Evaluation of deoxynivalenol-induced toxic effects on DF-1 cells in vitro: Cell-cycle arrest, oxidative stress, and apoptosis

Environmental Toxicology and Pharmacology

Volumn 37, Issue 1, 2014, Pages 141-149

  Li, Daotong ^a   Ye, Yaqiong ^a   Lin, Shaoqing ^a   Deng, Li ^a   Fan, Xiaolong ^a   Zhang, Yuan ^a   Deng, Xianbo ^a   Li, Yugu ^a   Yan, Haikuo ^a   Ma, Yongjiang ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Apoptosis; Cell cycle arrest; Cytotoxicity; Deoxynivalenol; DF 1 cells; Oxidative stress

Indexed keywords

APOPTOSIS INDUCING FACTOR; CASPASE 3; CASPASE 8; CASPASE 9; GLUTATHIONE; MALONALDEHYDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; VOMITOXIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL PROLIFERATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; G2 PHASE CELL CYCLE CHECKPOINT; IN VITRO STUDY; INHIBITION KINETICS; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; TIME; UPREGULATION;

APOPTOSIS; CELL CYCLE ARREST; CYTOTOXICITY; DEOXYNIVALENOL; DF-1 CELLS; OXIDATIVE STRESS;

ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CASPASES; CELL CYCLE; CELL LINE; CELL PROLIFERATION; CHICK EMBRYO; FOOD CONTAMINATION; GLUTATHIONE; MALONDIALDEHYDE; MEMBRANE POTENTIAL, MITOCHONDRIAL; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; TRICHOTHECENES;

EID: 84890029945     PISSN: 13826689     EISSN: 18727077     Source Type: Journal    
DOI: 10.1016/j.etap.2013.11.015     Document Type: Article

References (45)

1. Awad W.A., Bohm J., Razzazi-Fazeli E., Hulan H.W., Zentek J. Effects of deoxynivalenol on general performance and electrophysiological properties of intestinal mucosa of broiler chickens. Poult. Sci. 2004, 83:1964-1972.
2. Awad W.A., Bohm J., Razzazi-Fazeli E., Zentek J. Effects of feeding deoxynivalenol contaminated wheat on growth performance, organ weights and histological parameters of intestine of broiler chickens. J. Anim. Physiol. Anim. Nutr. 2006, 90:32-37.
3. Awad W.A., Ghareeb K., Bohm J., Razzazi E., Hellweg P., Zentek J. The impact of the fusarium toxin deoxynivalenol (DON) on poultry. Int. J. Poult. Sci. 2008, 7:827-842.
4. Bensassi F., Golli-Bennour E.E., Abid-Essefi S., Bouaziz C., Hajlaoui M.R., Bacha H. Pathway of deoxynivalenol-induced apoptosis in human colon carcinoma cells. Toxicology 2009, 264:104-109.
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
6. Calvert T.W., Aidoo K.E., Candlish A.G., Fuat A.R. Comparison of in vitro cytotoxicity of Fusarium mycotoxins, deoxynivalenol, T-2 toxin and zearalenone on selected human epithelial cell lines. Mycopathologia 2005, 159:413-419.
7. CAST, 2003. Mycotoxins: risks in plant, animal and human systems. Council for Agricultural Science and Technology-Potential economic costs of mycotoxins in United States. Task Force Rep. 138, 136-142.
8. Cheng G., Guo W., Han L., Chen E., Kong L.F., Wang L.L., Ai W.C., Song N.N., Li H.S., Chen H.M. Cerium oxide nanoparticles induce cytotoxicity in human hepatoma SMMC-7721 cells via oxidative stress and the activation of MAPK signaling pathways. Toxicol. in Vitro 2013, 27:1082-1088.
9. Chung Y.J., Zhou H.R., Petska J.J. Transcriptional and posttranscriptional roles for p38 mitogen-activated protein kinase in upregulation of TNF-a expression by deoxynivalenol (vomitoxin). Toxicol. Appl. Pharmacol. 2003, 193:188-201.
10. Dinu D., Bodea G.O., Ceapa C.D., Munteanu M.C., Roming F.I., Serban A.I., Hermenean A., Costache M., Zarnescu O., Dinischiotu A. Adapted response of the antioxidant defense system to oxidative stress induced by deoxynivalenol in Hek-293 cells. Toxicon 2011, 57:1023-1032.
11. Dusanic D., Bencina D., Oven I., Cizelj I., Bencina M., Narat M. Mycoplasma synoviae induces upregulation of apoptotic genes, secretion of nitric oxide and appearance of an apoptotic phenotype in infected chicken chondrocytes. Vet. Res. 2012, 43:7.
12. Eriksen G. Metabolism and Toxicity of Trichothecenes 2003, University of Agricultural Sciences, Uppsala, Doctoral thesis.
13. Guo D.D., Bi H.S., Liu B., Wu Q.X., Wang D.G., Cui Y. Reactive oxygen species-induced cytotoxic effects of zinc oxide nanoparticles in rat retinal ganglion cells. Toxicol. in Vitro 2013, 731-738.
14. Hotchkiss R.S., Strasser A., McDunn J.E., Swanson P.E. Cell death. N. Engl. J. Med. 2009, 361:1570-1583.
15. Islam Z., Gray J.S., Pestka J.J. P38 mitogen-activated protein kinase mediates IL-8 induction by the ribotoxin deoxynivalenol in human monocytes. Toxicol. Appl. Pharmacol. 2006, 213:235-244.
16. Jomova K., Valko M. Advances in metal-induced oxidative stress and human disease. Toxicology 2011, 283:65-87.
17. Katika M.R., Hendriksen P.J.M., Shao J., Van Loveren H., Peijnenburg A. Transcriptome analysis of the human T lymphocyte cell line Jurkat and human peripheral blood mononuclear cells exposed to deoxynivalenol (DON): New mechanistic insights. Toxicol. Appl. Pharmacol. 2012, 264:51-64.
18. Kim H., You S., Kim I.J., Farris J., Foster L.K., Foster D.N. Increased mitochondrial-encoded Gene Transcription in Immortal DF-1 Cells. Exp. Cell Res. 2001, 265:339-347.
19. Königs M., Lenczyk M., Schwerdt G., Holzinger H., Gekle N., Humpf H.U. Cytotoxicity, metabolism and cellular uptake of the mycotoxin deoxynivalenol in human proximal tubule cells and lung fibroblasts in primary culture. Toxicology 2007, 240:48-59.
20. Königs M., Schwerdt, Gekle N., Humpf H.U. Effects of the mycotoxin deoxynivalenol on human primary hepatocytes. Mol. Nutr. Food Res. 2008, 52:830-839.
21. Kouadio J.H., Mobio T.A., Baudrimont I., Moukha S., Dano S.D., Creppy E.E. Comparative study of cytotoxicity and oxidative stress induced by deoxynivalenol, zearalenone or fumonisin B1 in human intestinal cell line Caco-2. Toxicology 2005, 213:56-65.
22. Laskin J.D., Heck D.E., Laskin D.L. The ribotoxic stress response as a potential mechanism for MAP kinase activation in xenobiotic toxicity. Toxicol. Sci. 2002, 69:289-291.
23. Lee H., Liu -Z., Hsieh W.-Z., Tang W.-T., Chung F.-Y., Leung J.-G., Henry C.-W. Oxidative stress involvement in Physalis angulata-induced apoptosis in human oral cancer cells. Food Chem. Toxicol. 2009, 47:561-570.
24. Ma Y.N., Zhang A.H., Shi Z.Y., He C.H., Ding J.J., Wang X.C., Ma J.F., Zhang H.B. A mitochondria-mediated apoptotic pathway induced by deoxynivalenol in human colon cancer cells. Toxicol. in Vitro 2012, 26:414-420.
25. Moon Y., Pestka J.J. Vomitoxin-induced cyclooxygenase-2 gene expression in macrophages mediated by activation of ERK and p38 but not JNK mitogenactivated protein kinases. Toxicol. Sci. 2002, 69:373-382.
26. Nogueira da Costa A., Keen J.N., Wild C.P., Findlay J.B. An analysis of the phosphoproteome of immune cell lines exposed to the immunomodulatory mycotoxin deoxynivalenol. Biochim. Biophys. Acta 2011, 1814:850-857.
27. Osman A.M., Pennings J.L.A., Blokland M., Peijnenburg A., van Loveren H. Protein expression profiling of mouse thymoma cells upon exposure to the trichothecene deoxynivalenol (DON): implications for its mechanism of action. J. Immunotoxicol. 2010, 7:147-156.
28. Pan X., Whitten D.A., Wu M., Chan C., Wilkerson C.G., Pestka J.J. Global protein phosphorylation dynamics during deoxynivalenol-induced ribotoxic stress response in the macrophage. Toxicol. Appl. Pharmacol. 2013, 268:201-211.
29. Patel S., Hazel C.M., Winterton A.G., Mortby E. Survey of ethnic foods for mycotoxins. Food Addit. Contam. 1996, 13:833-841.
30. Pestka J.J., Uzarski R.L., Islam Z. Induction of apoptosis and cytokine production in the Jurkat human T cells by deoxynivalenol: role of mitogen-activated protein kinases and comparison to other 8-ketotrichothecenes. Toxicology 2005, 206:207-219.
31. Pestka J.J., Zhou H., Moon Y., Chung Y.J. Cellular and molecular mechanisms for immune modulation by deoxynivalenol and other trichothecenes: unraveling a paradox. Toxicol. Lett. 2004, 153:61-73.
32. Pestka J.J., Smolinski A.T. Deoxynivalenol: toxicology and potential effects on humans. J. Toxicol. Environ. Health B Crit. Rev. 2005, 8:39-69.
33. Pestka J.J. Deoxynivalenol: toxicity, mechanisms and animal health risks. Anim. Feed Sci. Technol. 2007, 137:283-298.
34. Pestka J.J. Mechanisms of deoxynivalenol-induced gene expression and apoptosis. Food Addit. Contam. 2008, 1-13.
35. Pestka J.J. Deoxynivalenol: mechanisms of action, human exposure, and toxicological relevance. Arch. Toxicol. 2010, 84:663-679.
36. Rotter B.A., Prelusky D.B., Pestka J.J. Toxicology of deoxynivalenol (vomitoxin). J. Toxicol. Environ. Health 1996, 48:1-34.
37. Sahu S.C., O'Donnell M.W., Wiesenfeld P.L. Comparative hepatotoxicity od deoxynivalenol in rat, mouse and human liver cells in culture. J. Appl. Toxicol. 2008, 30:566-573.
38. Saquib Q., Al-Khedhairy A.A., Siddiqui M.A., Abou-Tarboush F.M., Azam A., Musarrat J. Titanium dioxide nanoparticles induced cytotoxicity, oxidative stress and DNA damage in human amnion epithelial (WISH) cells. Toxicol. in Vitro 2012, 26:351-361.
39. Sergent T., Parys M., Garsou S., Pussemier L., Schneider Y.J., Larondelle Y. Deoxynivalenol transport across human intestinal Caco-2 cells and its effects on cellular metabolism at realistic intestinal concentrations. Toxicol. Lett. 2006, 164:167-176.
40. Shifrin V.I., Anderson P. Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogenactivated protein kinase and induces apoptosis. J. Biol. Chem. 1999, 274:13985-13992.
41. Smith S.S., Reyes J.R., Arbon K.S., Harvey W.A., Hunt L.M., Heggland S.J. Cadmium-induced decrease in RUNX2 mRNA expression and recovery by the antioxidant N-acetylcysteine (NAC) in the human osteoblast-like cell line, Saos-2. Toxicol. in Vitro 2009, 23:60-66.
42. Wang J., Sun P., Bao Y., Liu J., An L. Cytotoxicity of single-walled carbon nanotubes on PC12 cells. Toxicol. in Vitro 2011, 25:242-250.
43. Yang H., Chung D.H., Kim Y.B., Choi Y.H., Moon Y. Ribotoxic mycotoxin deoxynivalenol induces G2/M cell cycle arrest via p21Cip/WAF1 mRNA stabilization in human epithelial cells. Toxicology 2008, 243:145-154.
44. Zhang X., Jiang L., Geng C., Cao J., Zhong L. The role of oxidative stress in deoxynivalenol-induced DNA damage in HepG2 cells. Toxicon 2009, 54:513-518.
45. Zhou H.R., Islam Z., Pestka J.J. Induction of competing apoptotic and survival signaling pathways in the macrophage by the ribotoxic trichothecene deoxynivalenol. Toxicol. Sci. 2005, 87:113-122.