An effective strategy for increasing the radiosensitivity of Human lung Cancer cells by blocking Nrf2-dependent antioxidant responses

Free Radical Biology and Medicine

Volumn 53, Issue 4, 2012, Pages 807-816

  Lee, Saelooom ^a   Lim, Min Jin ^a   Kim, Mi Hyoung ^a,b   Yu, Chi Ho ^a   Yun, Yeon Sook ^a   Ahn, Jiyeon ^a   Song, Jie Young ^a  

^a Korea Institute of Radiation and Medical Science   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Free radicals; Nrf2; Radiosensitizer; Radiotherapy; Reactive oxygen species

Indexed keywords

4 (2 CYCLOHEXYLETHOXY)ANILINE; ANILINE DERIVATIVE; ANTIOXIDANT; CASPASE 3; KELCH LIKE ECH ASSOCIATED PROTEIN 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; RADIOSENSITIZING AGENT; REACTIVE OXYGEN METABOLITE; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CANCER RADIOTHERAPY; CELL CLONE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN FUNCTION; RADIOSENSITIVITY; TUMOR GROWTH; TUMOR XENOGRAFT;

ANILINE COMPOUNDS; ANIMALS; ANTIOXIDANT RESPONSE ELEMENTS; ANTIOXIDANTS; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, REPORTER; HEME OXYGENASE-1; HUMANS; HYDROQUINONES; INJECTIONS, INTRAPERITONEAL; LUCIFERASES, RENILLA; LUNG NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, NUDE; NF-E2-RELATED FACTOR 2; RADIATION TOLERANCE; RADIATION-SENSITIZING AGENTS; REACTIVE OXYGEN SPECIES; SMALL MOLECULE LIBRARIES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MUS;

EID: 84864405467     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.05.038     Document Type: Article

References (34)

1. E. Papadakis, A. Malliri, S. Linardopoulos, H. Karaiossifidi, J. Field, and D. Spandidos Ras and p53 expression in non-small-cell lung-cancer patients - p53 over-expression correlates with a poor prognosis Int. J. Oncol. 1 1992 403 413
2. A. Nadkar, C. Pungaliya, K. Drake, E. Zajac, S.S. Singhal, and S. Awasthi Therapeutic resistance in lung cancer Expert Opin. Drug Metab. Toxicol 2 2006 753 777
3. D. Trachootham, Y. Zhou, H. Zhang, Y. Demizu, Z. Chen, H. Pelicano, P.J. Chiao, G. Achanta, R.B. Arlinghaus, J. Liu, and P. Huang Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate Cancer Cell 10 2006 241 252
4. Y. Qu, J. Wang, P.S. Ray, H. Guo, J. Huang, M. Shin-Sim, B.A. Bukoye, B. Liu, A.V. Lee, X. Lin, P. Huang, J.W. Martens, A.E. Giuliano, N. Zhang, N.H. Cheng, and X. Cui Thioredoxin-like 2 regulates human cancer cell growth and metastasis via redox homeostasis and NF-kappaB signaling J. Clin. Invest. 121 2011 212 225
5. 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, and M.F. Clarke Association of reactive oxygen species levels and radioresistance in cancer stem cells Nature 458 2009 780 783
6. 2 accumulation in cancer cells by wogonin effectively blocks tumor necrosis factor-induced NF-kappaB activation and sensitizes apoptosis Cancer Sci. 102 2011 870 876
7. Y. Liu, Y. Liang, T. Zheng, G. Yang, X. Zhang, Z. Sun, C. Shi, and S. Zhao Inhibition of heme oxygenase-1 enhances anti-cancer effects of arsenic trioxide on glioma cells J. Neurooncol. 104 2011 449 458
8. S. Homma, Y. Ishii, Y. Morishima, T. Yamadori, Y. Matsuno, N. Haraguchi, N. Kikuchi, H. Satoh, T. Sakamoto, N. Hizawa, K. Itoh, and M. Yamamoto Nrf2 enhances cell proliferation and resistance to anticancer drugs in human lung cancer Clin. Cancer Res. 15 2009 3423 3432
9. J.M. Lee, J. Li, D.A. Johnson, T.D. Stein, A.D. Kraft, M.J. Calkins, R.J. Jakel, and J.A. Johnson Nrf2, a multi-organ protector? FASEB J 19 2005 1061 1066
10. U.A. Meyer Overview of enzymes of drug metabolism J. Pharmacokinet. Biopharm. 24 1996 449 459
11. A. Kobayashi, M.I. Kang, H. Okawa, M. Ohtsuji, Y. Zenke, T. Chiba, K. Igarashi, and M. Yamamoto Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2 Mol. Cell. Biol. 24 2004 7130 7139
12. K. Itoh, T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, M. Yamamoto, and Y. Nabeshima An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 236 1997 313 322
13. A. Singh, V. Misra, R.K. Thimmulappa, H. Lee, S. Ames, M.O. Hoque, J.G. Herman, S.B. Baylin, D. Sidransky, E. Gabrielson, M.V. Brock, and S. Biswal Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer PLoS Med. 3 2006 e420
14. T. Shibata, T. Ohta, K.I. Tong, A. Kokubu, R. Odogawa, K. Tsuta, H. Asamura, M. Yamamoto, and S. Hirohashi Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promote malignancy Proc. Natl. Acad. Sci. USA 105 2008 13568 13573
15. C. Koumenis, C. Naczki, M. Koritzinsky, S. Rastani, A. Diehl, N. Sonenberg, A. Koromilas, and B.G. Wouters Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha Mol. Cell. Biol. 22 2002 7405 7416
16. A. Masamune, T. Watanabe, K. Kikuta, K. Satoh, and T. Shimosegawa NADPH oxidase plays a crucial role in the activation of pancreatic stellate cells Am. J. Physiol. Gastrointest. Liver Physiol. 294 2008 G99 G108
17. C. Li, M.M. Wright, and R.M. Jackson Reactive species mediated injury of human lung epithelial cells after hypoxia-reoxygenation Exp. Lung Res. 28 2002 373 389
18. B. Padmanabhan, K.I. Tong, T. Ohta, Y. Nakamura, M. Scharlock, M. Ohtsuji, M.I. Kang, A. Kobayashi, S. Yokoyama, and M. Yamamoto Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer Mol. Cell 21 2006 689 700
19. T. Ohta, K. Iijima, M. Miyamoto, I. Nakahara, H. Tanaka, M. Ohtsuji, T. Suzuki, A. Kobayashi, J. Yokota, T. Sakiyama, T. Shibata, M. Yamamoto, and S. Hirohashi Loss of Keap1 function activates Nrf2 and provides advantages for lung cancer cell growth Cancer Res. 68 2008 1303 1309
20. A. Singh, M. Bodas, N. Wakabayashi, F. Bunz, and S. Biswal Gain of Nrf2 function in non-small-cell lung cancer cells confers radioresistance Antioxid. Redox Signaling 13 2010 1627 1637
21. Q.K. Li, A. Singh, S. Biswal, and F. Askin Gabrielson, E. KEAP1 gene mutations and NRF2 activation are common in pulmonary papillary adenocarcinoma J. Hum. Genet. 56 2011 230 234
22. T. Shibata, S. Saito, A. Kokubu, T. Suzuki, M. Yamamoto, and S. Hirohashi Global downstream pathway analysis reveals a dependence of oncogenic NF-E2-related factor 2 mutation on the mTOR growth signaling pathway Cancer Res. 70 2010 9095 9105
23. A. Singh, S. Boldin-Adamsky, R.K. Thimmulappa, S.K. Rath, H. Ashush, J. Coulter, A. Blackford, S.N. Goodman, F. Bunz, W.H. Watson, E. Gabrielson, E. Feinstein, and S. Biswal RNAi-mediated silencing of nuclear factor erythroid-2-related factor 2 gene expression in non-small cell lung cancer inhibits tumor growth and increases efficacy of chemotherapy Cancer Res. 68 2008 7975 7984
24. G. Sass, P. Leukel, V. Schmitz, E. Raskopf, M. Ocker, D. Neureiter, M. Meissnitzer, E. Tasika, A. Tannapfel, and G. Tiegs Inhibition of heme oxygenase 1 expression by small interfering RNA decreases orthotopic tumor growth in livers of mice Int. J. Cancer 123 2008 1269 1277
25. H.R. Kim, S. Kim, E.J. Kim, J.H. Park, S.H. Yang, E.T. Jeong, C. Park, M.J. Youn, H.S. So, and R. Park Suppression of Nrf2-driven heme oxygenase-1 enhances the chemosensitivity of lung cancer A549 cells toward cisplatin Lung Cancer 60 2008 47 56
26. H. Kuroda, M. Takeno, S. Murakami, N. Miyazawa, T. Kaneko, and Y. Ishigatsubo Inhibition of heme oxygenase-1 with an epidermal growth factor receptor inhibitor and cisplatin decreases proliferation of lung cancer A549 cells Lung Cancer 67 2010 31 36
27. R. Dey, S. Khan, and B. Saha A novel functional approach toward identifying definitive drug targets Curr. Med. Chem. 14 2007 2380 2392
28. J.T. McDonald, K. Kim, A.J. Norris, E. Vlashi, T.M. Phillips, C. Lagadec, L. Della Donna, J. Ratikan, H. Szelag, L. Hlatky, and W.H. McBride Ionizing radiation activates the Nrf2 antioxidant response Cancer Res. 70 2010 8886 8895
29. S.K. Manna, A. Mukhopadhyay, and B.B. Aggarwal Resveratrol suppresses TNF-induced activation of nuclear transcription factors NF-kappa B, activator protein-1, and apoptosis: potential role of reactive oxygen intermediates and lipid peroxidation J. Immunol 164 2000 6509 6519
30. C.Y. Chen, J.H. Jang, M.H. Li, and Y.J. Surh Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells Biochem. Biophys. Res. Commun. 331 2005 993 1000
31. E. Balogun, M. Hoque, P. Gong, E. Killeen, C.J. Green, R. Foresti, J. Alam, and R. Motterlini Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element Biochem. J. 371 2003 887 895
32. G.H. Liu, J. Qu, and X. Shen NF-kappaB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK Biochim. Biophys. Acta 713-727 1783 2008
33. K. Iida, K. Itoh, J.M. Maher, Y. Kumagai, R. Oyasu, Y. Mori, T. Shimazui, H. Akaza, and M. Yamamoto Nrf2 and p53 cooperatively protect against BBN-induced urinary bladder carcinogenesis Carcinogenesis 28 2007 2398 2403
34. R. Faraonio, P. Vergara, D. Di Marzo, M.G. Pierantoni, M. Napolitano, T. Russo, and F. Cimino p53 suppresses the Nrf2-dependent transcription of antioxidant response genes J. Biol. Chem. 281 2006 39776 39784