Induction of oxidative stress response by the mycotoxin patulin in mammalian cells

Toxicological Sciences

Volumn 95, Issue 2, 2007, Pages 340-347

  Liu, Biing Hui ^a   Wu, Ting Shuan ^a   Yu, Feng Yih ^a   Su, Ching Chyuan ^b  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b TIAN SHENG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

Catalase; CuZn SOD; ERK1 2 signaling; Mycotoxin; Patulin; Reactive oxygen species; siRNA

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; FLUORESCENT DYE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYCOTOXIN; PATULIN; REACTIVE OXYGEN METABOLITE; SCAVENGER; SMALL INTERFERING RNA; TIRON;

ANIMAL TISSUE; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL STRAIN HEK293; CELL STRAIN HL 60; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; KIDNEY HOMOGENATE; LIPID PEROXIDATION; MAMMAL CELL; MEMBRANE DAMAGE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; CATALASE; CELL LINE, TUMOR; CELL SURVIVAL; CHO CELLS; CLONING, MOLECULAR; CRICETINAE; CRICETULUS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FREE RADICAL SCAVENGERS; HUMANS; LIPID PEROXIDATION; MICE; OXIDATIVE STRESS; PATULIN; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

ASPERGILLUS; MAMMALIA; PENICILLIUM;

EID: 33846538771     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfl156     Document Type: Article

References (45)

1. Ahmad, I. M., Aykin-Burns, N., Sim, J. E., Walsh, S. A., Higashikubo, R., Buettner, G. R., Venkataraman, S., Mackey, M. A., Flanagan, S. W., Oberley, L. W., et al. (2005). Mitochondrial O2*- and H2O2 mediate glucose deprivation-induced stress in human cancer cells. J. Biol. Chem. 280, 4254-4263.
2. Allen, R. G., and Tresini, M. (2000). Oxidative stress and gene regulation. Free Radic. Biol. Med. 28, 463-499.
3. Bai, J., Rodriguez, A. M., Melendez, J. A., and Cederbaum, A. I. (1999). Overexpression of catalase in cytosolic ormitochondrial compartment protects HepG2 cells against oxidative injury. J. Biol. Chem. 274, 26217-26224.
4. Barhoumi, R., and Burghardt, R. C. (1996). Kinetic analysis of the chronology of patulin- and gossypol-induced cytotoxicity in vitro. Fundam. Appl. Toxicol. 30, 290-297.
5. Bartsch, H., and Nair, J. (2004). Oxidative stress and lipid peroxidation-derived DNA-lesions in inflammation driven carcinogenesis. Cancer Detect. Prev. 28, 385-391.
6. Bindokas, V. P., Jordan, J., Lee, C. C., and Miller, R. J. (1996). Superoxide production in rat hippocampal neurons: Selective imaging with hydro-ethidine. J. Neurosci. 16, 1324-1336.
7. Cakir, Y., and Ballinger, S. W. (2005). Reactive species-mediated regulation of cell signaling and the cell cycle: The role of MAPK. Antioxid. Redox. Signal. 7, 726-740.
8. Chen, Z., Oberley, T. D., Ho, Y., Chua, C. C., Siu, B., Hamdy, R. C., Epstein, C. J., and Chua, B. H. (2000). Overexpression of CuZnSOD in coronary vascular cells attenuates myocardial ischemia/reperfusion injury. Free Radic. Biol. Med. 29, 589-596.
9. Doores, S. (1983). The microbiology of apples and apple products. Crit. Rev. Food Sci. Nutr. 19, 133-149.
10. Fliege, R., and Metzler, M. (1999). The mycotoxin patulin induces intra- and intermolecular protein crosslinks in vitro involving cysteine, lysine, and histidine side chains, and alpha-amino groups. Chem. Biol. Interact. 123, 85-103.
11. Fridovich, I. (1986). Biological effects of the superoxide radical. Arch. Biochem. Biophys. 247, 1-11.
12. Hempel, S. L., Buettner, G. R., O'Malley, Y. Q., Wessels, D. A., and Flaherty, D. M. (1999). Dihydrofluorescein diacetate is superior for detecting intracellular oxidants: Comparison with 2′,7′-dichlorodihydrofluorescein diacetate, 5(and 6)- carboxy-2′,7′-dichlorodihydrofluorescein diacetate, and dihydrorhodamine 123. Free Radic. Biol. Med. 27, 146-159.
13. Henle, E. S., and Linn, S. (1997). Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide. J. Biol. Chem. 272, 19095-19098.
14. Janero, D. R. (1990). Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic. Biol. Med. 9, 515-540.
15. Khanzode, S. S., Muddeshwar, M. G., Khanzode, S. D., and Dakhale, G. N. (2004). Antioxidant enzymes and lipid peroxidation in different stages of breast cancer. Free Radic. Res. 38, 81-85.
16. Krishna, C. M., Liebmann, J. E., Kaufman, D., DeGraff, W., Hahn, S. M., McMurry, T., Mitchell, J. B., and Russo, A. (1992). The catecholic metal sequestering agent 1,2-dihydroxybenzene-3,5-disulfonate confers protection against oxidative cell damage. Arch. Biochem. Biophys. 294, 98-106.
17. Leach, J. K., Van Tuyle, G., Lin, P. S., Schmidt-Ullrich, R., and Mikkelsen, R. B. (2001). Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res. 61, 3894-3901.
18. Lee, Y. J., Galoforo, S. S., Sim, J. E., Ridnour, L.A.,Choi, J., Forman,H. J., Corry, P. M., and Spitz, D. R. (2000). Dominant-negative Jun N-terminal protein kinase (JNK-1) inhibitsmetabolic oxidative stress during glucose deprivation in a human breast carcinoma cell line. Free Radic. Biol. Med. 28, 575-584.
19. Liu, B. H., Wu, T. S., Yu, F. Y., and Wang, C. H. (2006). Mycotoxin patulin activates the p38 kinase and JNK signaling pathways in human embryonic kidney cells. Toxicol. Sci. 89, 423-430.
20. 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.
21. Liu, D., Liu, J., and Wen, J. (1999). Elevation of hydrogen peroxide after spinal cord injury detected by using the Fenton reaction. Free Radic. Biol. Med. 27, 478-482.
22. Mahfoud, R., Maresca, M., Garmy, N., and Fantini, J. (2002). The mycotoxin patulin alters the barrier function of the intestinal epithelium: Mechanism of action of the toxin and protective effects of glutathione. Toxicol. Appl. Pharmacol. 181, 209-218.
23. Mansfield, K. D., Simon, M. C., and Keith, B. (2004). Hypoxic reduction in cellular glutathione levels requires mitochondrial reactive oxygen species. J. Appl. Physiol. 97, 1358-1366.
24. Maxwell, M. M., Pasinelli, P., Kazantsev, A. G., and Brown, R. H., Jr (2004). RNA interference-mediated silencing of mutant superoxide dismutase rescues cyclosporin A-induced death in cultured neuroblastoma cells. Proc. Natl. Acad. Sci. U.S.A. 101, 3178-3183.
25. McKinley, E. R., Carlton, W. W., and Boon, G. D. (1982). Patulin mycotoxicosis in the rat: Toxicology, pathology and clinical pathology. Food Cosmet. Toxicol. 20, 289-300.
26. Milligan, S. A., Owens, M. W., and Grisham, M. B. (1998). Differential regulation of extracellular signal-regulated kinase and nuclear factor-κB signal transduction pathways by hydrogen peroxide and tumor necrosis factor. Arch. Biochem. Biophys. 352, 255-262.
27. Mockett, R. J., Bayne, A. C., Kwong, L. K., Orr,W. C., and Sohal, R. S. (2003). Ectopic expression of catalase in Drosophila mitochondria increases stress resistance but not longevity. Free Radic. Biol. Med. 34, 207-217.
28. Narayanan, P. K., Goodwin, E. H., and Lehnert, B. E. (1997). Alpha particles initiate biological production of superoxide anions and hydrogen peroxide in human cells. Cancer Res. 57, 3963-3971.
29. Pfeiffer, E., Diwald, T.T., and Metzler, M. (2005).Patulin reduces glutathione level and enzyme activities in rat liver slices. Mol. Nutr. Food Res. 49, 329-336.
30. Phillips, J. P., Campbell, S. D., Michaud, D., Charbonneau, M., and Hilliker, A. J. (1989). Null mutation of copper/zinc superoxide dismutase in Drosophila confers hypersensitivity to paraquat and reduced longevity. Proc. Natl. Acad. Sci. U.S.A. 86, 2761-2765.
31. Piemontese, L., Solfrizzo, M., and Visconti, A. (2005). Occurrence of patulin in conventional and organic fruit products in Italy and subsequent exposure assessment. Food Addit. Contam. 22, 437-442.
32. Reaume, A. G., Elliott, J. L., Hoffman, E. K., Kowall, N. W., Ferrante, R. J., Siwek, D. F., Wilcox, H. M., Flood, D. G., Beal, M. F., Brown, R. H., Jr, et al. (1996). Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat. Genet. 13, 43-47.
33. Riley, R. T., and Showker, J. L. (1991). The mechanism of patulin's cytotoxicity and the antioxidant activity of indole tetramic acids. Toxicol. Appl. Pharmacol. 109, 108-126.
34. Rothe, G., and Valet, G. (1990). Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2′,7′-dichlorofluorescin. J. Leukoc. Biol. 47, 440-448.
35. Schulz, J. B., Lindenau, J., Seyfried, J., and Dichgans, J. (2000). Glutathione, oxidative stress and neurodegeneration. Eur. J. Biochem. 267, 4904-4911.
36. Smith, E. E., Duffus, E. A., and Small, M. H. (1993). Effects of patulin on postimplantation rat embryos. Arch. Environ. Contam. Toxicol. 25, 267-270.
37. Song, J. J., and Lee, Y. J. (2003). Catalase, but not MnSOD, inhibits glucose deprivation-activated ASK1-MEK-MAPK signal transduction pathway and prevents relocalization of Daxx: Hydrogen peroxide as a major second messenger of metabolic oxidative stress. J. Cell. Biochem. 90, 304-314.
38. Srinivasan, A., Lehmler, H. J., Robertson, L. W., and Ludewig, G. (2001). Production of DNA strand breaks in vitro and reactive oxygen species in vitro and in HL-60 cells by PCB metabolites. Toxicol. Sci. 60, 92-102.
39. Sun, J., and Tower, J. (1999). FLP recombinase-mediated induction of Cu/ Znsuperoxide dismutase transgene expression can extend the life span of adult Drosophila melanogaster flies. Mol. Cell. Biol. 19, 216-228.
40. Susa, S., and Wakabayashi, I. (2003). Extracellular alkalosis activates ERK mitogen-activated protein kinase of vascular smooth muscle cells through NADPH-mediated formation of reactive oxygen species. FEBS Lett. 554, 399-402.
41. Van Egmond, H. P. (1989). Current situation on regulations for mycotoxins. Overview of tolerances and status of standard methods of sampling and analysis. Food Addit. Contam. 6, 139-188.
42. Woo, C. H., You, H. J., Cho, S. H., Eom, Y.W., Chun, J. S., Yoo, Y. J., and Kim, J. H. (2002). Leukotriene B(4) stimulates Rac-ERK cascade to generate reactive oxygen species that mediates chemotaxis. J. Biol. Chem. 277, 8572-8578.
43. Wu, T. S., Yu, F. Y., Su, C. C., Kan, J. C., Chung, C. P., and Liu, B. H. (2005). Activation of ERK mitogen-activated protein kinase in human cells by the mycotoxin patulin. Toxicol. Appl. Pharmacol. 207, 103-111.
44. Zhang, Y., Chen, S., Hsu, T., and Santella, R. M. (2002). Immunochemical detection of malondialdehyde-DNA adducts in human oral mucosa cells. Carcinogenesis 23, 207-211.
45. Zhong, W., Oberley, L. W., Oberley, T. D., and St Clair, D. K. (1997). Suppression of the malignant phenotype of human glioma cells by over-expression of manganese superoxide dismutase. Oncogene 14, 481-490.