The novel triterpenoid CDDO and its derivatives induce apoptosis by disruption of intracellular redox balance

Cancer Research

Volumn 63, Issue 17, 2003, Pages 5551-5558

  Ikeda, Takashi ^a   Sporn, Michael ^b   Honda, Tadashi ^c   Gribble, Gordon W ^c   Kufe, Donald ^a,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c Dartmouth College   (United States)

^d DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 CYANO 3,12 DIOXOOLEAN 1,9 DIEN 28 OIC ACID IMIDAZOLIDE ESTER; 2 CYANO 3,12 DIOXOOLEAN 1,9 DIEN 28 OIC ACID METHYL ESTER; 2 CYANO 3,12 DIOXOOLEANA 1,9 DIEN 28 OIC ACID; ACETYLCYSTEINE; CASPASE 3; CASPASE 8; CYSTEINE; CYTOCHROME C; GLUTATHIONE; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TRITERPENOID; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL STRAIN U937; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DRUG SCREENING; ENZYME ACTIVATION; HUMAN; HUMAN CELL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL;

ANTIOXIDANTS; APOPTOSIS; CASPASE 3; CASPASE 8; CASPASE 9; CASPASES; CYTOCHROME C GROUP; ENZYME ACTIVATION; GLUTATHIONE; HUMANS; INTRACELLULAR MEMBRANES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MEMBRANE POTENTIALS; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; OLEANOLIC ACID; OXIDANTS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SERPINS; U937 CELLS; VIRAL PROTEINS;

EID: 0141815939     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (47)

1. Suh, N., Wang, Y., Honda, T., Gribble, G. W., Dmitrovsky, E., Hickey, W. F., Maue, R. A., Placc, A. E., Porter, D. M., Spinella, M. J., Williams, C. R., Wu, G., Daunenberg, A. J., Flanders, K. C., Letterio, J. J., Mangelsdorf, D. J., Nathan, C. F., Nguyen, L., Porter, W. W., Ren, R. F., Roche, N. S., Subbaramaiah, K., and Sporn, M. B. A novel synthetic oleanane triterpenoid, 2-cyno-3, 12-dioxoolean-1, 9-dien-28-oic acid, with potent differentiating, antiproliferative and anti-inflammatory activity. Cancer Res., 59: 336-341, 1999.
2. Ito, Y., Pandey, P., Place, A., Sporn, M., Gribble, G., Honda, T., Kharbanda, S., and Kufe, D. The novel triterpenoid CDDO induces apoptosis of human myeloid leukemia cells by a caspase-8 dependent mechanism. Cell Growth Differ., 11: 261-267, 2000.
3. Konopleva, M., Tsao, T., Ruvolo, P., Stiouf, I., Estrov, Z., Leysath, C. E., Zhao, S., Harris, D., Chang, S., Jackson, C. E., Munsell, M., Suh, N., Gribble, G., Honda, T., May, W. S., Sporn, M. B., and Andreeff, M. Novel triterpenoid CDDO-Me is a potent inducer of apoptosis and differentiation in acute myelogenous leukemia. Blood, 99: 326-335, 2002.
4. Stadheim, T. A., Suh, N., Ganju, N., Sporn, M. B., and Eastman, A. The novel triterpenoid 2-cyano-3, 12-dioxooleana-1, 9-dien-28-oic acid (CDDO) potently enhances apoptosis induced by tumor necrosis factor in human leukemia cells. J. Biol. Chem., 277: 16448-16455, 2002.
5. Ito, Y., Pandey, P., Sporn, M., Datta, R., Kharbanda, S., and Kufe, D. The novel triterpenoid CDDO induces apoptosis and differentiation of human osteosarcoma cells by a caspase-8 dependent mechanism. Mol. Pharmacol., 59: 1094-1099, 2001.
6. Kim, K., Lotan, R., Yue, P., Sporn, M., Suh, N., Gribble, G., Honda, T., Wu, G., Hong, W., and Sun, S. Identification of a novel synthetic triterpenoid, methyl-2-cyano-3, 12-dioxoolcana-1, 9-dien-28-oate, that potently induces caspase-mediated apoptosis in human lung cancer cells. Mol. Cancer Ther., 1: 177-184, 2002.
7. Pedersen, I., Kitada, S., Schimmer, A., Kim, Y., Zapata, J., Charnoneau, L., Rassenti, L., Andreeff, M., Bennett, F., Sporn, M., Liotta, L., Kipps, T., and Reed, J. The triterpenoid CDDO induces apoptosis in refractory CLLB cells. Blood, 100: 2965-2972, 2002.
8. Wang, Y., Porter, W. W., Suh, N., Honda, T., Gribble, G. W., Leesnitzer, L. M., Plunket, K. D., Mangelsdorf, D. J., Blanchard, S. G., Willson, T. M., and Sporn, M. B. A synthetic triterpenoid, 2-cyano-3, 12-dioxooleana-1, 9-dien-28-oic acid (CDDO), is a ligand for the peroxisome proliferator-activated receptor gamma. Mol. Endocrinol., 14: 1550-1556, 2000.
9. Liu, X., Kim, C., 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.
10. Yang, J., Liu, X., Bhalla, K., Kackyung Kim, C., 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 (Wash. DC), 275: 1129-1132, 1997.
11. 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 (Wash. DC), 275: 1132-1136, 1997.
12. 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.
13. Srinivasula, S., Ahmad, M., Alnemri, T., and Alnemri, E. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol. Cell, 1: 949-957, 1998.
14. Muzio, M., Chinnaiyan, A. M., Kischkel, F. C., O'Rourke, K., Shevchenko, A., Ni, J., Scaffidi, C., Bretz, J. D., Zhang, M., Gentz, R., Mann, M., Krammer, P. H., Peter, M. E., and Dixit, V. M. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell, 85: 817-827, 1996.
15. Boldin, M., Goncharov, T., Goltsev, Y., and Wallach, D. Involvement of MACH, a novel MORTI/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell-death. Cell, 85: 803-815, 1996.
16. Stennicke, H., Jurgenmeier, J., Shin, H., Deveraux, B., Wolf, X., Yang, X., Zhou, Q., Ellerby, H., Ellerby, L., Bredesen, D., Green, D., Reed, J., Froelich, C., and Salvesen, G. Pro-caspase-3 is a major physiologic target of caspase-8. J. Biol. Chem., 273: 27084-27090, 1998.
17. Luo, X., Budiharjo, H., Zou, H., Slauhter, C., and Wang, X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell, 94: 481-490, 1998.
18. Li, H., Zhu, H., Xu, C-j., and Yuan, J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the fas pathway of apotosis. Cell, 94: 491-501, 1998.
19. Kroemer, G., and Reed, J. C. Mitochondrial control of cell death. Nat. Med., 6: 513-519, 2000.
20. Herr, I., and Debatin, K. M. Cellular stress response and apoptosis in cancer therapy. Blood, 98: 2603-2614, 2001.
21. L by cytotoxic drug exposure confers resistance to ionizing radiation-induced internucleosomal DNA fragmentation. Cell Growth Differ., 6: 363-370, 1995.
22. Bunz, F. Cell death and cancer therapy. Curr. Opin. Pharmacol., 1: 337-341, 2001.
23. Datta, R., Kojima, H., Banach, D., Bump, N. J., Talanian, R. V., Alnemri, E. S., Weichselbaum, R. R., Wong, W. W., and Kufe, D. W. Activation of a CrmA-insensitive, p35-sensitive, pathway in ionizing radiation-induced apoptosis. J. Biol. Chem., 272: 1965-1969, 1997.
24. Yoshida, K., Weichselbaum, R., Kharbanda, S., and Kufe, D. Role for Lyn tyrosine kinase as a regulator of stress-activated protein kinase activity in response to DNA damage. Mol. Cell. Biol., 20: 5370-5380, 2000.
25. Karp, D. R., Shimooku, K., and Lipsky, P. E. Expression of gamma-glutamyl transpeptidase protects ramos B cells from oxidation-induced cell death. J. Biol. Chem., 276: 3798-3804, 2001.
26. Lizard, G., Gueldry, S., Sordet, O., Monier, S., Athias, A., Miguet, C., Bessede, G., Lemaire, S., Solary, E., and Gambert, P. Glutathione is implied in the control of 7-ketocholesterol-induced apoptosis, which is associated with radical oxygen species production. FASEB J., 12: 1651-1663, 1998.
27. Shrieve, D. C., Bump, E. A., and Rice, G. C. Heterogeneity of cellular glutathione among cells derived from a murine fibrosarcoma or a human renal cell carcinoma detected by flow cytometric analysis. J. Biol. Chem., 263: 14107-14114, 1988.
28. Hulbert, P. B., and Yakubu, S. I. Monobromobimane: a substrate for the fluorimetric assay of glutathione transferase. J. Pharm. Pharmacol., 35: 384-386, 1983.
29. Shapiro, H. M. Membrane potential estimation by flow cytometry. Methods, 21: 271-279, 2000.
30. Davis, R. Signal transduction by the JNK group of MAP kinases. Cell, 103: 239-252, 2000.
31. Honda, T., Honda, Y., Favaloro, F. G., Jr., Gribble, G. W., Suh, N., Place, A. E., Rendi, M. H., and Sporn, M. B. A novel dicyanotriterpenoid, 2-cyano-3, 12-dioxooleana-1, 9(11)-dien-28-onitrile, active at picomolar concentrations for inhibition of nitric oxide production. Bio-org. Med. Chem. Lett., 12: 1027-1030, 2002.
32. Chen, Y. R., and Tan, T. H. The c-Jun N-terminal kinase pathway and apoptotic signaling (review). Int. J. Oncol., 16: 651-662, 2000.
33. Marchetti, P., Hirsch, T., Zamzami, N., Castedo, M., Decaudin, D., Susin, S. A., Masse, B., and Kroemer, G. Mitochondrial permeability transition triggers lymphocyte apoptosis. J. Immunol., 157: 4830-4836, 1996.
34. Briehl, M. M., Baker, A. F., Siemankowski, L. M., and Morreale, J. Modulation of antioxidant defenses during apoptosis. Oncol. Res., 9: 281-285, 1997.
35. Matsuyama, S., and Reed, J. C. Mitochondria-dependent apoptosis and cellular pH regulation. Cell Death Differ., 7: 1155-1165, 2000.
36. Matsuno-Yagi, A., and Hatefi, Y. Studies on the mechanism of oxidative phosphorylation. ATP synthesis by submitochondrial particles inhibited at F0 by venturicidin and organotin compounds. J. Biol. Chem., 268: 6168-6173, 1993.
37. Nordberg, J., and Arner, E. Reactive oxygen species, antioxidants, and mammalian thioredoxin system. Free Radic. Biol. Med., 31: 1287-1312, 2001.
38. Moran, L. K., Gutteridge, J. M., and Quinlan, G. J. Thiols in cellular redox signalling and control. Curr. Med. Chem., 8: 763-772, 2001.
39. Liu, W., Kato, M., Akhand, A. A., Hayakawa, A., Suzuki, H., Miyata, T., Kurokawa, K., Hotta, Y., Ishikawa, N., and Nakashima, I. 4-hydroxynonenal induces a cellular redox status-related activation of the caspase cascade for apoptotic cell death. J. Cell Sci., 113: 635-641, 2000.
40. 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: 47107-47115, 2001.
41. Tan, S., Somia, N., Maher, P., and Schubert, D. Regulation of antioxidant metabolism by translation initiation factor 2alpha. J. Cell Biol., 152: 997-1006, 2001.
42. 2. Proc. Natl. Acad. Sci. USA, 94: 11223-11237, 1997.
43. Sun, X., Wu, F., Datta, R., Kharbanda, S., and Kufe, D. Interaction between protein kinase C δ and the c-Abl tyrosine kinase in the cellular response to oxidative stress. J. Biol. Chem., 275: 7470-7473, 2000.
44. Sun, X., Majumder, P., Shioya, H., Wu, F., Kumar, S., Weichselbaum, R., Kharbanda, S., and Kufe, D. Activation of the cytoplasmic c-Abl tyrosine kinase by reactive oxygen species. J. Biol. Chem., 275: 17237-17240, 2000.
45. Kharbanda, S., Ren, R., Pandey, P., Shafinan, T. D., Feller, S. M., Weichselbaum, R. R., and Kufe, D. W. Activation of the c-Abl tyrosine kinase in the stress response to DNA-damaging agents. Nature (Lond.), 376: 785-788, 1995.
46. Gotoh, Y., and Cooper, J. Reactive oxygen specious and dimerization-induced activation of apoptosis signaling-regulating kinase 1 in tumor necrosis factor-α signaling transduction. J. Biol. Chem., 274: 17477-17482, 1998.
47. Saitoh, M., Nishitoh, H., Makiko, F., Takeda, K., Tobiume, K., Sawada, Y., Kawabata, M., Miyozono, K., and Ichijo, H. Mammalian thioredoxin is direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J., 17: 2596-2606, 1998.