Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Cellular Oncology
Published in: Cellular Oncology 2/2019

01-04-2019 | Radiotherapy | Review

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

Authors: Safieh Ebrahimi, Seyed Isaac Hashemy

Published in: Cellular Oncology | Issue 2/2019

Login to get access

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.
Literature
1.
D.B. Longley, P.G. Johnston, Molecular mechanisms of drug resistance. J. Pathol. 205, 275–292 (2005)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMed
4.
G. Frosina, DNA repair and resistance of gliomas to chemotherapy and radiotherapy. Mol. Cancer Res. 7, 989–999 (2009)CrossRefPubMed
5.
M. Dean, T. Fojo, S. Bates, Tumour stem cells and drug resistance. Nat. Rev. Cancer 5, 275–284 (2005)CrossRefPubMed
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)
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)CrossRefPubMed
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)CrossRefPubMed
9.
H. Sies, Oxidative stress: Introductory remarks. Oxidative Stress 501, 1–8 (1985)
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)CrossRef
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)PubMed
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)
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)
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)CrossRef
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)CrossRefPubMed
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)
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)CrossRef
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)CrossRef
19.
L. Li, M. Story, R.J. Legerski, Cellular responses to ionizing radiation damage. Int. J. Radiat. Oncol. Biol. Phys. 49, 1157–1162 (2001)CrossRefPubMed
20.
K.A. Conklin, Chemotherapy-associated oxidative stress: Impact on chemotherapeutic effectiveness. Integr. Cancer Ther. 3, 294–300 (2004)CrossRefPubMed
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)CrossRefPubMed
22.
S. Pervaiz, M.V. Clement, Superoxide anion: Oncogenic reactive oxygen species? Int. J. Biochem. Cell Biol. 39, 1297–1304 (2007)CrossRefPubMed
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)CrossRefPubMed
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)CrossRef
25.
J.E. Klaunig, L.M. Kamendulis, The role of oxidative stress in carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 44, 239–267 (2004)CrossRefPubMed
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)CrossRefPubMed
27.
S.I. Hashemy, The human Thioredoxin system: Modifications and clinical applications. Iran J. Basic Med. Sci. 14, 191–204 (2011)
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)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMed
32.
33.
34.
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)
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)CrossRef
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)PubMedPubMedCentral
40.
M. Kobayashi, M. Yamamoto, Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox Signal. 7, 385–394 (2005)CrossRefPubMed
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)CrossRefPubMed
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)PubMedPubMedCentral
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)CrossRefPubMed
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)
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMed
53.
H. Liu, X.H. Cheng, MiR-29b reverses oxaliplatin-resistance in colorectal cancer by targeting SIRT1. Oncotarget 9, 12304–12315 (2018)PubMedPubMedCentral
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMed
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)PubMedPubMedCentral
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)PubMedPubMedCentral
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
61.
L.E. Ailles, I.L. Weissman, Cancer stem cells in solid tumors. Curr. Opin. Biotechnol. 18, 460–466 (2007)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMed
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)PubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)PubMedPubMedCentral
68.
K.K. Khanna, S.P. Jackson, DNA double-strand breaks: Signaling, repair and the cancer connection. Nat. Genet. 27, 247–254 (2001)CrossRefPubMed
69.
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)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)
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)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRef
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)PubMed
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)CrossRefPubMedPubMedCentral
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)CrossRef
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)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
97.
N.M. Mazure, J. Pouyssegur, Hypoxia-induced autophagy: Cell death or cell survival? Curr. Opin. Cell. Biol. 22, 177–180 (2010)CrossRefPubMed
98.
J. Lee, S. Giordano, J. Zhang, Autophagy, mitochondria and oxidative stress: Cross-talk and redox signalling. Biochem. J. 441, 523–540 (2012)CrossRefPubMed
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)CrossRefPubMed
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)CrossRef
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)
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMed
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)CrossRefPubMed
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)PubMedPubMedCentral
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)CrossRefPubMed
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)
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)CrossRefPubMed
110.
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)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMed
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)PubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMed
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)PubMed
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)PubMed
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)PubMedPubMedCentral
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)PubMed
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMedPubMedCentral
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)CrossRef
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)CrossRefPubMedPubMedCentral
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)CrossRefPubMed
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)CrossRefPubMed
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)CrossRefPubMedPubMedCentral
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)
Metadata
Title
MicroRNA-mediated redox regulation modulates therapy resistance in cancer cells: clinical perspectives
Authors
Safieh Ebrahimi
Seyed Isaac Hashemy
Publication date
01-04-2019
Publisher
Springer Netherlands
Published in
Cellular Oncology / Issue 2/2019
Print ISSN: 2211-3428
Electronic ISSN: 2211-3436
DOI
https://doi.org/10.1007/s13402-018-00421-z

Other articles of this Issue 2/2019

Cellular Oncology 2/2019 Go to the issue

Review

Therapeutic targeting potential of chromatin-associated proteins in MLL-rearranged acute leukemia

Original Article

Interfering with bromodomain epigenome readers as therapeutic option in mucoepidermoid carcinoma

Original Paper

Secretome profiling of heterotypic spheroids suggests a role of fibroblasts in HIF-1 pathway modulation and colorectal cancer photodynamic resistance

Original Paper

SNHG6 is upregulated in primary breast cancers and promotes cell cycle progression in breast cancer-derived cell lines

Original Paper

Nanoquinacrine sensitizes 5-FU-resistant cervical cancer stem-like cells by down-regulating Nectin-4 via ADAM-17 mediated NOTCH deregulation

Commentary

Nuclear localization of PD-L1: artifact or reality?
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine
Image Credits