Enhancement of Auranofin-Induced Apoptosis in MCF-7 Human Breast Cells by Selenocystine, a Synergistic Inhibitor of Thioredoxin Reductase

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Liu, Chaoran ^a   Liu, Zhong ^a   Li, Meng ^a   Li, Xiaoling ^a   Wong, Yum Shing ^b   Ngai, Sai Ming ^b   Zheng, Wenjie ^a   Zhang, Yibo ^a   Chen, Tianfeng ^a  

^a JINAN UNIVERSITY   (China)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

AURANOFIN; DNA; GLUTATHIONE PEROXIDASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SELENOCYSTINE; THIOREDOXIN REDUCTASE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER INHIBITION; CELL STRAIN MCF 7; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; DOWN REGULATION; DRUG POTENTIATION; DRUG TARGETING; ENZYME ACTIVITY; GROWTH INHIBITION; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 84872284719     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053945     Document Type: Article

References (53)

1. Arner ES, Holmgren A, (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267: 6102-6109.
2. Arner ES, Holmgren A, (2006) The thioredoxin system in cancer. Semin Cancer Biol 16: 420-426.
3. Hoffmann FW, Hashimoto AS, Lee BC, Rose AH, Shohet RV, et al. (2011) Specific antioxidant selenoproteins are induced in the heart during hypertrophy. Arch Biochem Biophys 512: 38-44.
4. Eriksson SE, Prast-Nielsen S, Flaberg E, Szekely L, Arner ES, (2009) High levels of thioredoxin reductase 1 modulate drug-specific cytotoxic efficacy. Free Radic Biol Med 47: 1661-1671.
5. Myers JM, Myers CR, (2009) The effects of hexavalent chromium on thioredoxin reductase and peroxiredoxins in human bronchial epithelial cells. Free Radic Biol Med 47: 1477-1485.
6. Zhao F, Yan J, Deng S, Lan L, He F, et al. (2006) A thioredoxin reductase inhibitor induces growth inhibition and apoptosis in five cultured human carcinoma cell lines. Cancer Lett 236: 46-53.
7. Cassidy PB, Edes K, Nelson CC, Parsawar K, Fitzpatrick FA, et al. (2006) Thioredoxin reductase is required for the inactivation of tumor suppressor p53 and for apoptosis induced by endogenous electrophiles. Carcinogenesis 27: 2538-2549.
8. Anestal K, Prast-Nielsen S, Cenas N, Arner ES, (2008) Cell death by SecTRAPs: thioredoxin reductase as a prooxidant killer of cells. PLoS One 3: e1846.
9. Sasada T, Nakamura H, Ueda S, Sato N, Kitaoka Y, et al. (1999) Possible involvement of thioredoxin reductase as well as thioredoxin in cellular sensitivity to cis-diamminedichloroplatinum (II). Free Radic Biol Med 27: 504-514.
10. Marzano C, Gandin V, Folda A, Scutari G, Bindoli A, et al. (2007) Inhibition of thioredoxin reductase by auranofin induces apoptosis in cisplatin-resistant human ovarian cancer cells. Free Radic Biol Med 42: 872-881.
11. Shaw IC, (1999) Gold-based therapeutic agents. Chem Rev 99: 2589-2600.
12. Dvorakova K, Payne CM, Tome ME, Briehl MM, Vasquez MA, et al. (2002) Molecular and cellular characterization of imexon-resistant RPMI8226/I myeloma cells. Mol Cancer Ther 1: 185-195.
13. Chen T, Wong YS, (2008) Selenocystine induces apoptosis of A375 human melanoma cells by activating ROS-mediated mitochondrial pathway and p53 phosphorylation. Cell Mol Life Sci 65: 2763-2775.
14. Chen T, Wong YS, (2009) Selenocystine induces caspase-independent apoptosis in MCF-7 human breast carcinoma cells with involvement of p53 phosphorylation and reactive oxygen species generation. Int J Biochem Cell Biol 41: 666-676.
15. Sinha R, El-Bayoumy K, (2004) Apoptosis is a critical cellular event in cancer chemoprevention and chemotherapy by selenium compounds. Curr Cancer Drug Targets 4: 13-28.
16. Selenius M, Fernandes AP, Brodin O, Bjornstedt M, Rundlof AK, (2008) Treatment of lung cancer cells with cytotoxic levels of sodium selenite: effects on the thioredoxin system. Biochem Pharmacol 75: 2092-2099.
17. Madeja Z, Sroka J, Nystrom C, Bjorkhem-Bergman L, Nordman T, et al. (2005) The role of thioredoxin reductase activity in selenium-induced cytotoxicity. Biochem Pharmacol 69: 1765-1772.
18. Chen T, Zheng W, Wong YS, Yang F, (2008) Mitochondria-mediated apoptosis in human breast carcinoma MCF-7 cells induced by a novel selenadiazole derivative. Biomed Pharmacother 62: 77-84.
19. Zhao R, Xiang N, Domann FE, Zhong W, (2009) Effects of selenite and genistein on G2/M cell cycle arrest and apoptosis in human prostate cancer cells. Nutr Cancer 61: 397-407.
20. El-Sayed WM, Aboul-Fadl T, Lamb JG, Roberts JC, Franklin MR, (2006) Effect of selenium-containing compounds on hepatic chemoprotective enzymes in mice. Toxicology 220: 179-188.
21. Arner ES, Zhong L, Holmgren A, (1999) Preparation and assay of mammalian thioredoxin and thioredoxin reductase. Methods Enzymol 300: 226-239.
22. Tallarida RJ, (2001) Drug synergism: its detection and applications. J Pharmacol Exp Ther 298: 865-872.
23. Janicke RU, Sprengart ML, Wati MR, Porter AG, (1998) Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 273: 9357-9360.
24. van Gurp M, Festjens N, van Loo G, Saelens X, Vandenabeele P, (2003) Mitochondrial intermembrane proteins in cell death. Biochem Biophys Res Commun 304: 487-497.
25. Shiah HS, Lee WS, Juang SH, Hong PC, Lung CC, et al. (2007) Mitochondria-mediated and p53-associated apoptosis induced in human cancer cells by a novel selenophene derivative, D-501036. Biochem Pharmacol 73: 610-619.
26. Newmeyer DD, Ferguson-Miller S, (2003) Mitochondria: releasing power for life and unleashing the machineries of death. Cell 112: 481-490.
27. Green DR, Chipuk JE, (2008) Apoptosis: Stabbed in the BAX. Nature 455: 1047-1049.
28. Tanel A, Averill-Bates DA, (2007) P38 and ERK mitogen-activated protein kinases mediate acrolein-induced apoptosis in Chinese hamster ovary cells. Cell Signal 19: 968-977.
29. Simstein R, Burow M, Parker A, Weldon C, Beckman B, (2003) Apoptosis, chemoresistance, and breast cancer: insights from the MCF-7 cell model system. Exp Biol Med (Maywood) 228: 995-1003.
30. Boldt S, Weidle UH, Kolch W, (2002) The role of MAPK pathways in the action of chemotherapeutic drugs. Carcinogenesis 23: 1831-1838.
31. Gromer S, Gross JH, (2002) Methylseleninate is a substrate rather than an inhibitor of mammalian thioredoxin reductase. Implications for the antitumor effects of selenium. J Biol Chem 277: 9701-9706.
32. Cai W, Zhang L, Song Y, Wang B, Zhang B, et al. (2012) Small molecule inhibitors of mammalian thioredoxin reductase. Free Radic Biol Med 52: 257-265.
33. Rackham O, Shearwood AM, Thyer R, McNamara E, Davies SM, et al. (2011) Substrate and inhibitor specificities differ between human cytosolic and mitochondrial thioredoxin reductases: Implications for development of specific inhibitors. Free Radic Biol Med 50: 689-699.
34. Abdulah R, Miyazaki K, Nakazawa M, Koyama H, (2005) Chemical forms of selenium for cancer prevention. J Trace Elem Med Biol 19: 141-150.
35. Ip C, Thompson HJ, Zhu Z, Ganther HE, (2000) In vitro and in vivo studies of methylseleninic acid: evidence that a monomethylated selenium metabolite is critical for cancer chemoprevention. Cancer Res 60: 2882-2886.
36. Snider G, Grout L, Ruggles EL, Hondal RJ, (2010) Methaneseleninic acid is a substrate for truncated mammalian thioredoxin reductase: implications for the catalytic mechanism and redox signaling. Biochemistry 49: 10329-10338.
37. Zhao R, Masayasu H, Holmgren A, (2002) Ebselen: a substrate for human thioredoxin reductase strongly stimulating its hydroperoxide reductase activity and a superfast thioredoxin oxidant. Proc Natl Acad Sci U S A 99: 8579-8584.
38. Kondo N, Nakamura H, Masutani H, Yodoi J, (2006) Redox regulation of human thioredoxin network. Antioxid Redox Signal 8: 1881-1890.
39. Didier C, Kerblat I, Drouet C, Favier A, Beani JC, et al. (2001) Induction of thioredoxin by ultraviolet-A radiation prevents oxidative-mediated cell death in human skin fibroblasts. Free Radic Biol Med 31: 585-598.
40. Rigobello MP, Gandin V, Folda A, Rundlof AK, Fernandes AP, et al. (2009) Treatment of human cancer cells with selenite or tellurite in combination with auranofin enhances cell death due to redox shift. Free Radic Biol Med 47: 710-721.
41. Carvalho H, Evelson P, Sigaud S, Gonzalez-Flecha B, (2004) Mitogen-activated protein kinases modulate H(2)O(2)-induced apoptosis in primary rat alveolar epithelial cells. J Cell Biochem 92: 502-513.
42. Johnson GL, Lapadat R, (2002) Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298: 1911-1912.
43. Jiang C, Wang Z, Ganther H, Lu J, (2002) Distinct effects of methylseleninic acid versus selenite on apoptosis, cell cycle, and protein kinase pathways in DU145 human prostate cancer cells. Mol Cancer Ther 1: 1059-1066.
44. Hu H, Jiang C, Li G, Lu J, (2005) PKB/AKT and ERK regulation of caspase-mediated apoptosis by methylseleninic acid in LNCaP prostate cancer cells. Carcinogenesis 26: 1374-1381.
45. Unni E, Koul D, Yung WK, Sinha R, (2005) Se-methylselenocysteine inhibits phosphatidylinositol 3-kinase activity of mouse mammary epithelial tumor cells in vitro. Breast Cancer Res 7: R699-707.
46. Li S, Zhou Y, Wang R, Zhang H, Dong Y, et al. (2007) Selenium sensitizes MCF-7 breast cancer cells to doxorubicin-induced apoptosis through modulation of phospho-Akt and its downstream substrates. Mol Cancer Ther 6: 1031-1038.
47. Tichy A, Zaskodova D, Rezacova M, Vavrova J, Vokurkova D, et al. (2007) Gamma-radiation-induced ATM-dependent signalling in human T-lymphocyte leukemic cells, MOLT-4. Acta Biochim Pol 54: 281-287.
48. Lu J, Chew EH, Holmgren A, (2007) Targeting thioredoxin reductase is a basis for cancer therapy by arsenic trioxide. Proc Natl Acad Sci U S A 104: 12288-12293.
49. Vousden KH, Lu X, (2002) Live or let die: the cell's response to p53. Nat Rev Cancer 2: 594-604.
50. Li T, Kon N, Jiang L, Tan M, Ludwig T, et al. (2012) Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence. Cell 149: 1269-1283.
51. Fulda S, Debatin KM, (2002) IFNgamma sensitizes for apoptosis by upregulating caspase-8 expression through the Stat1 pathway. Oncogene 21: 2295-2308.
52. Nordberg J, Arner ES, (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 31: 1287-1312.
53. Du H, Wolf J, Schafer B, Moldoveanu T, Chipuk JE, et al. (2011) BH3 domains other than Bim and Bid can directly activate Bax/Bak. J Biol Chem 286: 491-501.