Tributyltin Oxide Exposure During in vitro Maturation Disrupts Oocyte Maturation and Subsequent Embryonic Developmental Competence in Pigs.

Yue Xiao,Boxing Sun,Jiabao Zhang,Weiyi Hu,Hao Jiang,Shuang Liang,Jiajia Qi,Bao Yuan

doi:10.3389/fcell.2021.683448

Abstract

Tributyltin oxide (TBTO), an organotin compound, has been demonstrated to have toxic effects on several cell types. Previous research has shown that TBTO impairs mouse denuded oocyte maturation. However, limited information is available on the effects of TBTO exposure on livestock reproductive systems, especially on porcine oocytes in the presence of dense cumulus cells. In the present research, we evaluated the effects of TBTO exposure on porcine oocyte maturation and the possible underlying mechanisms. Porcine cumulus-oocyte complexes were cultured in maturation medium with or without TBTO for 42 h. We found that TBTO exposure during oocyte maturation prevented polar body extrusion, inhibited cumulus expansion and impaired subsequent blastocyst formation after parthenogenetic activation. Further analysis revealed that TBTO exposure not only induced intracellular reactive oxygen species (ROS) accumulation but also caused a loss of mitochondrial membrane potential and reduced intracellular ATP generation. In addition, TBTO exposure impaired porcine oocyte quality by disrupting cellular iron homeostasis. Taken together, these results demonstrate that TBTO exposure impairs the porcine oocyte maturation process by inducing intracellular ROS accumulation, causing mitochondrial dysfunction, and disrupting cellular iron homeostasis, thus decreasing the quality and impairing the subsequent embryonic developmental competence of porcine oocytes.

Highlights

Increasing amounts of evidence indicate that environmental pollutants may harm human health because these contaminants can gradually accumulate in the human body after consumption of tainted water and food (Carbery et al, 2018; Kuckelkorn et al, 2018)
To determine the potential effect of TBTO exposure on porcine oocyte maturation during the in vitro Maturation (IVM) period, Cumulus-oocyte complexes (COCs) were treated with increasing concentrations of TBTO (5, 25, and 50 μM), and the percentages of oocytes with Polar body extrusion (PBE) were analyzed at the end of IVM
The results revealed that TBTO exposure dose-dependently decreased the percentage of oocytes with PBE (Figure 1)

Summary

Introduction

Increasing amounts of evidence indicate that environmental pollutants may harm human health because these contaminants can gradually accumulate in the human body after consumption of tainted water and food (Carbery et al, 2018; Kuckelkorn et al, 2018). The organotin compound tributyltin (TBT), a bioaccumulative and persistent environmental pollutant, has become a subject of great concern (Pereira et al, 2019; Jie et al, 2021). Humans can be exposed to TBT through consumption of contaminated fish and seafood, and the ingested. TBT can affect the reproductive system (Lang Podratz et al, 2012; Xiao et al, 2018) and immune system (Frouin et al, 2008; Brown and Whalen, 2015). Previous studies have reported that TBT exposure may disrupt oogenesis and serotonin synthesis (Xiao et al, 2018), decrease ovarian weight, unbalance the levels of female sex hormones, and elevate the numbers of atretic follicles and corpora lutea (Lang Podratz et al, 2012). TBT exposure inhibits estrogen receptor-dependent transcriptional activation and prevents the interaction between the human estrogen receptor β ligand-binding domain (LBD) and steroid receptor coactivator-1 in yeast (Cho et al, 2012)

Methods

Results

Discussion

Conclusion