Comparative analysis of the detrimental in vitro effects of three fusariotoxins on the selected structural and functional characteristics of rabbit spermatozoa

References

• Abid-Essefi, S., et al., 2004. Cytotoxicity, inhibition of DNA and protein syntheses and oxidative damage in cultured cells exposed to zearalenone. Toxicology in Vitro, 18 (4), 467–474.
   PubMed Web of Science ®Google Scholar
• Alshannaq, A. and Yu, J.H., 2017. Occurrence, toxicity, and analysis of major mycotoxins in food. International Journal of Environmental Research and Public Health, 14 (6), E632.
   PubMed Web of Science ®Google Scholar
• Awad, W.A., et al., 2012. Genotoxic effects of deoxynivalenol in broiler chickens fed low-protein feeds. Poultry Science, 91 (3), 550–555.
   PubMed Web of Science ®Google Scholar
• Banjerdpongchai, R., et al., 2010. Mitochondrial and endoplasmic reticulum stress pathways cooperate in zearalenone-induced apoptosis of human leukemic cells. Journal of Hematology & Oncology, 3, 50.
   PubMed Web of Science ®Google Scholar
• Barbagallo, F., et al., 2020. Evaluation of sperm mitochondrial function: a key organelle for sperm motility. Journal of Clinical Medicine, 9, 363.
   Web of Science ®Google Scholar
• Bensassi, F., et al., 2009. Pathway of deoxynivalenol-induced apoptosis in human colon carcinoma cells. Toxicology, 264 (1–2), 104–109.
   PubMed Web of Science ®Google Scholar
• Benzoni, E., et al., 2008. Influence of in vitro exposure to mycotoxin zearalenone and its derivatives on swine sperm quality. Reproductive Toxicology, 25 (4), 461–467.
   PubMed Web of Science ®Google Scholar
• Bielas, W., et al., 2017. Effect of zearalenone on circulating testosterone concentration, testicular and epididymal morphology and epididymal sperm characteristics in wild boars. Theriogenology, 102, 59–66.
   PubMed Web of Science ®Google Scholar
• Bouaziz, C., et al., 2008. Different apoptotic pathways induced by zearalenone, T-2 toxin and ochratoxin A in human hepatoma cells. Toxicology, 254 (1–2), 19–28.
   PubMed Web of Science ®Google Scholar
• Bouaziz, C., et al., 2009. Fusarial toxin-induced toxicity in cultured cells and in isolated mitochondria involves PTPC-dependent activation of the mitochondrial pathway of apoptosis. Toxicological Sciences, 110 (2), 363–375.
   PubMed Web of Science ®Google Scholar
• Cao, Z., et al., 2020. Deoxynivalenol induced spermatogenesis disorder by blood-testis barrier disruption associated with testosterone deficiency and inflammation in mice. Environmental Pollution, 264, 114748.
   PubMed Web of Science ®Google Scholar
• Dalcero, A., et al., 2002. Detection of ochratoxin A in animal feeds and capacity to produce this mycotoxin by Aspergillus section Nigri in Argentina. Food Additives and Contaminants, 19 (11), 1065–1072.
   PubMed Web of Science ®Google Scholar
• Demaegdt, H., et al., 2016. Endocrine activity of mycotoxins and mycotoxin mixtures. Food and Chemical Toxicology, 96, 107–116.
   PubMed Web of Science ®Google Scholar
• El Khoury, D., et al., 2019. Updates on the effect of mycotoxins on male reproductive efficiency in mammals. Toxins, 11, 515.
   Web of Science ®Google Scholar
• Ennamany, R., et al., 1995. Lipid peroxidation induced by bolesatine, a toxin of Boletus satanas: implication in m5dC variation in Vero cells related to inhibition of cell growth. Cell Biology and Toxicology, 11 (6), 347–354.
   PubMed Web of Science ®Google Scholar
• Ewuola, E.O. and Egbunike, G.N., 2010a. Effects of dietary fumonisin B1 on the onset of puberty, semen quality, fertility rates and testicular morphology in male rabbits. Reproduction, 139 (2), 439–445.
   PubMed Web of Science ®Google Scholar
• Ewuola, E.O. and Egbunike, G.N., 2010b. Gonadal and extra-gonadal sperm reserves and sperm production of pubertal rabbits fed dietary fumonisin B1. Animal Reproduction Science, 119 (3–4), 282–286.
   PubMed Web of Science ®Google Scholar
• Fan, W., et al., 2017. Zearalenone induces ROS-mediated mitochondrial damage in porcine IPEC-J2 cells. Journal of Biochemical and Molecular Toxicology, 31 (10), e21944.
   Web of Science ®Google Scholar
• Filannino, A., et al., 2011. Dose-response effects of estrogenic mycotoxins (zearalenone, alpha- and beta-zearalenol) on motility, hyperactivation and the acrosome reaction of stallion sperm. Reproductive Biology and Endocrinology: RB&E, 9, 134.
   PubMed Web of Science ®Google Scholar
• Frankic, T., et al., 2006. The role of dietary nucleotides in reduction of DNA damage induced by T-2 toxin and deoxynivalenol in chicken leukocytes. Food and Chemical Toxicology, 44 (11), 1838–1844.
   PubMed Web of Science ®Google Scholar
• Frizzell, C., et al., 2011. Endocrine disrupting effects of zearalenone, alpha- and beta-zearalenol at the level of nuclear receptor binding and steroidogenesis. Toxicology Letters, 206 (2), 210–217.
   PubMed Web of Science ®Google Scholar
• Gosalvez, J., et al., 2015. Unpacking the mysteries of sperm DNA fragmentation: ten frequently asked questions. Journal of Reproductive Biotechnology and Fertility, 4, 205891581559445–205891581559416.
   Google Scholar
• Greco, M.V., et al., 2012. Mycoflora and natural incidence of selected mycotoxins in rabbit and Chinchilla feeds. The Scientific World Journal, 2012, 1–6.
   Web of Science ®Google Scholar
• Hallaj Salahipour, M., et al., 2019. Deoxynivalenol reduces quality parameters and increases DNA damage in mice spermatozoa. Andrologia, 51 (5), e13238.
   PubMed Web of Science ®Google Scholar
• Hassen, W., et al., 2005. Cytotoxicity and Hsp 70 induction in Hep G2 cells in response to zearalenone and cytoprotection by sub-lethal heat shock. Toxicology, 207 (2), 293–301.
   PubMed Web of Science ®Google Scholar
• Hou, Y.J., et al., 2013. Mycotoxin-containing diet causes oxidative stress in the mouse. PLoS One, 8 (3), e60374.
   PubMed Web of Science ®Google Scholar
• Kachlek, M., et al., 2017. Preliminary results on the interactive effects of deoxynivalenol, zearalenone and fumonisin B1 on porcine lymphocytes. Acta Veterinaria Hungarica, 65 (3), 340–353.
   PubMed Web of Science ®Google Scholar
• Karacaoglu, E. and Selmanoglu, G., 2017. T-2 toxin induces cytotoxicity and disrupts tight junction barrier in SerW3 cells. Environmental Toxicology and Pharmacology, 56, 259–267.
   PubMed Web of Science ®Google Scholar
• Kashou, A.H., Sharma, R., and Agarwal, A., 2013. Assessment of oxidative stress in sperm and semen. Methods in Molecular Biology, 927, 351–361.
   PubMedGoogle Scholar
• Keller, N.P., Turner, G., and Bennett, J.W., 2005. Fungal secondary metabolism – from biochemistry to genomics. Nature Reviews Microbiology, 3 (12), 937–947.
   PubMed Web of Science ®Google Scholar
• Kouadio, J.H., et al., 2005. Comparative study of cytotoxicity and oxidative stress induced by deoxynivalenol, zearalenone or fumonisin B1 in human intestinal cell line Caco-2. Toxicology, 213 (1–2), 56–65.
   PubMed Web of Science ®Google Scholar
• Long, M., et al., 2017. Characterization of semen quality, testicular marker enzyme activities and gene expression changes in the blood testis barrier of Kunming mice following acute exposure to zearalenone. Environmental Science and Pollution Research International, 24 (35), 27235–27243.
   PubMed Web of Science ®Google Scholar
• López, T.A., et al., 1988. Hyperestrogenism in swine due to natural poisoning with zearalenone. Revista Argentina de Microbiologia, 20 (3), 119–123.
   PubMedGoogle Scholar
• Medveďová, M., et al., 2012. The effect of deoxynivalenol on rabbit spermatozoa motility in vitro. Journal of Microbiology, Biotechnology and Food Sciences, 2, 368–377.
   Google Scholar
• Mézes, M. and Balogh, K., 2009. Mycotoxins in rabbit feed: a review. World Rabbit Science, 17, 53–62.
   Web of Science ®Google Scholar
• Minervini, F. and Dell'Aquila, M.E., 2008. Zearalenone and reproductive function in farm animals. International Journal of Molecular Sciences, 9 (12), 2570–2584.
   PubMed Web of Science ®Google Scholar
• Mngadi, P.T., Govinden, R., and Odhav, B., 2008. Co-occurring mycotoxins in animal feeds. African Journal of Biotechnology, 7, 2239–2243.
   Google Scholar
• Mohanamba, T., Rao, M.R., and Habibi, S.M.M., 2007. Aflatoxin contamination in animal feeds. Indian Veterinary Journal, 84, 416.
   Google Scholar
• Molina-Molina, J.M., et al., 2014. Assessment of estrogenic and anti-androgenic activities of the mycotoxin zearalenone and its metabolites using in vitro receptor-specific c bioassays. Food and Chemical Toxicology, 74, 233–239.
   PubMed Web of Science ®Google Scholar
• Qin, X., et al., 2015. Oxidative stress induced by zearalenone in porcine granulosa cells and its rescue by curcumin in vitro. PLoS One, 10 (6), e0127551.
   PubMed Web of Science ®Google Scholar
• Reis, L.S., et al., 2016. Integrity of the plasma membrane, the acrosomal membrane, and the mitochondrial membrane potential of sperm in Nelore bulls from puberty to sexual maturity. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 68 (3), 620–628.
   Web of Science ®Google Scholar
• Rezar, V., et al., 2007. Dose-dependent effects of T-2 toxin on performance, lipid peroxidation, and genotoxicity in broiler chickens. Poultry Science, 86 (6), 1155–1111.
   PubMed Web of Science ®Google Scholar
• Rizzo, A.F., et al., 1994. Protective effect of antioxidants against free radical-mediated lipid peroxidation induced by DON or T-2 toxin. Zentralblatt Fur Veterinarmedizin. Reihe A, 41 (2), 81–90.
   PubMedGoogle Scholar
• Rocha, O., Ansari, K., and Doohan, F.M., 2005. Effects of trichothecene mycotoxins on eukaryotic cells: a review. Food Additives and Contaminants, 22 (4), 369–378.
   PubMed Web of Science ®Google Scholar
• Solakidi, S., et al., 2005. Estrogen receptors alpha and beta (ERalpha and ERbeta) and androgen receptor (AR) in human sperm: localization of ERbeta and AR in mitochondria of the midpiece. Human Reproduction, 20 (12), 3481–3487.
   PubMed Web of Science ®Google Scholar
• Sprando, R.L., et al., 2005. Characterization of the effect of deoxynivalenol on selected male reproductive endpoints. Food and Chemical Toxicology, 43 (4), 623–635.
   PubMed Web of Science ®Google Scholar
• Tkachev, A.V. and Tkacheva, O.L., 2017. Comparison of the cytotoxic effects of zearalenone and T-2 toxin on the horses and oxen germ cell in vitro before and after cryopreservation. Tsitologiia, 59, 45–52.
   PubMedGoogle Scholar
• Tsakmakidis, I.A., et al., 2006. In vitro effect of zearalenone and alpha-zearalenol on boar sperm characteristics and acrosome reaction. Reproduction in Domestic Animals, 41 (5), 394–401.
   PubMed Web of Science ®Google Scholar
• Tvrdá, E., et al., 2011. Impact of oxidative stress on male fertility – a review. Acta Veterinaria Hungarica, 59 (4), 465–484.
   PubMed Web of Science ®Google Scholar
• Tvrda, E., et al., 2015. Resveratrol offers protection to oxidative stress induced by ferrous ascorbate in bovine spermatozoa. Journal of Environmental Science and Health, Part A, 50, 1440–1451.
   PubMed Web of Science ®Google Scholar
• Tvrdá, E., et al., 2016. In vitro effects of selected trichothecenes on the rabbit spermatozoa motility behavior – a comparative study. Contemporary Agriculture, 65 (3–4), 21–26.
   Google Scholar
• Van De Walle, J., et al., 2008. Influence of deoxynivalenol on NF‐κB activation and IL‐8 secretion in human intestinal Caco‐2 cells. Toxicology Letters, 177 (3), 205–214.
   PubMed Web of Science ®Google Scholar
• Wan, L.Y., Turner, P.C., and El-Nezami, H., 2013. Individual and combined cytotoxic effects of Fusarium toxins (deoxynivalenol, nivalenol, zearalenone and fumonisins B1) on swine jejunal epithelial cells. Food and Chemical Toxicology, 57, 276–283.
   PubMed Web of Science ®Google Scholar
• Warikoo, P.K., et al., 1986. Interactions among motility, fertilizing ability, and testosterone binding on spermatozoa of bonnet monkey (Macaca radiata). Archives of Andrology, 16 (2), 135–141.
   PubMed Web of Science ®Google Scholar
• Wild, C.P. and Gong, Y.Y., 2010. Mycotoxins and human disease: a largely ignored global health issue. Carcinogenesis, 31 (1), 71–82.
   PubMed Web of Science ®Google Scholar
• Wu, Q.H., et al., 2014. Oxidative stress-mediated cytotoxicity and metabolism of T-2 toxin and deoxynivalenol in animals and humans: an update. Archives of Toxicology, 88 (7), 1309–1326.
   PubMed Web of Science ®Google Scholar
• Xu, Y., et al., 2019. Protective effects of melatonin against zearalenone toxicity on porcine embryos in vitro. Frontiers in Pharmacology, 10, 327.
   PubMed Web of Science ®Google Scholar
• Yang, J.Y., et al., 2007a. Toxic effects of zearalenone and its derivatives alpha-zearalenol on male reproductive system in mice. Reproductive Toxicology, 24 (3–4), 381–387.
   PubMed Web of Science ®Google Scholar
• Yang, J., et al., 2007b. Toxic effects of zearalenone and alpha-zearalenol on the regulation of steroidogenesis and testosterone production in mouse Leydig cells. Toxicology in Vitro, 21 (4), 558–565.
   PubMed Web of Science ®Google Scholar
• Yang, W., et al., 2014. Deoxynivalenol induced oxidative stress and genotoxicity in human peripheral blood lymphocytes. Food and Chemical Toxicology, 64, 383–396.
   PubMed Web of Science ®Google Scholar
• Yang, R., et al., 2016. Prepubertal exposure to T-2 toxin advances pubertal onset and development in female rats via promoting the onset of hypothalamic-pituitary-gonadal axis function. Human & Experimental Toxicology, 35 (12), 1276–1285.
   PubMed Web of Science ®Google Scholar
• Yang, X., et al., 2019. Spermatogenesis disorder caused by T-2 toxin is associated with germ cell apoptosis mediated by oxidative stress. Environmental Pollution, 251, 372–366.
   PubMed Web of Science ®Google Scholar
• Yu, J.Y., et al., 2011. Mycotoxin zearalenone induces AIF- and ROS-mediated cell death through p53- and MAPK-dependent signaling pathways in RAW264.7 macrophages. Toxicology in Vitro, 25 (8), 1654–1663.
   PubMed Web of Science ®Google Scholar
• Zhuang, Z., et al., 2013. Study on the apoptosis mechanism induced by T-2 toxin. PLoS One, 8 (12), e83105.
   PubMed Web of Science ®Google Scholar