Bcl-2-mediated resistance to apoptosis is associated with glutathione- induced inhibition of AP24 activation of nuclear DNA fragmentation

Cancer Research

Volumn 58, Issue 23, 1998, Pages 5570-5576

  Wright, Susan C ^a   Wang, Hong ^a   Wei, Qi Sheng ^a   Kinder, David H ^b   Larrick, James W ^a  

^a Palo Alto Institute of Molecular Medicine   (United States)

^b OHIO NORTHERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC PROTEASE AP24; DNA FRAGMENT; GLUTATHIONE; PROTEIN BCL 2; SERINE PROTEINASE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL STRAIN HL 60; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LEUKEMIA CELL; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROTEIN DEGRADATION; ULTRAVIOLET RADIATION;

APOPTOSIS; CELL NUCLEUS; DNA DAMAGE; DNA, NEOPLASM; ENZYME ACTIVATION; GLUTATHIONE; HL-60 CELLS; HUMANS; NUCLEOSOMES; OLIGOPEPTIDES; PROTO-ONCOGENE PROTEINS C-BCL-2; SERINE ENDOPEPTIDASES; TUMOR NECROSIS FACTOR-ALPHA; ULTRAVIOLET RAYS;

EID: 0032401880     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (46)

1. Reed, J. C. Double identity for the proteins of the Bcl-2 family. Nature (Lond.), 387: 773-776, 1997.
2. Kroemer, G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med., 3: 614-619, 1997.
3. Chen-Levy, Z., and Cleary, M. L. Membrane topology of the Bcl-2 proto-oncogenic protein demonstrated in vivo. J. Biol. Chem., 265: 4929-4933, 1990.
4. Jacobson, M. D., Burne, J. F., King, M. P., Miyashita, T., Reed, J. C., and Raff, M. C. Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA. Nature (Lond.) 361: 365-369, 1993.
5. Bafy, G., Miyashita, T., Williamson, J. R., and Reed, J. C. Apoptosis induced by withdrawal of interleukin-3 (IL-3) from an IL-3-dependent hematopoietic cell line is associated with repartitioning of intracellular calcium and is blocked by enforced Bcl-2 oncoprotein production. J. Biol. Chem., 268: 6511-6519, 1993.
6. 2+ fluxes. Proc. Natl. Acad. Sci. USA, 91: 6569-6573, 1994.
7. Hockenbery, D. M., Oltvai, Z. N., Yin, X. -M., Milliman, C. L., and Korsmeyer, S. J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell, 75: 241-251, 1993.
8. Kane, D. J., Sarafian, T. A., Anton, R., Hahn, H., Gralla, E. B., Valentine, J. S., Ord, T., and Bredesen, D. E. Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science (Washington DC), 262: 1274-1277, 1993.
9. Ellerby, L. M., Ellerby, H. M., Park, S. M., Holleran, A. L., Murphy, A. N., Fiskum, G., Kane, D. J., Testa, M. P., Kayalar, C., and Bredesen, D. E. Shift of the cellular oxidation-reduction potential in neural cells expressing Bcl-2. J. Neurochem., 67: 1259-1267, 1996.
10. Chinnaiyan, A. M., Orth, K., O'Rourke, K., Duan, H., Poirier, G. G., and Dixit, V. M. Molecular ordering of the cell death pathway. J. Biol. Chem., 271: 4573-4576, 1996.
11. Boulakia, C. A., Chen, G., Ng, F. W. H., Todaro, J. G., Branton, P. E., Nicholson, D. W., Poirier, G. G., and Shore, G. C. Bcl-2 and adenovirus E1B 19 kDA protein prevent E1A-induced processing of CPP32 and cleavage of poly(ADP-ribose) polymerase. Oncogene, 12: 529-535, 1996.
12. Shimizu, S., Eguchi, Y., Kamiike, W., Matsuda, H., and Tsujimoto, Y. Bcl-2 expression prevents activation of the ICE protease cascade. Oncogene, 12: 2251-2257, 1996.
13. Zamzami, N., Susin, S. A., Marchetti, P., Hirsch, T., Gomez-Monterrey, I., Castedo, M., and Kroemer, G. Mitochondrial control of nuclear apoptosis. J. Exp. Med., 183: 1533-1544, 1996.
14. Susin, S. A., Zamzami, N., Castedo, M., Hirsch, T., Marchetti, P., Macho, A., Daugas, E., Geuskens, M., and Kroemer, G. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med., 184: 1331-1341, 1996.
15. Yang, J., Liu, X., Bhalla, K., Kim, C. N., Ibrado, A. M., Cai, J., Peng, T-I., Jones, D. P., and Wang, X. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science (Washington DC), 275: 1129-1132, 1997.
16. Kluck, R. M., Bossy-Wetzel, E., Green, D. R., and Newmeyer, D. D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science (Washington DC), 275: 1132-1136, 1997.
17. Liu, X., Kim, C. N., Yang, J., Jemmerson, R., and Wang, X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell, 86: 147-157, 1996.
18. Wright, S. C., Wei, Q. S., Zhong, J., Zheng, H., Kinder, D. H., and Larrick, J. W. Purification of a 24-kD protease from apoptotic tumor cells that activates DNA fragmentation. J. Exp. Med., 180: 2113-2123, 1994.
19. Wright, S. C., Schellenberger, U., Wang, H., Wang, Y., and Kinder, D. H. Chemotherapeutic drug activation of the AP24 protease in apoptosis: requirement for caspase 3-like-proteases. Biochem. Biophys. Res. Commun., 245: 797-803, 1998.
20. Wright, S. C., Schellenberger, U., Ji, L., Wang, H., and Larrick, J. W. Calmodulin-dependent protein kinase II mediates signal transduction in apoptosis. FASEB J., 11: 843-849, 1997.
21. Wright, S. C., Wei, Q. S., Kinder, D. H., and Larrick, J. W. Biochemical pathways of apoptosis: nicotinamide adenine dinucleotide-deficient cells are resistant to tumor necrosis factor or ultraviolet light activation of the 24-kD apoptotic protease and DNA fragmentation. J. Exp. Med., 183: 463-471, 1996.
22. Wright, S. C., Zheng, H., and Zhong, J. Tumor cell resistance to apoptosis due to a defect in the activation of sphingomyelinase and the 24 kDa apoptotic protease (AP24). FASEB J., 10: 325-332, 1996.
23. Wright, S. C., Schellenberger, U., Wang, H., Kinder, D. H., Talhouk, J. W., and Larrick, J. W. Activation of CPP32-like proteases is not sufficient to trigger apoptosis: inhibition of apoptosis by agents that suppress activation of AP24, but not CPP32-like activity. J. Exp. Med., 186: 1107-1117, 1997.
24. Gilbert, M. S., Saad, A. H., Rupnow, B. A., and Knox, S. J. Association of BCL-2 with membrane hyperpolarization and radioresistance. J. Cell. Physiol., 168: 114-122, 1996.
25. +-ATPase pump activity: correlation with radiation-induced programmed cell death. J. Cell. Physiol., 171: 299-304, 1997.
26. Naumovski, L., and Cleary, M. L. Bcl2 inhibits apoptosis associated with terminal differentiation of HL-60 myeloid leukemia cells. Blood, 83: 2261-2267, 1994.
27. Wright, S. C., Kumar, P., Tam, A. W., Shen, N., Varma, M., and Larrick, J. W. Apoptosis and DNA fragmentation precede TNF-induced cytolysis in U937 cells. J. Cell. Biochem., 48: 344-355, 1992.
28. Kinder, D. H., and Katzenellenbogen, J. A. Acrylamino boronic acids and difluoroborane analogues of amino acids: potent inhibitors of chymotrypsin and elastase. J. Med. Chem., 28: 1917-1925, 1985.
29. Kinder, D. H., Elstad, C. A., Meadows, G. G., and Ames, M. M. Antimetastatic activity of boro-amino acid analog protease inhibitors against B16BL6 melanoma in vivo. Invasion Metastasis, 12: 309-405, 1992.
30. Hyde, H., Borthwick, N. J., Janossy, G., Salmon, M., and Akbar, A. N. Upregulation of intracellular glutathione by fibroblast-derived factor(s): enhanced survival of activated T cells in the presence of low Bcl-2. Blood, 7: 2453-2460, 1997.
31. Ghibelli, L., Coppola, S., Rotilio, G., Lafavia, E., Maresca, V., and Ciriolo, M. R. Nonoxidative loss of glutathione in apoptosis via GSH extrusion. Biochem. Biophys. Res. Commun., 216: 313-320, 1995.
32. 2+-mediated endogenous endonuclease activation in apoptotic thymocytes. J. Immunol., 155: 5133-5139, 1995.
33. Slater, A. F. G., Stefan, C., Nobel, I., Maellaro, E., Bustamante, J., Kimland, M., and Orrenius, S. Nitrone spin traps and a nitroxide antioxidant inhibit a common pathway of thymocyte apoptosis. Biochem. J., 306: 771-778, 1995.
34. van den Dobbelsteen, D. J., Stefan, C., Nobel, I., Schlegel, J., Cotgreave, I. A., Orrenius, S., and Slater, A. R. G. Rapid and specific efflux of reduced glutathione during apoptosis induced by anti-Fas/APO-1 antibody. J. Biol. Chem., 271: 15420-15427, 1996.
35. Macho, A., Hirsch, T., Marzo, I., Marchetti, P., Dallaporta, B., Susin, S. A., Zamzami, N., and Kroemer, G. Glutathione depletion is an early and calcium elevation is a late event of thymocyte apoptosis. J. Immunol., 158: 4612-4619, 1997.
36. Backway, K. L., McCulloch, E. A., Chow, S., and Hedley, D. W. Relationship between mitochondrial permeability transition and oxidative stress during ara-C toxicity. Cancer Res., 57: 2446-2452, 1997.
37. Ghibelli, L., Fanelli, C., Rotilio, G., Latavia, E., Coppola, S., Colussi, C., Civitareale, P., and Ciriolo, M. R. Rescue of cells from apoptosis by inhibition of active GSH extrusion. FASEB J., 12: 479-486, 1998.
38. Mirkovic, N., Voehringer, D. W., Story, M. D., McConkey, D. J., McDonnell, T. J., and Meyn, R. E. Resistance to radiation-induced apoptosis in Bcl-2-overexpressing cells is reversed by depleting cellular thiols. Oncogene, 15: 1461-1470, 1997.
39. Voehringer, D. W., McConkey, D. J., McDonnell, T. J., Brisbay, S., and Meyn, R. E. Bcl-2 expression causes redistribution of glutathione to the nucleus. Proc. Natl. Acad. Sci. USA, 95: 2956-2960, 1998.
40. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., and Wang, X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell, 91: 479-489, 1997.
41. Nicholson, D. W., Ali, A., Thomberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A., Munday, N. A., Raju, S. M., Smulson, M E., Yamin, T. T., Yu, V. L., and Miller, D. K. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature (Lond.), 376: 37-43, 1995.
42. Buttke, T. M., and Sandstrom, P. A. Oxidative stress as a mediator of apoptosis. Immunol. Today, 15: 7-10, 1994.
43. Shimizu, S., Eguchi, Y., Kosaka, H., Kamiike, W., Matsuda, H., and Tsujimoto, Y. Prevention of hypoxia-induced cell death by Bcl-2 and Bcl-xL. Nature (Lond.), 374: 811-813, 1995.
44. Jacobsen, M. D., and Raff, M. C. Programmed cell death and Bcl-2 protection in very low oxygen. Nature (Lond.), 374: 814-816, 1995.
45. Liu, B., and Hannun, Y. A. Inhibition of the neutral magnesium-dependent sphingomyelinase by glutathione. J. Biol. Chem., 272: 16281-16287, 1997.
46. Meister, A. Glutathione, ascorbate, and cellular protection. Cancer Res., 54(Suppl.): 1969s-1975s, 1994.