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Exposure of Oocytes to the Fusarium Toxins Zearalenone and Deoxynivalenol Causes Aneuploidy and Abnormal Embryo Development in Pigs¹

Departments of Veterinary Pharmacology, Pharmacy and Toxicology,⁴ Farm Animal Health,⁵ and Biochemistry and Cell Biology,⁶ Faculty of Veterinary Medicine, Utrecht University, 3584 CM Utrecht, The Netherlands

ABSTRACT

Fungi of the Fusarium species can infect food and feed commodities and produce the mycotoxins zearalenone (ZEA) and deoxynivalenol (DON). Since both toxins have been reported to reduce fertility, the mechanisms of ZEA and DON on inhibition of oocyte maturation were examined. Pig oocytes were matured in the presence of ZEA (a mycotoxin with estrogenlike activity), 17beta-estradiol, and DON (all 3.12 µmol/L). Zearalenone, 17beta-estradiol, and DON inhibited oocyte maturation and caused approximately 34% of the oocytes to form an aberrant spindle. Different ratios of ZEA:DON did not lead to a more severe inhibition of oocyte maturation. Both mycotoxins caused abnormal formation of the meiotic spindle. The developmental competence of oocytes matured in the presence of mycotoxins was further investigated after in vitro fertilization. Presence of ZEA (3.12 µmol/L) during maturation reduced the percentages of oocytes that cleaved and formed a blastocyst to about 12%, compared with 25% of control oocytes. Maturation in the presence of equimolar concentrations of DON was not compatible with development. The ploidy of blastomeres from blastocysts derived from mycotoxin-exposed oocytes was analyzed with fluorescent in situ hybridization. All blastocysts, even those from the control group, contained at least one blastomere with abnormal ploidy, but the variation in the percentages of aneuploid blastomeres was significantly larger in embryos from oocytes exposed to mycotoxins. It is concluded that ZEA and DON can lead to abnormal spindle formation, leading to less fertile oocytes and embryos with abnormal ploidy, and that the effects of ZEA and DON are not synergistic.

deoxynivalenol, early development, embryo, food safety, in vitro fertilization, meiosis, mixoploidy, reproduction, toxicology, zearalenone

³Current address: Department of Pharmacology and Toxicology, Faculty of Veterinary Medicine, Urmia University, PO Box 1177, Urmia, Iran.

¹Supported by the Iranian Ministry of Sciences, Research, and Technology.

Correspondence: ²Bernard A.J. Roelen, Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 104, 3584 CM, Utrecht, The Netherlands. FAX: 31 30 25348811; e-mail: b.a.j.roelen{at}vet.uu.nl