Cellular mechanisms of the cytotoxic effects of the zearalenone metabolites α-zearalenol and β-zearalenol on RAW264.7 macrophages

Toxicology in Vitro

Volumn 27, Issue 3, 2013, Pages 1007-1017

  Lu, Jia ^a   Yu, Ji Yeon ^b   Lim, Shin Saeng ^a   Son, Young Ok ^c   Kim, Dong Hern ^c   Lee, Seung Ah ^d   Shi, Xianglin ^c   Lee, Jeong Chae ^a,c  

^a Chonbuk National University   (South Korea)

^b Korea Research Institute of Chemical Technology   (South Korea)

^c UNIVERSITY OF KENTUCKY   (United States)

^d Chonnam Techno College   (South Korea)

Author keywords

Zearalenol; Zearalenol; Antioxidants; Mitochondrial stress; Reactive oxygen species; Signal transduction

Indexed keywords

1 (3,4 DIHYDROXYPHENETHYL) 3 (4 HYDROXYSTYRYL)UREA; ACTEOSIDE; ALPHA ZEARALENOL; APOPTOSIS INDUCING FACTOR; BETA ZEARALENOL; CASPASE; CASPASE 8; CATALASE; CYTOCHROME C; MITOGEN ACTIVATED PROTEIN KINASE P38; PANCASPASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; UNCLASSIFIED DRUG; UREA DERIVATIVE; ZEARALENONE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL NUCLEUS; CELL STRAIN; CELL STRAIN RAW264.7; CELL TYPE; CELL VIABILITY; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY; CYTOTOXICITY TEST; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; ENZYME RELEASE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MACROPHAGE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CELL LINE; CELL SURVIVAL; CYTOTOXINS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MYCOTOXINS; PROTEIN KINASE INHIBITORS; REACTIVE OXYGEN SPECIES; TUMOR SUPPRESSOR PROTEIN P53; ZEARALENONE; ZERANOL;

EID: 84874562306     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2013.01.011     Document Type: Article

References (52)

1. Abid-Essefi S., Baudrimont I., Hassen W., Ouanes Z., Mobio T.A., Anane R., Creppy E.E., 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 2003, 192:237-248.
2. Abid-Essefi S., Bouaziz C., Golli-Bennour E.E., Ouanes Z., Bacha H. Comparative study of toxic effects of zearalenone and its two major metabolites alpha-zearalenol and beta-zearalenol on cultured human Caco-2 cells. Journal of Biochemical and Molecular Toxicology 2009, 23:233-243.
3. Alm H., Greising T., Brüssow K.P., Torner H., Tiemann U. The influence of the mycotoxins deoxynivalenol and zearalenol on in vitro maturation of pig oocytes and in vitro culture of pig zygotes. Toxicology in Vitro 2002, 16:643-648.
4. Apel K., Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 2004, 55:373-399.
5. Ayed-Boussema I., Bouaziz C., Rjiba K., Valenti K., Laporte F., Bacha H., Hassen W. The mycotoxin zearalenone induces apoptosis in human hepatocytes (HepG2) via p53-dependent mitochondrial signaling pathway. Toxicology in Vitro 2008, 22:1671-1680.
6. Barbouti A., Doulias P.T., Nousis L., Tenopoulou M., Galaris D. DNA damage and apoptosis in hydrogen peroxide-exposed Jurkat cells: bolus addition versus continuous generation. Free Radical Biology & Medicine 2002, 33:691-702.
7. Bouaziz C., Sharaf El Dein O., El Golli E., Abid-Essefi S., Brenner C., Lemaire C., Bacha H. Different apoptotic pathways induced by zearalenone, T-2 toxin and ochratoxin A in human hepatoma cells. Toxicology 2008, 254:19-28.
8. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
9. Celius T., Haugen T.B., Grotmol T., Walther B.T. A sensitive zonagenetic assay for rapid in vitro assessment of estrogenic potency of xenobiotics and mycotoxins. Environmental Health Perspectives 1999, 107:63-68.
10. Cregan S.P., Dawson V.L., Slack R.S. Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 2004, 23:2785-2796.
11. Diekman M.A., Green M.L. Mycotoxins and reproduction in domestic livestock. Journal of Animal Science 1992, 70:1615-1627.
12. 2 and transition metal ions in the genotoxic action of ascorbic acid in cell culture models. Toxicology Letters 2007, 170:57-65.
13. EFSA (Eupropean Food Safety Authority), 2004. Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to zearalenone as undesirable substance in animal feed. 89, 1-35.
14. Eguchi Y., Shimizu S., Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Research 1997, 57:1835-1840.
15. Fitzpatrick D.W., Picken C.A., Murphy L.C., Buhr M.M. Measurement of the relative binding affinity of zearalenone, alpha-zearalenol and beta-zearalenol for uterine and oviduct estrogen receptors in swine, rats and chickens: an indicator of estrogenic potencies. Comparative Biochemistry and Physiology C 1989, 94:691-694.
16. Forman H.J., Torres M. Redox signaling in macrophages. Molecular Aspects of Medicine 2001, 22:189-216.
17. Gross A., McDonnell J.M., Korsmeyer S.J. BCL-2 family members and the mitochondria in apoptosis. Genes & Development 1999, 13:1899-1911.
18. Grosse Y., Chekir-Ghedira L., Huc A., Obrecht-Pflumio S., Dirheimer G., Bacha H., Pfohl-Leszkowicz A. Retinol, ascorbic acid and alpha-tocopherol prevent DNA adduct formation in mice treated with the mycotoxins ochratoxin A and zearalenone. Cancer Letters 1997, 114:225-229.
19. Halliwell B., Clement M.V., Long L.H. Hydrogen peroxide in the human body. FEBS Letters 2000, 486:10-13.
20. Hassen W., Ayed-Boussema I., Oscoz A.A., Lopez Ade C., Bacha H. The role of oxidative stress in zearalenone-mediated toxicity in HepG2 cells: oxidative DNA damage, glutathione depletion and stress proteins induction. Toxicology 2007, 232:294-302.
21. Imlay J.A., Chin S.M., Linn S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 1998, 240:640-642.
22. Kang Y.H., Yi M.J., Kim M.J., Park M.T., Bae S., Kang C.M., Cho C.K., Park I.C., Park M.J., Rhee C.H., Hong S.I., Chung H.Y., Lee Y.S., Lee S.J. Caspase-independent cell death by arsenic trioxide in human cervical cancer cells: reactive oxygen species-mediated poly (ADP-ribose) polymerase-1 activation signals apoptosis-inducing factor release from mitochondria. Cancer Research 2004, 64:8960-8967.
23. Kiessling K.H., Pettersson H. Metabolism of zearalenone in rat liver. Acta Pharmacologica et Toxicologica (Copenh) 1978, 43:285-290.
24. Kim S.S., Son Y.O., Chun J.C., Kim S.E., Chung G.H., Hwang K.J., Lee J.C. Antioxidant property of an active component purified from the leaves of paraquat-tolerant Rehmannia glutinosa. Redox Report 2005, 10:311-318.
25. Kook S.H., Son Y.O., Chung S.W., Lee S.A., Kim J.G., Jeon Y.M., Lee J.C. Caspase-independent death of human osteosarcoma cells by flavonoids is driven by p53-mediated mitochondrial stress and nuclear translocation of AIF and endonuclease G. Apoptosis 2007, 12:1289-1298.
26. Kroemer G., Reed J.C. Mitochondrial control of cell death. Nature Medicine 2000, 6:513-519.
27. Lee Y.J., Shacter E. Oxidative stress inhibits apoptosis in human lymphoma cells. The Journal of Biological Chemistry 1999, 274:19792-19798.
28. Le Guével R., Pakdel F. Assessment of oestrogenic potency of chemicals used as growth promoter by in vitro methods. Human Reproduction 2001, 16:1030-1036.
29. Leung M.C., Díaz-Llano G., Smith T.K. Mycotoxins in pet food: a review on worldwide prevalence and preventative strategies. Journal of Agriculture and Food Chemistry 2006, 54:9623-9635.
30. Li G.Y., Osborne N.N. Oxidative-induced apoptosis to an immortalized ganglion cell line is caspase independent but involves the activation of poly (ADP-ribose) polymerase and apoptosis-inducing factor. Brain Research 2008, 1188:35-43.
31. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91:479-489.
32. Marin D.E., Taranu I., Burlacu R., Tudor D.S. Effects of zearalenone and its derivatives on the innate immune response of swine. Toxicon 2010, 56:956-963.
33. Maulik N., Sato M., Price B.D., Das D.K. An essential role of NF-kappaB in tyrosine kinase signaling of p38 MAP kinase regulation of myocardial adaptation to ischemia. FEBS Letters 1998, 429:365-369.
34. Miksicek R.J. Interaction of naturally occurring nonsteroidal estrogens with expressed recombinant human estrogen receptor. The Journal of Steroid Biochemistry and Molecular Biology 1994, 49:153-160.
35. Mirocha C.J., Pathre S.V., Robison T.S. Comparative metabolism of zearalenone and transmission into bovine milk. Food and Cosmetics Toxicology 1981, 19:25-30.
36. Muller H.M., Reimann J., Schumacher U., Schwadorf K. Natural occurrence of fusarium toxins in oats harvested during 5years in an area of southwest Germany. Food Additives and Contaminants 1998, 15:801-806.
37. Newmeyer D.D., Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 2003, 112:481-490.
38. Palyusik M., Hagler W.M., Horváth L., Mirocha C.J. Biotransformation of zearalenone to zearalenol by Candida tropicalis. Acta Veterinaria Academiae Scientiarum Hungaricae 1980, 28:159-166.
39. Quanes Z., Ayed-Boussema I., Baati T., Creppy E.E., Bacha H. Zearalenone induces chromosome aberrations in mouse bone marrow: preventive effect of 17beta-estradiol, progesterone and Vitamin E. Mutation Research 2005, 565:139-149.
40. Ruffolo S.C., Breckenridge D.G., Nguyen M., Goping I.S., Gross A., Korsmeyer S.J., Li H., Yuan J., Shore G.C. BID-dependent and BID-independent pathways for BAX insertion into mitochondria. Cell Death and Differentiation 2000, 7:1101-1108.
41. Schollenderger M., Drochner W., Müller H.M. Fusarium toxins of the scirpentriol subgroup: a review. Mycopathologia 2007, 164:101-108.
42. Scudamore K.A., Patel S. Survey for aflatoxins, ochratoxin A, zearalenone and fumonisins in maize imported into the United Kingdom. Food Additives and Contaminants 2000, 17:407-416.
43. Shier W.T., Shier A.C., Xie W., Mirocha C.J. Structure-activity relationships for human estrogenic activity in zearalenone mycotoxins. Toxicon 2001, 39:1435-1438.
44. Son Y.O., Jang Y.S., Heo J.S., Chung W.T., Choi K.C., Lee J.C. Apoptosis-inducing factor plays a critical role in caspase-independent, pyknotic cell death in hydrogen peroxide-exposed cells. Apoptosis 2009, 14:796-808.
45. Son Y.O., Lee S.A., Kim S.S., Jang Y.S., Chun J.C., Lee J.C. Acteoside inhibits melanogenesis in B16F10 cells through ERK activation and tyrosinase down-regulation. Journal of Pharmacy and Pharmacology 2011, 63:1309-1319.
46. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Brenner C., Larochette N., Prévost M.C., Alzari P.M., Kroemer G. Mitochondrial release of caspase-2 and -9 during the apoptotic process. The Journal of Experimental Medicine 1999, 189:381-394.
47. 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., Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999, 397:441-446.
48. Tsujimoto Y. Cell death regulation by the Bcl-2 protein family in the mitochondria. Journal of Cellular Physiology 2003, 195:158-167.
49. Yu J.Y., Kim J.H., Kim T.G., Kim B.T., Jang Y.S., Lee J.C. (E)-1-(3,4-dihydroxyphenethyl)-3-styrylurea inhibits proliferation of MCF-7 cells through G1 cell cycle arrest and mitochondria-mediated apoptosis. Molecules and Cells 2010, 30:303-310.
50. Yu J.Y., Zheng Z.H., Son Y.O., Shi X., Jang Y.O., Lee J.C. Mycotoxin zearalenone induces AIF- and ROS-mediated cell death through p53- and MAPK-dependent signaling pathways in RAW264.7 macrophages. Toxicology in Vitro 2011, 25:1654-1663.
51. Zanna C., Ghelli A., Porcelli A.M., Martinuzzi A., Carelli V., Rugolo M. Caspase-independent death of Leber's hereditary optic neuropathy cybrids is driven by energetic failure and mediated by AIF and endonuclease G. Apoptosis 2005, 10:997-1007.
52. Zinedine A., Soriano J.M., Moltó J.C., Mañes J. Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin. Food and Chemical Toxicology 2007, 45:1-18.