The mode of cisplatin-induced cell death in CYP2E1-overexpressing HepG2 cells: Modulation by ERK, ROS, glutathione, and thioredoxin

Free Radical Biology and Medicine

Volumn 43, Issue 7, 2007, Pages 1061-1075

  Lu, Yongke ^a   Cederbaum, Arthur ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Cisplatin; CYP2E1; Extracellular signal regulated kinases; Free radicals; Glutathione; l Buthionine R,S sulfoximine; Necrosis; Thioredoxin

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; BUTHIONINE SULFOXIMINE; CASPASE; CISPLATIN; CYTOCHROME P450 2E1; GLUTATHIONE; GLUTATHIONE ETHYL ESTER; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; THIOREDOXIN;

APOPTOSIS; ARTICLE; CELL DEATH; CELL STRAIN HEPG2; CONTROLLED STUDY; DRUG CYTOTOXICITY; ENZYME ACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; NECROSIS; PRIORITY JOURNAL;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; BUTHIONINE SULFOXIMINE; CARCINOMA, HEPATOCELLULAR; CASPASES; CELL DEATH; CISPLATIN; CYTOCHROME P-450 CYP2E1; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GLUTATHIONE; HUMANS; LIVER NEOPLASMS; NECROSIS; REACTIVE OXYGEN SPECIES; THIOREDOXIN; TUMOR CELLS, CULTURED;

EID: 34548129941     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2007.06.021     Document Type: Article

References (53)

1. Chu G. Cellular response to cisplatin. J. Biol. Chem. 269 (1994) 787-790
2. Timmer-Bosscha H., Mulder N.H., and de Vries E.G.E. Modulation of cis-diamminedichloroplatinum (II) resistance: a review. Br. J. Cancer 66 (1992) 227-238
3. McGinness J.E., Proctor P.H., Demopoulos H.B., Hokanson J.A., and Kirkpatrick D.S. Amelioration of cis-platinum nephrotoxicity by Orgotein (superoxide dismutase). Physiol. Chem. Phys. 10 (1978) 267-277
4. Sugihara K., and Gemba M. Modification of cisplatin toxicity by antioxidants. Jpn. J. Pharmacol. 40 (1986) 353-355
5. Hannemann J., and Baumann K. Cisplatin-induced lipid peroxidation and decrease of gluconeogenesis in rat kidney cortex: different effects of antioxidants and radical scavengers. Toxicology 51 (1988) 119-132
6. 2 -) by murine macrophages in vitro after cisplatin treatment. Int. J. Immunopharmacol. 8 (1986) 709-714
7. Masuda H., Tanaka T., and Takahama U. Cisplatin generates superoxide anion by interaction with DNA in a cell-free system. Biochem. Biophys. Res. Commun. 203 (1994) 1175-1180
8. Murphy M.E., Scholich H., and Sies H. Protection by glutathione and other thiol compounds against the loss of protein thiols and tocopherol homologs during microsomal lipid peroxidation. Eur. J. Biochem. 210 (1992) 139-146
9. Lu Y., Kawashima A., Horii I., and Zhong L. Effects of BSO and l-cysteine on drug-induced cytotoxicity in primary cell cultures: drug-, cell type-, and species-specific difference. Drug Chem. Toxicol. 27 (2004) 269-280
10. Lu Y., Kawashima A., Horii I., and Zhong L. Cisplatin-induced cytotoxicity in BSO-exposed renal proximal tubular epithelial cells: sex, age, and species. Renal. Failure 27 (2005) 629-633
11. Lu Y., and Cederbaum A.I. Cisplatin-induced hepatotoxicity is enhanced by elevated expression of cytochrome P450 2E1. Toxicol. Sci. 89 (2005) 515-523
12. Guyton K.Z., Liu Y., Gorospe M., Xu Q., and Holbrook N.J. Activation of mitogen-activated protein kinase by H2O2: role in cell survival following oxidant injury. J. Biol. Chem. 271 (1996) 4138-4142
13. Chen Q., Olashaw N., and Wu J. Participation of reactive oxygen species in the lysophosphatidic acid-stimulated mitogen-activated protein kinase kinase activation pathway. J. Biol. Chem. 270 (1995) 28499-28502
14. Lander H.M. An essential role for free radicals and derived species in signal transduction. FASEB J. 11 (1997) 118-124
15. Bhat N.R., and Zhang P. Hydrogen peroxide activation of multiple mitogen-activated protein kinases in an oligodendrocyte cell line: role of extracellular signal-regulated kinase in hydrogen peroxide-induced cell death. J. Neurochem. 72 (1999) 112-119
16. Zhang W., and Liu H.T. MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell. Res. 12 (2003) 9-18
17. Wang X., Martindale J.L., and Holbrook N.J. Requirement for ERK activation in cisplatin-induced apoptosis. J. Biol. Chem. 275 (2000) 39435-39443
18. Choi B.K., Choi C.H., Oh H.L., and Kim Y.K. Role of ERK activation in cisplatin-induced apoptosis in A172 human glioma cells. Neurotoxicology 25 (2004) 915-924
19. Mansouri A., Ridgway L.D., Korapati A.L., Zhang Q., Tian L., Wang Y., Siddik Z.H., Mills G.B., and Claret F.X. Sustained activation of JNK/p38 MAPK pathways in response to cisplatin leads to Fas ligand induction and cell death in ovarian carcinoma cells. J. Biol. Chem. 278 (2003) 19245-19556
20. Wu Y.J., Muldoon L.L., and Neuwelt E.A. The chemoprotective agent N-acetylcysteine blocks cisplatin-induced apoptosis through caspase signaling pathway. J. Pharmacol. Exp. Ther. 312 (2005) 424-431
21. Ekstrom G., and Ingelman-Sundberg M. Rat liver microsomal NADPH-supported oxidase activity and lipid peroxidation dependent on ethanol-inducible cytochrome P-450 (P-450IIE1). Biochem. Pharmacol. 38 (1989) 1313-1319
22. Lu Y., Wang X., and Cederbaum A.I. Lipopolysaccharide-induced liver injury in rats treated with the CYP2E1 inducer pyrazole. Am. J. Physiol.: Gastrointest. Liver Physiol. 289 (2005) G308-G319
23. Lu Y., and Cederbaum A.I. Enhancement by pyrazole of lipopolysaccharide-induced liver injury in mice: role of cytochrome P450 2E1 and 2A5. Hepatology 44 (2006) 263-274
24. Wu D., and Cederbaum A.I. Removal of glutathione produces apoptosis and necrosis in HepG2 cells overexpressing CYP2E1. Alcohol. Clin. Exp. Res. 25 (2001) 619-628
25. Wu D., and Cederbaum A.I. Ethanol cytotoxicity to a transfected HepG2 cell line expressing human cytochrome P4502E1. J. Biol. Chem. 271 (1996) 23914-23919
26. Cederbaum A.I., Wu D., Mari M., and Bai J. CYP2E1-dependent toxicity and oxidative stress in HepG2 cells. Free Radic. Biol. Med. 31 (2001) 1539-1543
27. Chen Q., and Cederbaum A.I. Cytotoxicity and apoptosis produced by cytochrome P450 2E1 in Hep G2 cells. Mol. Pharmacol. 53 (1998) 638-648
28. Bai J., Rodriguez A.M., Melendez J.A., and Cederbaum A.I. Overexpression of catalase in cytosolic or mitochondrial compartment protects HepG2 cells against oxidative injury. J. Biol. Chem. 274 (1999) 26217-26224
29. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 27 (1969) 502-522
30. Kerr J.F., Wyllie A.H., and Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26 (1972) 239-257
31. Majno G., and Joris I. Apoptosis, oncosis, and necrosis: an overview of cell death. Am. J. Pathol. 146 (1995) 3-15
32. Dursun B., He Z., Somerset H., Oh J., Faubel S., and Edelstein C.L. Caspases and calpain are independent mediators of cisplatin-induced endothelial cell necrosis. Am. J. Physiol.: Renal Physiol. 291 (2006) F578-F587
33. Mitsui H., Takuwa N., Maruyama T., Maekawa H., Hirayama M., Sawatari T., Hashimoto N., Takuwa Y., and Kimura S. The MEK1-ERK MAP kinase pathway and the PI 3-kinase-Akt pathway independently mediate anti-apoptotic signals in HepG2 liver cancer cells. Int. J. Cancer 92 (2001) 55-62
34. Mari M., and Cederbaum A.I. CYP2E1 overexpression in HepG2 cells induces glutathione synthesis by transcriptional activation of gamma-glutamylcysteine synthetase. J. Biol. Chem. 275 (2000) 15563-15571
35. Troyano A., Sancho P., Fernandez C., de Blas E., Bernardi P., and Aller P. The selection between apoptosis and necrosis is differentially regulated in hydrogen peroxide-treated and glutathione-depleted human promonocytic cells. Cell. Death Differ. 10 (2003) 889-898
36. Troyano A., Fernandez C., Sancho P., de Blas E., and Aller P. Effect of glutathione depletion on antitumor drug toxicity (apoptosis and necrosis) in U-937 human promonocytic cells: the role of intracellular oxidation. J. Biol. Chem. 276 (2001) 47107-47115
37. Shin J.N., Seo Y.W., Kim M., Park S.Y., Lee M.J., Lee B.R., Oh J.W., Seol D.W., and Kim T.H. Cisplatin inactivation of caspases inhibits death ligand-induced cell death in vitro and fulminant liver damage in mice. J. Biol. Chem. 280 (2005) 10509-10515
38. Cotgreave I.A., and Gerdes R.G. Recent trends in glutathione biochemistry-glutathione-protein interactions: a molecular link between oxidative stress and cell proliferation?. Biochem. Biophys. Res. Commun. 242 (1998) 1-9
39. Biaglow J.E., and Miller R.A. The thioredoxin reductase/thioredoxin system: novel redox targets for cancer therapy. Cancer Biol. Ther. 4 (2005) 6-13
40. Zhuang S., and Schnellmann R.G. A death-promoting role for extracellular signal-regulated kinase. J. Pharmacol. Exp. Ther. 319 (2006) 991-997
41. Stanciu M., Wang Y., Kentor R., Burke N., Watkins S., Kress G., Reynolds I., Klann E., Angiolieri M.R., Johnson J.W., and DeFranco D.B. Persistent activation of ERK contributes to glutamate-induced oxidative toxicity in a neuronal cell line and primary cortical neuron cultures. J. Biol. Chem. 275 (2000) 12200-12206
42. Stanciu M., and DeFranco D.B. Prolonged nuclear retention of activated extracellular signal-regulated protein kinase promotes cell death generated by oxidative toxicity or proteasome inhibition in a neuronal cell line. J. Biol. Chem. 277 (2002) 4010-4017
43. Chu C.T., Levinthal D.J., Kulich S.M., Chalovich E.M., and DeFranco D.B. Oxidative neuronal injury: the dark side of ERK1/2. Eur. J. Biochem. 271 (2004) 2060-2066
44. Kulich S.M., and Chu C.T. Sustained extracellular signal-regulated kinase activation by 6-hydroxydopamine: implications for Parkinson's disease. J. Neurochem. 77 (2001) 1058-1066
45. Watson W.H., Yang X., Choi Y.E., Jones D.P., and Kehrer J.P. Thioredoxin and its role in toxicology. Toxicol. Sci. 78 (2004) 3-14
46. Sasada T., Iwata S., Sato N., Kitaoka Y., Hirota K., Nakamura K., Nishiyama A., Taniguchi Y., Takabayashi A., and Yodoi J. Redox control of resistance to cis-diamminedichloroplatinum (II) (CDDP): protective effect of human thioredoxin against CDDP-induced cytotoxicity. J. Clin. Invest. 97 (1996) 2268-2276
47. Arner E.S., Nakamura H., Sasada T., Yodoi J., Holmgren A., and Spyrou G. 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
48. Schweyer S., Soruri A., Heintze A., Radzun H.J., and Fayyazi A. The role of reactive oxygen species in cisplatin-induced apoptosis in human malignant testicular germ cell lines. Int. J. Oncol. 25 (2004) 1671-1676
49. Wu W.S., Tsai R.K., Chang C.H., Wang S., Wu J.R., and Chang Y.X. Reactive oxygen species mediated sustained activation of protein kinase C alpha and extracellular signal-regulated kinase for migration of human hepatoma cell HepG2. Mol. Cancer Res. 4 (2006) 747-758
50. Parinandi N.L., Kleinberg M.A., Usatyuk P.V., Cummings R.J., Pennathur A., Cardounel A.J., Zweier J.L., Garcia J.G., and Natarajan V. Hyperoxia-induced NAD(P)H oxidase activation and regulation by MAP kinases in human lung endothelial cells. Am. J. Physiol.: Lung Cell Mol. Physiol. 284 (2003) 26-38
51. Chess P.R., O'Reilly M.A., Sachs F., and Finkelstein J.N. Reactive oxidant and p42/44 MAP kinase signaling is necessary for mechanical strain-induced proliferation in pulmonary epithelial cells. J. Appl. Physiol. 99 (2005) 1226-1232
52. Gorsky L.D., Koop D.R., and Coon M.J. On the stoichiometry of the oxidase and monooxygenase reactions catalyzed by liver microsomal cytochrome P-450: products of oxygen reduction. J. Biol. Chem. 259 (1984) 6812-6817
53. Dai Y., Rashba-Step J., and Cederbaum A.I. Stable expression of human cytochrome P4502E1 in HepG2 cells: characterization of catalytic activities and production of reactive oxygen intermediates. Biochemistry 32 (1993) 6928-6937