Citrinin-generated reactive oxygen species cause cell cycle arrest leading to apoptosis via the intrinsic mitochondrial pathway in mouse skin

Toxicological Sciences

Volumn 122, Issue 2, 2011, Pages 557-566

  Kumar, Rahul ^a   Dwivedi, Premendra D ^a   Dhawan, Alok ^a   Das, Mukul ^a   Ansari, Kausar M ^a  

^a CSIR INDIAN INSTITUTE OF TOXICOLOGY RESEARCH   (India)

Author keywords

Antioxidants; Apoptosis; Citrinin; Mouse skin; ROS

Indexed keywords

CASPASE 3; CASPASE 9; CITRININ; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYTOCHROME C; DNA; GLUTATHIONE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN P53; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; FEMALE; LIPID PEROXIDATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN CARBONYLATION; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN SECRETION; SKIN TOXICITY;

ALPHA-TOCOPHEROL; ANIMALS; ANTIOXIDANTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BIOLOGICAL MARKERS; BUTYLATED HYDROXYANISOLE; CASPASE 9; CELL DIVISION; CITRININ; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; G1 PHASE; M PHASE CELL CYCLE CHECKPOINTS; MICE; MITOCHONDRIA; OXIDATIVE STRESS; POLY(ADP-RIBOSE) POLYMERASES; QUERCETIN; REACTIVE OXYGEN SPECIES; SKIN;

EID: 80051695193     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr143     Document Type: Article

References (40)

1. Abbas, T., and Dutta, A. (2009). p21 in cancer: intricate networks and multiple activities. Nat. Rev. Cancer. 9, 400-414.
2. Aleo, M. D., Wyatt, R. D., and Schnellmann, R. G. (1991). The role of altered mitochondrial function in citrinin-induced toxicity to rat renal proximal tubule suspensions. Toxicol. Appl. Pharmacol. 109, 455-463.
3. Arai, M., and Hibino, T. (1983). Tumorigenicity of citrinin in male F344 rats. Cancer Lett. 17, 281-287.
4. Berton, T. R., Conti, C. J., Mitchell, D. L., Aldaz, C. M., Lubet, R. A., and Fischer, S. M. (1998). The effect of vitamin E acetate on ultraviolet-induced mouse skin carcinogenesis. Mol. Carcinog. 23, 175-184.
5. CAST. (2003). Mycotoxins: Risks in Plant, Animal, and Human Systems. Council of Agricultural Science and Technology. Task force report No. 139. CAST, Ames, IA.
6. Cavin, C., Delatour, T., Marin-Kuan, M., Holzhauser, D., Higgins, L., Bezencon, C., Guignard, G., Junod, S., Richoz-Payot, J., Gremaud, E., et al. (2007). Reduction in antioxidant defences may contribute to Ochratoxin A toxicity and carcinogenicity. Toxicol. Sci. 96, 30-39.
7. Cecconi, F. (1999). Apaf1 and the apoptotic machinery. Cell Death Differ. 6, 1087-1098.
8. Chan, W. H. (2007). Citrinin induces apoptosis via a mitochondria-dependent pathway and inhibition of survival signals in embryonic stem cells, and causes developmental injury in blastocysts. Biochem. J. 404, 317-326.
9. Chang, C. H., Yu, F. Y., Wu, T. S., Wang, L. T., and Liu, B. H. (2011). Mycotoxin citrinin induced cell cycle G2/M arrest and numerical chromosomal aberration associated with disruption of microtubule formation in human cells. Toxicol. Sci. 119, 84-92.
10. Chen, C. C., and Chan, W. H. (2009). Inhibition of citrinin-induced apoptotic biochemical signaling in human hepatoma G2 cells by resveratrol. Int. J. Mol. Sci. 10, 3338-3357.
11. Cherouny, P. H., Ghodgaonkar, R. B., Gurtner, G. H., and Dubin, N. H. (1989). The effect of the antioxidant, butylated hydroxy anisole, on peroxideinduced and spontaneous activity of the uterus from the pregnant rat. Biol. Reprod. 41, 98-103.
12. Das, M., Ansari, K. M., Dhawan, A., Shukla, Y., and Khanna, S. K. (2005b). Correlation of DNA damage in Epidemic Dropsy patients to carcinogenic potential of argemone oil and isolated sanguinarine alkaloid in mice. Int. J. Cancer. 117, 709-717.
13. Das, M., Babu, K., Reddy, N., and Srivastava, L. M. (2005a). Oxidative damage of plasma proteins and lipids in Epidemic Dropsy patients: Alterations in antioxidant status. Biochem. Biophys. Acta. 1722, 209-217.
14. Das, M., and Ray, P. K. (1988). Lipid antioxidant properties of quercetin in vitro. Biochem. Int. 17, 203-209.
15. Ellman, G. L., and Lysko, H. (1967). Disulfide and sulfhydryl compounds in TCA extracts of human blood and plasma. J. Lab. Clin. Med. 70, 518-527.
16. Essers, J., Vermeulen, W., and Houtsmuller, A. B. (2006). DNA damage repair: anytime, anywhere? Curr. Opin. Cell. Biol. 18, 240-246.
17. FAO. (1990). Manuals of Food Quality Control. 10. Training in Mycotoxin Analysis. Food and Agriculture Organization of the United Nations, Rome, Italy.
18. Fridovich, I., and Freeman, B. (1986). Antioxidant defenses in the lung. Annu. Rev. Physiol. 48, 693-702.
19. Gutteridge, J. M., and Halliwell, B. (2010). Antioxidants: molecules, medicines, and myths. Biochem. Biophys. Res. Commun. 393, 561-564.
20. Jiang, L., Sheikh, M. S., and Huang, Y. (2010). Decision making by p53: life versus death. Mol. Cell. Pharmacol. 2, 69-77.
21. Jurgensmeier, J. M., Xie, Z., Deveraux, Q., Ellerby, L., Bredesen, D., and Reed, J. C. (1998). Bax directly induces release of cytochome c from isolated mitochondria. Proc. Natl. Acad. Sci. U. S. A. 95, 4997-5002.
22. Kemppainen, B. W., Riley, R. T., Joyave, J. L., and Hoerr, F. J. (1987). In vitro percutaneous penetration and metabolism of [3H] T-2 toxin: comparison of human, rabbit, guinea pig and rat. Toxicon 25, 185-194.
23. Kemppainen, B. W., Riley, R. T., and Pace, J. G. (1988). Skin absorption as a route of exposure for aflatoxin and trichothecenes. J. Toxicol. 7, 95-120.
24. Khan, M. A., Tania, M., Zhang, D., and Chen, H. (2010). Antioxidant enzymes and cancer. Chin. J. Cancer Res. 22, 87-92.
25. Kitabatake, N., Doi, E., and Trivedi, A. B. (1993). Toxicity evaluation of the mycotoxins, citrinin and ochatoxin A, using several animal cell lines. Comp. Biochem. Physiol. C. 105, 429-433.
26. Knasmüller, S., Cavin, C., Chakraborty, A., Darroudi, F., Majer, B. J., Huber, W. W., and Ehlich, V. A. (2004). Structurally related mycotoxins ochratoxin A, ochratoxin B, and citrinin differ in their genotoxic activities and in their mode of action in human-derived liver (HepG2) cells: implications for risk assessment. Nutr. Cancer 50, 190-197.
27. Liu, B. H., Yu, F. Y., Wu, T. S., Li, S. Y., Su, M. C., Wang, M. C., and Shih, S. M. (2003). Evaluation of genotoxic risk and oxidative DNA damage in mammalian cells exposed to mycotoxins, patulin and citrinin. Toxicol. Appl. Pharmacol. 191, 255-263.
28. Martin, K. R., and Barrett, J. C. (2002). Reactive oxygen species as doubleedged swords in cellular processes: low-dose cell signaling versus high-dose toxicity. Hum. Exp. Toxicol. 21, 71-75.
29. Rastogi, S., Dogra, R. K. S., Khanna, S. K., and Das, M. (2006). Skin tumorigenic potential of aflatoxin B1 in mice. Food Chem. Toxicol. 44, 670-677.
30. Rotruck, J. T., Pope, A. L., Ganther, H. E., Swanson, A. B., Hafeman, D. G., and Hoekstra, W. G. (1973). Selenium: biochemical role as a component of glutathione peroxidase. Science 179, 588-590.
31. Saxena, N., Ansari, K. M., Kumar, R., Dhawan, A., Dwivedi, P. D., and Das, M. (2009). Patulin causes DNA damage leading to cell cycle arrest and apoptosis though modulation of Bax, p53 and p21/WAF1 proteins in skin of mice. Toxicol. Appl. Pharmacol. 234, 192-201.
32. Scholz, R. W., Graham, K. S., Gumpricht, E., and Reddy, C. C. (1989). Mechanism of interaction of vitamin E and glutathione in the protection against membrane lipid peroxidation. Ann. N. Y. Acad. Sci. 570, 514-517.
33. Singh, N. P., Mecony, M. T., Tice, R. R., and Schneider, E. L. (1998). A simple technique of quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 175, 184-191.
34. Sinha, A. K. (1972). Colorimetric assay of catalase. Anal. Biochem. 47, 389-394.
35. Utley, G. H., Bernheim, F., and Hochstein, P. (1967). Effect of sulphydryl reagents on peroxidation in microsomes. Arch. Biochem. Biophys. 118, 29-32.
36. Vrabcheva, T., Usleber, E., Dietrich, R., and Märtlbauer, E. (2000). Cooccurrence of ochratoxin A and citrinin in cereals from Bulgarian villages with a history of Balkan endemic nephropathy. J. Agric. Food Chem. 48, 2483-2488.
37. Wang, T. S., Hsu, T. Y., Chung, C. H., Wang, A. S. S., Bau, D. T., and Jan, K. Y. (2001). Arsenite induces oxidatide DNA adducts and DNAprotein cross links in mammalian cells. Free Radic. Biol. Med. 31, 321-330.
38. WHO. (1998). Safety Evaluation of Certain Mycotoxins in Food Prepared by 49th meeting of JECFA Food Additives Series: 47. WHO, Geneva, Switzerland.
39. Xu, B. J., Jia, X. Q., Gu, L. J., and Sung, C. K. (2006). Review on the qualitative and quantitative analysis of the mycotoxin citrinin. Food Control 17, 271-285.
40. Yu, F. Y., Liao, Y. C., Chang, C. H., and Liu, B. H. (2006). Citrinin induces apoptosis in HL-60 cells via activation of the mitochondrial pathway. Toxicol. Lett. 161, 143-151.