Direct interaction of GD3 ganglioside with mitochondria generates reactive oxygen species followed by mitochondrial permeability transition, cytochrome c release, and caspase activation

FASEB Journal

Volumn 14, Issue 7, 2000, Pages 847-858

  García Ruiz, Carmen ^a   Colell, Anna ^a   París, Raquel ^a   Fernandez Checa J C ^a  

^a HOSPITAL CLÍNIC   (Spain)

Author keywords

Apoptosis; Glutathione; Necrosis; Oxidative stress

Indexed keywords

CASPASE; CYTOCHROME C; GANGLIOSIDE GD3; GLUTATHIONE; REACTIVE OXYGEN METABOLITE;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; ENZYME ACTIVATION; MITOCHONDRION; NECROSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; REGULATORY MECHANISM;

ANIMALIA;

EID: 0343883506     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.14.7.847     Document Type: Article

References (50)

1. Green, D. R., and Reed, J. C. (1998) Mitochondria and apoptosis. Science 281, 1309-1312
2. Green, D. R. (1998) Apoptotic pathways: the roads to ruin. Cell 94, 695-698
3. Kroemer, G., Zamzami, M., and Susin, S. A. (1997) Mitochondrial control of apoptosis. Immunol. Today 18, 44-51
4. Jurgensmeier, J., Xie, Z., Deveraux, Q., Ellerby, L., Bredesen, D., and Reed, J. C. (1998) Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci. USA 95, 4997-5002
5. Liu, X., Kim, N. C., Yang, J., Jemmerson, R., and Wang, X. (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86, 147-152
6. Zou, H., Henzel, W. J., Liu, X., Lutschg, A., and Wang, X. (1997) Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase 3. Cell 90, 405-413
7. Samali, A., Zhivotovsky, B., Jones, D. P., and Orrenius, S. (1998) Detection of procaspase 3 in cytosol and mitochondria of various tissues. FEBS Lett. 431, 167-169
8. Mancini, M., Nicholson, D. W., Roy, S., Thornberry, N. A., Peterson, E. P., Casciola-Rosen, L. A., and Rosen, A. (1998) The caspase 3 precursor has a cytosolic and mitochondrial distribution: implications for apoptotic signalling. J. Cell Biol. 140, 1485-1495
9. Susin, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Brenner, C., Larochetter, N., Prevost, M. C., Alzari, P. M., and Kroemer, G. (1999) Mitochondrial release of caspase 2 and 9 during the apoptotic process. J. Exp. Med. 189, 381-394
10. Susin, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Snow, B. E., Brothers, G. M., Mangion, J., Jacotot, E., Constantini, P., Loeffler, M., Larochette, N., Goodlett, D. R., Aebersold, R., Siderovski, D. P., Penninger, J. M., and Kroemer, G. (1999) Molecular characterization of the mitochondrial apoptosis-inducing factor. Nature (London) 397, 441-446
11. Kluck, R. M., Bossy-Wetzel, E., Green, D. R., and Newmeyer, D. D. (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275, 1132-1136
12. Yang, J., Lin, X., Bhalla, K., Kim, C. N., Ibrado, A. M., Cai, J., Peng, T.-I., Jones, D. J., and Wang, X. (1997) Prevention of apoptosis by bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129-1132
13. Rossé, T., Olivier, R., Monney, L., Rager, M., Conus, S., Fellay, I., Jansen, B., and Borner, C. (1998) Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature (London) 391, 490-499
14. Lemasters, J. J. (1999) Mechanisms of hepatic toxicity. Necrapoptosis and the mitochondrial permeability transition: shared pathways to necrosis and apoptosis. Am. J. Physiol. 276, G1-G6
15. Petronilli, V., Constantini, P., Scorrano, R., Colonna, S., Pasamonti, S., and Bernardi, P. (1994) The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction of vicinal thiols. J. Biol. Chem. 269, 16638-16642
16. Echten, G., and Sandhoff, K. (1993) Ganglioside metabolism. Enzymology, topology and regulation. J. Biol. Chem. 268, 5341-5344
17. Bhunia, A. K., Arai, T., Bulkey, G., and Chatterjee, S. (1998) Lactosylceramide mediates tumor necrosis factor-induced intercellular adhesion molecule-1 (ICAM-1) expression and the adhesion of neutrophils in human umbilical endothelial cells. J. Biol. Chem. 273, 34349-34357
18. Testi, R. (1997) Sphingomyelin breakdown and cell fate. Trends. Biochem. Sci. 21, 468-471
19. Kolesnick, R., and Golde, D. W. (1994) The sphingomyelin pathway in tumor necrosis factor and interlenkin-1 signalling. Cell 77, 325-328
20. DeMaria, R., Lenti, L., Malisan, F., d'Agostino, F., Tomassini, B., Zeuner, A., Rippo, M. R., and Testi, R. (1997) Requirement for GD3 ganglioside in CD95-and ceramide-induced apoptosis. Science 277, 1652-1655
21. Goosens, V., Grooten, J., Vos, K., and Fiers, W. (1995) Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen species intermediates and their involvement in cytotoxicity. Proc. Natl. Acad. Sci. USA 92, 8115-8119
22. García-Ruiz, C., Colell, A., Marí, M., Morales, A, and Fernández-Checa, J. C. (1997) Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione. J. Biol. Chem. 272, 11369-11377
23. Gudz, T. I., Tserng, K. Y., and Hoppel, C. L. (1997) Direct inhibition of mitochondrial respiratory chain complex III by cell-permeable ceramide. J. Biol. Chem. 272, 24154-24158
24. Degli Esposti, M., & McLennan, H. (1998) Mitochondrial and cell produce reactive oxygen species in virtual anaerobiosis: relevance to ceramide-induced apoptosis. FEBS Lett. 430, 338-342
25. Morales, A., García-Ruiz, C., Miranda, M., Marí, M., Colell, A., Ardite, E., and Fernandez-Checa, J. C. (1997) Tumor necrosis factor increases hepatocellular glutathione by transcriptional regulation of the heavy subunit chain of γ-glutamylcysteine synthetase. J. Biol. Chem. 272, 30371-30379
26. Colell, A., García-Ruiz, C., Miranda, M., Ardite, E., Marí, M., Morales, A., Corrales, F., Kaplowitz, N., and Fernández-Checa, J. C. (1998) Selective glutathione depletion of mitochondria by ethanol sensitizes hepatocytes to tumor necrosis factor. Gastro-enterology 115, 1541-1551
27. García-Ruiz, C., Morales, A., Colell, A., Ballesta, A., Rodés, J., Kaplowitz, N., and Fernández-Checa, J. C. (1994) Effect of chronic ethanol feeding on glutathione and functional integrity of mitochondrial in periportal and perivenous rat hepatocytes. J. Clin. Invest. 94, 193-201
28. García-Ruiz, C., Colell, A., Morales, A., Kaplowitz, N., and Fernández-Checa, J. C. (1995) Role of oxidative stress generated from the mitochondrial electron transport chain and mitochondrial GSH status in loss of mitochondrial function and activation of transcription factor NF-êB: studies in isolated mitochondria and rat hepatocytes. Mol. Pharmacol. 48, 825-834
29. Fariss, M. W., and Reed, D. J. (1989) High performance liquid chromatography of thiols and disulfides: dinitrophenol derivatives. Methods Enzymol. 143, 101-109
30. Morales, A., Miranda, M., Sánchez-Reyes, A., Biete, A., and Fernández-Checa, J. C. (1998) Oxidative damage of mitochondrial and nuclear DNA induced by ionizing radiation in human hepatoblastoma cells. Int. J. Radiat. Oncol. Biol. Phys. 42, 191-203
31. Veldman, R. J., Klappe, K., Hoekstra, D., and Kok, J. W. (1998) Metabolism and apoptotic properties of elevated ceramide in HT29 rev cells. Biochem. J. 331, 563-569
32. Bossy-Wetzel, W., Newmeyer, D. D., and Green, D. R. (1998) Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J. 17, 37-49
33. Bradham, C. A., Qian, T., Streetz, K., Trautwein, C., Brenner, D. A., and Lemasters, J. J. (1998) The mitochondrial permeability transition is required for tumor necrosis factor á-induced apoptosis and cytochrome c release. Mol. Cell. Biol. 18, 6353-6364
34. Zhang, Z., Huang, L., Shulmeister, V. M., Chi, Y., Kim, K. K., Hung, L. W., Crofts, A. R., Berry, E. A., and Kim, S. H. (1998) Electron transfer by domain movement in cytochrome bcl. Nature (London) 392, 677-682
35. Ishisaka, R., Utsumi, T., Yabuki, M., Kanno, T., Furuno, T., Inoue, M., and Utsumi, K. (1998) Activation of caspase 3-like protease by digitonin-treated lysosomes. FEBS Lett. 435, 233-236
36. Hakomori, S. (1981) Glycosphingolipids in cellular interaction, differentiation and oncogenesis. Ann. Rev. Biochem. 50, 733-764
37. Karlsson, K. A. (1989) Animal glycosphingolipids as membrane attachment sites for bacteria. Ann. Rev. Biochem. 58, 309-350
38. Lavie, Y., Cao, H., Bursten, S. L., Giuliano, A. E., and Cabot, M. C. (1996) Accumulation of glucosylceramide in multidrug-resistant cancel cells. J. Biol. Chem. 271, 19530-19536
39. Lavie, Y., Cao, H., Volner, A., Lucci, A., Han, T., Geffen, V., Giuliano, A. E., and Cabot, M. C. (1997) Agents that reverse multidrug resistance, tamoxifen, verapamil and cyclosporin A, block glycosphingolipids metabolism by inhibiting ceramide glycosylation in human cancer cells. J. Biol. Chem. 272, 1682-1687
40. García-Ruiz, C., París, R., Colell, A., and Fernández-Checa, J. C. (1999) GD3 ganglioside mediates the oxidative stress and cytotoxicity in rat hepatocytes induced by acidic sphingomyelinase. Hepatology 30, 411A (abstr.).
41. Ghafourifar, P., Klein, S. D., Schucht, O., Schenk, U., Pruschy, M., Rocha, S., and Richter, C. (1999) Ceramide induces cytochrome c release from isolated mitochondria. Importance of mitochondrial redox state. J. Biol. Chem. 274, 6080-6084
42. Fernández-Checa, J. C., Kaplowitz, N., García-Ruiz, C., Colell, A., Miranda, M., Marí, M., Ardite, E., and Morales, A. (1997) GSH transport in mitochondria: defense against TNF-induced oxidative stress and alcohol-induced defect. Am. J. Physiol. 273, G7-G17
43. Fernández-Checa, J. C., Kaplowitz, N., García-Ruiz, C., and Colell, A. (1998) Mitochondrial glutathione. Importance and transport. Sem. Liver Dis. 18, 389-401
44. Shan, X., Jones, D. P., Hashmi, M., and Anders, M. W. (1993) Selective depletion of mitochondrial glutathione concentration by (R,S)-3-hydroxyl-4-pentenoate potentiates oxidative cell death. Chem. Res. Toxicol. 6, 75-81
45. DiMaria, R., Rippo, M. R., Schuchman, E. H., and Testi, R. (1998) Acidic sphingomyelinase is necessary for Fas-mediated GD3 ganglioside accumulation and efficient apoptosis of lymphoid cells. J. Exp. Med. 187, 897-902
46. Scorrano, L., Petronilli, V., DiLisa, F., and Bernardi, P. (1999) Commitment to apoptosis by GD3 ganglioside depends on opening of the mitochondrial permeability transition pore. J. Biol. Chem. 274, 22581-22585
47. Kristal, B. S., and Brown, A. (1999) Apoptogenic ganglioside GD3 directly induces the mitochondrial permeability transition. J. Biol. Chem. 274, 23169-23175
48. Matyas, G. R., and Morre, D. R. (1987) Subcellular distribution and biosynthesis of rat liver gangliosides. Biochim. Biophys. Acta 921, 599-614
49. Braun, J. S., Novak, R., Herzog, K. H., Bodner, S. M., Cleveland, J. L., and Toumanen, E. I. (1999) Neuroprotection by a caspase inhibitor in acute bacterial meningitis. Nat. Med. 5, 298-302
50. Cursio, R., Gugenheim, J., Ricci, J. E., Crenesse, D., Rostagno, P., Marson, L., Saint-Paul, M., Ferrua, B., and Auberger, P. (1999) A caspase inhibitor fully protects rats against lethal normothemia liver ischemia by inhibition of liver apoptosis. FASEB J. 13, 253-261