Skip to main content
SpringerLink
Log in

Role of MicroRNAs in the Regulation of Redox-Dependent Processes

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ARE:

antioxidant-responsive element

GSH:

glutathione

HIF:

hypoxia-induced factor

miRNA:

microRNA

NF-κB:

nuclear factor κB

Nrf2:

NF-E2-dependent factor 2

OTA:

ochratoxin A

Pdcd4:

programmed cell death protein 4

Prx:

peroxiredoxin

ROS:

reactive oxygen species

SOD:

superoxide dismutase

Trx:

thioredoxin

TrxR:

thioredoxin reductase

UTR:

untranslated region

References

  1. Singh, A., Kukreti, R., Saso, L., and Kukreti, S. (2019) Oxidative stress: a key modulator in neurodegenerative diseases, Molecules, 24, E1583, doi: https://doi.org/10.3390/molecules24081583.

    Article  PubMed  CAS  Google Scholar 

  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: https://doi.org/10.1016/j.vph.2019.03.004.

    Article  CAS  Google Scholar 

  3. Sies, H., Berndt, C., and Jones, D. P. (2017) Oxidative stress, Annu. Rev. Biochem., 86, 715–748, doi: https://doi.org/10.1146/annurev-biochem-061516-045037.

    Article  CAS  PubMed  Google Scholar 

  4. Ursini, F., Maiorino, M., and Forman, H. J. (2016) Redox homeostasis: the golden mean of healthy living, Redox Biol., 8, 205–215, doi: https://doi.org/10.1016/j.redox.2016.01.010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1016/j.redox.2017.07.015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Jones, D. P. (2006) Redefining oxidative stress, Antioxid. Redox Signal., 8, 865–1879, doi: https://doi.org/10.1089/ars.2006.8.1865.

    Article  Google Scholar 

  7. Hopkins, B. L., and Neumann, C. A. (2019) Redoxins as gatekeepers of the transcriptional oxidative stress response, Redox Biol., 21, 101104, doi: https://doi.org/10.1016/j.redox.2019.101104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1134/S0006297908130099.

    Article  CAS  Google Scholar 

  9. Leisegang, M. S., Schroder, K., and Brandes, R. P. (2018) Redox regulation and noncoding RNAs, Antioxid. Redox Signal., 29, 793–812, doi: https://doi.org/10.1089/ars.2017.7276.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1089/ars.2017.7262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1155/2018/4968321.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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: https://doi.org/10.1016/j.canlet.2018.01.010.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1134/S0006297917110165.

    Article  Google Scholar 

  14. Vishnoi, A., and Rani, S. (2017) MiRNA biogenesis and regulation of diseases: an overview, Methods Mol. Biol., 1509, 1–10, doi: https://doi.org/10.1007/978-1-4939-6524-3_1.

    Article  CAS  PubMed  Google Scholar 

  15. Drusco, A., and Croce, C. M. (2017) MicroRNAs and cancer: a long story for short RNAs, Adv. Cancer Res., 135, 1–24, doi: https://doi.org/10.1016/bs.acr.2017.06.005.

    Article  PubMed  Google Scholar 

  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: https://doi.org/10.1016/j.gpb.2017.09.004.

    Article  Google Scholar 

  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: https://doi.org/10.1038/nature03868.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1186/1471-2407-14-533.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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: https://doi.org/10.1161/01.RES.0000265065.26744.17.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1016/j.molcel.2008.05.001.

    Article  PubMed  CAS  Google Scholar 

  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: https://doi.org/10.1093/nar/gks026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1074/jbc.M112.373365.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Wiesen, J. L., and Tomasi, T. B. (2009) Dicer is regulated by cellular stresses and interferons, Mol. Immunol., 46, 1222–1228, doi: https://doi.org/10.1016/j.molimm.2008.11.012.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1093/gerona/gls242.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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: https://doi.org/10.1016/j.freeradbiomed.2013.07.025.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1371/journal.pone.0020391.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1126/science.1226191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1016/j.freeradbiomed.2012.01.009.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1155/2017/2696071.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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: https://doi.org/10.1016/j.mad.2009.09.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1371/journal.pone.0069351.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1371/journal.pone.0042542.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1155/2014/960362.

    PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1371/journal.pone.0122674.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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: https://doi.org/10.1038/s41598-017-15011-6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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: https://doi.org/10.3390/ijms19041199.

    Article  PubMed  Google Scholar 

  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: https://doi.org/10.1038/mt.2014.79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.3109/10428194.2014.924115.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1681/ASN.2010040367.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1093/cvr/cvv238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1016/j.bbrc.2013.12.136.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1159/000322105.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.3389/fphys.2016.00284.

    PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1016/j.febslet.2015.06.029.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1016/j.yjmcc.2013.05.009.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.2337/db15-1283.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.15252/embr.201540750.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1089/ars.2016.6643.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1016/j.freeradbiomed.2017.01.010.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1016/j.mcn.2015.07.004.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1038/srep44141.

    Article  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1172/JCI66353.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Sripada, L., Tomar, D., and Singh, R. (2012) Mitochondria: one of the destinations of miRNAs, Mitochondrion, 12, 593–599, doi: https://doi.org/10.1016/j.mito.2012.10.009.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1371/journal.pone.0041462.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Wu, S., Lu, H., and Bai, Y. (2019) Nrf2 in cancers: a double-edged sword, Cancer Med., 8, 2252–2267, doi: https://doi.org/10.1002/cam4.2101.

    Article  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1093/carcin/bgt026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1371/journal.pone.0051111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1016/j.freeradbiomed.2014.06.010.

    Article  PubMed  CAS  Google Scholar 

  59. Yaribeygi, H., Atkin, S. L., and Sahebkar, A. (2018) Potential roles of microRNAs in redox state: an update, J. Cell. Biochem., doi: https://doi.org/10.1002/jcb.27475 [Epub ahead of print].

  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: https://doi.org/10.1016/j.febslet.2012.05.016.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1182/blood-2009-04-214817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1016/j.mam.2008.08.009.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1016/j.neulet.2017.06.045.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1002/mnfr.201200456.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1016/j.freeradbiomed.2015.09.010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1074/jbc.M111.275495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Urbanek, P., and Klotz, L. O. (2017) Posttranscriptional regulation of FOXO expression: microRNAs and beyond, Br. J. Pharmacol., 174, 1514–1532, doi: https://doi.org/10.1111/bph.13471.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1007/s12013-014-0244-6.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1002/jcb.25234.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1016/j.freeradbiomed.2017.11.023.

    Article  CAS  PubMed  Google Scholar 

  71. Helfinger, V., and Schroder, K. (2018) Redox control in cancer development and progression, Mol. Aspects Med., 63, 88–98, doi: https://doi.org/10.1016/j.mam.2018.02.003.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1038/leu.2015.101.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1073/pnas.0808042106.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1016/j.ccr.2010.09.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1080/15384101.2015.1026491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1038/onc.2013.597.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1038/ng.2007.30.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1089/ars.2014.6027.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Lingappan, K. (2018) NF-κB in oxidative stress, Curr. Opin. Toxicol., 7, 81–86, doi: https://doi.org/10.1016/j.cotox.2017.11.002.

    Article  PubMed  Google Scholar 

  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: https://doi.org/10.1093/jnci/djt101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.18632/oncotarget.20235.

    PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1158/0008-5472.CAN-09-4250.

    Article  CAS  PubMed  Google Scholar 

  83. Nusse, R., and Clevers, H. (2017) Wnt/β-catenin signaling, disease, and emerging therapeutic modalities, Cell, 169, 985–999, doi: https://doi.org/10.1016/j.cell.2017.05.016.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.18632/oncotarget.4125.

    PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1093/carcin/bgv098.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1038/onc.2010.237.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1016/j.ejca.2013.05.031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1038/nm.2512.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1371/journal.pone.0051655.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1053/j.gastro.2013.04.004.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1161/CIRCRESAHA.112.267732.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1038/cdd.2011.143.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.1002/stem.2274.

    Article  CAS  PubMed  Google Scholar 

  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: https://doi.org/10.18632/oncotarget.14489.

    PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1007/s10495-014-0987-y.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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: https://doi.org/10.1371/journal.pgen.1000795.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Funding

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

Author information

Authors and Affiliations

  1. Peoples’ Friendship University of Russia (RUDN University), 117198, Moscow, Russia

    E. V. Kalinina, V. I. Ivanova-Radkevich & N. N. Chernov

Authors
  1. E. V. Kalinina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. I. Ivanova-Radkevich
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. N. Chernov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. V. Kalinina.

Additional information

Conflict of interest

The authors declare no conflict of interest.

Compliance with ethical norms

This article does not contain description of studies with participation of humans and animals performed by any of the authors.

Russian Text © The Author(s), 2019, published in Biokhimiya, 2019, Vol. 84, No. 11, pp. 1538–1552.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kalinina, E.V., Ivanova-Radkevich, V.I. & Chernov, N.N. Role of MicroRNAs in the Regulation of Redox-Dependent Processes. Biochemistry Moscow 84, 1233–1246 (2019). https://doi.org/10.1134/S0006297919110026

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297919110026

Keywords

Search

Navigation