Exposure to Copper Compromises the Maturational Competency of Porcine Oocytes by Impairing Mitochondrial Function.

Jingyue Chen,Qian Gao,Huili Wang,Xingxing Zhang,Bo Xiong,Yilong Miao,Zhaokang Cui,Yawei Qiu,Fang Chen

doi:10.3389/fcell.2021.678665

Abstract

Copper (Cu) is an essential trace element for animals, and also an important nutritional component for the normal physiology and metabolism of animal reproductive systems. An excess or lack of Cu will directly or indirectly affect animal reproductive activities. However, the effect of Cu, in particular excessive Cu, on the reproductive performance of sows has not been studied. Here, we report that excessive Cu had negative effects on oocyte maturation and organelle functions. We showed that Cu exposure perturbed porcine oocyte meiotic maturation and impaired spindle/chromosome structure, resulting in a defective spindle assembly, as well as the abnormal distribution of actin dynamics and cortical granules. In addition, single-cell transcriptome analysis identified the target effectors of Cu actions in porcine oocytes, further demonstrating that Cu exposure affects the mitochondrial distribution and function, leading to the high levels of reactive oxygen species, DNA damage, and early apoptosis of porcine oocytes. These findings demonstrate that Cu exposure causes abnormalities in the mitochondrial distribution and function, resulting in the increased oxidative stress and levels of reactive oxygen species, DNA damage, and apoptosis, ultimately leading to a decreased porcine oocyte quality.

Highlights

Copper (Cu) is an essential trace element that plays an important role in a normal growth, development, metabolism, and reproduction
To confirm whether Cu exposure has effects on the porcine oocyte maturation, we chose different doses of Cu which were added to the maturation medium during the in vitro maturation (IVM)
Quantitative data displayed that the proportion of PBE was reduced in a dose-dependent manner after Cu exposure compared with the controls (68.8 ± 1.1%, n = 110, control vs. 57.3 ± 2.0%, n = 101, 15 μg/mL Cu, P = 0.133 vs. 37.9 ± 1.7%, n = 109, 25 μg/mL Cu, P < 0.0001 vs. 29.8 ± 1.6%, n = 119, 50 μg/mL Cu, P < 0.0001 vs. 5.1 ± 1.5%, n = 111, 100 μg/mL Cu, P < 0.0001; Figure 1B)

Summary

Introduction

Copper (Cu) is an essential trace element that plays an important role in a normal growth, development, metabolism, and reproduction. Excessive heavy metal levels pose a serious problem for animal feed safety in China. Enrichment of heavy metals in soil of forage crops or the addition of heavy metals may lead to excessive levels in animal feed (Hejna et al, 2018). The unsuitable use of Cu, a heavy metal, has adversely affected livestock production and, more importantly, excessive addition of dietary Cu to livestock has led to serious environmental problems via its excretion in feces (Sutton and Richert, 2004). Cu pollution in the environment could lead to Cu poisoning in animals, and sheep are very sensitive to Cu. Cu poisoning in sheep can cause renal degeneration, Copper Compromises Oocytes Quality hemolysis, and central nervous system diseases (Dewes, 1996; Grace, 2006). Cu pollution of environmental contaminants may influence a behavioral problem in children, and child Cu exposure was associated with higher internalizing symptoms (Maitre et al, 2021)

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Conclusion