Fumonisin B1 exposure adversely affects porcine oocyte maturation in vitro by inducing mitochondrial dysfunction and oxidative stress

Abstract

Fumonisin B1 (FB1), as the most toxic fumonisin, is a common Fusarium mycotoxin contaminant of feed stuff and food, posing a potential health hazard to animals and humans. FB1 has been reported to cause hepatotoxicity, neurotoxicity, nephrotoxicity, immunotoxicity and embryotoxicity; however, little information is available on whether FB1 has toxic effects on mammalian oocytes. Herein, we adopted porcine oocytes as models to explore the effects and potential mechanisms of FB1 on mammalian oocytes during in vitro maturation. Porcine cumulus oocyte complexes (COCs) were exposed to 0, 20, 30 and 40 μM FB1 for 44 h during in vitro maturation, and the results reported that first polar body (PB1) extrusion was significantly inhibited when the FB1 concentration reached 30 (P < 0.01) or 40 μM (P < 0.001). Further cell cycle analysis revealed that meiotic progression was disrupted, with a larger proportion of the 30 μM FB1-treated oocytes being arrested at the germinal vesicle breakdown (GVBD) stage (P < 0.01). After being treated with 30 μM FB1 for 28 h, the percentage of oocytes with aberrant spindle assembly was observably increased (P < 0.01), and the distribution of actin filaments on the plasma membrane was significantly reduced (P < 0.05). Furthermore, an observably higher rate of abnormal mitochondrial distribution (P < 0.05) and significantly decreased mitochondrial membrane potential (MMP) (P < 0.05) were observed in FB1-exposed oocytes. In addition, ROS generation in FB1-treated oocytes was rapidly increased (P < 0.05), while the transcriptional levels of antioxidant-related genes (CAT, SOD2 and GSH-Px) were sharply decreased compared with those in the control group. Additionally, the incidence of early apoptosis in FB1-treated oocytes was also significantly increased (P < 0.05), suggesting that FB1 exposure induced oxidative stress and further triggered apoptosis in porcine oocytes. Thus, these results suggested that FB1 adversely affected oocyte maturation by disturbing cell cycle progression, destroying cytoskeletal dynamics and damaging mitochondrial function, which eventually induced oxidative stress and apoptosis in porcine oocytes.