Apoptosis induction by T-2 toxin: Activation of caspase-9, caspase-3, and DFF-40/CAD through cytosolic release of cytochrome c in HL-60 cells

Bioscience, Biotechnology and Biochemistry

Volumn 65, Issue 8, 2001, Pages 1741-1747

  Nagase, Masahiro ^a   Alam, M Murshedul ^a   Tsushima, Akiko ^a   Yoshizawa, Takumi ^a   Sakato, Nobuo ^a  

^a KAGAWA UNIVERSITY   (Japan)

Author keywords

Apoptosis; Caspase 3; Cytochrome c; DFF 45 ICAD; Trichothecene mycotoxins

Indexed keywords

CASP3 PROTEIN, HUMAN; CASP9 PROTEIN, HUMAN; CASPASE; CASPASE 3; CASPASE 9; CYTOCHROME C; DEOXYRIBONUCLEASE; DFFB PROTEIN, HUMAN; DNA FRAGMENT; DYES, REAGENTS, INDICATORS, MARKERS AND BUFFERS; T 2 TOXIN;

APOPTOSIS; ARTICLE; CELL STRAIN HL 60; CHEMISTRY; CYTOSOL; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; HUMAN; METABOLISM; MITOCHONDRION; NUCLEOSOME; POLYACRYLAMIDE GEL ELECTROPHORESIS; WESTERN BLOTTING;

APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CASPASE 9; CASPASES; CYTOCHROME C GROUP; CYTOSOL; DEOXYRIBONUCLEASES; DNA FRAGMENTATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME ACTIVATION; HL-60 CELLS; HUMANS; INDICATORS AND REAGENTS; MITOCHONDRIA; NUCLEOSOMES; T-2 TOXIN;

EID: 0035433553     PISSN: 09168451     EISSN: None     Source Type: Journal    
DOI: 10.1271/bbb.65.1741     Document Type: Article

References (41)

1. World Health Organization, Trichothecenes In "Selected Mycotoxins: Ochratoxins, Trichothecenes, Ergot (Environmental Health Criteria 105)", ed. WHO, Geneva, pp. 71-164 (1990).
2. Pestka, J. J. and Bondy, G. S., Immunotoxic effect of mycotoxins. In "Mycotoxins in Grain", eds. Miller, J. D. and Trenholm, H. L., Eagan Press, St. Paul, pp. 339-358 (1994).
3. Joffe, A. Z., Foodborne diseases: Alimentary toxic aleukia. In "Handbook of Foodborne Diseases of Biological Origin", ed. Rechcigl, M., CRC Press, Boca Raton, pp. 353-495 (1983).
4. Islam, Z., Nagase, M., Yoshizawa, T., Yamauchi, K., and Sakato, N., T-2 toxin induces thymic apoptosis in vivo in mice. Toxicol. Appl. Pharmacol., 148, 205-214 (1998).
5. Islam, Z., Nagase, M., Ota, A., Ueda, S., Yoshizawa, T., and Sakato, N., Structure-function relationship of T-2 toxin and its metabolites in inducing thymic apoptosis in vivo in mice. Biosci. Biotechnol. Biochem., 62, 1492-1497 (1998).
6. Alam, M. M., Nagase, M., Yoshizawa, T., and Sakato, N., Thymocyte apoptosis by T-2 toxin in vivo in mice is independent of Fas/Fas ligand system. Biosci. Biotechnol. Biochem., 64, 210-213 (2000).
7. Kroemer, G., Mitochondrial control of apoptosis: an overview. Biochem. Soc. Symp., 66, 1-15 (1999).
8. Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Li, F., Tomaselli, K. J., Debatin, K. M., Krammer, P. H., and Peter, M. E., Two CD95 (APO-I/Fas) signaling pathways. EMBO J., 17, 1675-1687 (1998).
9. Susin, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Snow, B. E., Brothers, G. M., Mangion, J., Jacotot, E., Costantini, P., Loeffler, M., Larochette, N., Goodlett, D. R., Aebersold, R., Siderovski, D. P., Penninger, J. M., and Kroemer, G., Molecular characterization of mitochondrial apoptosis-inducing factor. Nature, 397, 441-446 (1999).
10. Islam, Z., Oto, J., Nagase, M., Yoshizawa, T., and Sakato, N., Studies on the induction of apoptosis by T-2 toxin and its metabolites in HL-60 human promyelotic leukemia cells. Mycotoxins, 48, 45-51 (1999).
11. Ueno, Y., Umemori, K., Niimi, E., Tanuma, S., Nagata, S., Sugamata, M., Ihara, T., Sekijima, M., Kawai, K., Ueno, I., and Tashiro, F., Induction of apoptosis by T-2 toxin and other natural toxins in HL-60 human promyelotic leukemia cells. Nat. Toxins, 3, 129-137 (1995).
12. Yoshizawa, T. and Morooka, N., Deoxynivalenol and its acetate: new mycotoxin from Fuzarium roseum and moldy barley. Agric. Biol. Chem., 37, 2933-2934 (1973).
13. Yoshizawa, T. and Morooka, N., Comparative studies on microbial and chemical modifications of trichothecene mycotoxins. Appl. Microbiol., 30, 38-43 (1975).
14. Yoshizawa, T. and Morooka, N., Biological modification of trichothecene mycotoxins: acetylation and deacetylation of deoxynivalenols by Fusarium spp. Appl. Microbiol., 29, 54-58 (1975).
15. Yoshizawa, T., Ohtsubo, K., Sasaki, T., and Nakamura, K., Acute toxicity of satratoxins G and H in mice - a histopathological observation with special reference to the liver injury caused by satratoxin G. Proc. Jpn. Assoc. Mycotoxicol., 23, 53-57 (1986).
16. Shimura, M., Okuma, E., Yuo, A., Sasaki, T., Mukai, C., Takaku, F., and Ishizaka, Y., Room temperature-induced apoptosis of Jurkat cells sensitive to both caspase-1 and caspase-3 inhibitors. Cancer Lett., 132, 7-16 (1998).
17. Wick, W., Grimmel, C., Wagenknecht, B., Dichgans, J., and Weller, M., Betulinic acid-induced apoptosis in glioma cells: A sequential requirement for new protein synthesis, formation of reactive oxygen species, and caspase processing. J. Pharmacol. Exp. Ther., 289, 1306-1312 (1999).
18. Liu, X., Zou, H., Slaughter, C., and Wang, X., DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell, 89, 175-184 (1997).
19. m) and cytochrome c release are caspase independent. J. Immunol., 163, 4683-4693 (1999).
20. Earnshaw, W. C., Martins, L. M., and Kaufmann, S. H., Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem., 68, 383-424 (1999).
21. Dantzer, F., Schreiber, V., Niedergang, C., Trucco, C., Flatter, E., De La Rubia, G., Oliver, J., Rolli, V., Menissier-de Murcia, J., and de Murcia, G., Involvement of poly(ADP-ribose) polymerase in base excision repair. Biochimie, 81, 69-75 (1999).
22. Liu, X., Li, P., Widlak, P., Zou, H., Luo, X., Garrard, W. T., and Wang, X., The 40-kDa subunit of DNA fragmentation factor induces DNA fragmentation and chromatin condensation during apoptosis. Proc. Natl. Acad. Sci. USA, 95, 8461-8466 (1998).
23. Sakahira, H., Enari, M., and Nagata, S., Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature, 391, 96-99 (1998).
24. Garland, J. M. and Rudin, C., Cytochrome c induces caspase-dependent apoptosis in intact hematopoietic cells and overrides apoptosis suppression mediated by bcl-2, growth factor signaling, MAP-kinase-kinase, and malignant change. Blood, 92, 1235-1246 (1998).
25. Hengartner, M. O., The biochemistry of apoptosis. Nature, 407, 770-776 (2000).
26. Shifrin, V. I. and Anderson, P., Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. J. Biol. Chem., 274, 13985-13992 (1999).
27. Yang, G. H., Jarvis, B. B., Chung, Y. J., and Pestka, J. J., Apoptosis induction by the satratoxins and other trichothecene mycotoxins: relationship to ERK, p38 MAPK, and SAPK/JNK activation. Toxicol. Appl. Pharmacol., 164, 149-160 (2000).
28. 2-induced apoptosis of PC12 cells independent of ceramide formation. Neurol. Res., 22, 556-564 (2000).
29. Ishisaka, R., Kanno, T., Akiyama, J., Yoshioka, T., Utsumi, K., and Utsumi, T., Activation of caspase-3 by lysosomal cysteine proteases and its role in 2,2′-azobis-(2-amidinopropane)dihydrochloride (AAPH)-induced apoptosis in HL-60 cells. J. Biochem., 129, 35-41 (2001).
30. Counis, M. F. and Torriglia, A., DNases and apoptosis. Biochem. Cell Biol., 78, 405-414 (2000).
31. Natoli, G., Costanzo, A., Ianni, A., Templeton, D. J., Woodgett, J. R., Balsano, C., and Levrero, M., Activation of SAPK/JNK by TNF receptor 1 through a noncytotoxic TRAF2-dependent pathway. Science, 275, 200-203 (1997).
32. Liu, Z. G., Hsu, H., Goeddel, D. V., and Karin, M., Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-κB activation prevents cell death. Cell, 87, 565-576 (1996).
33. Roulston, A., Reinhard, C., Amiri, P., and Williams, L. T., Early activation of c-Jun N-terminal kinase and p38 kinase regulate cell survival in response to tumor necrosis factor α. J. Biol. Chem., 273, 10232-10239 (1998).
34. Ip, Y. T. and Davis, R. J., Signal transduction by the c-Jun N-terminal kinase (JNK)-from inflammation to development. Curr. Opin. Cell Biol., 10, 205-219 (1998).
35. Cannon, M., Jimenez, A., and Vazquez, D., Competition between trichodermin and several other sesquiterpene antibiotics for binding to their receptor site(s) on eukaryotic ribosomes. Biochem. J., 160, 137-145 (1976).
36. Middlebrook, J. L. and Leatherman, D. L., Specific association of T-2 toxin with mammalian cells. Biochem. Pharmacol., 38, 3093-3102 (1989).
37. Rizzo, A. F., Atroshi, F., Ahotupa, M., Sankari, S., and Elovaara, E., Protective effect of antioxidants against free radical-mediated lipid peroxidation induced by DON or T-2 toxin. J. Vet. Med. A, 41, 81-90 (1994).
38. Mezes, M., Barta, M., and Nagy, G., Comparative investigation on the effect of T-2 mycotoxin on lipid peroxidation and antioxidant status in different poultry species. Res. Vet. Sci., 66, 19-23 (1999).
39. Hawkins, R. A., Sangster, K., and Arends, M. J., Apoptotic death of pancreatic cancer cells induced by polyunsaturated fatty acids varies with double bond number and involves an oxidative mechanism. J. Pathol., 185, 61-70 (1998).
40. Ma, Y., Ogino, T., Kawabata, T., Li, J., Eguchi, K., and Okada, S., Cupric nitrilotriacetate-induced apoptosis in HL-60 cells association with lipid peroxidation, release of cytochrome c from mitochondria, and activation of caspase-3. Free. Radic. Biol. Med., 27, 227-233 (1999).
41. Whitelaw, M. L., McGuire, J., Picard, D., Gustafsson, J. A., and Poellinger, L., Heat shock protein hsp90 regulates dioxin receptor function in vivo. Proc. Natl. Acad. Sci. USA, 92, 4437-4441 (1995).