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Cellular Oncology

, Volume 42, Issue 2, pp 131–141 | Cite as

MicroRNA-mediated redox regulation modulates therapy resistance in cancer cells: clinical perspectives

  • Safieh Ebrahimi
  • Seyed Isaac HashemyEmail author
Review

Abstract

Background

Chemotherapy and radiation therapy are the most common types of cancer therapy. The development of chemo/radio-resistance remains, however, a major obstacle. Altered redox balances are among of the main factors mediating therapy resistance. Therefore, redox regulatory strategies are urgently needed to overcome this problem. Recently, microRNAs have been found to act as major redox regulatory factors affecting chemo/radio-resistance. MicroRNAs play critical roles in regulating therapeutic resistance through the regulation of antioxidant enzymes, redox-sensitive signaling pathways, cancer stem cells, DNA repair mechanisms and autophagy.

Conclusions

Here, we summarize current knowledge on microRNA-mediated redox regulatory mechanisms underlying chemo/radio-resistance. This knowledge may form a basis for a better clinical management of cancer patients.

Keywords

Cancer Chemotherapy Radiotherapy Resistance MicroRNA Redox regulation 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    D.B. Longley, P.G. Johnston, Molecular mechanisms of drug resistance. J. Pathol. 205, 275–292 (2005)CrossRefPubMedGoogle Scholar
  2. 2.
    F. Perri, R. Pacelli, G. Della Vittoria Scarpati, L. Cella, M. Giuliano, F. Caponigro, S. Pepe, Radioresistance in head and neck squamous cell carcinoma: Biological bases and therapeutic implications. Head Neck 37, 763–770 (2015)CrossRefPubMedGoogle Scholar
  3. 3.
    S.K. Niture, A.K. Jaiswal, Nrf2-induced antiapoptotic Bcl-xL protein enhances cell survival and drug resistance. Free Radic. Biol. Med. 57, 119–131 (2013)CrossRefPubMedGoogle Scholar
  4. 4.
    G. Frosina, DNA repair and resistance of gliomas to chemotherapy and radiotherapy. Mol. Cancer Res. 7, 989–999 (2009)CrossRefPubMedGoogle Scholar
  5. 5.
    M. Dean, T. Fojo, S. Bates, Tumour stem cells and drug resistance. Nat. Rev. Cancer 5, 275–284 (2005)CrossRefPubMedGoogle Scholar
  6. 6.
    S. Chen, S.K. Rehman, W. Zhang, A. Wen, L. Yao, J. Zhang, Autophagy is a therapeutic target in anticancer drug resistance. Biochim. Biophys. Acta (BBA)-Reviews on Cancer 1806, 220–229 (2010)Google Scholar
  7. 7.
    S.L. Lomonaco, S. Finniss, C. Xiang, A. Decarvalho, F. Umansky, S.N. Kalkanis, T. Mikkelsen, C. Brodie, The induction of autophagy by gamma-radiation contributes to the radioresistance of glioma stem cells. Int. J. Cancer 125, 717–722 (2009)CrossRefPubMedGoogle Scholar
  8. 8.
    V.J. Victorino, L. Pizzatti, P. Michelletti, C. Panis, Oxidative stress, redox signaling and cancer chemoresistance: Putting together the pieces of the puzzle. Curr. Med. Chem. 21, 3211–3226 (2014)CrossRefPubMedGoogle Scholar
  9. 9.
    H. Sies, Oxidative stress: Introductory remarks. Oxidative Stress 501, 1–8 (1985)Google Scholar
  10. 10.
    H. Sies, E. Cadenas, Oxidative stress: Damage to intact cells and organs. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 311, 617–631 (1985)CrossRefGoogle Scholar
  11. 11.
    A. Pakfetrat, Z. Dalirsani, S.I. Hashemy, A. Ghazi, L.V. Mostaan, K. Anvari, A.M. Pour, Evaluation of serum levels of oxidized and reduced glutathione and total antioxidant capacity in patients with head and neck squamous cell carcinoma. J. Cancer Res. Ther. 14, 428–431 (2018)PubMedGoogle Scholar
  12. 12.
    S. Lorestani, S.I. Hashemy, M. Mojarad, M. Keyvanloo Shahrestanaki, A. Bahari, M. Asadi, F. Zahedi Avval, Increased glutathione reductase expression and activity in colorectal Cancer tissue samples: An investigational study in Mashhad, Iran. Middle East J. Cancer 9, 99–104 (2018)Google Scholar
  13. 13.
    A. Taheri, M.H. Tanipour, Z.K. Khorasani, B. Kiafar, P. Layegh, S.I. Hashemy, Serum protein carbonyl and total antioxidant capacity levels in pemphigus vulgaris and bullous pemphigoid. Iran J. Dermatol. 18, 156–162 (2016)Google Scholar
  14. 14.
    M. Sobhani, A.R. Taheri, A.H. Jafarian, S.I. Hashemy, The activity and tissue distribution of thioredoxin reductase in basal cell carcinoma. J. Cancer Res. Clin. 142, 2303–2307 (2016)CrossRefGoogle Scholar
  15. 15.
    S.I. Hashemy, S. Gharaei, S. Vasigh, S. Kargozar, B. Alirezaei, F.J. Keyhani, M. Amirchaghmaghi, Oxidative stress factors and C-reactive protein in patients with oral lichen planus before and 2 weeks after treatment. J. Oral Pathol. Med. 45, 35–40 (2016)CrossRefPubMedGoogle Scholar
  16. 16.
    M. Amirchaghmaghi, S.I. Hashemy, B. Alirezaei, F. Jahed Keyhani, S. Kargozar, S. Vasigh, S. Gharaei, A. Pakfetrat, Evaluation of plasma Isoprostane in patients with Oral lichen planus. J. Dent. 17, 21–25 (2016)Google Scholar
  17. 17.
    P. Sharma, S. Kumar, Metformin inhibits human breast cancer cell growth by promoting apoptosis via a ROS-independent pathway involving mitochondrial dysfunction: Pivotal role of superoxide dismutase (SOD). Cell. Oncol. 41, 637–650 (2018)CrossRefGoogle Scholar
  18. 18.
    S. Banskota, S. Dahal, E. Kwon, D.Y. Kim, J.A. Kim, beta-catenin gene promoter hypermethylation by reactive oxygen species correlates with the migratory and invasive potentials of colon cancer cells. Cell. Oncol. 41, 569–580 (2018)CrossRefGoogle Scholar
  19. 19.
    L. Li, M. Story, R.J. Legerski, Cellular responses to ionizing radiation damage. Int. J. Radiat. Oncol. Biol. Phys. 49, 1157–1162 (2001)CrossRefPubMedGoogle Scholar
  20. 20.
    K.A. Conklin, Chemotherapy-associated oxidative stress: Impact on chemotherapeutic effectiveness. Integr. Cancer Ther. 3, 294–300 (2004)CrossRefPubMedGoogle Scholar
  21. 21.
    S.I. Hashemy, J.S. Ungerstedt, F. Zahedi Avval, A. Holmgren, Motexafin gadolinium, a tumor-selective drug targeting thioredoxin reductase and ribonucleotide reductase. J. Biol. Chem. 281, 10691–10697 (2006)CrossRefPubMedGoogle Scholar
  22. 22.
    S. Pervaiz, M.V. Clement, Superoxide anion: Oncogenic reactive oxygen species? Int. J. Biochem. Cell Biol. 39, 1297–1304 (2007)CrossRefPubMedGoogle Scholar
  23. 23.
    V. Sosa, T. Moline, R. Somoza, R. Paciucci, H. Kondoh, L.L. ME, Oxidative stress and cancer: An overview. Ageing Res. Rev. 12, 376–390 (2013)CrossRefPubMedGoogle Scholar
  24. 24.
    S.A. Castaldo, J.R. Freitas, N.V. Conchinha, P.A. Madureira, The tumorigenic roles of the cellular REDOX regulatory systems. Oxidative Med. Cell. Longev. 2016, 8413032 (2016)CrossRefGoogle Scholar
  25. 25.
    J.E. Klaunig, L.M. Kamendulis, The role of oxidative stress in carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 44, 239–267 (2004)CrossRefPubMedGoogle Scholar
  26. 26.
    D. Trachootham, J. Alexandre, P. Huang, Targeting cancer cells by ROS-mediated mechanisms: A radical therapeutic approach? Nat. Rev. Drug Discov. 8, 579–591 (2009)CrossRefPubMedGoogle Scholar
  27. 27.
    S.I. Hashemy, The human Thioredoxin system: Modifications and clinical applications. Iran J. Basic Med. Sci. 14, 191–204 (2011)Google Scholar
  28. 28.
    A.M. Pisoschi, A. Pop, The role of antioxidants in the chemistry of oxidative stress: A review. Eur. J. Med. Chem. 97, 55–74 (2015)CrossRefPubMedGoogle Scholar
  29. 29.
    B. Ramanathan, K.Y. Jan, C.H. Chen, T.C. Hour, H.J. Yu, Y.S. Pu, Resistance to paclitaxel is proportional to cellular total antioxidant capacity. Cancer Res. 65, 8455–8460 (2005)CrossRefPubMedGoogle Scholar
  30. 30.
    M. Diehn, R.W. Cho, N.A. Lobo, T. Kalisky, M.J. Dorie, A.N. Kulp, D. Qian, J.S. Lam, L.E. Ailles, M. Wong, B. Joshua, M.J. Kaplan, I. Wapnir, F.M. Dirbas, G. Somlo, C. Garberoglio, B. Paz, J. Shen, S.K. Lau, S.R. Quake, J.M. Brown, I.L. Weissman, M.F. Clarke, Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458, 780–783 (2009)CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    M.A. Ogasawara, H. Zhang, Redox regulation and its emerging roles in stem cells and stem-like cancer cells. Antioxid. Redox Signal. 11, 1107–1122 (2009)CrossRefPubMedGoogle Scholar
  32. 32.
    J. He, B.H. Jiang, Interplay between reactive oxygen species and MicroRNAs in Cancer. Curr. Pharmacol. Rep. 2, 82–90 (2016)CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    D.P. Bartel, MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116, 281–297 (2004)CrossRefGoogle Scholar
  34. 34.
    F. Corra, C. Agnoletto, L. Minotti, F. Baldassari, S. Volinia, The network of non-coding RNAs in Cancer drug resistance. Front. Oncol. 8, 327 (2018)CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    A.K. Mueller, K. Lindner, R. Hummel, J. Haier, D.I. Watson, D.J. Hussey, MicroRNAs and their impact on radiotherapy for cancer. Radiat. Res. 185, 668–677 (2016)Google Scholar
  36. 36.
    G.S. Markopoulos, E. Roupakia, M. Tokamani, E. Chavdoula, M. Hatziapostolou, C. Polytarchou, K.B. Marcu, A.G. Papavassiliou, R. Sandaltzopoulos, E. Kolettas, A step-by-step microRNA guide to cancer development and metastasis. Cell. Oncol. 40, 303–339 (2017)CrossRefGoogle Scholar
  37. 37.
    N.L. Simone, B.P. Soule, D. Ly, A.D. Saleh, J.E. Savage, W. Degraff, J. Cook, C.C. Harris, D. Gius, J.B. Mitchell, Ionizing radiation-induced oxidative stress alters miRNA expression. PLoS One 4, e6377 (2009)CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    T. Templin, S. Paul, S.A. Amundson, E.F. Young, C.A. Barker, S.L. Wolden, L.B. Smilenov, Radiation-induced micro-RNA expression changes in peripheral blood cells of radiotherapy patients. Int. J. Radiat. Oncol. Biol. Phys. 80, 549–557 (2011)CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    J. Lin, C.C. Chuang, L. Zuo, Potential roles of microRNAs and ROS in colorectal cancer: Diagnostic biomarkers and therapeutic targets. Oncotarget 8, 17328–17346 (2017)PubMedPubMedCentralGoogle Scholar
  40. 40.
    M. Kobayashi, M. Yamamoto, Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox Signal. 7, 385–394 (2005)CrossRefPubMedGoogle Scholar
  41. 41.
    J.D. Hayes, M. McMahon, NRF2 and KEAP1 mutations: Permanent activation of an adaptive response in cancer. Trends Biochem. Sci. 34, 176–188 (2009)CrossRefPubMedGoogle Scholar
  42. 42.
    L. Zhao, M. Tang, Z. Hu, B. Yan, W. Pi, Z. Li, J. Zhang, L. Zhang, W. Jiang, G. Li, Y. Qiu, F. Hu, F. Liu, J. Lu, X. Chen, L. Xiao, Z. Xu, Y. Tao, L. Yang, A.M. Bode, Z. Dong, J. Zhou, J. Fan, L. Sun, Y. Cao, miR-504 mediated down-regulation of nuclear respiratory factor 1 leads to radio-resistance in nasopharyngeal carcinoma. Oncotarget 6, 15995–16018 (2015)PubMedPubMedCentralGoogle Scholar
  43. 43.
    L. Shi, L. Wu, Z. Chen, J. Yang, X. Chen, F. Yu, F. Zheng, X. Lin, MiR-141 activates Nrf2-dependent antioxidant pathway via Down-regulating the expression of Keap1 conferring the resistance of hepatocellular carcinoma cells to 5-fluorouracil. Cell. Physiol. Biochem. 35, 2333–2348 (2015)CrossRefPubMedGoogle Scholar
  44. 44.
    S. Zhou, W. Ye, Y. Zhang, D. Yu, Q. Shao, J. Liang, M. Zhang, miR-144 reverses chemoresistance of hepatocellular carcinoma cell lines by targeting Nrf2-dependent antioxidant pathway. Am. J. Transl. Res. 8, 2992–3002 (2016)Google Scholar
  45. 45.
    L. Shi, Z.G. Chen, L.L. Wu, J.J. Zheng, J.R. Yang, X.F. Chen, Z.Q. Chen, C.L. Liu, S.Y. Chi, J.Y. Zheng, H.X. Huang, X.Y. Lin, F. Zheng, miR-340 reverses cisplatin resistance of hepatocellular carcinoma cell lines by targeting Nrf2-dependent antioxidant pathway. Asian Pac. J. Cancer Prev. 15, 10439–10444 (2014)CrossRefPubMedGoogle Scholar
  46. 46.
    S.E. Gomes, D.M. Pereira, C. Roma-Rodrigues, A.R. Fernandes, P.M. Borralho, C.M.P. Rodrigues, Convergence of miR-143 overexpression, oxidative stress and cell death in HCT116 human colon cancer cells. PLoS One 13, e0191607 (2018)CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Y. Cui, K. She, D. Tian, P. Zhang, X. Xin, miR-146a inhibits proliferation and enhances Chemosensitivity in epithelial ovarian Cancer via reduction of SOD2. Oncol. Res. 23, 275–282 (2016)CrossRefPubMedGoogle Scholar
  48. 48.
    M.A. Cortez, D. Valdecanas, X. Zhang, Y. Zhan, V. Bhardwaj, G.A. Calin, R. Komaki, D.K. Giri, C.C. Quini, T. Wolfe, H.J. Peltier, A.G. Bader, J.V. Heymach, R.E. Meyn, J.W. Welsh, Therapeutic delivery of miR-200c enhances radiosensitivity in lung cancer. Mol. Ther. 22, 1494–1503 (2014)CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    C. Gao, F.H. Peng, L.K. Peng, MiR-200c sensitizes clear-cell renal cell carcinoma cells to sorafenib and imatinib by targeting heme oxygenase-1. Neoplasma 61, 680–689 (2014)CrossRefPubMedGoogle Scholar
  50. 50.
    H.C. Chen, Y.M. Jeng, R.H. Yuan, H.C. Hsu, Y.L. Chen, SIRT1 promotes tumorigenesis and resistance to chemotherapy in hepatocellular carcinoma and its expression predicts poor prognosis. Ann. Surg. Oncol. 19, 2011–2019 (2012)CrossRefPubMedGoogle Scholar
  51. 51.
    A. Salminen, K. Kaarniranta, A. Kauppinen, Crosstalk between oxidative stress and SIRT1: Impact on the aging process. Int. J. Mol. Sci. 14, 3834–3859 (2013)CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    M. Chang, L. Qiao, B. Li, J. Wang, G. Zhang, W. Shi, Z. Liu, N. Gu, Z. Di, X. Wang, Y. Tian, Suppression of SIRT6 by miR-33a facilitates tumor growth of glioma through apoptosis and oxidative stress resistance. Oncol. Rep. 38, 1251–1258 (2017)CrossRefPubMedGoogle Scholar
  53. 53.
    H. Liu, X.H. Cheng, MiR-29b reverses oxaliplatin-resistance in colorectal cancer by targeting SIRT1. Oncotarget 9, 12304–12315 (2018)PubMedPubMedCentralGoogle Scholar
  54. 54.
    B. Lian, D. Yang, Y. Liu, G. Shi, J. Li, X. Yan, K. Jin, X. Liu, J. Zhao, W. Shang, R. Zhang, miR-128 targets the SIRT1/ROS/DR5 pathway to sensitize colorectal Cancer to TRAIL-induced apoptosis. Cell. Physiol. Biochem. 49, 2151–2162 (2018)CrossRefPubMedGoogle Scholar
  55. 55.
    X. Xu, A. Wells, M.T. Padilla, K. Kato, K.C. Kim, Y. Lin, A signaling pathway consisting of miR-551b, catalase and MUC1 contributes to acquired apoptosis resistance and chemoresistance. Carcinogenesis 35, 2457–2466 (2014)CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Z. Dong, L. Ren, L. Lin, J. Li, Y. Huang, J. Li, Effect of microRNA-21 on multidrug resistance reversal in A549/DDP human lung cancer cells. Mol. Med. Rep. 11, 682–690 (2015)CrossRefPubMedGoogle Scholar
  57. 57.
    C. Lin, L. Xie, Y. Lu, Z. Hu, J. Chang, miR-133b reverses cisplatin resistance by targeting GSTP1 in cisplatin-resistant lung cancer cells. Int. J. Mol. Med. 41, 2050–2058 (2018)PubMedPubMedCentralGoogle Scholar
  58. 58.
    S. Chen, J.W. Jiao, K.X. Sun, Z.H. Zong, Y. Zhao, MicroRNA-133b targets glutathione S-transferase pi expression to increase ovarian cancer cell sensitivity to chemotherapy drugs. Drug Des. Devel. Ther. 9, 5225–5235 (2015)PubMedPubMedCentralGoogle Scholar
  59. 59.
    D. Wang, N. Zhang, Y. Ye, J. Qian, Y. Zhu, C. Wang, Role and mechanisms of microRNA-503 in drug resistance reversal in HepG2/ADM human hepatocellular carcinoma cells. Mol. Med. Rep. 10, 3268–3274 (2014)CrossRefPubMedGoogle Scholar
  60. 60.
    G.K. Patel, M.A. Khan, A. Bhardwaj, S.K. Srivastava, H. Zubair, M.C. Patton, S. Singh, M. Khushman, A.P. Singh, Exosomes confer chemoresistance to pancreatic cancer cells by promoting ROS detoxification and miR-155-mediated suppression of key gemcitabine-metabolising enzyme, DCK. Br. J. Cancer 116, 609–619 (2017)CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    L.E. Ailles, I.L. Weissman, Cancer stem cells in solid tumors. Curr. Opin. Biotechnol. 18, 460–466 (2007)CrossRefPubMedGoogle Scholar
  62. 62.
    H.Q. Ju, Y.X. Lu, D.L. Chen, T. Tian, H.Y. Mo, X.L. Wei, J.W. Liao, F. Wang, Z.L. Zeng, H. Pelicano, M. Aguilar, W.H. Jia, R.H. Xu, Redox regulation of stem-like cells though the CD44v-xCT Axis in colorectal Cancer: Mechanisms and therapeutic implications. Theranostics 6, 1160–1175 (2016)CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    B. Mateescu, L. Batista, M. Cardon, T. Gruosso, Y. de Feraudy, O. Mariani, A. Nicolas, J.P. Meyniel, P. Cottu, X. Sastre-Garau, F. Mechta-Grigoriou, miR-141 and miR-200a act on ovarian tumorigenesis by controlling oxidative stress response. Nat. Med. 17, 1627–1635 (2011)CrossRefPubMedGoogle Scholar
  64. 64.
    W. Yang, Y. Shen, J. Wei, F. Liu, MicroRNA-153/Nrf-2/GPx1 pathway regulates radiosensitivity and stemness of glioma stem cells via reactive oxygen species. Oncotarget 6, 22006–22027 (2015)PubMedPubMedCentralGoogle Scholar
  65. 65.
    S. Venkataraman, I. Alimova, R. Fan, P. Harris, N. Foreman, R. Vibhakar, MicroRNA 128a increases intracellular ROS level by targeting Bmi-1 and inhibits medulloblastoma cancer cell growth by promoting senescence. PLoS One 5, e10748 (2010)CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    X. Sun, Y. Li, M. Zheng, W. Zuo, W. Zheng, MicroRNA-223 increases the sensitivity of triple-negative breast Cancer stem cells to TRAIL-induced apoptosis by targeting HAX-1. PLoS One 11, e0162754 (2016)CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    J. Liu, Q. Tang, S. Li, X. Yang, Inhibition of HAX-1 by miR-125a reverses cisplatin resistance in laryngeal cancer stem cells. Oncotarget 7, 86446–86456 (2016)PubMedPubMedCentralGoogle Scholar
  68. 68.
    K.K. Khanna, S.P. Jackson, DNA double-strand breaks: Signaling, repair and the cancer connection. Nat. Genet. 27, 247–254 (2001)CrossRefPubMedGoogle Scholar
  69. 69.
    S.P. Jackson, J. Bartek, The DNA-damage response in human biology and disease. Nature 461, 1071–1078 (2009)CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    M. Kuhne, E. Riballo, N. Rief, K. Rothkamm, P.A. Jeggo, M. Lobrich, A double-strand break repair defect in ATM-deficient cells contributes to radiosensitivity. Cancer Res. 64, 500–508 (2004)CrossRefPubMedGoogle Scholar
  71. 71.
    M. Pajic, D. Froio, S. Daly, L. Doculara, E. Millar, P.H. Graham, A. Drury, A. Steinmann, C.E. de Bock, A. Boulghourjian, A. Zaratzian, S. Carroll, J. Toohey, S.A. O'Toole, A.L. Harris, F.M. Buffa, H.E. Gee, G.E. Hollway, T.J. Molloy, miR-139-5p modulates radiotherapy resistance in breast Cancer by repressing multiple gene networks of DNA repair and ROS defense. Cancer Res. 78, 501–515 (2018)CrossRefPubMedGoogle Scholar
  72. 72.
    H. Hu, X. Zhao, Z. Jin, M. Hou, Hsa-let-7g miRNA regulates the anti-tumor effects of gastric cancer cells under oxidative stress through the expression of DDR genes. J. Toxicol. Sci. 40, 329–338 (2015)CrossRefPubMedGoogle Scholar
  73. 73.
    D. Yan, W.L. Ng, X. Zhang, P. Wang, Z. Zhang, Y.Y. Mo, H. Mao, C. Hao, J.J. Olson, W.J. Curran, Y. Wang, Targeting DNA-PKcs and ATM with miR-101 sensitizes tumors to radiation. PLoS One 5, e11397 (2010)CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    H. Hu, L. Du, G. Nagabayashi, R.C. Seeger, R.A. Gatti, ATM is down-regulated by N-Myc-regulated microRNA-421. Proc. Natl. Acad. Sci. U. S. A. 107, 1506–1511 (2010)CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    J. Wang, J. He, F. Su, N. Ding, W. Hu, B. Yao, W. Wang, G. Zhou, Repression of ATR pathway by miR-185 enhances radiation-induced apoptosis and proliferation inhibition. Cell Death Dis. 4, e699 (2013)CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    L. Song, C. Lin, Z. Wu, H. Gong, Y. Zeng, J. Wu, M. Li, J. Li, miR-18a impairs DNA damage response through downregulation of ataxia telangiectasia mutated (ATM) kinase. PLoS One 6, e25454 (2011)CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    A. Cataldo, D.G. Cheung, A. Balsari, E. Tagliabue, V. Coppola, M.V. Iorio, D. Palmieri, C.M. Croce, miR-302b enhances breast cancer cell sensitivity to cisplatin by regulating E2F1 and the cellular DNA damage response. Oncotarget 7, 786–797 (2016)CrossRefPubMedGoogle Scholar
  78. 78.
    S. Xu, H. Huang, Y.N. Chen, Y.T. Deng, B. Zhang, X.D. Xiong, Y. Yuan, Y. Zhu, H. Huang, L. Xie, X. Liu, DNA damage responsive miR-33b-3p promoted lung cancer cells survival and cisplatin resistance by targeting p21(WAF1/CIP1). Cell Cycle 15, 2920–2930 (2016)CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    P. Carotenuto, D. Zito, M.C. Previdi, M. Raj, M. Fassan, A. Lampis, F. Scalafani, A. Lanese, I. Said-Huntingford and J.C. Hahne, (AACR, 2018)Google Scholar
  80. 80.
    A. Besse, J. Sana, R. Lakomy, L. Kren, P. Fadrus, M. Smrcka, M. Hermanova, R. Jancalek, S. Reguli, R. Lipina, M. Svoboda, P. Slampa, O. Slaby, MiR-338-5p sensitizes glioblastoma cells to radiation through regulation of genes involved in DNA damage response. Tumour. Biol. 37, 7719–7727 (2016)CrossRefPubMedGoogle Scholar
  81. 81.
    R.L. Liu, Y. Dong, Y.Z. Deng, W.J. Wang, W.D. Li, Tumor suppressor miR-145 reverses drug resistance by directly targeting DNA damage-related gene RAD18 in colorectal cancer. Tumour. Biol. 36, 5011–5019 (2015)CrossRefPubMedGoogle Scholar
  82. 82.
    Y.N. Shen, I.S. Bae, G.H. Park, H.S. Choi, K.H. Lee, S.H. Kim, MicroRNA-196b enhances the radiosensitivity of SNU-638 gastric cancer cells by targeting RAD23B. Biomed. Pharmacother. 105, 362–369 (2018)CrossRefPubMedGoogle Scholar
  83. 83.
    M. Xiao, J. Cai, L. Cai, J. Jia, L. Xie, Y. Zhu, B. Huang, D. Jin, Z. Wang, Let-7e sensitizes epithelial ovarian cancer to cisplatin through repressing DNA double strand break repair. J. Ovarian Res. 10, 24 (2017)CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    T.H. Lai, B. Ewald, A. Zecevic, C. Liu, M. Sulda, D. Papaioannou, R. Garzon, J.S. Blachly, W. Plunkett, D. Sampath, HDAC inhibition induces MicroRNA-182, which targets RAD51 and impairs HR repair to sensitize cells to Sapacitabine in acute myelogenous leukemia. Clin. Cancer Res. 22, 3537–3549 (2016)CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Y. Wang, J.W. Huang, P. Calses, C.J. Kemp, T. Taniguchi, MiR-96 downregulates REV1 and RAD51 to promote cellular sensitivity to cisplatin and PARP inhibition. Cancer Res. 72, 4037–4046 (2012)CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    J.W. Huang, Y. Wang, K.K. Dhillon, P. Calses, E. Villegas, P.S. Mitchell, M. Tewari, C.J. Kemp, T. Taniguchi, Systematic screen identifies miRNAs that target RAD51 and RAD51D to enhance chemosensitivity. Mol. Cancer Res. 11, 1564–1573 (2013)CrossRefPubMedGoogle Scholar
  87. 87.
    P. Gasparini, F. Lovat, M. Fassan, L. Casadei, L. Cascione, N.K. Jacob, S. Carasi, D. Palmieri, S. Costinean, C.L. Shapiro, K. Huebner, C.M. Croce, Protective role of miR-155 in breast cancer through RAD51 targeting impairs homologous recombination after irradiation. Proc. Natl. Acad. Sci. U. S. A. 111, 4536–4541 (2014)CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    G. Antoniali, F. Serra, L. Lirussi, M. Tanaka, C. D'Ambrosio, S. Zhang, S. Radovic, E. Dalla, Y. Ciani, A. Scaloni, M. Li, S. Piazza, G. Tell, Mammalian APE1 controls miRNA processing and its interactome is linked to cancer RNA metabolism. Nat. Commun. 8, 797 (2017)CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    D. Ramotar, A. Nepveu, Apurinic/apyrimidinic endonuclease 1 performs multiple roles in controlling the outcome of cancer cells toward radiation and chemotherapeutic agents. J. Rad. Cancer Res. 9, 67 (2018)CrossRefGoogle Scholar
  90. 90.
    J.R. Silber, M.S. Bobola, A. Blank, K.D. Schoeler, P.D. Haroldson, M.B. Huynh, D.D. Kolstoe, The apurinic/apyrimidinic endonuclease activity of Ape1/Ref-1 contributes to human glioma cell resistance to alkylating agents and is elevated by oxidative stress. Clin. Cancer Res. 8, 3008–3018 (2002)PubMedGoogle Scholar
  91. 91.
    H. Chen, X. Li, W. Li, H. Zheng, miR-130a can predict response to temozolomide in patients with glioblastoma multiforme, independently of O6-methylguanine-DNA methyltransferase. J. Transl. Med. 13, 69 (2015)CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    L. Tinaburri, M. D'Errico, S. Sileno, R. Maurelli, P. Degan, A. Magenta, E. Dellambra, miR-200a modulates the expression of the DNA repair protein OGG1 playing a role in aging of primary human keratinocytes. Oxidative Med. Cell. Longev. 2018, 9147326 (2018)CrossRefGoogle Scholar
  93. 93.
    T. Izumi, L.R. Wiederhold, G. Roy, R. Roy, A. Jaiswal, K.K. Bhakat, S. Mitra, T.K. Hazra, Mammalian DNA base excision repair proteins: Their interactions and role in repair of oxidative DNA damage. Toxicology 193, 43–65 (2003)CrossRefPubMedGoogle Scholar
  94. 94.
    H.L. Huang, Y.P. Shi, H.J. He, Y.H. Wang, T. Chen, L.W. Yang, T. Yang, J. Chen, J. Cao, W.M. Yao, G. Liu, MiR-4673 modulates paclitaxel-induced oxidative stress and loss of mitochondrial membrane potential by targeting 8-Oxoguanine-DNA Glycosylase-1. Cell. Physiol. Biochem. 42, 889–900 (2017)CrossRefPubMedGoogle Scholar
  95. 95.
    Y.T. Gao, X.B. Chen, H.L. Liu, Up-regulation of miR-370-3p restores glioblastoma multiforme sensitivity to temozolomide by influencing MGMT expression. Sci. Rep. 6, 32972 (2016)CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    S. Josson, S.Y. Sung, K. Lao, L.W. Chung, P.A. Johnstone, Radiation modulation of microRNA in prostate cancer cell lines. Prostate 68, 1599–1606 (2008)CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    N.M. Mazure, J. Pouyssegur, Hypoxia-induced autophagy: Cell death or cell survival? Curr. Opin. Cell. Biol. 22, 177–180 (2010)CrossRefPubMedGoogle Scholar
  98. 98.
    J. Lee, S. Giordano, J. Zhang, Autophagy, mitochondria and oxidative stress: Cross-talk and redox signalling. Biochem. J. 441, 523–540 (2012)CrossRefPubMedGoogle Scholar
  99. 99.
    Y. Kondo, T. Kanzawa, R. Sawaya, S. Kondo, The role of autophagy in cancer development and response to therapy. Nat. Rev. Cancer 5, 726–734 (2005)CrossRefPubMedGoogle Scholar
  100. 100.
    A.C. Gurkan, E.D. Arisan, P.O. Yerlikaya, H. Ilhan, N.P. Unsal, Inhibition of autophagy enhances DENSpm-induced apoptosis in human colon cancer cells in a p53 independent manner. Cell. Oncol. 41, 297–317 (2018)CrossRefGoogle Scholar
  101. 101.
    W. Khaodee, N. Inboot, S. Udomsom, W. Kumsaiyai, R. Cressey, Glucosidase II beta subunit (GluIIbeta) plays a role in autophagy and apoptosis regulation in lung carcinoma cells in a p53-dependent manner. Cell. Oncol. 40, 579–591 (2017)Google Scholar
  102. 102.
    X. Sui, R. Chen, Z. Wang, Z. Huang, N. Kong, M. Zhang, W. Han, F. Lou, J. Yang, Q. Zhang, X. Wang, C. He, H. Pan, Autophagy and chemotherapy resistance: A promising therapeutic target for cancer treatment. Cell Death Dis. 4, e838 (2013)CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    A. Chatterjee, D. Chattopadhyay, G. Chakrabarti, miR-17-5p downregulation contributes to paclitaxel resistance of lung cancer cells through altering beclin1 expression. PLoS One 9, e95716 (2014)CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    X. Wu, X. Feng, X. Zhao, F. Ma, N. Liu, H. Guo, C. Li, H. Du, B. Zhang, Role of Beclin-1-mediated autophagy in the survival of pediatric leukemia cells. Cell. Physiol. Biochem. 39, 1827–1836 (2016)CrossRefPubMedGoogle Scholar
  105. 105.
    X. Yang, F. Bai, Y. Xu, Y. Chen, L. Chen, Intensified Beclin-1 mediated by low expression of Mir-30a-5p promotes Chemoresistance in human small cell lung Cancer. Cell. Physiol. Biochem. 43, 1126–1139 (2017)CrossRefPubMedGoogle Scholar
  106. 106.
    J. Xu, H. Huang, R. Peng, X. Ding, B. Jiang, X. Yuan, J. Xi, MicroRNA-30a increases the chemosensitivity of U251 glioblastoma cells to temozolomide by directly targeting beclin 1 and inhibiting autophagy. Exp. Ther. Med. 15, 4798–4804 (2018)PubMedPubMedCentralGoogle Scholar
  107. 107.
    Y. Zhang, X. Meng, C. Li, Z. Tan, X. Guo, Z. Zhang, T. Xi, MiR-9 enhances the sensitivity of A549 cells to cisplatin by inhibiting autophagy. Biotechnol. Lett. 39, 959–966 (2017)CrossRefPubMedGoogle Scholar
  108. 108.
    W. Li, Y. Yang, Z. Ba, S. Li, H. Chen, X. Hou, L. Ma, P. He, L. Jiang, L. Li, R. He, L. Zhang, D. Feng, MicroRNA-93 regulates hypoxia-induced autophagy by targeting ULK1. Oxidative Med. Cell. Longev. 2017, 2709053 (2017)Google Scholar
  109. 109.
    S.I. Rothschild, O. Gautschi, J. Batliner, M. Gugger, M.F. Fey, M.P. Tschan, MicroRNA-106a targets autophagy and enhances sensitivity of lung cancer cells to Src inhibitors. Lung Cancer 107, 73–83 (2017)CrossRefPubMedGoogle Scholar
  110. 110.
    L. Hua, G. Zhu and J. Wei, MicroRNA-1 overexpression increases chemosensitivity of non-small cell lung cancer cells by inhibiting autophagy related 3-mediated autophagy. Cell. Biol. Int. (2018).  https://doi.org/10.1002/cbin.10995
  111. 111.
    Y. Xu, Y. An, Y. Wang, C. Zhang, H. Zhang, C. Huang, H. Jiang, X. Wang, X. Li, miR-101 inhibits autophagy and enhances cisplatin-induced apoptosis in hepatocellular carcinoma cells. Oncol. Rep. 29, 2019–2024 (2013)CrossRefPubMedGoogle Scholar
  112. 112.
    J. Zhao, Y. Nie, H. Wang, Y. Lin, MiR-181a suppresses autophagy and sensitizes gastric cancer cells to cisplatin. Gene 576, 828–833 (2016)CrossRefPubMedGoogle Scholar
  113. 113.
    A.M. Gao, X.Y. Zhang, J.N. Hu, Z.P. Ke, Apigenin sensitizes hepatocellular carcinoma cells to doxorubic through regulating miR-520b/ATG7 axis. Chem. Biol. Interact. 280, 45–50 (2018)CrossRefPubMedGoogle Scholar
  114. 114.
    H. Zhang, J. Tang, C. Li, J. Kong, J. Wang, Y. Wu, E. Xu, M. Lai, MiR-22 regulates 5-FU sensitivity by inhibiting autophagy and promoting apoptosis in colorectal cancer cells. Cancer Lett. 356, 781–790 (2015)CrossRefPubMedGoogle Scholar
  115. 115.
    J. Xiong, D. Wang, A. Wei, N. Ke, Y. Wang, J. Tang, S. He, W. Hu, X. Liu, MicroRNA-410-3p attenuates gemcitabine resistance in pancreatic ductal adenocarcinoma by inhibiting HMGB1-mediated autophagy. Oncotarget 8, 107500–107512 (2017)PubMedPubMedCentralGoogle Scholar
  116. 116.
    W.W. Ren, D.D. Li, X. Chen, X.L. Li, Y.P. He, L.H. Guo, L.N. Liu, L.P. Sun, X.P. Zhang, MicroRNA-125b reverses oxaliplatin resistance in hepatocellular carcinoma by negatively regulating EVA1A mediated autophagy. Cell Death Dis. 9, 547 (2018)CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    L. Huang, C. Hu, H. Cao, X. Wu, R. Wang, H. Lu, H. Li, H. Chen, MicroRNA-29c increases the Chemosensitivity of pancreatic Cancer cells by inhibiting USP22 mediated autophagy. Cell. Physiol. Biochem. 47, 747–758 (2018)CrossRefPubMedGoogle Scholar
  118. 118.
    P.H. Chen, A.J. Liu, K.H. Ho, Y.T. Chiu, Z.H. Anne Lin, Y.T. Lee, C.M. Shih, K.C. Chen, microRNA-199a/b-5p enhance imatinib efficacy via repressing WNT2 signaling-mediated protective autophagy in imatinib-resistant chronic myeloid leukemia cells. Chem. Biol. Interact. 291, 144–151 (2018)CrossRefPubMedGoogle Scholar
  119. 119.
    H. Gu, M. Liu, C. Ding, X. Wang, R. Wang, X. Wu, R. Fan, Hypoxia-responsive miR-124 and miR-144 reduce hypoxia-induced autophagy and enhance radiosensitivity of prostate cancer cells via suppressing PIM1. Cancer Med. 5, 1174–1182 (2016)CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    P. Wang, J. Zhang, L. Zhang, Z. Zhu, J. Fan, L. Chen, L. Zhuang, J. Luo, H. Chen, L. Liu, Z. Chen, Z. Meng, MicroRNA 23b regulates autophagy associated with radioresistance of pancreatic cancer cells. Gastroenterology 145, 1133–1143 e1112 (2013)CrossRefPubMedGoogle Scholar
  121. 121.
    X. Zhang, H. Shi, S. Lin, M. Ba, S. Cui, MicroRNA-216a enhances the radiosensitivity of pancreatic cancer cells by inhibiting beclin-1-mediated autophagy. Oncol. Rep. 34, 1557–1564 (2015)CrossRefPubMedGoogle Scholar
  122. 122.
    H. Liao, Y. Xiao, Y. Hu, Y. Xiao, Z. Yin, L. Liu, microRNA-32 induces radioresistance by targeting DAB2IP and regulating autophagy in prostate cancer cells. Oncol. Lett. 10, 2055–2062 (2015)CrossRefPubMedPubMedCentralGoogle Scholar
  123. 123.
    J. Luo, J. Chen, L. He, mir-129-5p attenuates irradiation-induced autophagy and decreases radioresistance of breast cancer cells by targeting HMGB1. Med. Sci. Monit. 21, 4122–4129 (2015)CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Q. Sun, T. Liu, Y. Yuan, Z. Guo, G. Xie, S. Du, X. Lin, Z. Xu, M. Liu, W. Wang, Q. Yuan, L. Chen, MiR-200c inhibits autophagy and enhances radiosensitivity in breast cancer cells by targeting UBQLN1. Int. J. Cancer 136, 1003–1012 (2015)CrossRefPubMedGoogle Scholar
  125. 125.
    C. Meng, Y. Liu, Y. Shen, S. Liu, Z. Wang, Q. Ye, H. Liu, X. Liu, L. Jia, MicroRNA-26b suppresses autophagy in breast cancer cells by targeting DRAM1 mRNA, and is downregulated by irradiation. Oncol. Lett. 15, 1435–1440 (2018)PubMedGoogle Scholar
  126. 126.
    W. Wang, J. Liu, Q. Wu, MiR-205 suppresses autophagy and enhances radiosensitivity of prostate cancer cells by targeting TP53INP1. Eur. Rev. Med. Pharmacol. Sci. 20, 92–100 (2016)PubMedGoogle Scholar
  127. 127.
    J. Liu, Y. Xing, L. Rong, miR-181 regulates cisplatin-resistant non-small cell lung cancer via downregulation of autophagy through the PTEN/PI3K/AKT pathway. Oncol. Rep. 39, 1631–1639 (2018)PubMedPubMedCentralGoogle Scholar
  128. 128.
    X. Du, B. Liu, X. Luan, Q. Cui, L. Li, miR-30 decreases multidrug resistance in human gastric cancer cells by modulating cell autophagy. Exp. Ther. Med. 15, 599–605 (2018)PubMedGoogle Scholar
  129. 129.
    B. Zheng, H. Zhu, D. Gu, X. Pan, L. Qian, B. Xue, D. Yang, J. Zhou, Y. Shan, MiRNA-30a-mediated autophagy inhibition sensitizes renal cell carcinoma cells to sorafenib. Biochem. Biophys. Res. Commun. 459, 234–239 (2015)CrossRefPubMedGoogle Scholar
  130. 130.
    S. Comincini, G. Allavena, S. Palumbo, M. Morini, F. Durando, F. Angeletti, L. Pirtoli, C. Miracco, microRNA-17 regulates the expression of ATG7 and modulates the autophagy process, improving the sensitivity to temozolomide and low-dose ionizing radiation treatments in human glioblastoma cells. Cancer Biol. Ther. 14, 574–586 (2013)CrossRefPubMedPubMedCentralGoogle Scholar
  131. 131.
    W. Hou, L. Song, Y. Zhao, Q. Liu, S. Zhang, Inhibition of Beclin-1-mediated autophagy by MicroRNA-17-5p enhanced the Radiosensitivity of glioma cells. Oncol. Res. 25, 43–53 (2017)CrossRefPubMedGoogle Scholar
  132. 132.
    H.S. Gwak, T.H. Kim, G.H. Jo, Y.J. Kim, H.J. Kwak, J.H. Kim, J. Yin, H. Yoo, S.H. Lee, J.B. Park, Silencing of microRNA-21 confers radio-sensitivity through inhibition of the PI3K/AKT pathway and enhancing autophagy in malignant glioma cell lines. PLoS One 7, e47449 (2012)CrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    J.L. Hu, G.Y. He, X.L. Lan, Z.C. Zeng, J. Guan, Y. Ding, X.L. Qian, W.T. Liao, Y.Q. Ding, L. Liang, Inhibition of ATG12-mediated autophagy by miR-214 enhances radiosensitivity in colorectal cancer. Oncogene 7, 16 (2018)CrossRefGoogle Scholar
  134. 134.
    Z. Liu, S. Huang, Inhibition of miR-191 contributes to radiation-resistance of two lung cancer cell lines by altering autophagy activity. Cancer Cell. Int. 15, 16 (2015)CrossRefPubMedPubMedCentralGoogle Scholar
  135. 135.
    H. Yi, B. Liang, J. Jia, N. Liang, H. Xu, G. Ju, S. Ma, X. Liu, Differential roles of miR-199a-5p in radiation-induced autophagy in breast cancer cells. FEBS Lett. 587, 436–443 (2013)CrossRefPubMedGoogle Scholar
  136. 136.
    M.T. van Jaarsveld, J. Helleman, A.W. Boersma, P.F. van Kuijk, W.F. van Ijcken, E. Despierre, I. Vergote, R.H. Mathijssen, E.M. Berns, J. Verweij, J. Pothof, E.A. Wiemer, miR-141 regulates KEAP1 and modulates cisplatin sensitivity in ovarian cancer cells. Oncogene 32, 4284–4293 (2013)CrossRefPubMedGoogle Scholar
  137. 137.
    N. Duru, R. Gernapudi, Y. Zhang, Y. Yao, P.K. Lo, B. Wolfson, Q. Zhou, NRF2/miR-140 signaling confers radioprotection to human lung fibroblasts. Cancer Lett. 369, 184–191 (2015)CrossRefPubMedPubMedCentralGoogle Scholar
  138. 138.
    M.S. Joo, C.G. Lee, J.H. Koo, S.G. Kim, miR-125b transcriptionally increased by Nrf2 inhibits AhR repressor, which protects kidney from cisplatin-induced injury. Cell Death Dis. e899, 4 (2013)Google Scholar

Copyright information

© International Society for Cellular Oncology 2019

Authors and Affiliations

  1. 1.Department of Clinical Biochemistry, Faculty of MedicineMashhad University of Medical SciencesMashhadIran
  2. 2.Student Research CommitteeMashhad University of Medical SciencesMashhadIran
  3. 3.Surgical Oncology Research CenterMashhad University of Medical SciencesMashhadIran

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