Auranofin induces apoptosis and necrosis in HeLa cells via oxidative stress and glutathione depletion

Molecular Medicine Reports

Volumn 11, Issue 2, 2015, Pages 1428-1434

  You, Bo Ra ^a   Shin, Hye Rim ^a   Han, Bo Ram ^a   Kim, Suhn Hee ^a   Park, Woo Hyun ^a  

^a Chonbuk National University   (South Korea)

Author keywords

Apoptosis; Auranofin; Glutathione; Necrosis; Reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; ANTINEOPLASTIC AGENT; ANTIOXIDANT; AURANOFIN; BENZYLOXYCARBONYL-VALYL-ALANYL-ASPARTIC ACID; BUTHIONINE SULFOXIMINE; CASPASE INHIBITOR; GLUTATHIONE; OLIGOPEPTIDE; SINGLET OXYGEN;

APOPTOSIS; CELL PROLIFERATION; DEFICIENCY; DRUG EFFECTS; HELA CELL LINE; HUMAN; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; NECROSIS; OXIDATIVE STRESS;

ACETYLCYSTEINE; ANTINEOPLASTIC AGENTS; ANTIOXIDANTS; APOPTOSIS; AURANOFIN; BUTHIONINE SULFOXIMINE; CASPASE INHIBITORS; CELL PROLIFERATION; GLUTATHIONE; HELA CELLS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; NECROSIS; OLIGOPEPTIDES; OXIDATIVE STRESS; SINGLET OXYGEN;

EID: 84916204293     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2014.2830     Document Type: Article

References (37)

1. Lu J and Holmgren A: Thioredoxin system in cell death progression. Antioxid Redox Signal 17: 1738-1747, 2012.
2. Collet JF and Messens J: Structure, function, and mechanism of thioredoxin proteins. Antioxid Redox Signal 13: 1205-1216, 2010.
3. Burke-Gaffney A, Callister ME and Nakamura H: Thioredoxin: friend or foe in human disease? Trends Pharmacol Sci 26: 398-404, 2005.
4. Rundlöf AK and Arner ES: Regulation of the mammalian selenoprotein thioredoxin reductase 1 in relation to cellular phenotype, growth, and signaling events. Antioxida Redox Signal 6: 41-52, 2004.
5. Noike T, Miwa S, Soeda J, Kobayashi A and Miyagawa S: Increased expression of thioredoxin-1, vascular endothelial growth factor, and redox factor-1 is associated with poor prognosis in patients with liver metastasis from colorectal cancer. Hum Pathol 39: 201-208, 2008.
6. Karlenius TC, Shah F, Di Trapani G, Clarke FM and Tonissen KF: Cycling hypoxia up-regulates thioredoxin levels in human MDA-MB-231 breast cancer cells. Biochem Biophys Res Commun 419: 350-355, 2012.
7. Fernandes AP, Capitanio A, Selenius M, Brodin O, Rundlöf AK and Björnstedt M: Expression profiles of thioredoxin family proteins in human lung cancer tissue: correlation with proliferation and differentiation. Histopathology 55: 313-320, 2009.
8. Poerschke RL and Moos PJ: Thioredoxin reductase 1 knockdown enhances selenazolidine cytotoxicity in human lung cancer cells via mitochondrial dysfunction. Biochem Pharmacol 81: 211-221, 2011.
9. Fu JN, Li J, Tan Q, et al: Thioredoxin reductase inhibitor ethaselen increases the drug sensitivity of the colon cancer cell line LoVo towards cisplatin via regulation of G1 phase and reversal of G2/M phase arrest. Invest New Drugs 29: 627-636, 2011.
10. Madeira JM, Gibson DL, Kean WF and Klegeris A: The biological activity of auranofin: implications for novel treatment of diseases. Inflammopharmacology 20: 297-306, 2012.
11. Suarez-Almazor ME, Spooner CH, Belseck E and Shea B: Auranofin versus placebo in rheumatoid arthritis. Cochrane Database Syst Rev : CD002048, 2000.
12. Han S, Kim K, Kim H, et al: Auranofin inhibits overproduction of pro-inflammatory cytokines, cyclooxygenase expression and PGE2 production in macrophages. Arch Pharm Res 31: 67-74, 2008.
13. Han S, Kim K, Song Y, et al: Auranofin, an immunosuppressive drug, inhibits MHC class I and MHC class II pathways of antigen presentation in dendritic cells. Arch Pharm Res 31: 370-376, 2008.
14. Liu C, Liu Z, Li M, et al: Enhancement of auranofin-induced apoptosis in MCF-7 human breast cells by selenocystine, a synergistic inhibitor of thioredoxin reductase. PloS One 8: e53945, 2013.
15. Nakaya A, Sagawa M, Muto A, Uchida H, Ikeda Y and Kizaki M: The gold compound auranofin induces apoptosis of human multiple myeloma cells through both down-regulation of STAT3 and inhibition of NF-kappaB activity. Leuk Res 35: 243-249, 2011.
16. Rigobello MP, Scutari G, Boscolo R and Bindoli A: Induction of mitochondrial permeability transition by auranofin, a gold(I)-phosphine derivative. Br J Pharmacol 136: 1162-1168, 2002.
17. Rigobello MP, Folda A, Baldoin MC, Scutari G and Bindoli A: Effect of auranofin on the mitochondrial generation of hydrogen peroxide. Role of thioredoxin reductase. Free Rad Res 39: 687-695, 2005.
18. Haverkos H, Rohrer M and Pickworth W: The cause of invasive cervical cancer could be multifactorial. Biomed Pharmacother 54: 54-59, 2000.
19. De Marco F, Bucaj E, Foppoli C, et al: Oxidative stress in HPV-driven viral carcinogenesis: redox proteomics analysis of HPV-16 dysplastic and neoplastic tissues. PloS One 7: e34366, 2012.
20. Kim NH, Park HJ, Oh MK and Kim IS: Antiproliferative effect of gold(I) compound auranofin through inhibition of STAT3 and telomerase activity in MDA-MB 231 human breast cancer cells. BMB Rep 46: 59-64, 2013.
21. Marzano C, Gandin V, Folda A, Scutari G, Bindoli A and Rigobello MP: Inhibition of thioredoxin reductase by auranofin induces apoptosis in cisplatin-resistant human ovarian cancer cells. Free Rad Biol Med 42: 872-881, 2007.
22. Rigobello MP, Gandin V, Folda A, et al: Treatment of human cancer cells with selenite or tellurite in combination with auranofin enhances cell death due to redox shift. Free Rad Biol Med 47: 710-721, 2009.
23. Han YH, Moon HJ, You BR, Kim SZ, Kim SH and Park WH: Effects of carbonyl cyanide p-(trifluoromethoxy) phenylhydrazone on the growth inhibition in human pulmonary adenocarcinoma Calu-6 cells. Toxicology 265: 101-107, 2009.
24. Han YH, Moon HJ, You BR and Park WH: The effect of MG132, a proteasome inhibitor on HeLa cells in relation to cell growth, reactive oxygen species and GSH. Oncol Rep 22: 215-221, 2009.
25. You BR and Park WH: Zebularine inhibits the growth of HeLa cervical cancer cells via cell cycle arrest and caspase-dependent apoptosis. Mol Biol Rep 39: 9723-9731, 2012.
26. Han YH, Kim SH, Kim SZ and Park WH: Carbonyl cyanide p-(trifluoromethoxy) phenylhydrazone (FCCP) as an O2 (∗-) generator induces apoptosis via the depletion of intracellular GSH contents in Calu-6 cells. Lung Cancer 63: 201-209, 2009.
27. Han YH and Park WH: Propyl gallate inhibits the growth of HeLa cells via regulating intracellular GSH level. Food Chem Toxicol 47: 2531-2538, 2009.
28. You BR and Park WH: Suberoyl bishydroxamic acid-induced apoptosis in HeLa cells via ROS-independent, GSH-dependent manner. Mol Biol Rep 40: 3807-3816, 2013.
29. Martinou JC and Youle RJ: Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev Cell 21: 92-101, 2011.
30. Niquet J, Allen SG, Baldwin RA and Wasterlain CG: Evidence of caspase-3 activation in hyposmotic stress-induced necrosis. Neurosci Letters 356: 225-227, 2004.
31. Honda A, Abe S, Hiroki E, et al: Activation of caspase 3, 9, 12, and Bax in masseter muscle of mdx mice during necrosis. J Muscle Res Cell Motil 28: 243-247, 2007.
32. Park SJ and Kim IS: The role of p38 MAPK activation in auranofin-induced apoptosis of human promyelocytic leukaemia HL-60 cells. Br J Pharmacol 146: 506-513, 2005.
33. Hatem E, Berthonaud V, Dardalhon M, et al: Glutathione is essential to preserve nuclear function and cell survival under oxidative stress. Free Radic Biol Med 67: 103-114, 2014.
34. Ortega AL, Mena S and Estrela JM: Glutathione in cancer cell death. Cancers 3: 1285-1310, 2011.
35. Franco R and Cidlowski JA: Glutathione efflux and cell death. Antioxid Redox Signal 7: 1694-1713, 2012.
36. Sobhakumari A, Love-Homan L, Fletcher EV, et al: Susceptibility of human head and neck cancer cells to combined inhibition of glutathione and thioredoxin metabolism. PloS One 7: e48175, 2012.
37. Scarbrough PM, Mapuskar KA, Mattson DM, Gius D, Watson WH and Spitz DR: Simultaneous inhibition of glutathione-and thioredoxin-dependent metabolism is necessary to potentiate 17AAG-induced cancer cell killing via oxidative stress. Free Radic Biol Med 52: 436-443, 2012.