Gain of Nrf2 function in non-small-cell lung cancer cells confers radioresistance

Antioxidants and Redox Signaling

Volumn 13, Issue 11, 2010, Pages 1627-1637

  Singh, Anju ^a   Bodas, Manish ^a   Wakabayashi, Nobunao ^a   Bunz, Fred ^b   Biswal, Shyam ^a,b,c  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ALPHA TOCOPHEROL; CARBONYL DERIVATIVE; GLUTATHIONE; REACTIVE OXYGEN METABOLITE; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CELL DEATH; CELL SURVIVAL; CLONOGENIC ASSAY; CONTROLLED STUDY; FIBROBLAST; GAMMA IRRADIATION; IONIZING RADIATION; LETHALITY; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; RADIATION INJURY; RADIOSENSITIVITY; RNA INTERFERENCE;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DOWN-REGULATION; FIBROBLASTS; HUMANS; MICE; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; OXIDATIVE STRESS; RADIATION TOLERANCE; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 77958129306     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2010.3219     Document Type: Article

References (45)

1. Baek SH, Min JN, Park EM, Han MY, Lee YS, Lee YJ, and Park YM. Role of small heat shock protein HSP25 in radio-resistance and glutathione-redox cycle. J Cell Physiol 183: 100-107, 2000.
2. Bravard A, Ageron-Blanc A, Alvarez S, Drane P, Le Rhun Y, Paris F, Luccioni C, and May E. Correlation between anti-oxidant status, tumorigenicity and radiosensitivity in sister rat cell lines. Carcinogenesis 23: 705-711, 2002.
3. Brognard J, Clark AS, Ni Y, and Dennis PA. Akt/protein kinase B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to che-motherapy and radiation. Cancer Res 61: 3986-3997, 2001.
4. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M, Joshua B, Kaplan MJ, Wapnir I, Dirbas FM, Somlo G, Garberoglio C, Paz B, Shen J, Lau SK, Quake SR, Brown JM, Weissman IL, and Clarke MF. Association of reactive oxygen species levels and radio-resistance in cancer stem cells. Nature 458: 780-783, 2009.
5. Gromer S, Urig S, and Becker K. The thioredoxin system\ From science to clinic. Med Res Rev 24: 40-89, 2004.
6. Hayashi A, Suzuki H, Itoh K, Yamamoto M, and Sugiyama Y. Transcription factor Nrf2 is required for the constitutive and inducible expression of multidrug resistance-associated protein 1 in mouse embryo fibroblasts. Biochem Biophys Res Commun 310: 824-829, 2003.
7. Hensley K and Floyd RA. Reactive oxygen species and protein oxidation in aging: A look back, a look ahead. Arch Biochem Biophys 397: 377-383, 2002.
8. Kensler TW, Wakabayashi N, and Biswal S. Cell sur-vival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47: 89-116, 2007.
9. Kim YJ, Ahn JY, Liang P, Ip C, Zhang Y, and Park YM. Human prx1 gene is a target of Nrf2 and is up-regulated by hypoxia/reoxygenation: Implication to tumor biology. Can-cer Res 67: 546-554, 2007.
10. Kirsch M and De Groot H. NAD(P)H, a directly operating antioxidant? FASEB J 15: 1569-1574, 2001.
11. Kobayashi A, Kang MI, Okawa H, Ohtsuji M, Zenke Y, Chiba T, Igarashi K, and Yamamoto M. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol 24: 7130-7139, 2004.
12. Kotlo KU, Yehiely F, Efimova E, Harasty H, Hesabi B, Shchors K, Einat P, Rozen A, Berent E, and Deiss LP. Nrf2 is an inhibitor of the Fas pathway as identified by Achilles' Heel Method, a new function-based approach to gene identification in human cells. Oncogene 22: 797-806, 2003.
13. Kumar KS, Vaishnav YN, and Weiss JF. Radioprotection by antioxidant enzymes and enzyme mimetics. Pharmacol Ther 39: 301-309, 1988.
14. Lee HC, Kim DW, Jung KY, Park IC, Park MJ, Kim MS, Woo SH, Rhee CH, Yoo H, Lee SH, and Hong SI. Increased ex-pression of antioxidant enzymes in radioresistant variant from U251 human glioblastoma cell line. Int J Mol Med 13: 883-887, 2004.
15. Lee JM and Bernstein A. p53 mutations increase resistance to ionizing radiation. Proc Natl Acad Sci USA 90: 5742-5746, 1993.
16. Lee TD, Yang H, Whang J, and Lu SC. Cloning and char-acterization of the human glutathione synthetase 5'-flanking region. Biochem J 390: 521-528, 2005.
17. Mirkovic N, Voehringer DW, Story MD, McConkey DJ, McDonnell TJ, and Meyn RE. Resistance to radiation-induced apoptosis in Bcl-2-expressing cells is reversed by depleting cellular thiols. Oncogene 15: 1461-1470, 1997.
18. Morito N, Yoh K, Itoh K, Hirayama A, Koyama A, Yama-moto M, and Takahashi S. Nrf2 regulates the sensitivity of death receptor signals by affecting intracellular glutathione levels. Oncogene 22: 9275-9281, 2003.
19. Nguyen T, Sherratt PJ, and Pickett CB. Regulatory mecha-nisms controlling gene expression mediated by the anti-oxidant response element. Annu Rev Pharmacol Toxicol 43: 233-260, 2003.
20. Nioi P and Nguyen T. A mutation of Keap1 found in breast cancer impairs its ability to repress Nrf2 activity. Biochem Biophys Res Commun 362: 816-821, 2007.
21. Padmanabhan B, Tong KI, Ohta T, Nakamura Y, Scharlock M, Ohtsuji M, Kang MI, Kobayashi A, Yokoyama S, and Yamamoto M. Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Mol Cell 21: 689-700, 2006.
22. Pleshakova OV, Kutsyi MP, Sukharev SA, Sadovnikov VB, and Gaziev AI. Study of protein carbonyls in subcellular fractions isolated from liver and spleen of old and gamma-irradiated rats. Mech Ageing Dev 103: 45-55, 1998.
23. Rangasamy T, Cho CY, Thimmulappa RK, Zhen L, Srisuma SS, Kensler TW, Yamamoto M, Petrache I, Tuder RM, and Biswal S. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest 114: 1248-1259, 2004.
24. Rangasamy T, Guo J, Mitzner WA, Roman J, Singh A, Fryer AD, Yamamoto M, Kensler TW, Tuder RM, Georas SN, and Biswal S. Disruption of Nrf2 enhances susceptibility to se-vere airway inflammation and asthma in mice. J Exp Med 202: 47-59, 2005.
25. Reddy NM, Kleeberger SR, Cho HY, Yamamoto M, Kensler TW, Biswal S, and Reddy SP. Deficiency in Nrf2-GSH sig-naling impairs type II cell growth and enhances sensitivity to oxidants. Am J Respir Cell Mol Biol 37: 3-8, 2007.
26. Shibata T, Kokubu A, Gotoh M, Ojima H, Ohta T, Yama-moto M, and Hirohashi S. Genetic alteration of Keap1 con-fers constitutive Nrf2 activation and resistance to chemotherapy in gallbladder cancer. Gastroenterology 135: 1358-1368, 2008.
27. Shibata T, Ohta T, Tong KI, Kokubu A, Odogawa R, Tsuta K, Asamura H, Yamamoto M, and Hirohashi S. Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promote malignancy. Proc Natl Acad Sci USA 105: 13568-13573, 2008.
28. Shin S, Wakabayashi N, Misra V, Biswal S, Lee GH, Agoston ES, Yamamoto M, and Kensler TW. NRF2 modulates aryl hydrocarbon receptor signaling: Iinfluence on adipogenesis. Mol Cell Biol 27: 7188-7197, 2007.
29. Singh A, Boldin-Adamsky S, Thimmulappa RK, Rath SK, Ashush H, Coulter J, Blackford A, Goodman SN, Bunz F, Watson WH, Gabrielson E, Feinstein E, and Biswal S. RNAi-mediated silencing of nuclear factor erythroid-2-related fac-tor 2 gene expression in non-small cell lung cancer inhibits tumor growth and increases efficacy of chemotherapy. Cancer Res 68: 7975-7984, 2008.
30. Singh A, Misra V, Thimmulappa RK, Lee H, Ames S, Hoque MO, Herman JG, Baylin SB, Sidransky D, Gabrielson E, Brock MV, and Biswal S. Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med 3: e420, 2006.
31. Singh A, Rangasamy T, Thimmulappa RK, Lee H, Osburn WO, Brigelius-Flohe R, Kensler TW, Yamamoto M, and Biswal S. Glutathione peroxidase 2, the major cigarette smoke-inducible isoform of GPX in lungs, is regulated by Nrf2. Am J Respir Cell Mol Biol 35: 639-650, 2006.
32. Sjoblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, Mandelker D, Leary RJ, Ptak J, Silliman N, Szabo S, Buc-khaults P, Farrell C, Meeh P, Markowitz SD, Willis J, Daw-son D, Willson JK, Gazdar AF, Hartigan J, Wu L, Liu C, Parmigiani G, Park BH, Bachman KE, Papadopoulos N, Vogelstein B, Kinzler KW, and Velculescu VE. The consen-sus coding sequences of human breast and colorectal can-cers. Science 314: 268-274, 2006.
33. Stadtman ER. Protein oxidation in aging and age-related diseases. Ann NY Acad Sci 928: 22-38, 2001.
34. Sun SY, Yue P, Wu GS, El-Deiry WS, Shroot B, Hong WK, and Lotan R. Implication of p53 in growth arrest and apo-ptosis induced by the synthetic retinoid CD437 in human lung cancer cells. Cancer Res 59: 2829-2833, 1999. (Pubitemid 29283118)
35. Tanito M, Agbaga MP, and Anderson RE. Upregulation of thioredoxin system via Nrf2-antioxidant responsive element pathway in adaptive-retinal neuroprotection in vivo and in vitro. Free Radic Biol Med 42: 1838-1850, 2007.
36. Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yama-moto M, and Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res 62: 5196-5203, 2002.
37. Thimmulappa RK, Scollick C, Traore K, Yates M, Trush MA, Liby KT, Sporn MB, Yamamoto M, Kensler TW, and Biswal S. Nrf2-dependent protection from LPS induced inflamma-tory response and mortality by CDDO-Imidazolide. Biochem Biophys Res Commun 351: 883-889, 2006.
38. Trachootham D, Zhou Y, Zhang H, Demizu Y, Chen Z, Pe-licano H, Chiao PJ, Achanta G, Arlinghaus RB, Liu J, and Huang P. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell 10: 241-252, 2006.
39. Tuttle S, Stamato T, Perez ML, and Biaglow J. Glucose-6-phosphate dehydrogenase and the oxidative pentose phos-phate cycle protect cells against apoptosis induced by low doses of ionizing radiation. Radiat Res 153: 781-787, 2000.
40. Vollrath V, Wielandt AM, Iruretagoyena M, and Chianale J. Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene. Biochem J 395: 599-609, 2006.
41. Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, Takahashi S, Imakado S, Kotsuji T, Otsuka F, Roop DR, Harada T, Engel JD, and Yamamoto M. Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activa-tion. Nat Genet 35: 238-245, 2003.
42. Weiss JF and Landauer MR. Protection against ionizing radiation by antioxidant nutrients and phytochemicals. Toxicology 189: 1-20, 2003.
43. Weiss JF and Landauer MR. Radioprotection by antioxi-dants. Ann NY Acad Sci 899: 44-60, 2000.
44. Yang CT, Li JM, Weng HH, Li YC, Chen HC, and Chen MF. Adenovirus-mediated transfer of siRNA against survivin enhances the radiosensitivity of human non-small cell lung cancer cells. Cancer Gene Ther 17: 120-130, 2010.
45. Zhang DD, Lo SC, Cross JV, Templeton DJ, and Hannink M. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol Cell Biol 24: 10941-10953, 2004