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Luteolin Orchestrates Porcine Oocyte Meiotic Progression by Maintaining Organelle Dynamics Under Oxidative Stress

Increasing evidence has demonstrated that oxidative stress impairs oocyte maturation, but the underlying mechanisms remain largely unknown. Here, for the first time, we examined the antioxidant role of luteolin in meiotic progression and the underlying mechanisms. Supplementation of 5 μM luteolin in...

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Autores principales: Park, Soo-Hyun, Jeong, Pil-Soo, Joo, Ye Eun, Kang, Hyo-Gu, Kim, Min Ju, Lee, Sanghoon, Song, Bong-Seok, Kim, Sun-Uk, Cho, Seong-Keun, Sim, Bo-Woong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8239245/
https://www.ncbi.nlm.nih.gov/pubmed/34211977
http://dx.doi.org/10.3389/fcell.2021.689826
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author Park, Soo-Hyun
Jeong, Pil-Soo
Joo, Ye Eun
Kang, Hyo-Gu
Kim, Min Ju
Lee, Sanghoon
Song, Bong-Seok
Kim, Sun-Uk
Cho, Seong-Keun
Sim, Bo-Woong
author_facet Park, Soo-Hyun
Jeong, Pil-Soo
Joo, Ye Eun
Kang, Hyo-Gu
Kim, Min Ju
Lee, Sanghoon
Song, Bong-Seok
Kim, Sun-Uk
Cho, Seong-Keun
Sim, Bo-Woong
author_sort Park, Soo-Hyun
collection PubMed
description Increasing evidence has demonstrated that oxidative stress impairs oocyte maturation, but the underlying mechanisms remain largely unknown. Here, for the first time, we examined the antioxidant role of luteolin in meiotic progression and the underlying mechanisms. Supplementation of 5 μM luteolin increased the rates of first polar body extrusion and blastocyst formation after parthenogenetic activation, and the expression levels of oocyte competence (BMP15 and GDF9)-, mitogen-activated protein kinase (MOS)-, and maturation promoting factor (CDK1 and Cyclin B)-related genes were also improved. Luteolin supplementation decreased intracellular reactive oxygen species levels and increased the expression levels of oxidative stress-related genes (SOD1, SOD2, and CAT). Interestingly, luteolin alleviated defects in cell organelles, including actin filaments, the spindle, mitochondria, the endoplasmic reticulum, and cortical granules, caused by H(2)O(2) exposure. Moreover, luteolin significantly improved the developmental competence of in vitro-fertilized embryos in terms of the cleavage rate, blastocyst formation rate, cell number, cellular survival rate, and gene expression and markedly restored the competencies decreased by H(2)O(2) treatment. These findings revealed that luteolin supplementation during in vitro maturation improves porcine meiotic progression and subsequent embryonic development by protecting various organelle dynamics against oxidative stress, potentially increasing our understanding of the underlying mechanisms governing the relationship between oxidative stress and the meiotic events required for successful oocyte maturation.
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spelling pubmed-82392452021-06-30 Luteolin Orchestrates Porcine Oocyte Meiotic Progression by Maintaining Organelle Dynamics Under Oxidative Stress Park, Soo-Hyun Jeong, Pil-Soo Joo, Ye Eun Kang, Hyo-Gu Kim, Min Ju Lee, Sanghoon Song, Bong-Seok Kim, Sun-Uk Cho, Seong-Keun Sim, Bo-Woong Front Cell Dev Biol Cell and Developmental Biology Increasing evidence has demonstrated that oxidative stress impairs oocyte maturation, but the underlying mechanisms remain largely unknown. Here, for the first time, we examined the antioxidant role of luteolin in meiotic progression and the underlying mechanisms. Supplementation of 5 μM luteolin increased the rates of first polar body extrusion and blastocyst formation after parthenogenetic activation, and the expression levels of oocyte competence (BMP15 and GDF9)-, mitogen-activated protein kinase (MOS)-, and maturation promoting factor (CDK1 and Cyclin B)-related genes were also improved. Luteolin supplementation decreased intracellular reactive oxygen species levels and increased the expression levels of oxidative stress-related genes (SOD1, SOD2, and CAT). Interestingly, luteolin alleviated defects in cell organelles, including actin filaments, the spindle, mitochondria, the endoplasmic reticulum, and cortical granules, caused by H(2)O(2) exposure. Moreover, luteolin significantly improved the developmental competence of in vitro-fertilized embryos in terms of the cleavage rate, blastocyst formation rate, cell number, cellular survival rate, and gene expression and markedly restored the competencies decreased by H(2)O(2) treatment. These findings revealed that luteolin supplementation during in vitro maturation improves porcine meiotic progression and subsequent embryonic development by protecting various organelle dynamics against oxidative stress, potentially increasing our understanding of the underlying mechanisms governing the relationship between oxidative stress and the meiotic events required for successful oocyte maturation. Frontiers Media S.A. 2021-06-15 /pmc/articles/PMC8239245/ /pubmed/34211977 http://dx.doi.org/10.3389/fcell.2021.689826 Text en Copyright © 2021 Park, Jeong, Joo, Kang, Kim, Lee, Song, Kim, Cho and Sim. 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
Park, Soo-Hyun
Jeong, Pil-Soo
Joo, Ye Eun
Kang, Hyo-Gu
Kim, Min Ju
Lee, Sanghoon
Song, Bong-Seok
Kim, Sun-Uk
Cho, Seong-Keun
Sim, Bo-Woong
Luteolin Orchestrates Porcine Oocyte Meiotic Progression by Maintaining Organelle Dynamics Under Oxidative Stress
title Luteolin Orchestrates Porcine Oocyte Meiotic Progression by Maintaining Organelle Dynamics Under Oxidative Stress
title_full Luteolin Orchestrates Porcine Oocyte Meiotic Progression by Maintaining Organelle Dynamics Under Oxidative Stress
title_fullStr Luteolin Orchestrates Porcine Oocyte Meiotic Progression by Maintaining Organelle Dynamics Under Oxidative Stress
title_full_unstemmed Luteolin Orchestrates Porcine Oocyte Meiotic Progression by Maintaining Organelle Dynamics Under Oxidative Stress
title_short Luteolin Orchestrates Porcine Oocyte Meiotic Progression by Maintaining Organelle Dynamics Under Oxidative Stress
title_sort luteolin orchestrates porcine oocyte meiotic progression by maintaining organelle dynamics under oxidative stress
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8239245/
https://www.ncbi.nlm.nih.gov/pubmed/34211977
http://dx.doi.org/10.3389/fcell.2021.689826
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