High Temperature Disrupts Organelle Distribution and Functions Affecting Meiotic Maturation in Porcine Oocytes.

Song-Hee Lee,Ming-Hong Sun,Geun Heo,Xiao-Han Li,Xiang-Shun Cui,Dongjie Zhou,Wen-Jie Jiang

doi:10.3389/fcell.2022.826801

Abstract

Heat stress (HS) has been known to cause reproductive failure in animals, especially in summer. HS severely affects the developmental potential of oocytes and leads to low fertility rates. Previous studies have reported that HS compromises embryo development in bovine oocytes, and reduces ovarian development in mice, thereby impairing reproductive function in animals. However, the effect of high temperature (HT) on the organelles of porcine oocytes is unknown. In this study, we reported that exposure to HT for 24 h (41°C) significantly decreased meiotic maturation in porcine oocytes (p < 0.05). Further experiments on organelles found that HT induced mitochondrial dysfunction, increased abnormal mitochondrial distribution, and decreased mitochondrial membrane potential (MMP). We also found that HT induced abnormal endoplasmic reticulum (ER) distribution and higher expression of glucose regulatory protein 78 (GRP78), suggesting that HT exposure induces ER stress. Our results also indicated that exposure to HT induced abnormal distribution and dysfunction of the Golgi apparatus, which resulted from a decrease in the expression of the vesicle transporter, Ras-related protein Rab-11A (RAB11A). In addition, we found that HT exposure led to lysosomal damage by increasing the expression of lysosome-associated membrane protein 2 (LAMP2) and microtubule-associated protein 1A/1B-light chain 3 (LC3). In summary, our study revealed that HT exposure disrupts organelle dynamics, which further leads to the failure of meiotic maturation in porcine oocytes.

Highlights

Global warming is a major environmental issue that leads to climate change, which causes an increase in the annual average ambient temperature
Our results showed that high temperature (HT) exposure for 24 h induced mitochondrial dysfunction and abnormal distribution, which may have contributed to endoplasmic reticulum (ER) stress and abnormal ER distribution
To evaluate the harmful effects of HT on porcine oocytes, we first investigated the maturation of oocytes incubated at 41°C for 15 h or 24 h

Summary

INTRODUCTION

Global warming is a major environmental issue that leads to climate change, which causes an increase in the annual average ambient temperature. High Temperature Affects Meiotic Maturation embryos, disrupting fertilization and embryo development (Jin et al, 2007; Hansen, 2019) This causes huge economic damage to livestock and influences the welfare of animals (Boni, 2019). Cellular waste is recycled in lysosomes through the autophagy pathway, which sequesters damaged organelles and misfolded proteins for lysosomal degradation (Ballabio and Bonifacino, 2020) Several factors, such as maternal feeding, management, stress, and various environmental factors, affect oocyte developmental competence (Belhadj Slimen et al, 2016). Our results showed that HT exposure for 24 h induced mitochondrial dysfunction and abnormal distribution, which may have contributed to ER stress and abnormal ER distribution These dysfunctions further contributed to Golgi apparatus dysfunction and affected lysosome function in porcine oocytes. Our study demonstrated the negative effect of HS on organelle functions in mammalian oocytes

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RESULTS

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