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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Frontiers Media S.A.
2021-06-01
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Series: | Frontiers in Cell and Developmental Biology |
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Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2021.689826/full |
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doaj-f57e88a79512486ca0c7279befb77ae3 |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Soo-Hyun Park Soo-Hyun Park Pil-Soo Jeong Ye Eun Joo Ye Eun Joo Hyo-Gu Kang Hyo-Gu Kang Min Ju Kim Min Ju Kim Sanghoon Lee Bong-Seok Song Sun-Uk Kim Sun-Uk Kim Seong-Keun Cho Bo-Woong Sim |
spellingShingle |
Soo-Hyun Park Soo-Hyun Park Pil-Soo Jeong Ye Eun Joo Ye Eun Joo Hyo-Gu Kang Hyo-Gu Kang Min Ju Kim Min Ju Kim Sanghoon Lee Bong-Seok Song Sun-Uk Kim Sun-Uk Kim Seong-Keun Cho Bo-Woong Sim Luteolin Orchestrates Porcine Oocyte Meiotic Progression by Maintaining Organelle Dynamics Under Oxidative Stress Frontiers in Cell and Developmental Biology luteolin antioxidant oxidative stress organelle dynamics in vitro maturation porcine oocyte |
author_facet |
Soo-Hyun Park Soo-Hyun Park Pil-Soo Jeong Ye Eun Joo Ye Eun Joo Hyo-Gu Kang Hyo-Gu Kang Min Ju Kim Min Ju Kim Sanghoon Lee Bong-Seok Song Sun-Uk Kim Sun-Uk Kim Seong-Keun Cho Bo-Woong Sim |
author_sort |
Soo-Hyun Park |
title |
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_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_sort |
luteolin orchestrates porcine oocyte meiotic progression by maintaining organelle dynamics under oxidative stress |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Cell and Developmental Biology |
issn |
2296-634X |
publishDate |
2021-06-01 |
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 H2O2 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 H2O2 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. |
topic |
luteolin antioxidant oxidative stress organelle dynamics in vitro maturation porcine oocyte |
url |
https://www.frontiersin.org/articles/10.3389/fcell.2021.689826/full |
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doaj-f57e88a79512486ca0c7279befb77ae32021-06-15T07:13:43ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2021-06-01910.3389/fcell.2021.689826689826Luteolin Orchestrates Porcine Oocyte Meiotic Progression by Maintaining Organelle Dynamics Under Oxidative StressSoo-Hyun Park0Soo-Hyun Park1Pil-Soo Jeong2Ye Eun Joo3Ye Eun Joo4Hyo-Gu Kang5Hyo-Gu Kang6Min Ju Kim7Min Ju Kim8Sanghoon Lee9Bong-Seok Song10Sun-Uk Kim11Sun-Uk Kim12Seong-Keun Cho13Bo-Woong Sim14Futuristic Animal Resource and Research Center, Korea Research Institute of Bioscience and Biotechnology, Cheongju, South KoreaDepartment of Animal Science, College of Natural Resources and Life Science, Pusan National University, Miryang, South KoreaFuturistic Animal Resource and Research Center, Korea Research Institute of Bioscience and Biotechnology, Cheongju, South KoreaFuturistic Animal Resource and Research Center, Korea Research Institute of Bioscience and Biotechnology, Cheongju, South KoreaDepartment of Animal Science, College of Natural Resources and Life Science, Pusan National University, Miryang, South KoreaFuturistic Animal Resource and Research Center, Korea Research Institute of Bioscience and Biotechnology, Cheongju, South KoreaDepartment of Animal Science and Biotechnology, College of Agriculture and Life Science, Chungnam National University, Daejeon, South KoreaFuturistic Animal Resource and Research Center, Korea Research Institute of Bioscience and Biotechnology, Cheongju, South KoreaDepartment of Animal Science, College of Natural Resources and Life Science, Pusan National University, Miryang, South KoreaFuturistic Animal Resource and Research Center, Korea Research Institute of Bioscience and Biotechnology, Cheongju, South KoreaFuturistic Animal Resource and Research Center, Korea Research Institute of Bioscience and Biotechnology, Cheongju, South KoreaFuturistic Animal Resource and Research Center, Korea Research Institute of Bioscience and Biotechnology, Cheongju, South KoreaDepartment of Functional Genomics, University of Science and Technology, Daejeon, South KoreaDepartment of Animal Science, College of Natural Resources and Life Science, Life and Industry Convergence Research Institute, Pusan National University, Miryang, South KoreaFuturistic Animal Resource and Research Center, Korea Research Institute of Bioscience and Biotechnology, Cheongju, South KoreaIncreasing 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 H2O2 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 H2O2 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.https://www.frontiersin.org/articles/10.3389/fcell.2021.689826/fullluteolinantioxidantoxidative stressorganelle dynamicsin vitro maturationporcine oocyte |