–744, doi: Scholar
  18. 18.
    Bandara, V., Michael, M. Z., and Gleadle, J. M. (2014) Hypoxia represses microRNA biogenesis proteins in breast cancer cells, BMC Cancer, 14, 533, doi: Scholar
  19. 19.
    Suarez, Y., Fernandez-Hernando, C., Pober, J. S., and Sessa, W. C. (2007) Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells, Circ. Res., 100, 1164–1173, doi: Scholar
  20. 20.
    Orom, U. A., Nielsen, F. C., and Lund, A. H. (2008) MicroRNA-10a binds the 5′-UTR of ribosomal protein mRNAs and enhances their translation, Mol. Cell, 30, 460–471, doi: Scholar
  21. 21.
    Havens, M. A., Reich, A. A., Duelli, D. M., and Hastings, M. L. (2012) Biogenesis of mammalian microRNAs by a non-canonical processing pathway, Nucleic Acids Res., 40, 4626–4640, doi: Scholar
  22. 22.
    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., The, B. T., Ohh, M., and Marsden, P. A. (2012) Functional importance of Dicer protein in the adaptive cellular response to hypoxia, J. Biol. Chem., 287, 29003–29020, doi: Scholar
  23. 23.
    Wiesen, J. L., and Tomasi, T. B. (2009) Dicer is regulated by cellular stresses and interferons, Mol. Immunol., 46, 1222–1228, doi: Scholar
  24. 24.
    Ungvari, Z., Tucsek, Z., Sosnowska, D., Toth, P., Gautam, T., Podlutsky, A., Csiszar, A., Losonczy, G., Valcarcel-Ares, M. N., Sonntag, W. E., and Csiszar, A. (2012) Aging-induced dysregulation of Dicer1-dependent microRNA expression impairs angiogenic capacity of rat cerebromicrovascular endothelial cells, J. Gerontol. A Biol. Sci. Med. Sci., 68, 877–891, doi: Scholar
  25. 25.
    Cheng, X., Ku, C.-H., and Siow, R. C. M. (2013) Regulation of the Nrf2 antioxidant pathway by microRNAs: new players in micromanaging redox homeostasis, Free Radic. Biol. Med., 64, 4–11, doi: Scholar
  26. 26.
    Tang, X., Li, M., Tucker, L., and Ramratnam, B. (2011) Glycogen synthase kinase 3 beta (GSK3β) phosphorylates the RNase III enzyme Drosha at S300 and S302, PLoS One, 6, e20391, doi: Scholar
  27. 27.
    Upton, J. P., Wang, L., Han, D., Wang, E. S., Huskey, N. E., Lim, L., Truitt, M., McManus, M. T., Ruggero, D., Goga, A., Papa, F. R., and Oakes, S. A. (2012) IRE1α cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2, Science, 338, 818–822, doi: Scholar
  28. 28.
    Poulsen, H. E., Specht, E., Broedbaek, K., Henriksen, T., Ellervik, C., Mandrup-Poulsen, T., Tonnesen, M., Nielsen, P. E., Andersen, H. U., and Weimann, A. (2012) RNA modifications by oxidation: a novel disease mechanism? Free Radic. Biol. Med., 52, 1353–1361, doi: Scholar
  29. 29.
    Karihtala, P., Porvari, K., Soini, Y., and Haapasaari, K. M. (2017) Redox regulating enzymes and connected microRNA regulators have prognostic value in classical Hodgkin lymphomas, Oxid. Med. Cell. Longev., 2017, 2696071, doi: Scholar
  30. 30.
    Li, G., Luna, C., Qiu, J., Epstein, D. L., and Gonzalez, P. (2009) Alterations in microRNA expression in stress-induced cellular senescence, Mech. Ageing Dev., 130, 731–741, doi: Scholar
  31. 31.
    Ji, G., Lv, K., Chen, H., Wang, T., Wang, Y., Zhao, D., Qu, L., and Li, Y. (2013) MiR-146a regulates SOD2 expression in H2O2 stimulated PC12 cells, PLoS One, 8, e69351, doi: Scholar
  32. 32.
    Haque, R., Chun, E., Howell, J. C., Sengupta, T., Chen, D., and Kim, H. (2012) MicroRNA-30b-mediated regulation of catalase expression in human ARPE-19 cells, PLoS One, 7, e42542, doi: Scholar
  33. 33.
    Wang, L., Huang, H., Fan, Y., Kong, B., Hu, H., Hu, K., Guo, J., Mei, Y., and Liu, W. L. (2014) Effects of downregulation of microRNA-181a on H2O2-induced H9c2 cell apoptosis via the mitochondrial apoptotic pathway, Oxid. Med. Cell. Longev., 2014, 960362, doi: Scholar
  34. 34.
    Zhang, Y., Zheng, S., Geng, Y., Xue, J., Wang, Z., Xie, X., Wang, J., Zhang, S., and Hou, Y. (2015) MicroRNA profiling of atrial fibrillation in canines: miR-206 modulates intrinsic cardiac autonomic nerve remodeling by regulating SOD1, PLoS One, 10, e0122674, doi: Scholar
  35. 35.
    Dubois-Deruy, E., Cuvelliez, M., Fiedler, J., Charrier, H., Mulder, P., Hebbar, E., Pfanne, A., Beseme, O., Chwastyniak, M., Amouyel, P., Richard, V., Bauters, C., Thum, T., and Pinet, F. (2017) MicroRNAs regulating superoxide dismutase 2 are new circulating biomarkers of heart failure, Sci. Rep., 7, 14747, doi: Scholar
  36. 36.
    Matouskova, P., Hanouskova, B., and Skalova, L. (2018) MicroRNAs as potential regulators of glutathione peroxidases expression and their role in obesity and related pathologies, Int. J. Mol. Sci., 19, E1199, doi: Scholar
  37. 37.
    Cortez, M. A., Valdecanas, D., Zhang, X., Zhan, Y., Bhardwaj, V., Calin, G. A., Komaki, R., Giri, D. K., Quini, C. C., Wolfe, T., Peltier, H. J., Bader, A. G., Heymach, J. V., Meyn, R. E., and Welsh, J. W. (2014) Therapeutic delivery of miR-200c enhances radio-sensitivity in lung cancer, Mol. Ther., 22, 1494–1503, doi: Scholar
  38. 38.
    Jiang, W., Min, J., Sui, X., Qian, Y., Liu, Y., Liu, Z., Zhou, H., Li, X., and Gong, Y. (2015) MicroRNA-26a-5p and microRNA-23b-3p up-regulate peroxiredoxin III in acute myeloid leukemia, Leuk. Lymphoma, 56, 460–471, doi: Scholar
  39. 39.
    Bai, X. Y., Ma, Y., Ding, R., Fu, B., Shi, S., and Chen, X. M. (2011) MiR-335 and miR-34a promote renal senescence by suppressing mitochondrial antioxidative enzymes, J. Am. Soc. Nephrol., 22, 1252–1261, doi: Scholar
  40. 40.
    Kyrychenko, S., Kyrychenko, V., Badr, M. A., Ikeda, Y., Sadoshima, J., and Shirokova, N. (2015) Pivotal role of miR-448 in the development of ROS-induced cardiomyopathy, Cardiovasc. Res., 108, 324–334, doi: Scholar
  41. 41.
    Li, S. Z., Hu, Y. Y., Zhao, J., Zhao, Y. B., Sun, J. D., Yang, Y. F., Ji, C. C., Liu, Z. B., Cao, W. D., Qu, Y., Liu, W. P., Cheng, G., and Fei, Z. (2014) MicroRNA-34a induces apoptosis in the human glioma cell line, A172, through enhanced ROS production and NOX2 expression, Biochem. Biophys. Res. Commun., 444, 6–12, doi: Scholar
  42. 42.
    Fu, Y., Zhang, Y., Wang, Z., Wang, L., Wei, X., Zhang, B., Wen, Z., Fang, H., Pang, Q., and Yi, F. (2010) Regulation of NADPH oxidase activity is associated with miRNA-25-mediated NOX4 expression in experimental diabetic nephropathy, Am. J. Nephrol., 32, 581–589, doi: Scholar
  43. 43.
    Chen, F., Yin, C., Dimitropoulou, C., and Fulton, D. J. (2016) Cloning, characteristics, and functional analysis of rabbit NADPH oxidase 5, Front. Physiol., 7, 284, doi: Scholar
  44. 44.
    Yang, S., Gao, Y., Liu, G., Li, J., Shi, K., Du, B., Si, D., and Yang, P. (2015) The human ATF1 rs11169571 polymorphism increases essential hypertension risk through modifying miRNA binding, FEBS Lett., 589, 2087–2093, doi: Scholar
  45. 45.
    Varga, Z. V., Kupai, K., Szucs, G., Gaspar, R., Paloczi, J., Farago, N., Zvara, A., Puskas, L. G., Razga, Z., Tiszlavicz, L., Bencsik, P., Gorbe, A., Csonka, C., Ferdinandy, P., and Csont, T. (2013) MicroRNA-25-dependent up-regulation of NADPH oxidase 4 (NOX4) mediates hypercholesterolemia-induced oxidative/nitrative stress and subsequent dysfunction in the heart, J. Mol. Cell. Cardiol., 62, 111–121, doi: Scholar
  46. 46.
    Wang, Y., Zhao, X., Wu, X., Dai, Y., Chen, P., and Xie, L. (2016) MicroRNA-182 mediates Sirt1-induced diabetic corneal nerve regeneration, Diabetes, 65, 2020–2031, doi: Scholar
  47. 47.
    Fierro-Fernandez, M., Busnadiego, O., Sandoval, P., Espinosa-Diez, C., Blanco-Ruiz, E., Rodriguez, M., Pian, H., Ramos, R., Lopez-Cabrera, M., Garcia-Bermejo, M. L., and Lamas, S. (2015) MiR-9-5p suppresses pro-fibrogenic transformation of fibroblasts and prevents organ fibrosis by targeting NOX4 and TGFBR2, EMBO Reports, 16, 1358–1377, doi: Scholar
  48. 48.
    Carlomosti, F., D’Agostino, M., Beji, S., Torcinaro, A., Rizzi, R., Zaccagnini, G., Maimone, B., Di Stefano, V., De Santa, F., Cordisco, S., Antonini, A., Ciarapica, R., Dellambra, E., Martelli, F., Avitabile, D., Capogrossi, M. C., and Magenta, A. (2017) Oxidative stress-induced miR-200c disrupts the regulatory loop among SIRT1, FOXO1, and eNOS, Antioxid. Redox Signal., 27, 328–344, doi: Scholar
  49. 49.
    Kim, J., Lee, K. S., Kim, J. H., Lee, D. K., Park, M., Choi, S., Park, W., Kim, S., Choi, Y. K., Hwang, J. Y., Choe, J., Won, M. H., Jeoung, D., Lee, H., Ryoo, S., Ha, K. S., Kwon, Y. G., and Kim, Y. M. (2017) Aspirin prevents TNF-α-induced endothelial cell dysfunction by regulating the NF-κB-dependent miR-155/eNOS pathway: role of a miR-155/eNOS axis in preeclampsia, Free Radic. Biol. Med., 104, 185–198, doi: Scholar
  50. 50.
    Cho, K. J., Song, J., Oh, Y., and Lee, J. E. (2015) MicroRNA-Let-7a regulates the function of microglia in inflammation, Mol. Cell. Neurosci., 68, 167–176, doi: Scholar
  51. 51.
    Muxel, S. M., Laranjeira-Silva, M. F., Zampieri, R. A., and Floeter-Winter, L. M. (2017) Leishmania (Leishmania) amazonensis induces macrophage miR-294 and miR-721 expression and modulates infection by targeting NOS2 and L-arginine metabolism, Sci. Rep., 7, 44141, doi: Scholar
  52. 52.
    Singh, A., Happel, C., Manna, S. K., Acquaah-Mensah, G., Carrerero, J., Kumar, S., Nasipuri, P., Krausz, K. W., Wakabayashi, N., Dewi, R., Boros, L. G., Gonzalez, F. J., Gabrielson, E., Wong, K. K., Girnun, G., and Biswal, S. (2013) Transcription factor NRF2 regulates miR-1 and miR-206 to drive tumorigenesis, J. Clin. Invest., 123, 2921–2934, doi: Scholar
  53. 53.
    Sripada, L., Tomar, D., and Singh, R. (2012) Mitochondria: one of the destinations of miRNAs, Mitochondrion, 12, 593–599, doi: Scholar
  54. 54.
    Muratsu-Ikeda, S., Nangaku, M., Ikeda, Y., Tanaka, T., Wada, T., and Inagi, R. (2012) Downregulation of miR-205 modulates cell susceptibility to oxidative and endoplasmic reticulum stresses in renal tubular cells, PLoS One, 7, e41462, doi: Scholar
  55. 55.
    Wu, S., Lu, H., and Bai, Y. (2019) Nrf2 in cancers: a double-edged sword, Cancer Med., 8, 2252–2267, doi: Scholar
  56. 56.
    Singh, B., Ronghe, A. M., Chatterjee, A., Bhat, N. K., and Bhat, H. K. (2013) MicroRNA-93 regulates NRF2 expression and is associated with breast carcinogenesis, Carcinogenesis, 34, 1165–1172, doi: Scholar
  57. 57.
    Narasimhan, M., Patel, D., Vedpathak, D., Rathinam, M., Henderson, G., and Mahimainathan, L. (2012) Identification of novel microRNAs in posttranscriptional control of Nrf2 expression and redox homeostasis in neuronal, SH-SY5Y cells, PLoS One, 7, e51111, doi: Scholar
  58. 58.
    Do, M. T., Kim, H. G., Choi, J. H., and Jeong, H. G. (2014) Metformin induces microRNA-34a to downregulate the Sirt1/Pgc-1a/Nrf2 pathway, leading to increased susceptibility of wild-type p53 cancer cells to oxidative stress and therapeutic agents, Free Radic. Biol. Med., 74, 21–34, doi: Scholar
  59. 59.
    Yaribeygi, H., Atkin, S. L., and Sahebkar, A. (2018) Potential roles of microRNAs in redox state: an update, J. Cell. Biochem., doi: [Epub ahead of print].
  60. 60.
    Papp, D., Lenti, K., Modos, D., Fazekas, D., Dul, Z., Turei, D., Foldvari-Nagy, L., Nussinov, R., Csermely, P., and Korcsmaros, T. (2012) The NRF2-related interactome and regulome contain multifunctional proteins and fine-tuned autoregulatory loops, FEBS Lett., 586, 1795–1802, doi: Scholar
  61. 61.
    Sangokoya, C., Telen, M. J., and Chi, J. T. (2010) MicroRNA miR-144 modulates oxidative stress tolerance and associates with anemia severity in sickle cell disease, Blood, 116, 4338–4348, doi: Scholar
  62. 62.
    Franklin, C. C., Backos, D. S., Mohar, I., White, C. C., Forman, H. J., and Kavanagh, T. J. (2009) Structure, function, and post-translational regulation of the catalytic and modifier subunits of glutamate cysteine ligase, Mol. Aspects Med., 30, 86–98, doi: Scholar
  63. 63.
    Zhou, C., Zhao, L., Zheng, J., Wang, K., Deng, H., Liu, P., Chen, L., and Mu, H. (2017) MicroRNA-144 modulates oxidative stress tolerance in SH-SY5Y cells by regulating nuclear factor erythroid 2-related factor 2-glutathione axis, Neurosci. Lett., 655, 21–27, doi: Scholar
  64. 64.
    Stachurska, A., Ciesla, M., Kozakowska, M., Wolffram, S., Boesch-Saadatmandi, C., Rimbach, G., Jozkowicz, A., Dulak, J., and Loboda, A. (2013) Cross-talk between microRNAs, nuclear factor E2-related factor 2, and heme oxygenase-1 in ochratoxin A-induced toxic effects in renal proximal tubular epithelial cells, Mol. Nutr. Food Res., 57, 504–515, doi: Scholar
  65. 65.
    Kabaria, S., Choi, D. C., Chaudhuri, A. D., Jain, M. R., Li, H., and Junn, E. (2015) MicroRNA-7 activates Nrf2 pathway by targeting Keap1 expression, Free Radic. Biol. Med., 89, 548–556, doi: Scholar
  66. 66.
    Eades, G., Yang, M., Yao, Y., Zhang, Y., and Zhou, Q. (2011) MiR-200a regulates Nrf2 activation by targeting Keap1 mRNA in breast cancer cells, J. Biol. Chem., 286, 40725–40733, doi: Scholar
  67. 67.
    Urbanek, P., and Klotz, L. O. (2017) Posttranscriptional regulation of FOXO expression: microRNAs and beyond, Br. J. Pharmacol., 174, 1514–1532, doi: Scholar
  68. 68.
    Gheysarzadeh, A., and Yazdanparast, R. (2015) STAT5 reactivation by catechin modulates H2O2-induced apoptosis through miR-182/FOXO1 pathway in SK-N-MC cells, Cell Biochem. Biophys., 71, 649–656, doi: Scholar
  69. 69.
    Liu, Y., Pan, Q., Zhao, Y., He, C., Bi, K., Chen, Y., Zhao, B., Chen, Y., and Ma, X. (2015) 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, 2870–2881, doi: Scholar
  70. 70.
    Kinoshita, C., Aoyama, K., and Nakaki, T. (2018) Neuroprotection afforded by circadian regulation of intracellular glutathione levels: a key role for miRNAs, Free Radic. Biol. Med., 119, 17–33, doi: Scholar
  71. 71.
    Helfinger, V., and Schroder, K. (2018) Redox control in cancer development and progression, Mol. Aspects Med., 63, 88–98, doi: Scholar
  72. 72.
    Jeong, D., Kim, J., Nam, J., Sun, H., Lee, Y. H., Lee, T. J., Aguiar, R. C., and Kim, S. W. (2015) MicroRNA-124 links p53 to the NF-κB pathway in B-cell lymphomas, Leukemia, 29, 1868–1874, doi: Scholar
  73. 73.
    Sachdeva, M., Zhu, S., Wu, F., Wu, H., Walia, V., Kumar, S., Elble, R., Watabe, K., and Mo, Y Y. (2009) p53 represses c-Myc through induction of the tumor suppressor miR-145, Proc. Natl. Acad. Sci. USA, 106, 3207–3212, doi: Scholar
  74. 74.
    Pichiorri, F., Suh, S. S., Rocci, A., De Luca, L., Taccioli, C., Santhanam, R., Zhou, W., Benson, D. M., Jr., Hofmainster, C., Alder, H., Garofalo, M., Di Leva, G., Volinia, S., Lin, H. J., Perrotti, D., Kuehl, M., Aqeilan, R. I., Palumbo, A., and Croce, C. M. (2010) Downregulation of p53-inducible microRNAs 192, 194, and 215 impairs the p53/MDM2 autoregulatory loop in multiple myeloma development, Cancer Cell, 18, 367–381, doi: Scholar
  75. 75.
    Xiao, Y., Yan, W., Lu, L., Wang, Y., Lu, W., Cao, Y., and Cai, W. (2015) p38/p53/miR-200a-3p feedback loop promotes oxidative stress-mediated liver cell death, Cell Cycle, 14, 1548–1558, doi: Scholar
  76. 76.
    Yin, M., Ren, X., Zhang, X., Luo, Y., Wang, G., Huang, K., Feng, S., Bao, X., Huang, K., He, X., Liang, P., Wang, Z., Tang, H., He, J., and Zhang, B. (2015) Selective killing of lung cancer cells by miRNA-506 molecule through inhibiting NF-κB p65 to evoke reactive oxygen species generation and p53 activation, Oncogene, 34, 691–703, doi: Scholar
  77. 77.
    Chang, T. C., Yu, D., Lee, Y. S., Wentzel, E. A., Arking, D. E., West, K. M., Dang, C. V., Thomas-Tikhonenko, A., and Mendell, J. T. (2008) Widespread microRNA repression by Myc contributes to tumorigenesis, Nat. Genet., 40, 43–50, doi: Scholar
  78. 78.
    Yang, H., Li, T. W., Zhou, Y., Peng, H., Liu, T., Zandi, E., Martinez-Chantar, M. L., Mato, J. M., and Lu, S. C. (2015) Activation of a novel c-Myc-miR27-prohibitin 1 circuitry in cholestatic liver injury inhibits glutathione synthesis in mice, Antioxid. Redox Signal., 22, 259–274, doi: Scholar
  79. 79.
    Lingappan, K. (2018) NF-κB in oxidative stress, Curr. Opin. Toxicol., 7, 81–86, doi: Scholar
  80. 80.
    Toiyama, Y., Takahashi, M., Hur, K., Nagasaka, T., Tanaka, K., Inoue, Y., Kusunoki, M., Boland, C. R., and Goel, A. (2013) Serum miR-21 as a diagnostic and prognostic biomarker in colorectal cancer, J. Natl. Cancer Inst., 105, 849–859, doi: Scholar
  81. 81.
    Hong, J., Wang, Y., Hu, B. C., Xu, L., Liu, J. Q., Chen, M. H., Wang, J. Z., Han, F., Zheng, Y., Chen, X., Li, Q., Yang, X. H., Sun, R. H., and Mo, S. J. (2017) Transcriptional downregulation of microRNA-19a by ROS production and NF-κB deactivation governs resistance to oxidative stress-initiated apoptosis, Oncotarget, 8, 70967–70981, doi: Scholar
  82. 82.
    Jiang, S., Zhang, H. W., Lu, M. H., He, X. H., Li, Y., Gu, H., Liu, M. F., and Wang, E. D. (2010) MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene, Cancer Res., 70, 3119–3127, doi: Scholar
  83. 83.
    Nusse, R., and Clevers, H. (2017) Wnt/β-catenin signaling, disease, and emerging therapeutic modalities, Cell, 169, 985–999, doi: Scholar
  84. 84.
    Wang, P., Zhu, C. F., Ma, M. Z., Chen, G., Song, M., Zeng, Z. L., Lu, W. H., Yang, J., Wen, S., Chiao, P. J., Hu, Y., and Huang, P. (2015) Micro-RNA-155 is induced by K-Ras oncogenic signal and promotes ROS stress in pancreatic cancer, Oncotarget, 6, 21148–21158, doi: Scholar
  85. 85.
    Beccafico, S., Morozzi, G., Marchetti, M. C., Riccardi, C., Sidoni, A., Donato, R., and Sorci, G. (2015) Artesunate induces ROS- and p38 MAPK-mediated apoptosis and counteracts tumor growth in vivo in embryonal rhabdomyosarcoma cells, Carcinogenesis, 36, 1071–1083, doi: Scholar
  86. 86.
    Liu, W., Zabirnyk, O., Wang, H., Shiao, Y. H., Nickerson, M. L., Khalil, S., Anderson, L. M., Perantoni, A. O., and Phang, J. M. (2010) MicroRNA-23b targets proline oxidase, a novel tumor suppressor protein in renal cancer, Oncogene, 29, 4914–4924, doi: Scholar
  87. 87.
    Saxena, A., Shoeb, M., Ramana, K. V., and Srivastava, S. K. (2013) Aldose reductase inhibition suppresses colon cancer cell viability by modulating microRNA-21 mediated programmed cell death 4 (PDCD4) expression, Eur. J. Cancer, 49, 3311–3319, doi: Scholar
  88. 88.
    Mateescu, B., Batista, L., Cardon, M., Gruosso, T., de Feraudy, Y., Mariani, O., Nicolas, A., Meyniel, J. P., Cottu, P., Sastre-Garau, X., and Mechta-Grigoriou, F. (2011) MiR-141 and miR-200a act on ovarian tumorigenesis by controlling oxidative stress response, Nat. Med., 17, 1627–1635, doi: Scholar
  89. 89.
    Sheth, S., Jajoo, S., Kaur, T., Mukherjea, D., Sheehan, K., Rybak, L. P., and Ramkumar, V. (2012) Resveratrol reduces prostate cancer growth and metastasis by inhibiting the Akt/microRNA-21 pathway, PLoS One, 7, e51655, doi: Scholar
  90. 90.
    Meng, X., Wu, J., Pan, C., Wang, H., Ying, X., Zhou, Y., Yu, H., Zuo, Y., Pan, Z., Liu, R. Y., and Huang, W. (2013) Genetic and epigenetic down-regulation of microRNA-212 promotes colorectal tumor metastasis via dysregulation of MnSOD, Gastroenterology, 145, 426–436, doi: Scholar
  91. 91.
    Das, S., Ferlito, M., Kent, O. A., Fox-Talbot, K., Wang, R., Liu, D., Raghavachari, N., Yang, Y., Wheelan, S. J., Murphy, E., and Steenbergen, C. (2012) Nuclear miRNA regulates the mitochondrial genome in the heart, Circ. Res., 110, 1596–1603, doi: Scholar
  92. 92.
    Faraonio, R., Salerno, P., Passaro, F., Sedia, C., Iaccio, A., Bellelli, R., Nappi, T. C., Comegna, M., Romano, S., Salvatore, G., Santoro, M., and Cimino, F. (2012) A set of miRNAs participates in the cellular senescence program in human diploid fibroblasts, Cell Death Differ., 19, 713–721, doi: Scholar
  93. 93.
    Liao, L., Su, X., Yang, X., Hu, C., Li, B., Lv, Y., Shuai, Y., Jing, H., Deng, Z., and Jin, Y. (2016) TNF-α inhibits FoxO1 by upregulating miR-705 to aggravate oxidative damage in bone marrow-derived mesenchymal stem cells during osteoporosis, Stem Cells, 34, 1054–1067, doi: Scholar
  94. 94.
    Cheng, L. B., Li, K. R., Yi, N., Li, X. M., Wang, F., Xue, B., Pan, Y. S., Yao, J., Jiang, Q., and Wu, Z. F. (2017) miRNA-141 attenuates UV-induced oxidative stress via activating Keap1-Nrf2 signaling in human retinal pigment epithelium cells and retinal ganglion cells, Oncotarget, 8, 13186–13194, doi: Scholar
  95. 95.
    Zhang, L., Zhou, M., Wang, Y., Huang, W., Qin, G., Weintraub, N. L., and Tang, Y. (2014) MiR-92a inhibits vascular smooth muscle cell apoptosis: role of the MKK4-JNK pathway, Apoptosis, 19, 975–983, doi: Scholar
  96. 96.
    Li, J., Donath, S., Li, Y., Qin, D., Prabhakar, B. S., and Li, P. (2010) MiR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway, PLoS Genet., 6, e1000795, doi: Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  • E. V. Kalinina
    • 1
    Email author
  • V. I. Ivanova-Radkevich
    • 1
  • N. N. Chernov
    • 1
  1. 1.Peoples’ Friendship University of Russia (RUDN University)MoscowRussia

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