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

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 de...

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Autores principales: Lee, Song-Hee, Sun, Ming-Hong, Zhou, Dongjie, Jiang, Wen-Jie, Li, Xiao-Han, Heo, Geun, Cui, Xiang-Shun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8894851/
https://www.ncbi.nlm.nih.gov/pubmed/35252192
http://dx.doi.org/10.3389/fcell.2022.826801
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author Lee, Song-Hee
Sun, Ming-Hong
Zhou, Dongjie
Jiang, Wen-Jie
Li, Xiao-Han
Heo, Geun
Cui, Xiang-Shun
author_facet Lee, Song-Hee
Sun, Ming-Hong
Zhou, Dongjie
Jiang, Wen-Jie
Li, Xiao-Han
Heo, Geun
Cui, Xiang-Shun
author_sort Lee, Song-Hee
collection PubMed
description 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.
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spelling pubmed-88948512022-03-05 High Temperature Disrupts Organelle Distribution and Functions Affecting Meiotic Maturation in Porcine Oocytes Lee, Song-Hee Sun, Ming-Hong Zhou, Dongjie Jiang, Wen-Jie Li, Xiao-Han Heo, Geun Cui, Xiang-Shun Front Cell Dev Biol Cell and Developmental Biology 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. Frontiers Media S.A. 2022-02-18 /pmc/articles/PMC8894851/ /pubmed/35252192 http://dx.doi.org/10.3389/fcell.2022.826801 Text en Copyright © 2022 Lee, Sun, Zhou, Jiang, Li, Heo and Cui. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Lee, Song-Hee
Sun, Ming-Hong
Zhou, Dongjie
Jiang, Wen-Jie
Li, Xiao-Han
Heo, Geun
Cui, Xiang-Shun
High Temperature Disrupts Organelle Distribution and Functions Affecting Meiotic Maturation in Porcine Oocytes
title High Temperature Disrupts Organelle Distribution and Functions Affecting Meiotic Maturation in Porcine Oocytes
title_full High Temperature Disrupts Organelle Distribution and Functions Affecting Meiotic Maturation in Porcine Oocytes
title_fullStr High Temperature Disrupts Organelle Distribution and Functions Affecting Meiotic Maturation in Porcine Oocytes
title_full_unstemmed High Temperature Disrupts Organelle Distribution and Functions Affecting Meiotic Maturation in Porcine Oocytes
title_short High Temperature Disrupts Organelle Distribution and Functions Affecting Meiotic Maturation in Porcine Oocytes
title_sort high temperature disrupts organelle distribution and functions affecting meiotic maturation in porcine oocytes
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8894851/
https://www.ncbi.nlm.nih.gov/pubmed/35252192
http://dx.doi.org/10.3389/fcell.2022.826801
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