Different apoptotic pathways induced by zearalenone, T-2 toxin and ochratoxin A in human hepatoma cells

Toxicology

Volumn 254, Issue 1-2, 2008, Pages 19-28

  Bouaziz, Chayma ^a   Sharaf el dein, Ossama ^b   El Golli, Emna ^a   Abid Essefi, Salwa ^a   Brenner, Catherine ^b   Lemaire, Christophe ^b   Bacha, Hassen ^a  

^a Faculty of Dentistry   (Tunisia)

^b LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

Author keywords

Caspases; Mitochondria; Mycotoxins; p53; ROS

Indexed keywords

APOPTOSIS INDUCING FACTOR; CASPASE; CYTOCHROME C; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; OCHRATOXIN; PIFITHRIN ALPHA; PROTEIN BAX; PROTEIN P53; REACTIVE OXYGEN METABOLITE; T 2 TOXIN; ZEARALENONE;

APOPTOSIS; ARTICLE; CELL DEATH; CELL STRAIN HEPG2; CONTROLLED STUDY; DNA FRAGMENTATION; ENZYME ACTIVATION; HEPATOMA CELL; HUMAN; HUMAN CELL; MEMBRANE POTENTIAL; MITOCHONDRION; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SECRETION; WESTERN BLOTTING;

APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CASPASES; CELL LINE, TUMOR; DNA FRAGMENTATION; ENZYME ACTIVATION; HUMANS; LIVER NEOPLASMS; MEMBRANE POTENTIAL, MITOCHONDRIAL; OCHRATOXINS; REACTIVE OXYGEN SPECIES; T-2 TOXIN; TUMOR SUPPRESSOR PROTEIN P53; ZEARALENONE;

ANIMALIA;

EID: 56049092723     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2008.08.020     Document Type: Article

References (53)

1. Abid-Essefi S., Baudrimont I., Hassen W., Ouanes Z., Mobio T.A., Anane R., Creppy E.E., and Bacha H. DNA fragmentation, apoptosis and cell cycle arrest induced by zearalenone in cultured DOK, Vero and Caco-2 cells: prevention by Vitamin E. Toxicology 192 (2003) 237-248
2. Abid-Essefi S., Ouanes Z., Hassen W., Baudrimont I., Creppy E.E., and Bacha H. Cytotoxicity, inhibition of DNA and protein syntheses and oxidative damage in cultured cells exposed to zearalenone. Toxicol. In Vitro 18 4 (2004) 467-474
3. Albano E. Oxidative mechanisms in the pathogenesis of alcoholic liver disease. Mol. Asp. Med. 29 (2008) 9-16
4. Apel K., and Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal Transduction. Annu. Rev. Plant. Biol. 55 (2004) 373-399
5. Ardestani A., Yazdanparast R., and Sarraf Nejad A. 2-Deoxy-d-ribose-induced oxidative stress causes apoptosis in human monocytic cells: prevention by pyridoxal-50-phosphate. Toxicol. In Vitro 22 (2008) 968-979
6. Arnoult D., Gaume B., Karbowski M., Sharpe J.C., Cecconi F., and Youle R.J. Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. EMBO J. 22 17 (2003) 4385-4399
7. Ayed-Boussema I., Ouanes Z., Bacha H., and Abid S. Toxicities induced in cultured cells exposed to Zearalenone: apoptosis or mutagenesis?. J. Biochem. Mol. Toxicol. 21 3 (2007) 136-144
8. Bennett J.W., and Klich M. Mycotoxins. Clin. Microbiol. Rev. 16 3 (2003) 497-516
9. Bindokas V.P., Jordan J., Lee C.C., and Miller R.J. Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J. Neurosci. 16 (1996) 1324-1336
10. Bradford M. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal. Biochem. 72 (1976) 248-254
11. Canady, R.A., Coker, R.D., Egan, S.K., Krska, R., Olsen, M., Resnik, S., Schlatter, J., 2001. T-2 and HT-2 toxins. In: Joint FAO/WHO Expert Committee on Food Additives (JECFA) (Eds.), Safety Evaluation of Certain Mycotoxins in Food, International Program of Chemical Safety (IPCS), WHO Food Additives Series 47, Geneva, pp. 557-597.
12. Cao G., Clark R.S., Pei W., Yin W., Zhang F., Sun F.Y., Graham S.H., and Chen J. Translocation of apoptosis-inducing factor in vulnerable neurons after transient cerebral ischemia and in neuronal cultures after oxygen-glucose deprivation. J. Cereb. Blood Flow Metab. 23 (2003) 1137-1150
13. CAST, 2003. Mycotoxins risks in plant, animal and human systems, Task Force Report, No. 139. Council for Agricultural Science and Technology, Ames, Iowa, pp. 1-191.
14. Chen Q., Gong B., and Almasan A. Distinct stages of cytochrome c release from mitochondria: evidence for a feedback amplification loop linking caspase activation to mitochondrial dysfunction in genotoxic stress induced apoptosis. Cell Death Differ. 7 2 (2000) 227-233
15. Creppy E.E. Update of survey, regulation and toxic effects of mycotoxins in Europe. Toxicol. Lett. 127 1-3 (2002) 19-28
16. Daugas E., Susin S.A., Zamzami N., Ferri K.F., Irinopoulou T., Larochette N., Prévost M.C., Leber B., Andrews D., Penninger J., and Kroemer G. Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J. 14 (2000) 729-739
17. Deniaud A., Sharaf el dein O., Maillier E., Poncet D., Kroemer G., Lemaire C., and Brenner C. Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis. Oncogene. 27 3 (2008) 285-299
18. El Golli E., Hassen W., Bouslimi A., Bouaziz C., Ladjimi M.M., and Bacha H. Induction of Hsp 70 in Vero cells in response to mycotoxins cytoprotection by sub-lethal heat shock and by Vitamin E. Toxicol. Lett. 166 2 (2006) 122-130
19. Finlan L.E., and Hupp T.R. The life cycle of p53: a key target in drug development. In: Los M., and Gibson S.B. (Eds). Apoptotic Pathways as Target for Novel Therapies in Cancer and Other Diseases (2005), Springer Academic Press, New York
20. Gutleb A.C., Morrison E., and Albertina J.M. Cytotoxicity Assays for mycotoxins produced by Fusarium strains: a review. Environ. Toxicol. Pharmacol. 11 (2002) 309-320
21. Hengartner M.O. The biochemistry of apoptosis. Nature 407 (2000) 770-776
22. Holme J.A., Gorria M., Arlt Volker M., Øvrebø S., Solhaug A., Tekpli X., Landvik Nina E., Huc L., Fardel O., and Lagadic-Gossmann D. Different mechanisms involved in apoptosis following exposure to benzo[a]pyrene in F258 and Hepa1c1c7 cells. Chem. Biol. Interact. 167 (2007) 41-55
23. Holme J.A., Morrison E., Samuelsen J.T., Wiger R., Lag M., Schwarze P.E., Bernhoft A., and Refsnes M. Mechanisms involved in the induction of apoptosis by T-2 and HT-2 toxins in HL-60 human promyelocytic leukaemia cells. Cell Biol. Toxicol. 19 (2003) 53-68
24. IARC, 1993. IARC Monographs on the evaluation of the carcinogenic risk of chemicals to humans, some naturally occurring substances: heterocyclic aromatic amines and mycotoxins. Lyon 56, 397-444.
25. Joza N., Susin S.A., Daugas E., Stanford W.L., Cho S.K., Li C.Y., Sasak T., Elia A.J., Cheng H.Y., Ravagnan L., Ferri K.F., Zamzami N., Wakeham A., Hakem R., Yoshida H., Kong Y.Y., Mak T.W., Zuniga-Pflucker J.C., Kroemer G., and Penninger J.M. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410 (2001) 549-554
26. Kamer I., Sarig R., Zaltsman Y., Niv H., Oberkovitz G., Regev L., Haimovich G., Lerenthal Y., Marcellus R.C., and Gross A. Proapoptotic BID is an ATM effector in the DNA-damage response. Cell 122 4 (2005) 593-603
27. Kidd V.J. Proteolytic activities that mediate apoptosis. Annu. Rev. Physiol. 60 (1998) 533-573
28. Komarov P.G., Komarova E.A., Kondratov R.V., Christov-Tselkov K., Coon J.S., Chernov M.V., and Gudkov A.V. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 285 5434 (1999) 1733-1737
29. Kroemer G., Galluzzi L., and Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87 1 (2007) 99-163
30. Le Bras M., Clément M.V., Pervaiz S., and Brenner C. Reactive oxygen species and the mitochondrial signalling pathway of cell death. Histol. Histopathol. 1 (2005) 205-219
31. Lioi M.B., Santoro A., Barbieri R., Salzano S., and Ursini M.V. Ochratoxin A and zearalenone: a comparative study on genotoxic effects and cell death induced in bovine lymphocytes. Mutat. Res. 557 1 (2004) 19-27
32. Mattia C.J., LeBel C.P., and Bondy S.C. Effects of toluene and its metabolites on cerebral reactive oxygen species generation. Biochem. Pharmacol. 42 4 (1991) 879-882
33. Nagase M., Alam M.M., Tsushima A., Yoshizawa T., and Sakato N. Apoptosis induction by T-2 tox activation of caspase-9 caspase-3 F DFF-40/CAD through cytosolic release of cytochrome c in F HL-60. Biosci. Biotechnol. Biochem. 65 (2001) 1741-1747
34. Niyo K.A., Richard J.L., and Tiffany L.H. Effect of T-2 mycotoxin ingestion on phagocytosis of Aspergillus fumigatus conidia by rabbit alveolar macrophages and on hematologic, serum biochemical, and pathologic changes in rabbits. Am. J. Vet. Res. 49 (1988) 1766-1773
35. Otera H., Ohsakaya S., Nagaura Z., Ishihara N., and Mihara K. Export of mitochondrial AIF in response to proapoptotic stimuli depends on processing at the intermembrane space. EMBO. J. 24 (2005) 1375-1386
36. Ouanes Z., Abid S., Ayed I., Anane R., Mobio T., Creppy E.E., and Bacha H. Induction of micronuclei by Zearalenone in Vero monkey kidney cells and in bone marrow cells of mice: protective effect of Vitamin E. Mutat. Res. 538 1-2 (2003) 63-70
37. Ouanes Z., Ayed-Boussema I., Baati T., Creppy E.E., and Bacha H. Zearalenone induces chromosome aberrations in mouse bone marrow: preventive effect of 17beta-estradiol, progesterone and Vitamin E. Mutat. Res. 565 2 (2005) 139-149
38. Petronilli V., Miotto G., Canton M., Brini M., Colonna R., Bernardi P., et al. Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys. J. 76 (1999) 725-734
39. Pfohl-Leszkowicz A., Chekir-Ghedira L., and Bacha H. Genotoxicity of zearalenone, an estrogenic mycotoxin: DNA adduct formation in female mouse tissues. Carcinogenesis 16 10 (1995) 2315-2320
40. Pfohl-Leszkowicz A., Petkova-Bocharova T., Chernozemsky I.N., and Castegnaro M. Balkan endemic nephropathy and associated urinary tract tumours: a review on aetiological causes and the potential role of mycotoxins. Food Addit. Contam. 3 (2002) 282-302
41. Poncet D., Boya P., Metivier D., Zamzami N., and Kroemer G. Cytofluorometric quantitation of apoptosis-driven inner mitochondrial membrane permeabilization. Apoptosis 8 (2003) 521-530
42. Richard J.L. Some major mycotoxins and their mycotoxicoses-an overview. Int. J. Food Microbiol. 119 1-2 (2007) 3-10
43. Richard J.L. Mycotoxins as immunomodulators in animal systems. In: Bray G.A., and Ryan D.H. (Eds). Mycotoxins, Cancer, and Health, Pennington Center Nutrition Series (1991), Louisiana State University Press, Baton Rouge, Louisiana 197-220
44. Rincheval V., Renaud F., Lemaire C., Godefroy N., Trotot P., Boulo V., Mignotte B., and Vayssière J.L. Bcl-2 can promote p53-dependent senescence versus apoptosis without affecting the G1/S transition. Biochem. Biophys. Res. Commun. 298 2 (2002) 282-288
45. Schollenberger M., Drochner W., and Müller H.M. Fusarium toxins of the scirpentriol subgroup: a review. Mycopathologia 164 3 (2007) 101-118
46. Sehata S., Kiyosawa N., Makino T., Atsumi F., Ito K., Yamoto T., Teranishi M., Baba Y., Uetsuka K., and Nakayama H.K. Morphological and microarray analysis of T-2 toxin-induced rat fetal brain lesion. Food Chem. Toxicol. 42 11 (2004) 1727-1736
47. Shier W.T., Shier A.C., Xie W., and Mirocha C.J. Structure-activity relationships for human estrogenic activity in zearalenone mycotoxins. Toxicon. 39 9 (2001) 1435-1438
48. Song G., Chen G.G., Chau D.K., Miao J., and Lai P.B. Bid exhibits S phase checkpoint activation and plays a pro-apoptotic role in response to etoposide-induced DNA damage in hepatocellular carcinoma cells. Apoptosis 5 (2008) 693-701
49. Tjamos S.E., Antoniou P.P., Kazantizidou A., Antonopoulos D.F., Papageorgiou I., and Tjamos E.C. Aspergillus niger and Aspergillus carbonarius in Corinth raisin and wine-producing vineyards in Greece: population composition, ochratoxin A production and chemical control. J. Phytopathol. 152 (2004) 250-255
50. Walrand S., Valeix S., Rodriguez C., Ligot P., Chassagne J., and Vasson M.P. Flow cytometry study of polymorphonuclear neutrophil oxidative burst: a comparison of three fluorescent probes. Clin. Chim. Acta 331 (2003) 103-110
51. Zaied, C., Abid, S., Zorgui, L., Bouaziz, C., Chouchane, S., Jomaa, M., Bacha, H., in press. Natural occurrence of ochratoxin A in Tunisian cereals. Food Control.
52. Zhivotovsky B., and Orrenius S. Caspase-2 function in response to DNA damage. Biochem. Biophys. Res. Commun. 331 3 (2005) 859-867
53. Zinkel S.S., Hurov K.E., Ong C., Abtahi F.M., Gross A., and Korsmeyer S.J. A role for proapoptotic BID in the DNA-damage response. Cell 122 4 (2005) 579-591