Decrease in intracellular superoxide sensitizes Bcl-2-overexpressing tumor cells to receptor and drug-induced apoptosis independent of the mitochondria

Cell Death and Differentiation

Volumn 10, Issue 11, 2003, Pages 1273-1285

  Clement M V ^a   Hirpara, J L ^a   Pervaiz, S ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Acidification; Apoptosis; Caspase activation; Superoxide; Tumor cells

Indexed keywords

CELL RECEPTOR; CYTOCHROME C; FAS ANTIGEN; GUANINE NUCLEOTIDE BINDING PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PROTEIN BCL 2; RAC1 PROTEIN; SUPEROXIDE;

ACIDIFICATION; APOPTOSIS; ARTICLE; CELL DEATH; CELL PH; CONTROLLED STUDY; DNA FLANKING REGION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; LEUKEMIA CELL LINE; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN SECRETION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR CELL;

ANTIGENS, CD95; APOPTOSIS; CASPASE 8; CASPASE 9; CASPASES; CELL LINE, TUMOR; DOWN-REGULATION; ENZYME INHIBITORS; HUMANS; HYDROGEN PEROXIDE; INTRACELLULAR FLUID; MITOCHONDRIA; NADPH OXIDASE; PROTO-ONCOGENE PROTEINS C-BCL-2; RAC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SUPEROXIDES; THIOBARBITURATES;

EID: 0242524405     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401302     Document Type: Article

References (39)

1. Wyllie AH (1981) Cell death: a new classification separating apoptosis from necrosis. In Cell Death in Biology and Pathology Bowen ID, Lockshin RA (eds) London: Chapman & Hall, pp. 9-34
2. Kroemer G and Reed JC (2000) Mitochondrial control of cell death. Nat. Med. 6: 513-519
3. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ, Debatin KM, Krammer PH and Peter ME (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17: 1675-1687
4. Gottlieb RA, Nordberg J, Skowronski E and Babior BM (1996) Apoptosis induced in Jurkat cells by several agents is preceded by intracellular acidification. Proc. Natl. Acad. Sci. USA 93: 654-658
5. Pervaiz S and Clement MV (2002) A permissive apoptotic environment: function of a decrease in intracellular superoxide anion and cytosolic acidification. Biochem. Biophys. Res. Commun. 290: 1145-1150
6. Matsuyama S and Reed JC (2000) Mitochondria-dependent apoptosis and cellular pH regulation. Cell Death Differ. 7: 1155-1165
7. Matsuyama S, Llopis J, Deveraux QL, Tsien RY and Reed JC (2000) Changes in intramitochondrial and cytosolic pH: early events that modulate caspase activation during apoptosis. Nat. Cell Biol. 2: 318-325
8. Hirpara JL, Clement MV and Pervaiz S (2001) Intracellular acidification triggered by mitochondrial-derived hydrogen peroxide is an effector mechanism for drug-induced apoptosis in tumor cells. J. Biol. Chem. 276: 514-521
9. Liu D, Martino G, Thangaraju M, Sharma M, Halwani F, Shen SH, Patel YC and Srikant CB (2000) Caspase-8-mediated intracellular acidification precedes mitochondrial dysfunction in somatostatin-induced apoptosis. J. Biol. Chem. 275: 9244-9250
10. Clement MV, Ponton A and Pervaiz S (1998) Apoptosis induced by hydrogen peroxide is mediated by decreased superoxide anion concentration and reduction of intracellular milieu. FEBS Lett. 440: 13-18
11. Adachi S, Cross AR, Babior BM and Gottlieb RA (1997) Bcl-2 and the outer mitochondrial membrane in the inactivation of cytochrome c during Fas-mediated apoptosis. J. Biol. Chem. 272: 21878-21882
12. Meisenholder GW, Martin SJ, Green DR, Nordberg J, Babior BM and Gottlieb RA (1996) Events in apoptosis. Acidification is downstream of protease activation and BCL-2 protection. J. Biol. Chem. 271: 16260-16262
13. Thangaraju M, Sharma K, Leber B, Andrews DW, Shen SH and Srikant CB (1999) Regulation of acidification and apoptosis by SHP-1 and Bcl-2. J. Biol. Chem. 274: 29549-29557
14. Pervaiz S, Cao J, Chao OS, Chin YY and Clement MV (2001) Activation of the RacGTPase inhibits apoptosis in human tumor cells. Oncogene 20: 6263-6268
15. Pervaiz S, Ramalingam JK, Hirpara JL and Clement MV (1999) Superoxide anion inhibits drug-induced tumor cell death. FEBS Lett. 459: 343-348
16. Clement MV and Stamenkovic I (1996) Superoxide anion is a natural inhibitor of FAS-mediated cell death. EMBO J. 15: 216-225
17. Thangaraju M, Sharma K, Liu D, Shen SH and Srikant CB (1999) Interdependent regulation of intracellular acidification and SHP-1 in apoptosis. Cancer Res. 59: 1649-1654
18. Engels IH, Stepczynska A, Stroh C, Lauber K, Berg C, Schwenzer R, Wajant H, Janicke RU, Porter AG, Belka C, Gregor M, Schulze-Osthoff K and Wesselborg W (2001) Caspase-8/FLICE functions as an executioner caspase in anticancer drug-induced apoptosis. Oncogene 19: 4563-4573
19. Fulda S, Meyer E, Friesen C, Susin SA, Kroemer G and Debatin KM (2001) Cell type specific involvement of death receptor and mitochondrial pathways in drug-induced apoptosis. Oncogene 20: 1063-1075
20. Korsmeyer SJ, Yin X-M, Oltvai Z, Veis-Novack DJ and Linette GP (1995) Reactive oxygen species and regulation of cell death by the Bcl-2 gene family. Biochem. Biophys. Acta 1271: 63-66
21. Steinman HM (1995) The Bcl-2 oncoprotein functions as a pro-oxidant. J. Biol. Chem. 270: 3487-3490
22. Voehringer DW and Meyn RE (2000) Redox aspects of Bcl-2 function. Antioxid. Redox Signal 2: 537-550
23. Clement MV and Pervaiz S (1999) Reactive oxygen intermediates regulate cellular response to apoptotic stimuli: an hypothesis. Free Radic. Res. 30: 247-252
24. Armstrong JS and Jones DP (2002) Glutathione depletion enforces the mitochondrial permeability transition and causes cell death in HL60 cells that overexpress Bcl-2. FASEB J. 10: 1263-1265
25. Babior BM (1999) NADPH oxidase: an update. Blood 93: 1464-1476
26. Kobayashi T, Tsunawaki S and Seguchi H (2001) Evaluation of the process for superoxide production by NADPH oxidase in human neutrophils: evidence for cytoplasmic origin of superoxide. Redox Rep. 6: 27-36
27. Irani K and Goldschmidt-Clermont PJ (1998) Ras, superoxide and signal transduction. Biochem. Pharmacol. 55: 1339-1346
28. Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, Fearon ER, Sundaresan M, Finkel T and Goldschmidt-Clermont PJ (1997) Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275: 1649-1652
29. Sundaresan M, Yu ZX, Ferrans VJ, Sulciner DJ, Gutkind JS, Irani K, Goldschmidt-Clermont PJ and Finkel T (1996) Regulation of reactive-oxygen-species generation in fibroblasts by Rac1. Biochem. J. 318 (Part 2): 379-382
30. Babior BM (2000) The NADPH oxidase of endothelial cells. IUBMB Life 50: 267-269
31. Hockenbery D, Oltvai ZN, Yin X-M, Milliman CL and Korsmeyer SJ (1993) Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75: 241-251
32. Nomura K, Imai H, Koumura T, Kobayashi T and Nakagawa Y (2000) Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis. Biochem. J. 351 (Part 1): 183-193
33. Huang DC, Tschopp J and Strasser A (2000) Bcl-2 does not inhibit cell death induced by the physiological Fas ligand: implications for the existence of type I and type II cells. Cell Death Differ. 7: 754-755
34. Huang DC, Hahne M, Schroeter M, Frei K, Fontana A, Villunger A, Newton K, Tschopp J and Strasser A (1999) Activation of Fas by FasL induces apoptosis by a mechanism that cannot be blocked by Bcl-2 or Bcl-x(L). Proc. Natl. Acad. Sci. USA 96: 14871-14876
35. Pervaiz S, Seyed MA, Hirpara JL, Clement MV and Loh KW (1999) Purified photoproducts of merocyanine 540 trigger cytochrome C release and caspase 8-dependent apoptosis in human leukemia and melanoma cells. Blood 93: 4096-4108
36. Musgrove EA and Hedley DW (1990) Measurement of intracellular pH. Methods Cell Biol. 33: 59-69
37. Gyllenhammar H (1987) Lucigenin chemiluminescence in the assessment of neutrophil superoxide production. J. Immunol. Methods 97: 209-220
38. Liochev SI and Fridovich I (1997) Lucigenin luminescence as a measure of intracellular superoxide dismutase activity in Escherichia coli. Proc. Natl. Acad. Sci. USA 94: 2891-2896
39. Li Y, Kuppusamy P, Roubaud V, Zweier JL and Trush MA (1998) Validation of lucigenin (bis-N-methylacridinium) as a chemilumigenic probe for detecting superoxide anion radical production by enzymatic and cellular systems. J. Biol. Chem. 273: 2015-2023