The Essential Role of the Mitochondria and Reactive Oxygen Species in Cisplatin-Mediated Enhancement of Fas Ligand-Induced Apoptosis in Malignant Pleural Mesothelioma

Journal of Surgical Research

Volumn 141, Issue 1, 2007, Pages 120-131

  Stewart IV, John H ^a,b   Tran, Thai Lan ^b   Levi, Nicole ^a   Tsai, Wilson S ^b   Schrump, David S ^b   Nguyen, Dao M ^b  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

apoptosis; caspase; cisplatin; Fas ligand; malignant pleural mesothelioma; mitochondria; reactive oxygen species

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; CISPLATIN; FAS LIGAND; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; FEEDBACK SYSTEM; FLUORESCENCE; GENE AMPLIFICATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MALIGNANT NEOPLASTIC DISEASE; MITOCHONDRION; MOUSE; NICK END LABELING; NITROBLUE TETRAZOLIUM TEST; NONHUMAN; PLEURA MESOTHELIOMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; VIRAL GENE DELIVERY SYSTEM; XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASE 8; CELL LINE, TUMOR; CELL SURVIVAL; CISPLATIN; DRUG SYNERGISM; FAS LIGAND PROTEIN; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MESOTHELIOMA; MICE; MICE, NUDE; MITOCHONDRIA; PLEURAL NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 34250304348     PISSN: 00224804     EISSN: 10958673     Source Type: Journal    
DOI: 10.1016/j.jss.2007.03.048     Document Type: Article

References (52)

1. Price B., and Ware A. Mesothelioma trends in the United States: An update based on surveillance, epidemiology, and end results program data for 1973 through 2003. Am J Epidemiol 159 (2004) 107
2. Weill H., Hughes J.M., and Churg A.M. Changing trends in U.S. mesothelioma incidence. Occup Environ Med 61 (2004) 438
3. Carbone M., Kratzke R.A., and Testa J.R. The pathogenesis of mesothelioma. Semin Oncol 29 (2002) 2
4. Zellos L., and Sugarbaker D.J. Current surgical management of malignant pleural mesothelioma. Curr Oncol Rep 4 (2002) 354
5. Nicholson D.W. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ 6 (1999) 1028
6. Salvesen G.S., and Dixit V.M. Caspase activation: The induced-proximity model. Proc Natl Acad Sci USA 96 (1999) 10964
7. Boatright K.M., Renatus M., Scott F.L., et al. A unified model for apical caspase activation. Mol Cell 11 (2003) 529
8. Ruffolo S.C., Breckenridge D.G., Nguyen M., et al. BID-dependent and BID-independent pathways for BAX insertion into mitochondria. Cell Death Differ 7 (2000) 1101
9. Korsmeyer S.J., Wei M.C., Saito M., et al. Proapoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ 7 (2000) 1166
10. Scorrano L., and Korsmeyer S.J. Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem Biophys Res Commun 304 (2003) 437
11. Scaffidi C., Fulda S., Srinivasan A., et al. Two CD95 (APO-1/Fas) signaling pathways. EMBO J 17 (1998) 1675
12. van Loo G., Saelens X., van Gurp M., et al. The role of mitochondrial factors in apoptosis: A Russian roulette with more than one bullet. Cell Death Differ 9 (2002) 1031
13. Saelens X., Festjens N., Vande W.L., et al. Toxic proteins released from mitochondria in cell death. Oncogene 23 (2004) 2861
14. Kroemer G., Dallaporta B., and Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol 60 (1998) 619
15. Slee E.A., Harte M.T., Kluck R.M., et al. Ordering the cytochrome c-initiated caspase cascade: Hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 144 (1999) 281
16. Ozoren N., and el Deiry W.S. Defining characteristics of types I and II apoptotic cells in response to TRAIL. Neoplasia 4 (2002) 551
17. Ricci J.E., Gottlieb R.A., and Green D.R. Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J Cell Biol 160 (2003) 65
18. Stewart J.H., Nguyen D.M., Chen G.A., et al. Induction of apoptosis in malignant pleural mesothelioma cells by activation of the Fas (Apo-1/CD95) death-signal pathway. J Thorac Cardiovasc Surg 123 (2002) 295
19. Micheau O., Solary E., Hammann A., et al. Sensitization of cancer cells treated with cytotoxic drugs to Fas-mediated cytotoxicity. J Natl Cancer Inst 89 (1997) 783
20. Mizutani Y., Yoshida O., and Bonavida B. Sensitization of human bladder cancer cells to Fas-mediated cytotoxicity by cis-diamminedichloroplatinum (II). J Urol 160 (1998) 561
21. Frost P.J., Belldegrun A., and Bonavida B. Sensitization of immunoresistant prostate carcinoma cell lines to Fas/Fas ligand-mediated killing by cytotoxic lymphocytes: Independence of de novo protein synthesis. Prostate 41 (1999) 20
22. Lautermann J., Crann S.A., McLaren J., et al. Glutathione-dependent antioxidant systems in the mammalian inner ear: Effects of aging, ototoxic drugs and noise. Heart Res 114 (1997) 75
23. Durak I., Ozbek H., Karaayvaz M., et al. Cisplatin induces acute renal failure by impairing antioxidant system in guinea pigs: Effects of antioxidant supplementation on the cisplatin nephrotoxicity. Drug Chem Toxicol 25 (2002) 1
24. Goto S., Yoshida K., Morikawa T., et al. Augmentation of transport for cisplatin-glutathione adduct in cisplatin-resistant cancer cells. Cancer Res 55 (1995) 4297
25. Sadzuka Y., Shimizu Y., Takino Y., et al. Protection against cisplatin-induced nephrotoxicity in the rat by inducers and an inhibitor of glutathione S-transferase. Biochem Pharmacol 48 (1994) 453
26. Chen Q.M., Liu J., and Merrett J.B. Apoptosis or senescence-like growth arrest: Influence of cell-cycle position, p53, p21, and Bax in H2O2 response of normal human fibroblasts. Biochem J 347 (2000) 543
27. Lee J.E., Sohn J., Lee J.H., et al. Regulation of bcl-2 family in hydrogen peroxide-induced apoptosis in human leukemia HL-60 cells. Exp Mol Med 32 (2000) 42
28. Riou C., Tonoli H., Bernier-Valentin F., et al. Susceptibility of differentiated thyrocytes in primary culture to undergo apoptosis after exposure to hydrogen peroxide: Relation with the level of expression of apoptosis regulatory proteins, Bcl-2 and Bax. Endocrinology 140 (1999) 1990
29. Charo J., Finkelstein S.E., Grewal N., et al. Bcl-2 overexpression enhances tumor-specific T-cell survival. Cancer Res 65 (2005) 2001
30. Yamaguchi H., Paranawithana S.R., Lee M.W., et al. Epothilone B analogue (BMS-247550)-mediated cytotoxicity through induction of Bax conformational change in human breast cancer cells. Cancer Res 62 (2002) 466
31. Reddy R.M., Yeow W.S., Chua A., et al. Rapid and profound potentiation of Apo2L/TRAIL-mediated cytotoxicity and apoptosis in thoracic cancer cells by the histone deacetylase inhibitor trichostatin A: The essential role of the mitochondria-mediated caspase activation cascade. Apoptosis 12 (2007) 55
32. Tsai W.S., Yeow W.S., Chua A., et al. Enhancement of Apo2L/TRAIL-mediated cytotoxicity in esophageal cancer cells by cisplatin. Mol Cancer Ther 5 (2006) 2977
33. Ziauddin M.F., Yeow W.S., Maxhimer J.B., et al. Valproic acid, an antiepileptic drug with histone deacetylase inhibitory activity, potentiates the cytotoxic effect of Apo2L/TRAIL on cultured thoracic cancer cells through mitochondria-dependent caspase activation. Neoplasia 8 (2006) 446
34. Inoue S., MacFarlane M., Harper N., et al. Histone deacetylase inhibitors potentiate TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in lymphoid malignancies. Cell Death Differ 2 11 Suppl (2004) S193
35. Izeradjene K., Douglas L., Tillman D.M., et al. Reactive oxygen species regulate caspase activation in tumor necrosis factor-related apoptosis-inducing ligand-resistant human colon carcinoma cell lines. Cancer Res 65 (2005) 7436
36. Morales A., Miranda M., Sanchez-Reyes A., et al. Oxidative damage of mitochondrial and nuclear DNA induced by ionizing radiation in human hepatoblastoma cells. Int J Radiat Oncol Biol Phys 42 (1998) 191
37. Ikeda S., and Ozaki K. Action of mitochondrial endonuclease G on DNA damaged by L-ascorbic acid, peplomycin, and cis-diamminedichloroplatinum (II). Biochem Biophys Res Commun 235 (1997) 291
38. Yakes F.M., and Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci USA 94 (1997) 514
39. Ide T., Tsutsui H., Hayashidani S., et al. Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ Res 88 (2001) 529
40. Esposito L.A., Melov S., Panov A., et al. Mitochondrial disease in mouse results in increased oxidative stress. Proc Natl Acad Sci USA 96 (1999) 4820
41. Luo X., Budihardjo I., Zou H., et al. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94 (1998) 481
42. Gross A., Yin X.M., Wang K., et al. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem 274 (1999) 1156
43. Desagher S., Osen-Sand A., Nichols A., et al. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 144 (1999) 891
44. Eskes R., Desagher S., Antonsson B., et al. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 20 (2000) 929
45. Hsu Y.T., and Youle R.J. Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations. J Biol Chem 273 (1998) 10777
46. Nechushtan A., Smith C.L., Hsu Y.T., et al. Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO J 18 (1999) 2330
47. Wood D.E., Thomas A., Devi L.A., et al. Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene 17 (1998) 1069
48. Makin G.W., Corfe B.M., Griffiths G.J., et al. Damage-induced Bax N-terminal change, translocation to mitochondria and formation of Bax dimers/complexes occur regardless of cell fate. EMBO J 20 (2001) 6306
49. Eskes R., Antonsson B., Osen-Sand A., et al. Bax-induced cytochrome c release from mitochondria is independent of the permeability transition pore but highly dependent on Mg2+ ions. J Cell Biol 143 (1998) 217
50. Kluck R.M., Esposti M.D., Perkins G., et al. The proapoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol. J Cell Biol 147 (1999) 809
51. Ogasawara J., Watanabe-Fukunaga R., Adachi M., et al. Lethal effect of the anti-Fas antibody in mice. Nature 364 (1993) 806
52. Greaney P., Nahimana A., Lagopoulos L., et al. A Fas agonist induces high levels of apoptosis in haematological malignancies. Leuk Res 30 (2006) 415