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.

Keywords: Cytoskeletal dynamics; Fumonisin B(1); Mitochondria; Oxidative stress; Porcine oocytes.