Toxic effects of zearalenone on oxidative stress, inflammatory cytokines, biochemical and pathological changes induced by this toxin in the kidney of pregnant rats

Environmental Toxicology and Pharmacology

Volumn 37, Issue 2, 2014, Pages 580-591

  Jia, Zhiqiang ^a   Liu, Min ^a   Qu, Zhe ^a   Zhang, Yuanyuan ^a   Yin, Shutong ^a   Shan, Anshan ^a  

^a NORTHEAST AGRICULTURAL UNIVERSITY   (China)

Author keywords

Biochemical and pathological changes; Inflammatory cytokines; Kidney; Oxidative stress; Pregnant rats; Zearalenone

Indexed keywords

CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; ZEARALENONE; TLR4 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE PRODUCTION; DEGENERATIVE DISEASE; FEMALE; GENE SEQUENCE; GESTATION PERIOD; KIDNEY FIBROSIS; KIDNEY INJURY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; TUBULAR DEGENERATION; UPREGULATION; URINALYSIS; ANIMAL; DRUG EFFECTS; GENETICS; KIDNEY; METABOLISM; PATHOLOGY; PREGNANCY; SPRAGUE DAWLEY RAT; TOXICITY;

ANIMALS; CYTOKINES; FEMALE; KIDNEY; OXIDATIVE STRESS; PREGNANCY; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RELA; ZEARALENONE;

EID: 84896726507     PISSN: 13826689     EISSN: 18727077     Source Type: Journal    
DOI: 10.1016/j.etap.2014.01.010     Document Type: Article

References (83)

1. Abbès S., Salah-Abbès J.B., Ouanes Z., Houas Z., Othman O., Bacha H., Abdel-Wahhab M.A., Oueslati R. Preventive role of phyllosilicate clay on the immunological and biochemical toxicity of zearalenone in Balb/c mice. International Immunopharmacology 2006, 6:1251-1258.
2. Abbès S., Ouanes Z., Ben Salah-Abbès J., Houas Z., Oueslati R., Bacha H., Othman O. The protective effect of hydrated sodium calcium aluminosilicate against haematological, biochemical and pathological changes induced by zearalenone in mice. Toxicon 2006, 5:567-574.
3. Abbès S., Ben Salah-Abbès J., Sharafi H., Oueslati R., Noghabi K.A. Lactobacillus paracasei BEJ01 prevents immunotoxic effects during chronic zearalenone exposure in Balb/c mice. Immunopharmacology and Immunotoxicology 2013, 35(3):341-348.
4. 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.
5. An Y., Xin H., Yan W., Zhou X. Amelioration of cisplatin-induced nephrotoxicity by pravastatin in mice. Experimental and Toxicologic Pathology 2009, 63:215-219.
6. Andreakos E.T., Foxwell B.M., Brennan F.M., Maini R.N., Feldmann M. Cytokines and anti-cytokine biologicals in autoimmunity: present and future. Cytokine and Growth Factor Reviews 2002, 13:299-313.
7. Aronson D., Hammerman H., Beyar R., Yalonetsky S., Kapeliovich M., Markiewicz W., Goldberg A. Serum blood urea nitrogen and long-term mortality in acute ST-elevation myocardial infarction. International Journal of Cardiology 2008, 127:380-385.
8. Arumugam T.V., Okun E., Tang S.C., Thundyil J., Taylor S.M., Woodruff T.M. Toll-like receptors in ischemia-reperfusion injury. Shock 2009, 32:4-16.
9. Atkinson H.A., Miller K. Inhibitory effect of deoxynivalenol, 3-acetyldeoxynivalenol and zearalenone on induction of rat and human lymphocyte proliferation. Toxicology Letters 1984, 23:215-221.
10. Bacha H., Chekir L., Ellouz F., Hadidane R., Creppy E.E. Effect of zearalenone on fertilisation and gestation in rats. Proceeding of UK Workshop on Occurrence in Significance of Mycotoxins 1993, 258-262. Central Science Laboratory, London. K.A. Scudamore (Ed.).
11. Barry H., John G. Free Radicals in Biology and Medicine 1999, Oxford University Press, Oxford.
12. Bennett J.W., Klich M. Mycotoxins. Clinical Microbiology Reviews 2003, 16:497-516.
13. Berek L., Petri I.B., Mesterhazy A., Teren J., Molnar J. Effects of mycotoxins on human immune functions in vitro. Toxicology In Vitro 2001, 15:25-30.
14. Borutova R., Faix S., Placha I., Gresakova L., Cobanova K., Leng L. Effects of deoxynivalenol and zearalenone on oxidative stress and blood phagocytic activity in broilers. Archives of Animal Nutrition 2008, 62:303-312.
15. Cheung C.C., Zheng G.J., Richardson B.J., Lam P.K.S. Relationship between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels. Aquatic Toxicology 2001, 52:189-203.
16. Chiba N., Masuda A., Yoshikai Y., Matsuguchi T. Ceramide inhibits LPS-induced production of IL-5, IL-10, and IL-13 from mast cells. Journal of Cellular Physiology 2007, 213:126-136.
17. Chowdhury S.R., Smith T.K. Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on performance and metabolism of laying hens. Poultry Science 2004, 83:1849-1856.
18. Collins T.F.X., Sprando R.L., Black T.N., et al. Effects of aminopentol on in utero development in rats. Food and Chemical Toxicology 2006, 44:161-169.
19. Collins T.F.X., Sprando R.L., Black T.N., Olejnik N., Eppley R.M., et al. Effects of zearalenone on in utero development in rats. Food and Chemical Toxicology 2006, 44:1455-1465.
20. Conkova E., Laciakova A., Pastorova B., Seidel H., Kovac G. The effect of zearalenone on some enzymatic parameters in rabbits. Toxicology Letters 2001, 121:145-149.
21. D'Mello J.P.F., Placinta C.M., Macdonald M.C. Fusarium mycotoxins, a review of global implications for animal health, welfare and productivity. Animal Feed Science and Technology 1999, 80:183-205.
22. Dong M., He X.J., Tulayakul P., Li J.Y., Dong K.S., Manabe N., Nakayama H., Kumagai S. The toxic effects and fate of intravenously administered zearalenone in goats. Toxicon 2010, 55:523-530.
23. El-Achkar T.M., Dagher P.C. Renal Toll-like receptors: recent advances and implications for disease. Nature Clinical Practice Nephrology 2006, 2:568-581.
24. El-Sawi M.N.M., El-Wassimy M.M., Youssef O.A. Effect of Verrucarin J toxin on liver and kidney tissue of male mice. Texas Journal of Science 2001, 53:375-384.
25. Eriksen G.S., Alexander J. Fusarium Toxins in Cereals - A Risk Assessment 1998, vol. 502:7-58. Tema Nord, Copenhagen.
26. Etienne M., Dourmand J.Y. Effects of zearalenone or glucosinolates in the diet on reproduction in sows: a review. Livestock Production Science 1994, 40:99-113.
27. Freeman B.A., Crapo J.D. Hyperoxia increases oxygen radical production in rat lung and lung mitochondria. Journal of Biological Chemistry 1981, 256:10986-10992.
28. Garcia A.R., Avila E., Rosiles R., Petrone V.M. Evaluation of two mycotoxin binders to reduce toxicity of broiler diets containing ochratoxin A and T-2 toxin contaminated grain. Avian Diseases 2003, 47:691-699.
29. Green M.L., Diekman M.A., Malayer J.R., Scheidt A.B., Long G.G. Effect of prepubertal consumption of zearalenone on puberty and subsequent reproduction of gilts. Journal of Animal Science 1990, 68:171-178.
30. JECFA Joint FAO/WHO Expert Committee on Food Additives, 53rd Report. Safety Evaluation of Certain Food Additives. WHO Food Additives Series 44 2000.
31. Jiang S.Z., Yang Z.B., Yang W.R., Yao B.Q., Zhao H., Liu F.X., Chen C.C., Chi F. Effects of feeding purified zearalenone contaminated diets with or without clay enterosorbent on growth, nutrient availability, and genital organs in post-weaning female pigs. Asian-Australasian Journal of Animal Science 2010, 23:74-81.
32. Jiang S.Z., Yang Z.B., Yang W.R., Gao J., Liu F.X., Broomhead J., Chi F. Effects of purified zearalenone on growth performance, organ size, serum metabolites, and oxidative stress in postweaning gilts. Journal of Animal Science 2011, 89:3008-3015.
33. Jo S.K., Sung S.A., Cho W.Y., Go K.J., Kim H.K. Macrophages contribute to the initiation of ischaemic acute renal failure in rats. Nephrology Dialysis Transplantation 2006, 21:1231-1239.
34. Kiessling K.H., Pettersson H. Metabolism of zearalenone in rat liver. Acta Pharmacologica et Toxicologica 1978, 43:285-290.
35. Koraichi F., Videmanna B., Mazallona M., Benahmedb M., Prouillaca C., Lecoeurc S. Zearalenone exposure modulates the expression of ABC transporters and nuclear receptors in pregnant rats and fetal liver. Toxicology Letters 2012, 211(3):246-256.
36. Kouadio J., Dano S.D., Moukha S., Mobio T.A., Creppy E.E. Effects of combinations of Fusarium mycotoxins on the inhibition of macromolecular synthesis, malondialdehyde levels, DNA methylation and fragmentation, and viability in Caco-2 cells. Toxicon 2007, 49:306-317.
37. Kuiper-Goodman T., Scott P.M., Watanabe H. Risk assessment of mycotoxin zearalenone. Regulatory Toxicology and Pharmacology 1987, 7:253-306.
38. Liang Z.S.M.A., Liu Y.J., Deng C.Y., Fan X.B.X., Yan L., Hu H.K.Q.X. In vivo toxicity of zearalenone on liver and kidney in mice. Chinese Journal of Veterinary Science 2010, 30:673-676.
39. Liu M., Chien C.C., Burne-Taney M., Molls R.R., Racusen L.C., Colvin R.B., Rabb H. A pathophysiologic role for T lymphocytes in murine acute cisplatin nephrotoxicity. Journal of the American Society of Nephrology 2006, 17:765-774.
40. Liu Z.K., Luo B.R. The investigation of sow reproductive condition in part scale pig farms from seven provinces in China. Swine Production 2010, 5:65-68.
41. Luongo D., De Luna R., Russo R., Severino L. Effects of four Fusarium toxins (fumonisin B(1), alpha-zearalenol, nivalenol and deoxynivalenol) on porcine whole-blood cellular proliferation. Toxicon 2008, 52:156-162.
42. 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.
43. Marin D.E., Taranu I., Burlacu R., Manda G., Motiu M., Neagoe I., Dragomir C., Stancu M., Calin L. Effects of zearalenone and its derivatives on porcine immune response. Toxicology In Vitro 2011, 25:1981-1988.
44. Maaroufi K., Chekir L., Creppy E.E., Ellouz F., Bacha H. Zearalenone induces modifications of haematological and biochemical parameters in rats. Toxicon 1996, 34:535-540.
45. Mak W.M., Saunders M.E. The Immune Response 2006, Elsevier, London. T. Lebedeva, V. Picknett (Eds.).
46. McCormick S.P. Microbial detoxification of mycotoxins. Journal of Chemical Ecology 2013, 39(7):907-918.
47. Murata H., Sultana P., Shimada N., Yashioka M. Structure-activity relationships among zearalenone and its derivatives based on bovine neutrophil chemiluminescence. Veterinary and Human Toxicology 2003, 45(1):18-20.
48. National Research Council Institute of Laboratory Animal Resources Guide for the Care and Use of Laboratory Animals 1996, 8-12. National Academy Press, Washington, DC.
49. Navarro J.F., Milena F.J., Mora C., Leon C., Garcia J. Renal proinflammatory cytokine gene expression in diabetic nephropathy: effect of angiotensin-converting enzyme inhibition and pentoxifylline administration. American Journal of Nephrology 2006, 26:562-570.
50. NTP Technical Report on the Carcinogenesis Bioassay of Zearalenone (CAS No. 17924-92-4) in F 344/N Rats and B6C3F1 Mice (Feed Study) 1982, NIH Publication No. 83-1791, National Toxicology Program, Research Triangle Park, NC, USA.
51. O'Brien E. Mycotoxins Affecting the Kidney 2005, Bibliothek der Universität Konstanz.
52. Ouanes Z., Abid S., Ayed I., Anane R., Mobio T., Creppy E.E., Bacha H. Induction of micronuclei by zearalenone in Vero monkey kidney cells and in bone marrow cells of mice: protective effect of vitamin E. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 2003, 538:63-70.
53. Pandey P.C., Mishra A.P. Novel potentiometric sensing of creatinine. Sensors and Actuators B: Chemical 2004, 99:230-235.
54. Pestka J.J., Tai J.H., Witt M.F., Dixon D.E., Forsell J.H. Suppression of immune response in the B6C3F1 mouse after dietary exposure to the Fusarium mycotoxins deoxynivalenol (vomitoxin) and zearalenone. Food and Chemical Toxicology 1987, 25:297-304.
55. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 2001, 29:e45.
56. Placinta C.M., D'Mello J.P.F., Macdonald A.M.C. A review of worldwide contamination of cereal grains and animal feed with Fusarium mycotoxins. Animal Feed Science and Technology 1999, 78:21-37.
57. Raveh D., Shemesh O., Ashkenazi Y.J., Winkler R., Barak V. Tumor necrosis factor-α blocking agent as a treatment for nephrotic syndrome. Pediatric Nephrology 2004, 19:1281-1284.
58. Reddy K.R.N., Salleh B., Saad B., et al. An overview of mycotoxin contamination in foods and its implications for human health. Toxin Reviews 2010, 29(1):3-26.
59. Reeves P.G., Nielsen F.H., Fahey G.C. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. Journal of Nutrition 1993, 123(11):1939-1951.
60. Richard J.L. Some major mycotoxins and their mycotoxicoses - an overview. International Journal of Food Microbiology 2007, 119:3-10.
61. Ruh M.F., Bi Y., Cox L., Berk D., Howlett A.C., Bellone C.J. Effect of environmental estrogens on IL-1beta promoter activity in a macrophage cell line. Endocrine 1998, 9:207-211.
62. Saenz de Rodriguez C.A., Bougovanni A.M., Conde de Borrego L. An epidemic of precocious development in Puerto Rican children. Journal of Pediatrics 1985, 107:393-396.
63. Salah-Abbès J.B., Abbès S., Houas Z., Abdel-Wahhab M.A., Oueslati R. Zearalenone induces immunotoxicity in mice: possible protective effects of radish extract (Raphanus sativus). Journal of Pharmacy and Pharmacology 2008, 60:761-770.
64. Salah-Abbès J.B., Abbès S., Houas Z., Ouanes Z., Abdel-Wahhab M.A., Bacha H., Oueslati R. Tunisian radish extract (Raphanus sativus) enhances the antioxidant status and protects against oxidative stress induced by zearalenone in Balb/c mice. Journal of Applied Toxicology 2008, 28:6-14.
65. Salah-Abbès J.B., Abbès S., Abdel-Wahhab M.A., Oueslati R. Raphanus sativus extract protects against zearalenone induced reproductive toxicity, oxidative stress and mutagenic alterations in male Balb/c mice. Toxicon 2009, 53:525-533.
66. Satoshi S., Kiyoji T., Hiroyo K., Fumio N. Exercise induced lipid peroxidation and leakage of enzyme before and after vitamin E supplementation. International Journal of Biochemistry 1989, 21:835-838.
67. Scudamore K.A., Patel S. Survey for aflatoxins, ochratoxin A, zearalenone and fumonisins in maize imported into the United Kingdom. Food Additives Contaminants 2000, 17:30-55.
68. Sheryanna A., Bhangal G., McDaid J., Smith J., Manning A., Foxwell B.M., Feldmann M., Cook H.T., Pusey C.D., Tam F.W. Inhibition of p38 mitogen-activated protein kinase is effective in the treatment of experimental crescentic glomerulonephritis and suppresses monocyte chemoattractant protein-1 but not IL-1 or IL-6. Journal of the American Society of Nephrology 2007, 18:1167-1179.
69. Singh G. A possible cellular mechanism of cisplatin-induced nephrotoxicity. Toxicology 1989, 58:71-80.
70. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M., Klenk D.C. Measurement of protein using bicinchoninic acid. Analytical biochemistry 1985, 150(1):76-85.
71. Suzuki N., Suzuki S., Duncan G.S., et al. Severe impairment of interleukin-1 and TOLL-like receptor signalling in mice lacking IRAK-4. Nature 2002, 416:750-756.
72. Swamy H.V.L.N., Smith T.K., Karrow N.A., Boermans H.J. Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on growth and immunological parameters of broiler chickens. Poultry Science 2004, 83:533-543.
73. Tomaszewski J., Miturski R., Semczuk A., Kotarski J., Jakowicki J. Tissue zearalenone concentration in normal, hyperplastic and neoplastic human endometrium. Ginekologia Polska 1998, 69:363-366.
74. Turcotte J.C., Hunt P.J.B., Blaustein J.D. Estrogenic effects of zearalenone on the expression of progestin receptors and sexual behavior in female rats. Hormones and Behavior 2005, 47:178-184.
75. Vander A., Sherman J., Luciano D. Human Physiology: The Mechanism of Body Function 2001, 554-587. McGraw Hill, New York.
76. Wang D.F., Zhang N.Y., Peng Y.Z., Desheng Q. Interaction of zearalenone and soybean isoflavone in diets on the growth performance, organ development and serum parameters in prepubertal gilts. Journal of Animal Physiology and Animal Nutrition (Berlin) 2012, 96:939-946.
77. Wu H., Chen G., Wyburn K.R., Yin J., et al. TLR4 activation mediates kidney ischemia/reperfusion injury. Journal of Clinical Investigation 2007, 117:2487-2859.
78. Yoshio U., Noriko S., Yagasaki S., Enomoto M. Toxicological approaches to the metabolites of Fusaria. VII: Effects of zearalenone on the uteri of mice and rats. Chemical and Pharmaceutical Bulletin 1974, 22:2830-2835.
79. Young L.G., Ping H., King G.J. Effects of feeding zearalenone to sows on rebreeding and pregnancy. Journal of Animal Science 1990, 68:15-20.
80. Yuk J.M., Shin D.M., Lee H.M., Kim J.J., Kim S.W., Jin H.S., et al. The orphan nuclear receptor SHP acts as a negative regulator in inflammatory signaling triggered by Toll-like receptors. Nature Immunology 2011, 12:742-751.
81. Zhou H.R., Yan D., Pestka J.J. Differential cytokine mRNA expression in mice after oral exposure to the trichothecene vomitoxin (deoxynivalenol): dose response and time course. Toxicology and Applied Pharmacology 1997, 144:294-305.
82. Zourgui L., Golli E.E., Bouaziz C., Bacha H., Hassen W. Cactus (Opuntia ficus-indica) cladodes prevent oxidative damage induced by the mycotoxin zearalenone in Balb/C mice. Food and Chemical Toxicology 2008, 46:1817-1824.
83. Zinedine A., Soriano J.M., Molto J.C., et al. Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin. Food and Chemical Toxicology 2007, 45(1):1-18.