The overexpression and nuclear translocation of Trx-1 during hypoxia confers on HepG2 cells resistance to DDP, and GL-V9 reverses the resistance by suppressing the Trx-1/Ref-1 axis

Free Radical Biology and Medicine

Volumn 82, Issue , 2015, Pages 29-41

  Zhao, Li ^a   Li, Wei ^a   Zhou, Yuxin ^a   Zhang, Yi ^a   Huang, Shaoliang ^a   Xu, Xuefen ^a   Li, Zhiyu ^b   Guo, Qinglong ^a  

^a BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^b CHINA PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

Free radicals; GL V9; Hypoxia DR; Reverse; ROS; Trx 1 Ref 1 axis

Indexed keywords

ANTINEOPLASTIC AGENT; CISPLATIN; DNA BINDING PROTEIN; FLAVONOID; GL V9; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LIPOCORTIN 5; REDOX EFFECTOR FACTOR 1; SMALL INTERFERING RNA; THIOREDOXIN 1; UNCLASSIFIED DRUG; 5-HYDROXY-8-METHOXY-2-PHENYL-7-(4-(PYRROLIDIN-1-YL)BUTOXY)4H-CHROMEN-4-ONE; APEX1 PROTEIN, HUMAN; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; GLUCOSE; HIF1A PROTEIN, HUMAN; LACTIC ACID; PDHX PROTEIN, HUMAN; PYRUVATE DEHYDROGENASE COMPLEX; REACTIVE OXYGEN METABOLITE; THIOREDOXIN; TXN PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREATHING; CELL STRUCTURE; CONTROLLED STUDY; DNA BINDING; DRUG TOXICITY; G2 PHASE CELL CYCLE CHECKPOINT; GEL MOBILITY SHIFT ASSAY; GENE INTERACTION; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOLYSIS; HUMAN; HUMAN CELL; HYPOXIA; IC50; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; TRANSIENT TRANSFECTION; TUMOR VOLUME; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL HYPOXIA; DRUG RESISTANCE; GENETICS; HEPG2 CELL LINE; METABOLISM; NUDE MOUSE; PHYSIOLOGY; RNA INTERFERENCE; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL HYPOXIA; CELL LINE, TUMOR; CISPLATIN; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; DNA-BINDING PROTEINS; DRUG RESISTANCE, NEOPLASM; FLAVONOIDS; GLUCOSE; GLYCOLYSIS; HEP G2 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LACTIC ACID; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PYRUVATE DEHYDROGENASE COMPLEX; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, SMALL INTERFERING; THIOREDOXINS;

EID: 84924245829     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.01.014     Document Type: Article

References (64)

1. D. Pan, W. Li, H. Miao, J. Yao, Z. Li, L. Wei, L. Zhao, and Q. Guo LW-214, a newly synthesized flavonoid, induces intrinsic apoptosis pathway by down-regulating Trx-1 in MCF-7 human breast cells Biochem. Pharmacol. 87 2014 598 610
2. C. Li, M.A. Thompson, A.T. Tamayo, Z. Zuo, J. Lee, F. Vega, R.J. Ford, and L.V. Pham Over-expression of thioredoxin-1 mediates growth, survival, and chemoresistance and is a druggable target in diffuse large B-cell lymphoma Oncotarget 3 2012 314 326
3. J. Zhou, C. Eleni, G. Spyrou, and B. Brune The mitochondrial thioredoxin system regulates nitric oxide-induced HIF-1α protein Free Radic. Biol. Med. 44 2008 91 98
4. A. Vlamis-Gardikas, and A. Holmgren Thioredoxin and glutaredoxin isoforms Methods Enzymol. 347 2002 286 296
5. Y. Kabe, K. Ando, S. Hirao, M. Yoshida, and H. Handa Redox regulation of NF-kappaB activation: distinct redox regulation between the cytoplasm and the nucleus Antioxid. Redox Signaling 7 2005 395 403
6. R.B. Penney, and D. Roy Thioredoxin-mediated redox regulation of resistance to endocrine therapy in breast cancer Biochim. Biophys. Acta 1836 2013 60 79
7. M. Wangpaichitr, E.J. Sullivan, G. Theodoropoulos, C. Wu, M. You, L.G. Feun, T.J. Lampidis, M.T. Kuo, and N. Savaraj The relationship of thioredoxin-1 and cisplatin resistance: its impact on ROS and oxidative metabolism in lung cancer cells Mol. Cancer Ther 11 2012 604 615
8. D. Dixit, V. Sharma, S. Ghosh, N. Koul, P.K. Mishra, and E. Sen Manumycin inhibits STAT3, telomerase activity, and growth of glioma cells by elevating intracellular reactive oxygen species generation Free Radic. Biol. Med. 47 2009 364 374
9. S.J. Welsh, R.R. Williams, A. Birmingham, D.J. Newman, D.L. Kirkpatrick, and G. Powis The thioredoxin redox inhibitors 1-methylpropyl 2-imidazolyl disulfide and pleurotin inhibit hypoxia-induced factor 1alpha and vascular endothelial growth factor formation Mol. Cancer Ther 2 2003 235 243
10. R.S. Adluri, M. Thirunavukkarasu, L. Zhan, Y. Akita, S.M. Samuel, H. Otani, Y.S. Ho, G. Maulik, and N. Maulik Thioredoxin 1 enhances neovascularization and reduces ventricular remodeling during chronic myocardial infarction: a study using thioredoxin 1 transgenic mice J. Mol. Cell. Cardiol. 50 2011 239 247
11. J. Qin, G.M. Clore, W.P. Kennedy, J. Kuszewski, and A.M. Gronenborn The solution structure of human thioredoxin complexed with its target from Ref-1 reveals peptide chain reversal Structure 4 1996 613 620
12. D.L. Kirkpatrick, M. Kuperus, M. Dowdeswell, N. Potier, L.J. Donald, M. Kunkel, M. Berggren, M. Angulo, and G. Powis Mechanisms of inhibition of the thioredoxin growth factor system by antitumor 2-imidazolyl disulfides Biochem. Pharmacol. 55 1998 987 994
13. A. Mukherjee, and S.G. Martin The thioredoxin system: a key target in tumour and endothelial cells Br. J. Radiol. 81(Special Issue 1 2008 S57 S68
14. G. Fritz, S. Grosch, M. Tomicic, and B. Kaina APE/Ref-1 and the mammalian response to genotoxic stress Toxicology 193 2003 67 78
15. H.J.K. Hawkes, T.C. Karlenius, and K.F. Tonissen Regulation of the human thioredoxin gene promoter and its key substrates: a study of functional and putative regulatory elements Biochim. Biophys. Acta 1840 2014 303 314
16. D.M. Flaherty, M.M. Monick, and G.W. Hunninghake AP endonucleases and the many functions of Ref-1 Am. J. Respir. Cell Mol. Biol. 25 2001 664 667
17. S.J. Wei, A. Botero, K. Hirota, C.M. Bradbury, S. Markovina, A. Laszlo, D.R. Spitz, P.C. Goswami, J. Yodoi, and D. Gius Thioredoxin nuclear translocation and interaction with redox factor-1 activates the activator protein-1 transcription factor in response to ionizing radiation Cancer Res. 60 2000 6688 6695
18. H. Wang, L. Zhao, L.T. Zhu, Y. Wang, D. Pan, J. Yao, Q.D. You, and Q.L. Guo Wogonin reverses hypoxia resistance of human colon cancer HCT116 cells via downregulation of HIF-1alpha and glycolysis, by inhibiting PI3K/Akt signaling pathway Mol. Carcinog. 53 Suppl. 1 2014 E107 E118
19. N. Rohwer, and T. Cramer Hypoxia-mediated drug resistance: novel insights on the functional interaction of HIFs and cell death pathways Drug Resist. Updates 14 2011 191 201
20. A.L. Harris Hypoxia - a key regulatory factor in tumour growth Nat. Rev. Cancer 2 2002 38 47
21. E.D. Michelakis, V. Hampl, A. Nsair, X. Wu, G. Harry, A. Haromy, R. Gurtu, and S.L. Archer Diversity in mitochondrial function explains differences in vascular oxygen sensing Circ. Res. 90 2002 1307 1315
22. N. Rohwer, C. Dame, A. Haugstetter, B. Wiedenmann, K. Detjen, C.A. Schmitt, and T. Cramer Hypoxia-inducible factor 1alpha determines gastric cancer chemosensitivity via modulation of p53 and NF-kappaB PLoS One 5 2010 e12038
23. K.A. Cottrill, S.Y. Chan, and J. Loscalzo Hypoxamirs and mitochondrial metabolism Antioxid. Redox Signaling 21 2014 1189 1202
24. R.B. Robey, and N. Hay Is Akt the Warburg kinase? - Akt-energy metabolism interactions and oncogenesis Semin. Cancer Biol. 19 2009 25 31
25. O.A. Aiyegoro, and A.I. Okoh Phytochemical screening and polyphenolic antioxidant activity of aqueous crude leaf extract of Helichrysum pedunculatum Int. J. Mol. Sci 10 2009 4990 5001
26. J. Cao, X. Xia, X. Chen, J. Xiao, and Q. Wang Characterization of flavonoids from Dryopteris erythrosora and evaluation of their antioxidant, anticancer and acetylcholinesterase inhibition activities Food Chem. Toxicol. 51 2013 242 250
27. E. Middleton Jr, C. Kandaswami, and T.C. Theoharides The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer Pharmacol. Rev. 52 2000 673 751
28. L.W. Li, N. Lu, Q.S. Dai, L.B. Wei, Q. Zhao, Z.Y. Li, Q.H. He, Y. Dai, and Q.L. Guo GL-V9, a newly synthetic flavonoid derivative, induces mitochondrial-mediated apoptosis and G2/M cell cycle arrest in human hepatocellular carcinoma HepG2 cells Eur. J. Pharmacol. 670 2011 13 21
29. L. Li, P. Chen, Y. Ling, X. Song, Z. Lu, Q. He, Z. Li, N. Lu, and Q. Guo Inhibitory effects of GL-V9 on the invasion of human breast carcinoma cells by downregulating the expression and activity of matrix metalloproteinase-2/9 Eur. J. Pharm. Sci. 43 2011 393 399
30. Y. Zhong, F. Zhang, Z. Sun, W. Zhou, Z.Y. Li, Q.D. You, Q.L. Guo, and R. Hu Drug resistance associates with activation of Nrf2 in MCF-7/DOX cells, and wogonin reverses it by down-regulating Nrf2-mediated cellular defense response Mol. Carcinog. 52 2013 824 834
31. X. Li, B. Sun, C.J. Zhu, H.Q. Yuan, Y.Q. Shi, J. Gao, S.J. Li, and H.X. Lou Reversal of p-glycoprotein-mediated multidrug resistance by macrocyclic bisbibenzyl derivatives in adriamycin-resistant human myelogenous leukemia (K562/A02) cells Toxicol. In Vitro 23 2009 29 36
32. J.M. Lluis, F. Buricchi, P. Chiarugi, A. Morales, and J.C. Fernandez-Checa Dual role of mitochondrial reactive oxygen species in hypoxia signaling: activation of nuclear factor-κB via c-SRC and oxidant-dependent cell death Cancer Res. 67 2007 7368 7377
33. L. Qiang, Y. Yang, Q.D. You, Y.J. Ma, L. Yang, F.F. Nie, H.Y. Gu, L. Zhao, N. Lu, Q. Qi, W. Liu, X.T. Wang, and Q.L. Guo Inhibition of glioblastoma growth and angiogenesis by gambogic acid: an in vitro and in vivo study Biochem. Pharmacol. 75 2008 1083 1092
34. Y.H. Zhang, Y. Wang, A.H. Yusufali, F. Ashby, D. Zhang, Z.F. Yin, G.V. Aslanidi, A. Srivastava, C.Q. Ling, and C. Ling Cytotoxic genes from traditional Chinese medicine inhibit tumor growth both in vitro and in vivo J. Integr. Med 12 2014 483 494
35. H. Gu, X. Wang, S. Rao, J. Wang, J. Zhao, F.L. Ren, R. Mu, Y. Yang, Q. Qi, W. Liu, N. Lu, H. Ling, Q. You, and Q. Guo Gambogic acid mediates apoptosis as a p53 inducer through down-regulation of mdm2 in wild-type p53-expressing cancer cells Mol. Cancer Ther 7 2008 3298 3305
36. J. Yao, R. Hu, J. Sun, B. Lin, L. Zhao, Y. Sha, B. Zhu, Q.D. You, T. Yan, and Q.L. Guo Oroxylin A prevents inflammation-related tumor through down-regulation of inflammatory gene expression by inhibiting NF-kappaB signaling Mol. Carcinog. 53 2014 145 158
37. W. Xia, P. Wang, C. Lin, Z. Li, X. Gao, G. Wang, and X. Zhao Bioreducible polyethylenimine-delivered siRNA targeting human telomerase reverse transcriptase inhibits HepG2 cell growth in vitro and in vivo J. Controlled Release 157 2012 427 436
38. L.X. Shi, R. Ma, R. Lu, Q. Xu, Z.F. Zhu, L. Wang, C.L. Zhou, X.L. Li, H.L. Zhang, and Z. Yao Reversal effect of tyroservatide (YSV) tripeptide on multi-drug resistance in resistant human hepatocellular carcinoma cell line BEL-7402/5-FU Cancer Lett. 269 2008 101 110
39. J.A. Menendez, T. Alarcon, and J. Joven Gerometabolites: the pseudohypoxic aging side of cancer oncometabolites Cell Cycle 13 2014 699 709
40. R.H. Xu, H. Pelicano, Y. Zhou, J.S. Carew, L. Feng, K.N. Bhalla, M.J. Keating, and P. Huang Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia Cancer Res. 65 2005 613 621
41. H. Lu, R.A. Forbes, and A. Verma Hypoxia-inducible factor 1 activation by aerobic glycolysis implicates the Warburg effect in carcinogenesis J. Biol. Chem. 277 2002 23111 23115
42. L. Milane, Z. Duan, and M. Amiji Role of hypoxia and glycolysis in the development of multi-drug resistance in human tumor cells and the establishment of an orthotopic multi-drug resistant tumor model in nude mice using hypoxic pre-conditioning Cancer Cell Int 11 2011 3
43. A. Das, B. Gopalakrishnan, O.H. Voss, A.I. Doseff, and F.A. Villamena Inhibition of ROS-induced apoptosis in endothelial cells by nitrone spin traps via induction of phase II enzymes and suppression of mitochondria-dependent pro-apoptotic signaling Biochem. Pharmacol. 84 2012 486 497
44. Y. Li, L. Fu, J.B. Li, Y. Qin, T.T. Zeng, J. Zhou, Z.L. Zeng, J. Chen, T.T. Cao, X. Ban, C. Qian, Z. Cai, D. Xie, P. Huang, and X.Y. Guan Increased expression of EIF5A2, via hypoxia or gene amplification, contributes to metastasis and angiogenesis of esophageal squamous cell carcinoma Gastroenterology 146 2014 1701 1713 e1709
45. P.R. Subbarayan, M. Sarkar, S. Nagaraja Rao, S. Philip, P. Kumar, N. Altman, I. Reis, M. Ahmed, B. Ardalan, and B.L. Lokeshwar Achyranthes aspera (Apamarg) leaf extract inhibits human pancreatic tumor growth in athymic mice by apoptosis J. Ethnopharmacol. 142 2012 523 530
46. S. Al-Hashmi, Z. Hassan, B. Sadeghi, B. Rozell, and M. Hassan Dynamics of early histopathological changes in GVHD after busulphan/cyclophosphamide conditioning regimen Int. J. Clin. Exp. Pathol. 4 2011 596 605
47. Y. Yang, H. Liu, F. Liu, and Z. Dong Mitochondrial dysregulation and protection in cisplatin nephrotoxicity Arch. Toxicol. 88 2014 1249 1256
48. R.F. McQuillan, E. Chiu, S. Nessim, C.E. Lok, J.M. Roscoe, P. Tam, and S.V. Jassal A randomized controlled trial comparing mupirocin and polysporin triple ointments in peritoneal dialysis patients: the MP3 Study Clin. J. Am. Soc. Nephrol. 7 2012 297 303
49. I.F. Tannock Conventional cancer therapy: promise broken or promise delayed? Lancet 351 Suppl. 2 1998 SII9-16
50. R.E. Durand The influence of microenvironmental factors during cancer therapy In Vivo 8 1994 691 702
51. R.C. Sun, and N.C. Denko Hypoxic regulation of glutamine metabolism through HIF1 and SIAH2 supports lipid synthesis that is necessary for tumor growth Cell Metab. 19 2014 285 292
52. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
53. M.C. Brahimi-Horn, J. Chiche, and J. Pouyssegur Hypoxia signalling controls metabolic demand Curr. Opin. Cell Biol. 19 2007 223 229
54. T.C. Karlenius, F. Shah, G. Di Trapani, F.M. Clarke, and K.F. Tonissen Cycling hypoxia up-regulates thioredoxin levels in human MDA-MB-231 breast cancer cells Biochem. Biophys. Res. Commun. 419 2012 350 355
55. K.F. Tonissen, and G. Di Trapani Thioredoxin system inhibitors as mediators of apoptosis for cancer therapy Mol. Nutr. Food Res. 53 2009 87 103
56. E.S. Arner, H. Nakamura, T. Sasada, J. Yodoi, A. Holmgren, and G. Spyrou Analysis of the inhibition of mammalian thioredoxin, thioredoxin reductase, and glutaredoxin by cis-diamminedichloroplatinum(II) and its major metabolite, the glutathione-platinum complex Free Radic. Biol. Med. 31 2001 1170 1178
57. B.M. Byrne, and J. Welsh Altered thioredoxin subcellular localization and redox status in MCF-7 cells following 1,25-dihydroxyvitamin D3 treatment J. Steroid Biochem. Mol. Biol. 97 2005 57 64
58. M. Ema, K. Hirota, J. Mimura, H. Abe, J. Yodoi, K. Sogawa, L. Poellinger, and Y. Fujii-Kuriyama Molecular mechanisms of transcription activation by HLF and HIF1alpha in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300 EMBO J. 18 1999 1905 1914
59. S.J. Wei, A. Botero, K. Hirota, C.M. Bradbury, S. Markovina, A. Laszlo, D.R. Spitz, P.C. Goswami, J. Yodoi, and D. Gius Thioredoxin nuclear translocation and interaction with redox factor-1 activates the activator protein-1 transcription factor in response to ionizing radiation Cancer Res. 60 2000 6688 6695
60. Y.M. Go, T.R. Ziegler, J.M. Johnson, L. Gu, J.M. Hansen, and D.P. Jones Selective protection of nuclear thioredoxin-1 and glutathione redox systems against oxidation during glucose and glutamine deficiency in human colonic epithelial cells Free Radic. Biol. Med. 42 2007 363 370
61. N. Gurusamy, G. Malik, N.V. Gorbunov, and D.K. Das Redox activation of Ref-1 potentiates cell survival following myocardial ischemia reperfusion injury Free Radic. Biol. Med. 43 2007 397 407
62. A. Hielscher, and S. Gerecht Hypoxia and free radicals: role in tumor progression and the use of engineering-based platforms to address these relationships Free Radic. Biol. Med. 79 2015 281 291
63. 2 sensing J. Biol. Chem. 275 2000 25130 25138
64. S. Bonello, C. Zahringer, R.S. BelAiba, T. Djordjevic, J. Hess, C. Michiels, T. Kietzmann, and A. Gorlach Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site Arterioscler. Thromb. Vasc. Biol. 27 2007 755 761