Effects of zearalenone on oxidative stress and inflammation in weanling piglets

Food and Chemical Toxicology

Volumn 58, Issue , 2013, Pages 408-415

  Marin, Daniela E ^a   Pistol, Gina C ^a   Neagoe, Ionela V ^b   Calin, Loredana ^a   Taranu, Ionelia ^a  

^a NATIONAL INSTITUTE FOR RESEARCH AND DEVELOPMENT IN MICROTECHNOLOGIES   (Romania)

^b VICTOR BABES NATIONAL INSTITUTE OF PATHOLOGY   (Romania)

Author keywords

Inflammation; Oxidative stress; Swine; Zearalenone

Indexed keywords

CATALASE; GAMMA INTERFERON; GLUTATHIONE PEROXIDASE; INTERLEUKIN 1BETA; PROSTAGLANDIN SYNTHASE; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA; ZEARALENONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATALASE GENE; CONTROLLED STUDY; CYCLOOXIGENASE GENE; CYTOKINE PRODUCTION; FOOD CONTAMINATION; FOOD INTAKE; GENE; GENE EXPRESSION; GLUTATHIONE PEROXIDASE GENE; GRANULOCYTE; INFLAMMATION; INTOXICATION; LIVER TOXICITY; LYMPHOCYTE PROLIFERATION; MONOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PIGLET; RESPIRATORY BURST; SUPEROXIDE DISMUTASE GENE;

INFLAMMATION; OXIDATIVE STRESS; SWINE; ZEARALENONE;

ANIMALS; BASE SEQUENCE; CELL PROLIFERATION; CYTOKINES; DNA PRIMERS; ESTROGENS, NON-STEROIDAL; GENE EXPRESSION PROFILING; INFLAMMATION; ORGAN SIZE; OXIDATIVE STRESS; REAL-TIME POLYMERASE CHAIN REACTION; SWINE; ZEARALENONE;

FUNGI; FUSARIUM; SUIDAE;

EID: 84879316669     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2013.05.033     Document Type: Article

References (76)

1. Abbès S., Ouanes Z., Salah-Abbès J.B., Abdel-Wahhab M.A., Oueslati R., Bacha H. Preventive role of aluminosilicate clay against induction of micronuclei and chromosome aberrations in bone-marrow cells of Balb/c mice treated with Zearalenone. Mutat. Res. 2007, 631:85-92.
2. 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.
3. Abid-Essefi S., Ouanes Z., Hassen W., Baudrimont I., Creppy E., Bacha H. Cytotoxicity, inhibition of DNA and protein syntheses and oxidative damage in cultured cells exposed to zearalenone. Toxicol. In Vitro 2004, 18:467-474.
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. J. Biochem. Mol. Toxicol. 2009, 23:233-243.
5. Abid-Essefi S., Zaied C., Bouaziz C., Salem I.B., Kaderi R., Bacha H. Protective effect of aqueous extract of Allium sativum against zearalenone toxicity mediated by oxidative stress. Exp. Toxicol. Pathol. 2012, 64:689-695.
6. Atkinson H.A., Miller K. Inhibitory effect of deoxynivalenol, 3-acetyldeoxynivalenol and zearalenone on induction of rat and human lymphocyte proliferation. Toxicol. Lett. 1984, 23:215-221.
7. Ayed Y., Ayed-Boussema I., Ouanes Z., Bacha H. In vitro and in vivo induction of chromosome aberrations by alpha- and beta-zearalenols: comparison with zearalenone. Mutat. Res. - Genet. Toxicol. Environ. Mutagen. 2011, 726:42-46.
8. Bennett J.W., Klich M. Mycotoxins. Clin. Microbiol. 2003, 16:497-516.
9. Blomberg L.A., Long E.L., Sonstegard T.S., Van Tassell C.P., Dobrinsky J.R., Zuelke K.A. Serial analysis of gene expression during elongation of the peri-implantation porcine trophectoderm (conceptus). Physiol. Genomics. 2005, 20:188-194.
10. Blunden G., Roch O.G., Rogers D.J., Coker R.D., Bradburn N., John A.E. Mycotoxins in food. Med. Lab. Sci. 1991, 48:271-282.
11. Bouaziz C., Bouslimi A., Kadri R., Zaied C., Bacha H., Abid-Essefi S. The in vitro effects of zearalenone and T-2 toxins on Vero cells. Exp. Toxicol. Pathol. 2012, (Epub ahead of print).
12. Boyd P.A., Wittliff J.L. Mechanism of Fusarium mycotoxin action in mammary gland. J. Toxicol. Environ. Health 1978, 4:1-8.
13. Busk Ø.L., Ndossi D., Verhaegen S., Connolly L., Eriksen G., Ropstad E., Sørlie M. Relative quantification of the proteomic changes associated with the mycotoxin zearalenone in the H295R steroidogenesis model. Toxicon 2011, 58:533-542.
14. Conková E., Laciaková A., Pástorová B., Seidel H., Kovác G. The effect of zearalenone on some enzymatic parameters in rabbits. Toxicol. Lett. 2001, 121:145-149.
15. Diekman M.A., Green M.L. Mycotoxins and reproduction in domestic livestock. J. Anim. Sci. 1992, 70:1615-1627.
16. Döll S., Dänicke S. The Fusarium toxins deoxynivalenol (DON) and zearalenone (ZON) in animal feeding. Prev. Vet. Med. 2011, 102:132-145.
17. EFSA (European food Safety Authority) 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. EFSA J. 2004, 89:1-35.
18. El-Makawy A., Hassanane M.S., Abd Alla E.-S.A.M. Genotoxic evaluation for the estrogenic mycotoxin zearalenone. Reprod. Nutr. Dev. 2001, 41:79-89.
19. Engelhardt G., Barthel J., Sparrer D. Fusarium mycotoxins and ochratoxin A in cereals and cereal products: results from the bavarian health and food safety authority in 2004. Mol. Nutr. Food Res. 2006, 50:401-405.
20. FAO/WHO Expert Committee on Food Additives (JECFA) Safety evaluation of certain food additives and contaminants. WHO food additive series 44, zearalenone 2000, World Health Organisation, Geneva, Switzerland, pp. 393-482.
21. Forsell J.H., Pestka J.J. Relation of 8-ketotrichothecene and zearalenone analog structure to inhibition of mitogen-induced human lymphocyte blastogenesis. Appl. Environ. Microbiol. 1985, 50:1304-1307.
22. Frouin H., Ménard L., Measures L., Brousseau P., Fournier M.T. Lymphocyte-proliferative responses of a grey seal (Halichoerus grypus) exposed to heavy metals and PCBs in vitro. Aquat. Mammals 2010, 36:365-371.
23. Ghédira-Chékir L., Maaroufi K., Creppy E.E., Bacha H. Cytotoxic and genotoxic effects of zearalenone: prevention by vitamin E. J. Toxicol. - Toxin Rev. 1999, 18:355-368.
24. 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. J. Anim. Sci. 1990, 68:171-178.
25. Grešáková L., Bořutová R., Faix S., Plachá I., Cobanová K., Košíková B., Leng L. Effect of lignin on oxidative stress in chickens fed a diet contaminated with zearalenone. Acta Vet. Hung. 2012, 60:103-114.
26. Hassen W., Ayed-Boussema I., Azqueta Oscoz A., de Cerain Lopez A., Bacha H. The role of oxidative stress in zearalenone-mediated toxicity in Hep G2 cells: oxidative DNA damage, gluthatione depletion and stress proteins induction. Toxicology 2007, 232:294-302.
27. Hostetler C.E., Michal J., Robison M., Ott T.L., Kincaid R.L. Effect of selenium intake and fetal age on mRNA levels of two selenoproteins in porcine fetal and maternal liver. J. Anim. Sci. 2006, 84:2382-2390.
28. Hussein H.S., Brasel J.M. Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology 2001, 167:101-134.
29. James L.J., Smith T.K. Effect of dietary alfalfa on zearalenone toxicity and metabolism in rats and swine. J. Anim. Sci. 1982, 55:110-118.
30. Jenny N.S. Inflammation in aging: cause, effect, or both?. Discov. Med. 2012, 13:451-460.
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-Aust. J. Anim. Sci. 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. J. Anim. Sci. 2011, 89:3008-3015.
33. Jiang S.Z., Yang Z.B., Yang W.R., Wang S.J., Wang Y., Broomhead J., Johnston S.L., Chi F. Effect on hepatonephric organs, serum metabolites and oxidative stress in post-weaning piglets fed purified zearalenone-contaminated diets with or without Calibrin-Z. J. Anim. Physiol. Anim. Nutr. (Berl.) 2012, 96:1147-1156.
34. Jung K., Park H.J., Kim Y.H., Hong J.P. Expression of tumor necrosis factor-alpha and cyclooxygenase-2 mRNA in porcine split-thickness wounds treated with epidermal growth factor by quantitative real-time PCR. Res. Vet. Sci. 2007, 82:344-348.
35. Kabak B., Dobson A.D., Var I. Strategies to prevent mycotoxin contamination of food and animal feed: a review. Crit. Rev. Food Sci. Nutr. 2006, 46:593-619.
36. Kiessling K.H., Pettersson H. Metabolism of zearalenone in rat liver. Acta Pharmacol. Toxicol. (Copenh) 1978, 43:285-290.
37. Kim Y.J., Kim E.H., Hahm K.B. Oxidative stress in inflammation-based gastrointestinal tract diseases: challenges and opportunities. J. Gastroenterol. Hepatol. 2012, 27:1004-1010.
38. Koraichi F., Videmann B., Mazallon M., Benahmed M., Prouillac C., Lecoeur S. Zearalenone exposure modulates the expression of ABC transporters and nuclear receptors in pregnant rats and fetal liver. Toxicol. Lett. 2012, 211:246-256.
39. Kostro K., Dudek K., Lisiecka U., Majer-dziedzic B., Aleksiewicz R., Lutnicki K. Concentrations of proinflammatory mediators of the arachidonic acid cascade in serum of sheep with natural zearalenone intoxication. Bull. Vet. Inst. Pulawy 2012, 56:75-81.
40. Kuiper-Goodman T., Scott P.M., Watanabe H. Risk assessment of the mycotoxin zearalenone. Regul. Toxicol. Pharmacol. 1987, 7:253-306.
41. Liska D.J. The detoxification enzyme systems. Altern. Med. Rev. 1998, 3:187-198.
42. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
43. 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.
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. MacDonald S.J., Anderson S., Brereton P., Wood R., Damant A.J. Determination of zearalenone in barley, maize and wheat flour, polenta, and maize-based baby food by immunoaffinity column cleanup with liquid chromatography: interlaboratory study. AOAC Int. 2005, 88:1733-1740.
46. Marczuk-Krynicka D., Hryniewiecki T., Piatek J., Paluszak J. The effect of brief food withdrawal on the elevation of free radicals and other parameters of oxidative status in the liver. Med. Sci. Monit. 2003, 9:131-135.
47. Marin D.E., Taranu I. Overview on aflatoxins and oxidative stress. Toxin Rev. 2012, 31:32-43.
48. 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.
49. 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. Toxicol. In Vitro 2011, 25:1981-1988.
50. Minervini F., Dell'Aquila M.E. Zearalenone and reproductive function in farm animals. Int. J. Mol. Sci. 2008, 9:2570-2584.
51. Minervini F., Giannoccaro A., Fornelli F., Dell'Aquila M.E., Minoia P., Visconti A. Influence of mycotoxin zearalenone and its derivatives (alpha and beta zearalenol) on apoptosis and proliferation of cultured granulosa cells from equine ovaries. Reprod. Biol. Endocrinol. 2006, 4:62.
52. Mitak M., Gojmerac T., Cvrtila D., Cvetnić Z. Effect of atrazine and zearalenone on the number of receptor binding sites for 3H-estradiol in the rat uterus cytosol. Vet. Med. Czech 2002, 47:12-16.
53. NTP, 1982. Technical Report on the Carcinogenesis Bioassay of Zearalenone in F344/n Rats and B6c3f1 Mice (feed study).
54. Pazaiti A., Kontos M., Fentiman I.S. ZEN and the art of breast health maintenance. Int. J. Clin. Pract. 2012, 66:28-36.
55. 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 Chem. Toxicol. 1987, 25:297-304.
56. Richard J.L. Some major mycotoxins and their mycotoxicoses - an overview. Int. J. Food Microbiol. 2007, 119:3-10.
57. Ruh M.F., Bi Y., Cox L., Berk D., Howlett A.C., Bellone C.J. Effect of environmental estrogens on IL-1β promoter activity in a macrophage cell line. Endocrine 1998, 9:207-211.
58. 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). J. Pharm. Pharmacol. 2008, 60:761-770.
59. 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.
60. Scislowski V., Bauchart D., Gruffat D., Laplaud P.M., Durand D. Effect of dietary n-6 and n-3 polyunsaturated fatty acids on peroxidizability of lipoproteins in steers. Lipids 2005, 40:1245-1256.
61. Speranda M., Liker B., Speranda T., Seric V., Antunovic Z., Grabarevic Z., Sencic D., Grguric D., Steiner Z. Haematological and biochemical parameters of weaned piglets fed on fodder mixture contaminated by zearalenone with addition of clinoptilolite. Acta Vet. - Beograd. 2006, 56:121-136.
62. Streit E., Schatzmayr G., Tassis P., Tzika E., Marin D., Taranu I., Tabuc C., Nicolau A., Aprodu I., Puel O., Oswald I.P. Current situation of mycotoxin contamination and co-occurrence in animal feed-focus on Europe. Toxins (Basel) 2012, 4:788-809.
63. Tabuc C., Marin D., Guerre P., Sesan T., Bailly J.D. Molds and mycotoxin content of cereals in southeastern Romania. J. Food Prot. 2009, 72:662-665.
64. Takemura H., Shim J.Y., Sayama K., Tsubura A., Zhu T., Shimoi K. Characterization of the estrogenic activities of zearalenone and zeranol in vivo and in vitro. J. Steroid Biochem. Mol. Biol. 2007, 103:170-177.
65. Taranu I., Marin D.E., Burlacu R., Pinton P., Damian V., Oswald I.P. Comparative aspects of in vitro proliferation of human and porcine lymphocytes exposed to mycotoxins. Arch. Anim. Nutr. 2010, 64:383-393.
66. Taranu I., Marin D.E., Manda G., Motiu M., Neagoe I., Tabuc C., Stancu M., Olteanu M. Assessment of the potential of a boron-fructose additive in counteracting the toxic effect of Fusarium mycotoxins. Br. J. Nutr. 2011, 106:398-407.
67. Tiemann U., Brüssow K.P., Küchenmeister U., Jonas L., Kohlschein P., Pöhland R., Dänicke S. Influence of diets with cereal grains contaminated by graded levels of two Fusarium toxins on selected enzymatic and histological parameters of liver in gilts. Food Chem. Toxicol. 2006, 44:1228-1235.
68. Vlata Z., Porichis F., Tzanakakis G., Tsatsakis A., Krambovitis E. A study of zearalenone cytotoxicity on human peripheral blood mononuclear cells. Toxicol. Lett. 2006, 165:274-281.
69. Waclavicek M., Stich N., Rappan I., Bergmeister H., Eibl M.M. Analysis of the early response to TSST-1 reveals Vbeta-unrestricted extravasation, compartmentalization of the response, and unresponsiveness but not energy to TSST-1. J. Leukoc. Biol. 2009, 85:44-54.
70. 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. J. Anim. Physiol. Anim. Nutr. (Berl). 2012, 96:939-946.
71. World Health Organisation (WHO), 1991. Mycotoxins. Fact Sheet No. 5. Basic Food Safety for Health Workers.
72. Young L.G., King G.J. Low concentrations of zearalenone in diets of boars for a prolonged period of time. J. Anim. Sci. 1986, 63:1197-1200.
73. 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. Toxicol. In Vitro 2011, 25:1654-1663.
74. Zhu L., Yuan H., Guo C., Lu Y., Deng S., Yang Y., Wei Q., Wen L., He Z. Zearalenone induces apoptosis and necrosis in porcine granulosa cells via a caspase-3- and caspase-9-dependent mitochondrial signaling pathway. J. Cell Physiol. 2012, 227:1814-1820.
75. Zinedine A., Soriano J.M., Molto J.C., Manes J. Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin. Food Chem. Toxicol. 2007, 45:1-18.
76. Zourgui L., El Golli 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 Chem. Toxicol. 2008, 46:1817-1824.